Liptovszky, Mátyás; Perge, Edina; Molnár, Viktor; Sós, Endre
The Grey Mouse Lemur (Microcebus murinus) is a nocturnal lemur species that lives only in Madagascar. It is one of the most abundant lemur species and its native populations are not endangered, but animals belonging to this species are rarely exhibited in zoos. While tumours are quite frequently described in other primates, there are very few publications about neoplasia in lemurs. In this case report we describe a mandibular osteoblastic osteosarcoma in a Grey Mouse Lemur (Microcebus murinus). To the best of the authors' knowledge, this is the first scientific article describing osteosarcoma in a prosimian and also reporting a tumour in the mandible in this taxon.
Canron, Marie-Hélène; Perret, Martine; Vital, Anne; Bézard, Erwan; Dehay, Benjamin
Since age-dependent deposition of Aβ-amyloid has been reported in the Microcebus murinus, we posited that this animal could as well be a model of age-related synucleinopathy. We characterized the distribution of Aβ-amyloid, α-synuclein and two of its modified forms in the brain of Microcebus murinus aged from 1.5 to 10 years. Intracytoplasmic α-synuclein aggregates were observed only in aged animals in different brain regions, which were also phospho-Ser129 and nitrated α-synuclein immunoreactive. Age-dependent α-synuclein aggregation occurs spontaneously in mouse lemur primates. Microcebus murinus may provide a model to study age-associated α-synucleinopathy and for testing putative therapeutic interventions for both Alzheimer's and Parkinson's diseases. PMID:23205271
Schmid, J; Speakman, J R
We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (Tsk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (Ta) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7-8.9 h with a daily mean of 3.4 h, and their Tsk s fell to a minimum of 18.8 degrees C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 +/- 65.4 kJ x day(-1)) was about the same of that of normothermic mouse lemurs in the dry season (115.5 +/- 27.3 kJ x day(-1)). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 +/- 32.7 kJ x day(-1) which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between Tsk and Ta (r2 = 0.37) and with torpor bout length (r2 = 0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 +/- 4.1 ml x day(-1)) was significantly lower than that of mouse lemurs remaining normothermic (19.4 +/- 3.8 ml x day(-1)), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus
Unsworth, Jennifer; Loxley, Grace M.; Davidson, Amanda; Hurst, Jane L.; Gómez-Baena, Guadalupe; Mundy, Nicholas I.; Beynon, Robert J.; Zimmermann, Elke; Radespiel, Ute
Mouse lemurs are basal primates that rely on chemo- and acoustic signalling for social interactions in their dispersed social systems. We examined the urinary protein content of two mouse lemurs species, within and outside the breeding season, to assess candidates used in species discrimination, reproductive or competitive communication. Urine from Microcebus murinus and Microcebus lehilahytsara contain a predominant 10 kDa protein, expressed in both species by some, but not all, males during the breeding season, but at very low levels by females. Mass spectrometry of the intact proteins confirmed the protein mass and revealed a 30 Da mass difference between proteins from the two species. Tandem mass spectrometry after digestion with three proteases and sequencing de novo defined the complete protein sequence and located an Ala/Thr difference between the two species that explained the 30 Da mass difference. The protein (mature form: 87 amino acids) is an atypical member of the whey acidic protein family (WFDC12). Seasonal excretion of this protein, species difference and male-specific expression during the breeding season suggest that it may have a function in intra- and/or intersexual chemical signalling in the context of reproduction, and could be a cue for sexual selection and species recognition. PMID:28225021
Tessier, Shannon N.; Katzenback, Barbara A.; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.
During food shortages, the gray mouse lemur (Microcebus murinus) of Madagascar experiences daily torpor thereby reducing energy expenditures. The present study aimed to understand the impacts of torpor on the immune system and antioxidant response in the gut of these animals. This interaction may be of critical importance given the trade-off between the energetically costly immune response and the need to defend against pathogen entry during hypometabolism. The protein levels of cytokines and antioxidants were measured in the small intestine (duodenum, jejunum, and ileum) and large intestine of aroused and torpid lemurs. While there was a significant decrease of some pro-inflammatory cytokines (IL-6 and TNF-α) in the duodenum and jejunum during torpor as compared to aroused animals, there was no change in anti-inflammatory cytokines. We observed decreased levels of cytokines (IL-12p70 and M-CSF), and several chemokines (MCP-1 and MIP-2) but an increase in MIP-1α in the jejunum of the torpid animals. In addition, we evaluated antioxidant response by examining the protein levels of antioxidant enzymes and total antioxidant capacity provided by metabolites such as glutathione (and others). Our results indicated that levels of antioxidant enzymes did not change between torpor and aroused states, although antioxidant capacity was significantly higher in the ileum during torpor. These data suggest a suppression of the immune response, likely as an energy conservation measure, and a limited role of antioxidant defenses in supporting torpor in lemur intestine. PMID:26092185
Tessier, Shannon N; Katzenback, Barbara A; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B
During food shortages, the gray mouse lemur (Microcebus murinus) of Madagascar experiences daily torpor thereby reducing energy expenditures. The present study aimed to understand the impacts of torpor on the immune system and antioxidant response in the gut of these animals. This interaction may be of critical importance given the trade-off between the energetically costly immune response and the need to defend against pathogen entry during hypometabolism. The protein levels of cytokines and antioxidants were measured in the small intestine (duodenum, jejunum, and ileum) and large intestine of aroused and torpid lemurs. While there was a significant decrease of some pro-inflammatory cytokines (IL-6 and TNF-α) in the duodenum and jejunum during torpor as compared to aroused animals, there was no change in anti-inflammatory cytokines. We observed decreased levels of cytokines (IL-12p70 and M-CSF), and several chemokines (MCP-1 and MIP-2) but an increase in MIP-1α in the jejunum of the torpid animals. In addition, we evaluated antioxidant response by examining the protein levels of antioxidant enzymes and total antioxidant capacity provided by metabolites such as glutathione (and others). Our results indicated that levels of antioxidant enzymes did not change between torpor and aroused states, although antioxidant capacity was significantly higher in the ileum during torpor. These data suggest a suppression of the immune response, likely as an energy conservation measure, and a limited role of antioxidant defenses in supporting torpor in lemur intestine.
Cannibalism, defined as the eating of conspecific flesh, has been observed in a number of primate species, although it is still a relatively rare phenomenon. In cases where primates were seen feeding on an individual of the same species, the victims have exclusively been infants or juveniles. Here, I report an event of a free-living, adult male gray mouse lemur, Microcebus murinus, cannibalizing an adult conspecific female that died of an unknown cause. This observation has implications for the basic ecology of the species and highlights the potential for great flexibility in diet and behavior by a primate. This is, to my knowledge, the first communication of cannibalistic behavior in this species, as well as the first reported case of a nonhuman primate cannibalizing an adult conspecific.
Schilling, Alain; Danilova, Vicktoria; Hellekant, Goran
This study presents the results from two-bottle preference (TBP) tests performed on the gray mouse lemur (Microcebus murinus), a small Malagasy primate. We found that of 18 compounds considered sweet by humans, M. murinus preferred only six: D-tryptophan, dulcin, fructose, sucrose, SC45647, and xylitol. The animals neither preferred nor rejected acesulfame-K, alitame, aspartame, N-4-cyanophenyl-N'-cyanoguanidineacetate (CCGA), cyanosuosan, cyclamate, monellin, saccharin, suosan, super-aspartame, N-trifluoroacetyl-L-glutamyl-4-aminophenylcarbonitrile (TGC), and thaumatin. Together with previously recorded taste-nerve responses in M. murinus to acesulfame-K, alitame, aspartame, cyclamate, monellin, saccharin, and suosan [Hellekant et al., Chem Senses 18:307-320, 1993b], the current results suggest that these compounds either do not taste sweet to M. murinus or they have an aversive taste component. In this work we also relate these findings to phylogeny. Copyright 2004 Wiley-Liss, Inc.
Kobbe, Susanne; Ganzhorn, Jörg U; Dausmann, Kathrin H
Flexibility in physiological processes is essential to adequately respond to changes in environmental conditions. Madagascar is a particularly challenging environment because climatic conditions seem less predictable than in comparative ecosystems in other parts of the world. We used the reddish-gray mouse lemur (Microcebus griseorufus) from the most unpredictable environment in Madagascar as a model to investigate the flexibility of energy saving strategies to cope with the unpredictability of their habitat. For this we measured T (sk) of free-ranging mouse lemurs throughout the year using temperature data loggers. M. griseorufus showed a very strong seasonal as well as an individual flexibility in thermoregulation. During the rainy season all M. griseorufus remained normothermic. At the beginning of the dry season individuals started to exhibit different energy saving strategies: irregular short torpor bouts, regular daily torpor, prolonged torpor of a few days, and hibernation over several weeks. The accumulation of sufficient seasonal body fat was the crucial factor determining the thermal behavior of individuals. The observed intraspecific and sex independent variation in thermoregulatory patterns within one population inhabiting the same small geographical area is exceptional and gives M. griseorufus the ability to respond to current environmental as well as individual conditions. This thermal plasticity might be seen as a key to success and survival for M. griseorufus in an extremely unpredictable environment.
Yoder, Anne D.; Campbell, C. Ryan; Blanco, Marina B.; dos Reis, Mario; Ganzhorn, Jörg U.; Goodman, Steven M.; Hunnicutt, Kelsie E.; Larsen, Peter A.; Kappeler, Peter M.; Rasoloarison, Rodin M.; Ralison, José M.; Swofford, David L.; Weisrock, David W.
Phylogeographic analysis can be described as the study of the geological and climatological processes that have produced contemporary geographic distributions of populations and species. Here, we attempt to understand how the dynamic process of landscape change on Madagascar has shaped the distribution of a targeted clade of mouse lemurs (genus Microcebus) and, conversely, how phylogenetic and population genetic patterns in these small primates can reciprocally advance our understanding of Madagascar's prehuman environment. The degree to which human activity has impacted the natural plant communities of Madagascar is of critical and enduring interest. Today, the eastern rainforests are separated from the dry deciduous forests of the west by a large expanse of presumed anthropogenic grassland savanna, dominated by the Family Poaceae, that blankets most of the Central Highlands. Although there is firm consensus that anthropogenic activities have transformed the original vegetation through agricultural and pastoral practices, the degree to which closed-canopy forest extended from the east to the west remains debated. Phylogenetic and population genetic patterns in a five-species clade of mouse lemurs suggest that longitudinal dispersal across the island was readily achieved throughout the Pleistocene, apparently ending at ∼55 ka. By examining patterns of both inter- and intraspecific genetic diversity in mouse lemur species found in the eastern, western, and Central Highland zones, we conclude that the natural environment of the Central Highlands would have been mosaic, consisting of a matrix of wooded savanna that formed a transitional zone between the extremes of humid eastern and dry western forest types. PMID:27432945
Patterns and energetic consequences of spontaneous daily torpor were measured in the gray mouse lemur (Microcebus murinus) under natural conditions of ambient temperature and photoperiod in a dry deciduous forest in western Madagascar. Over a period of two consecutive dry seasons, oxygen consumption (VO2) and body temperature (T b) were measured on ten individuals kept in outdoor enclosures. In all animals, spontaneous daily torpor occurred on a daily basis with torpor bouts lasting from 3.6 to 17.6 h, with a mean torpor bout duration of 9.3 h. On average, body temperatures in torpor were 17.3±4.9°C with a recorded minimum value of 7.8°C. Torpor was not restricted to the mouse lemurs' diurnal resting phase: entries occurred throughout the night and arousals mainly around midday, coinciding with the daily ambient temperature maximum. Arousal from torpor was a two-phase process with a first passive, exogenous heating where the T b of animals increased from the torpor T b minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise T b to normothermic values. Metabolic rate during torpor (28.6±13.2 ml O2 h(-1)) was significantly reduced by about 76% compared to resting metabolic rate (132.6±50.5 ml O2 h(-1)). On average, for all M. murinus individuals measured, hypometabolism during daily torpor reduced daily energy expenditure by about 38%. In conclusion, all these energy-conserving mechanisms of the nocturnal mouse lemurs, with passive exogenous heating during arousal from torpor, low minimum torpor T bs, and extended torpor bouts into the activity phase, comprise an important and highly adapted mechanism to minimize energetic costs in response to unfavorable environmental conditions and may play a crucial role for individual fitness.
Schmid, J; Speakman, J R
Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T (a)). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T (sk)) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.
Schmid, J.; Speakman, J. R.
Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature ( T a). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature ( T sk) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.
Biggar, Kyle K; Wu, Cheng-Wei; Tessier, Shannon N; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B
A variety of mammals employ torpor as an energy-saving strategy in environments of marginal or severe stress either on a daily basis during their inactive period or on a seasonal basis during prolonged multi-day hibernation. Recently, a few Madagascar lemur species have been identified as the only primates that exhibit torpor; one of these is the gray mouse lemur (Microcebus murinus). To explore the regulatory mechanisms that underlie daily torpor in a primate, we analyzed the expression of 28 selected genes that represent crucial survival pathways known to be involved in squirrel and bat hibernation. Array-based real-time PCR was used to compare gene expression in control (aroused) versus torpid lemurs in five tissues including the liver, kidney, skeletal muscle, heart, and brown adipose tissue. Significant differences in gene expression during torpor were revealed among genes involved in glycolysis, fatty acid metabolism, antioxidant defense, apoptosis, hypoxia signaling, and protein protection. The results showed upregulation of select genes primarily in liver and brown adipose tissue. For instance, both tissues showed elevated gene expression of peroxisome proliferator activated receptor gamma (ppargc), ferritin (fth1), and protein chaperones during torpor. Overall, the data show that the expression of only a few genes changed during lemur daily torpor, as compared with the broader expression changes reported for hibernation in ground squirrels. These results provide an indication that the alterations in gene expression required for torpor in lemurs are not as extensive as those needed for winter hibernation in squirrel models. However, identification of crucial genes with altered expression that support lemur torpor provides key targets to be explored and manipulated toward a goal of translational applications of inducible torpor as a treatment option in human biomedicine. Copyright © 2015. Production and hosting by Elsevier Ltd.
Biggar, Kyle K.; Wu, Cheng-Wei; Tessier, Shannon N.; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.
A variety of mammals employ torpor as an energy-saving strategy in environments of marginal or severe stress either on a daily basis during their inactive period or on a seasonal basis during prolonged multi-day hibernation. Recently, a few Madagascar lemur species have been identified as the only primates that exhibit torpor; one of these is the gray mouse lemur (Microcebus murinus). To explore the regulatory mechanisms that underlie daily torpor in a primate, we analyzed the expression of 28 selected genes that represent crucial survival pathways known to be involved in squirrel and bat hibernation. Array-based real-time PCR was used to compare gene expression in control (aroused) versus torpid lemurs in five tissues including the liver, kidney, skeletal muscle, heart, and brown adipose tissue. Significant differences in gene expression during torpor were revealed among genes involved in glycolysis, fatty acid metabolism, antioxidant defense, apoptosis, hypoxia signaling, and protein protection. The results showed upregulation of select genes primarily in liver and brown adipose tissue. For instance, both tissues showed elevated gene expression of peroxisome proliferator activated receptor gamma (ppargc), ferritin (fth1), and protein chaperones during torpor. Overall, the data show that the expression of only a few genes changed during lemur daily torpor, as compared with the broader expression changes reported for hibernation in ground squirrels. These results provide an indication that the alterations in gene expression required for torpor in lemurs are not as extensive as those needed for winter hibernation in squirrel models. However, identification of crucial genes with altered expression that support lemur torpor provides key targets to be explored and manipulated toward a goal of translational applications of inducible torpor as a treatment option in human biomedicine. PMID:26093281
Burke, Ryan J; Lehman, Shawn M
Edge effects are an inevitable and important consequence of forest loss and fragmentation. These effects include changes in species biology and biogeography. Here we examine variations in body mass and morphometrics for 2 sympatric species of mouse lemurs (Microcebus murinus and M. ravelobensis) between edge and interior habitats in the dry deciduous forest at Ankarafantsika National Park. Between May and August 2012, we conducted mark-recapture experiments on mouse lemurs trapped along edge and interior forest transects within continuous forest adjacent to a large savannah. Of the 34 M. murinus captured during our study, 82% (n = 28) were trapped in interior habitats. Conversely, 72% (n = 47) of M. ravelobensis were captured in edge habitats. We found that mean body mass of M. murinus and M. ravelobensis did not differ between edge and interior habitats. However, female M. ravelobensis weighed significantly more in edge habitats (56.09 ± 1.74 g) than in interior habitats (48.14 ± 4.44 g). Our study provides some of the first evidence of sex differences in edge responses for a primate species.
Background Hematologic and biochemical data are needed to characterize the health status of animal populations over time to determine the habitat quality and captivity conditions. Blood components and the chemical entities that they transport change predominantly with sex and age. The aim of this study was to utilize blood chemistry monitoring to establish the reference levels in a small prosimian primate, the Grey Mouse Lemur (Microcebus murinus). Method In the captive colony, mouse lemurs may live 10–12 years, and three age groups for both males and females were studied: young (1–3 years), middle-aged (4–5 years) and old (6–10 years). Blood biochemical markers were measured using the VetScan Comprehensive Diagnostic Profile. Because many life history traits of this primate are highly dependent on the photoperiod (body mass and reproduction), the effect of season was also assessed. Results The main effect of age was observed in blood markers of renal functions such as creatinine, which was higher among females. Additionally, blood urea nitrogen significantly increased with age and is potentially linked to chronic renal insufficiency, which has been described in captive mouse lemurs. The results demonstrated significant effects related to season, especially in blood protein levels and glucose rates; these effects were observed regardless of gender or age and were likely due to seasonal variations in food intake, which is very marked in this species. Conclusion These results were highly similar with those obtained in other primate species and can serve as references for future research of the Grey Mouse Lemur. PMID:23131178
Thorén, Sandra; Linnenbrink, Miriam; Radespiel, Ute
Interspecific competition has been suggested to influence the biogeographic distribution patterns of species. A high competitive potential could entail species-specific advantages during resource acquisition that could translate into a higher potential for range expansion. We investigated whether differences in the competitive potential of the morphologically similar and partially sympatric gray mouse lemur (Microcebus murinus) and golden-brown mouse lemur (Microcebus ravelobensis) may help to explain differences in their geographic range sizes. We carried out encounter experiments with 14 pairs of captured female mouse lemurs of both species. The experimental dyads were tested in a two-cage arrangement, with individuals being separated from each other outside the experiments. Two days of habituation and four subsequent days of 1-h encounter experiments were conducted, before releasing the animals again in the wild. In general, the M. murinus individuals won significantly more conflicts than their partners. In eight of 14 tested pairs, there was a significant species bias in winning conflicts, and in 87.5% of these dyads, M. murinus was the "dyad winner". A high competitive potential did not depend on body mass. Furthermore, "dyad winners" spent more time feeding (P < 0.05) and were less spatially restricted than "dyad losers". To conclude, our results suggest that the widely distributed M. murinus may indeed have a higher competitive potential than the regional endemic M. ravelobensis, which may, among other possible factors, have enabled this species to expand geographically, despite the presence of other competing congeners.
Terrien, J; Blanc, S; Zizzari, P; Epelbaum, J; Aujard, F
Epidemiological evidence related to increased death from hyperthermia suggests higher frailty in the elderly when exposed to high ambient temperatures. Despite the recent awareness of such public health problems, integrative studies investigating the effects of age on the physiological responses to heat wave thermal conditions remain scarce. Daily rhythmicity of core temperature (T(c)) and locomotor activity (LA), as well as parameters representative of energy balance and IGF-1 levels which are involved in the aging process and stress resistance, were monitored in a non-human primate species, the gray mouse lemur (Microcebus murinus). Adult and aged animals, acclimated to long days (LD) or short days (SD), were monitored during 8-day periods of exposure to 25 ° C and 34 ° C. Adult animals displayed efficient coping with heat exposure, regardless of the photoperiod. Hence, efficient responses resulted in decrease of energy intake, energy expenditure, IGF-1 levels and LA levels, promoting hyperthermia avoidance. Positive energy balance was maintained and water turnover did not change significantly after heat exposure. In contrast, while aged animals acclimated to LD responded similarly to adults, aged mouse lemurs acclimated to SD showed great difficulties coping with heat exposure. Indeed, in this group, normothermia impairment was associated with increased T(c) levels, alterations in daily rhythmicity, negative energy balance and increased IGF-1 levels. Impaired responses to heat exposure were seen in aged mouse lemurs acclimated to SD only. The main effects were observed during diurnal resting periods, suggesting decreased capacities with age to dissipate excess body heat. Taken together, these data highlight daily rhythmicity and IGF-1 pathway as main targets in the impaired response to heat exposure in the elderly. Copyright © 2011 Elsevier Inc. All rights reserved.
Durden, Lance A; Zohdy, Sarah; Laakkonen, Juha
Sucking lice and ticks were collected from live-trapped eastern rufous mouse lemurs, Microcebus rufus Geoffroy, in and around the periphery of Ranomafana National Park, southeastern Madagascar, from 2007 to 2009. Samples of 53 sucking lice (Insecta: Phthiraptera: Anoplura) and 28 hard ticks (Acari: Ixodidae) were collected from 36 lemur captures representing 26 different host individuals. All of the lice were Lemurpediculus verruculosus (Ward) (6 males, 46 females, 1 third instar nymph). Only the holotype female was known previously for this louse and the host was stated to be a "mouse lemur." Therefore, we describe the male and third instar nymph of L. verruculosus and confirm M. rufus as a host (possibly the only host) of this louse. All of the ticks were nymphs and consisted of 16 Haemaphysalis lemuris Hoogstraal, 11 Haemaphysalis sp., and 1 Ixodes sp. The last 2 ticks listed did not morphologically match any of the Madagascar Haemaphysalis or Ixodes ticks for which nymphal stages have been described.
Wu, Cheng-Wei; Biggar, Kyle K.; Zhang, Jing; Tessier, Shannon N.; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.
A natural tolerance of various environmental stresses is typically supported by various cytoprotective mechanisms that protect macromolecules and promote extended viability. Among these are antioxidant defenses that help to limit damage from reactive oxygen species and chaperones that help to minimize protein misfolding or unfolding under stress conditions. To understand the molecular mechanisms that act to protect cells during primate torpor, the present study characterizes antioxidant and heat shock protein (HSP) responses in various organs of control (aroused) and torpid gray mouse lemurs, Microcebus murinus. Protein expression of HSP70 and HSP90α was elevated to 1.26 and 1.49 fold, respectively, in brown adipose tissue during torpor as compared with control animals, whereas HSP60 in liver of torpid animals was 1.15 fold of that in control (P < 0.05). Among antioxidant enzymes, protein levels of thioredoxin 1 were elevated to 2.19 fold in white adipose tissue during torpor, whereas Cu–Zn superoxide dismutase 1 levels rose to 1.1 fold in skeletal muscle (P < 0.05). Additionally, total antioxidant capacity was increased to 1.6 fold in liver during torpor (P < 0.05), while remaining unchanged in the five other tissues. Overall, our data suggest that antioxidant and HSP responses are modified in a tissue-specific manner during daily torpor in gray mouse lemurs. Furthermore, our data also show that cytoprotective strategies employed during primate torpor are distinct from the strategies in rodent hibernation as reported in previous studies. PMID:26092183
Schmid, J; Ruf, T; Heldmaier, G
Thermoregulation, energetics and patterns of torpor in the pygmy mouse lemur, Microcebus myoxinus, were investigated under natural conditions of photoperiod and temperature in the Kirindy/CFPF Forest in western Madagascar. M. myoxinus entered torpor spontaneously during the cool dry season. Torpor only occurred on a daily basis and torpor bout duration was on average 9.6 h, and ranged from 4.6 h to 19.2 h. Metabolic rates during torpor were reduced to about 86% of the normothermic value. Minimum body temperature during daily torpor was 6.8 degrees C at an ambient temperature of 6.3 degrees C. Entry into torpor occurred randomly between 2000 and 0620 hours, whereas arousals from torpor were clustered around 1300 hours within a narrow time window of less than 4 h. Arousal from torpor was a two-step process with a first passive climb of body temperature to a mean of 27 degrees C, carried by the daily increase of ambient temperature when oxygen consumption remained more or less constant, followed by a second active increase of oxygen consumption to further raise the body temperature to normothermic values. In conclusion, daily body temperature rhythms in M. myoxinus further reduce the energetic costs of daily torpor seen in other species: they extend to unusually low body temperatures and consequently low metabolic rates in torpor, and they employ passive warming to reduce the energetic costs of arousal. Thus, these energy-conserving adaptations may represent an important energetic aid to the pygmy mouse lemur and help to promote their individual fitness.
Lutermann, Heike; Schmelting, Barthel; Radespiel, Ute; Ehresmann, Petra; Zimmermann, Elke
It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry. PMID:16959645
Braune, Pia; Schmidt, Sabine; Zimmermann, Elke
Background A central question in evolutionary biology is how cryptic species maintain species cohesiveness in an area of sympatry. The coexistence of sympatrically living cryptic species requires the evolution of species-specific signalling and recognition systems. In nocturnal, dispersed living species, specific vocalisations have been suggested to act as an ideal premating isolation mechanism. We studied the structure and perception of male advertisement calls of three nocturnal, dispersed living mouse lemur species, the grey mouse lemur (Microcebus murinus), the golden brown mouse lemur (M. ravelobensis) and the Goodman's mouse lemur (M. lehilahytsara). The first two species occur sympatrically, the latter lives allopatrically to them. Results A multi-parameter sound analysis revealed prominent differences in the frequency contour and in the duration of advertisement calls. To test whether mouse lemurs respond specifically to calls of the different species, we conducted a playback experiment with M. murinus from the field using advertisement calls and alarm whistle calls of all three species. Individuals responded significantly stronger to conspecific than to heterospecific advertisement calls but there were no differences in response behaviour towards statistically similar whistle calls of the three species. Furthermore, sympatric calls evoked weaker interest than allopatric advertisement calls. Conclusion Our results provide the first evidence for a specific relevance of social calls for speciation in cryptic primates. They furthermore support that specific differences in signalling and recognition systems represent an efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species. PMID:18462484
Blanco, Marina B; Rasoazanabary, Emilienne; Godfrey, Laurie R
Small-bodied, nocturnal mouse lemurs (Microcebus) are widespread across diverse forest habitats in Madagascar. They are strict seasonal breeders and can, depending on the habitat and species, undergo daily or prolonged torpor to minimize energy expenditure during periods of food and water scarcity. Duration of reproduction, number of litters per season and timing of births vary across individuals and species. The "polyestry-seasonality" hypothesis proposes that the duration of reproduction and number of litters per year are positively correlated with rainfall but negatively correlated with longevity, whereas the "hypervariability" hypothesis suggests that the duration of reproduction is negatively correlated with the degree of predictability of food resources. We test these hypotheses in two mouse lemur species inhabiting contrasting habitats, the brown mouse lemurs, Microcebus rufus, from Ranomafana (a less seasonal and more climatically predictable habitat) and the gray-brown mouse lemurs, M. griseorufus, from Beza Mahafaly (a more seasonal and less climatically predictable environment). We use capture/mark/recapture techniques and records of female reproductive status. We found evidence of polyestry at both study sites but faster population turnover and longer duration of the reproductive season at Beza Mahafaly. The "polyestry-seasonality" hypothesis is not supported but the "hypervariability" hypothesis could not be rejected. We conclude that reproductive output cannot be tied to climatic factors in a simple manner. Paradoxically, polyestry can be expressed in contrasting habitats: less seasonal forests where females can sustain multiple reproductive events, but also highly seasonal environments where females may not fatten sufficiently to sustain prolonged torpor but instead remain active throughout the year by relying on fallback resources. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.
Giroud, Sylvain; Blanc, Stéphane; Aujard, Fabienne; Bertrand, Frédéric; Gilbert, Caroline; Perret, Martine
The extent to which seasonal plasticity in torpor displayed by one of the smallest Malagasy primates (Microcebus murinus) will help survival in the context of ongoing global change-induced chronic food shortage, is unknown. Body temperature (Tb) and locomotor activity were measured by telemetry in short- (SD, winter-acclimated) and long-days (LD, summer-acclimated) males (n = 24) during an experimental 35-day calorie restriction of 40 or 80%. Under SD exposure, regardless of calorie restriction intensity, mouse lemurs immediately increased torpor depth and duration by 4.6-fold, and showed greater phase-advanced entry into torpor (2.4-fold). Tb adjustments were efficient under 40% calorie restriction to maintain body mass, whereas they did not prevent a 0.71 +/- 0.11 g/day mass loss during 80% calorie restriction. The 40% food-deprived LD animals combined an early shallow deepening of torpor (1 degrees C) and a late 18% decrease in locomotor activity, resulting in a moderate 6% mass loss. After 15 days of 80% calorie restriction, LD animals exhibited a SD phenotype by increasing their torpor duration and phase-advancing the entry of torpor (16 min/day). Those adjustments had no impact on mass loss (0.93 +/- 0.07 g/day) as locomotor activity increased four-fold. Daily torpor allows M. murinus to face moderate food shortage whatever the photoperiod but poorly mitigates energy imbalance during severe food deprivation, especially under LD exposure. Although the behavioral thermoregulation role warrants further investigation in energy savings, M. murinus survival would be impaired during long-term food shortage in summer.
Biggar, Kyle K.; Wu, Cheng-Wei; Tessier, Shannon N.; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.
Very few selected species of primates are known to be capable of entering torpor. This exciting discovery means that the ability to enter a natural state of dormancy is an ancestral trait among primates and, in phylogenetic terms, is very close to the human lineage. To explore the regulatory mechanisms that underlie primate torpor, we analyzed signal transduction cascades to discover those involved in coordinating tissue responses during torpor. The responses of mitogen-activated protein kinase (MAPK) family members to primate torpor were compared in six organs of control (aroused) versus torpid gray mouse lemurs, Microcebus murinus. The proteins examined include extracellular signal-regulated kinases (ERKs), c-jun NH2-terminal kinases (JNKs), MAPK kinase (MEK), and p38, in addition to stress-related proteins p53 and heat shock protein 27 (HSP27). The activation of specific MAPK signal transduction pathways may provide a mechanism to regulate the expression of torpor-responsive genes or the regulation of selected downstream cellular processes. In response to torpor, each MAPK subfamily responded differently during torpor and each showed organ-specific patterns of response. For example, skeletal muscle displayed elevated relative phosphorylation of ERK1/2 during torpor. Interestingly, adipose tissues showed the highest degree of MAPK activation. Brown adipose tissue displayed an activation of ERK1/2 and p38, whereas white adipose tissue showed activation of ERK1/2, p38, MEK, and JNK during torpor. Importantly, both adipose tissues possess specialized functions that are critical for torpor, with brown adipose required for non-shivering thermogenesis and white adipose utilized as the primary source of lipid fuel for torpor. Overall, these data indicate crucial roles of MAPKs in the regulation of primate organs during torpor. PMID:26093282
Eichmueller, Pia; Thorén, Sandra; Radespiel, Ute
Female dominance is a well-known trait of lemurs, although it has not been reported from all species and is still often unexplored, especially in the nocturnal species. We examined the intersexual dominance relationships in Microcebus ravelobensis, a congener of M. murinus who is well known for its female dominance. Given the many similarities in biology, it was predicted that M. ravelobensis should also possess female dominance. Seventeen unfamiliar male-female pairs were formed with animals captured in northwestern Madagascar and kept in a two-cage setting (one cage for each animal) for up to 1 week. Four encounter experiments were conducted with each pair. In contrast to the expectations, females were not consistently dominant over their male partners. Only 3 of 17 dyads developed a clear agonistic asymmetry, among which were two cases of male dominance and only one case of female dominance. Because body mass differences did not explain the findings, various other possible explanations are discussed. It is suggested that food may not be the driving factor of female dominance in mouse lemurs. Instead, it is hypothesized that species-specific differences in the quality of sleeping sites (i.e., tree holes) and in social grouping patterns may better explain why some mouse lemur species have female dominance, whereas others like the golden-brown mouse lemur do not. It is concluded thatthese arguments and hypotheses may even hold true for other solitary foragers and may thereby lead to a better understanding of the variable social evolution in lemurs and primates in general.
Jürges, Vivian; Kitzler, Johanne; Zingg, Robert; Radespiel, Ute
Following current socio-ecological hypotheses, the social organisation of a species is mainly determined by resource quality and distribution. In the case of Microcebus spp., a taxon-specific socio-ecological model was formulated earlier to explain their variable social organisation. The aim of this study was to test predictions from this model in Goodman's mouse lemur based on a data set from animals living in the semi-free colony of Zurich Zoo. During a 2-month study, we observed 5 females and 5 males using radiotelemetry. We collected data on space use and social behaviour, on sleeping sites and on sleeping group composition. Predictions were only partly confirmed. As expected, Goodman's mouse lemurs were solitary foragers with an increased level of sociality due to crowding effects at the feeding stations. In contrast to the prediction, females and males formed unisexual sleeping groups, which were stable in females and of a fission-fusion type in males. Whereas the formation of sleeping groups by both sexes may be triggered by thermoregulatory benefits, the formation of unisexual sleeping groups may result from divergent interests of the sexes. We conclude that the existing model for the evolution of mouse lemur social organisation needs to be refined.
Pifferi, F; Rahman, A; Languille, S; Auffret, A; Babiloni, C; Blin, O; Lamberty, Y; Richardson, J C; Aujard, F
Converging evidence shows that the non-human primate gray mouse lemur (Microcebus murinus) is ideal for the study of the aging process and for testing the effects of new therapies and dietary interventions on age-associated pathologies. One such dietary supplement is resveratrol (RSV), a dietary polyphenolic compound with several positive effects on metabolic functions and longevity. However, little is known about the effect of RSV on the lemur sleep-wake cycle, which reflects mammalian brain function and health. In the present study, the authors investigated this effect by comparing sleep-wake cycles in adult lemurs based on electroencephalographic (EEG) rhythms. The effect of short-term RSV supplementation on the sleep-wake cycle of mouse lemurs was evaluated in entrained conditions (long-day photoperiods, light:dark 14:10). After 3 wks of RSV supplementation, the animals exhibited a significantly increased proportion of active-wake time, occurring mainly during the resting phase of the sleep-wake cycle (+163%). The increase in active-wake time with RSV supplementation was accompanied by a significant reduction of both paradoxical sleep (-95%) and slow-wave sleep (-38%). These changes mainly occurred during the resting phase of the sleep-wake cycle (RSV supplementation induced negligible changes in active-wake time during the active phase of the sleep-wake cycle). The present data suggest that RSV may be a potent regulator of sleep-wake rhythms and could be of major interest in the study of sleep perturbations associated with aging and neuropathology.
Menet, Marie-Claude; Marchal, Julia; Dal-Pan, Alexandre; Taghi, Méryam; Nivet-Antoine, Valérie; Dargère, Delphine; Laprévote, Olivier; Beaudeux, Jean-Louis; Aujard, Fabienne; Epelbaum, Jacques; Cottart, Charles-Henry
The grey mouse lemur (Microcebus murinus) is a non-human primate used to study the ageing process. Resveratrol is a polyphenol that may increase lifespan by delaying age-associated pathologies. However, no information about resveratrol absorption and metabolism is available for this primate. Resveratrol and its metabolites were qualitatively and quantitatively analyzed in male mouse-lemur plasma (after 200 mg.kg−1 of oral resveratrol) by ultra-high performance liquid chromatography (UHPLC), coupled to a quadrupole-time-of-flight (Q-TOF) mass spectrometer used in full-scan mode. Data analyses showed, in MSE mode, an ion common to resveratrol and all its metabolites: m/z 227.072, and an ion common to dihydro-resveratrol metabolites: m/z 229.08. A semi-targeted study enabled us to identify six hydrophilic resveratrol metabolites (one diglucurono-conjugated, two monoglucurono-conjugated, one monosulfo-conjugated and two both sulfo- and glucurono-conjugated derivatives) and three hydrophilic metabolites of dihydro-resveratrol (one monoglucurono-conjugated, one monosulfo-conjugated, and one both sulfo- and glucurono-conjugated derivatives). The presence of such metabolites has been already detected in the mouse, rat, pig, and humans. Free resveratrol was measurable for several hours in mouse-lemur plasma, and its two main metabolites were trans-resveratrol-3-O-glucuronide and trans-resveratrol-3-sulfate. Free dihydro-resveratrol was not measurable whatever the time of plasma collection, while its hydrophilic metabolites were present at 24 h after intake. These data will help us interpret the effect of resveratrol in mouse lemurs and provide further information on the inter-species characteristics of resveratrol metabolism. PMID:24663435
Valenta, Kim; Burke, Ryan J.; Styler, Sarah A.; Jackson, Derek A.; Melin, Amanda D.; Lehman, Shawn M.
Animals and fruiting plants are involved in a complex set of interactions, with animals relying on fruiting trees as food resources, and fruiting trees relying on animals for seed dispersal. This interdependence shapes fruit signals such as colour and odour, to increase fruit detectability, and animal sensory systems, such as colour vision and olfaction to facilitate food identification and selection. Despite the ecological and evolutionary importance of plant-animal interactions for shaping animal sensory adaptations and plant characteristics, the details of the relationship are poorly understood. Here we examine the role of fruit chromaticity, luminance and odour on seed dispersal by mouse lemurs. We show that both fruit colour and odour significantly predict fruit consumption and seed dispersal by Microcebus ravelobensis and M. murinus. Our study is the first to quantify and examine the role of bimodal fruit signals on seed dispersal in light of the sensory abilities of the disperser. PMID:23939534
Tessier, Shannon N; Zhang, Jing; Biggar, Kyle K; Wu, Cheng-Wei; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B
Gray mouse lemurs (Microcebus murinus) from Madagascar present an excellent model for studies of torpor regulation in a primate species. In the present study, we analyzed the response of the insulin signaling pathway as well as controls on carbohydrate sparing in six different tissues of torpid versus aroused gray mouse lemurs. We found that the relative level of phospho-insulin receptor substrate (IRS-1) was significantly increased in muscle, whereas the level of phospho-insulin receptor (IR) was decreased in white adipose tissue (WAT) of torpid animals, both suggesting an inhibition of insulin/insulin-like growth factor-1 (IGF-1) signaling during torpor in these tissues. By contrast, the level of phospho-IR was increased in the liver. Interestingly, muscle, WAT, and liver occupy central roles in whole body homeostasis and each displays regulatory controls operating at the plasma membrane. Changes in other tissues included an increase in phospho-glycogen synthase kinase 3α (GSK3α) and decrease in phospho-ribosomal protein S6 (RPS6) in the heart, and a decrease in phospho-mammalian target of rapamycin (mTOR) in the kidney. Pyruvate dehydrogenase (PDH) that gates carbohydrate entry into mitochondria is inhibited via phosphorylation by pyruvate dehydrogenase kinase (e.g., PDK4). In the skeletal muscle, the protein expression of PDK4 and phosphorylated PDH at Ser 300 was increased, suggesting inhibition during torpor. In contrast, there were no changes in levels of PDH expression and phosphorylation in other tissues comparing torpid and aroused animals. Information gained from these studies highlight the molecular controls that help to regulate metabolic rate depression and balance energetics during primate torpor.
Dammhahn, Melanie; Kappeler, Peter M
The relationships between resource distribution, type of competition, and consequences for social organization have been formalized in the socioecological model (SEM) which predicts that ecological factors are the main determinants of female distribution. We tested this basic prediction in two solitary primates (Microcebus berthae and M. murinus) which differ in female association patterns. Using stable nitrogen and carbon isotope data of hair samples and food sources we quantified inter-specific differences in diet. delta(13)C in M. berthae reflected a diet composed mainly of insect secretions. Higher within-species as well as seasonal variation in delta(13)C of M. murinus indicated a wider trophic niche including plant and animal source food. Constantly elevated delta(15)N in M. murinus most likely reflected extended torpor during the lean season. This energy-saving strategy together with a wider, more opportunistic feeding niche might reduce female competition in this species, facilitating smaller female ranges, and a higher association potential. In contrast, delta(15)N fluctuated seasonally in M. berthae, most likely indicating varying amounts of arthropod food in the diet. Intense scramble competition over small and seasonally limited resources might lead to female spatial avoidance and a reduced association potential in M. berthae. Thus, differences in female association patterns between these two solitary foragers are due to different types of competition and overall intensities of intra-specific competition.
Rahman, Anisur; Lamberty, Yves; Schenker, Esther; Cella, Massimo; Languille, Solène; Bordet, Régis; Richardson, Jill; Pifferi, Fabien; Aujard, Fabienne
The development of novel therapeutics to prevent cognitive decline of Alzheimer's disease (AD) is facing paramount difficulties since the translational efficacy of rodent models did not resulted in better clinical results. Currently approved treatments, including the acetylcholinesterase inhibitor donepezil (DON) and the N-methyl-D-aspartate antagonist memantine (MEM) provide marginal therapeutic benefits to AD patients. There is an urgent need to develop a predictive animal model that is phylogenetically proximal to humans to achieve better translation. The non-human primate grey mouse lemur (Microcebus murinus) is increasingly used in aging research, but there is no published results related to the impact of known pharmacological treatments on age-related cognitive impairment observed in this primate. In the present study we investigated the effects of DON and MEM on sleep-deprivation (SD)-induced memory impairment in young and aged male mouse lemurs. In particular, spatial memory impairment was evaluated using a circular platform task after 8 h of total SD. Acute single doses of DON or MEM (0.1 and 1mg/kg) or vehicle were administered intraperitoneally 3 h before the cognitive task during the SD procedure. Results indicated that both doses of DON were able to prevent the SD-induced deficits in retrieval of spatial memory as compared to vehicle-treated animals, both in young and aged animals Likewise, MEM show a similar profile at 1 mg/kg but not at 0.1mg/kg. Taken together, these results indicate that two widely used drugs for mitigating cognitive deficits in AD were partially effective in sleep deprived mouse lemurs, which further support the translational potential of this animal model. Our findings demonstrate the utility of this primate model for further testing cognitive enhancing drugs in development for AD or other neuropsychiatric conditions.
Crowley, Brooke E; Rasoazanabary, Emilienne; Godfrey, Laurie R
We examine the ecology of reddish-gray mouse lemurs from three habitats at Beza Mahafaly Special Reserve using focal follows and stable carbon and nitrogen isotope data. Focal observations indicate dietary differences among habitats as well as sexes and seasons. Both sexes consume more arthropods during the rainy season but overall, females consume more sugar-rich exudates and fruit than males, and individuals from riparian forest consume fewer arthropods and more fruit than those in xeric or dry forest. We ask whether these observations are isotopically detectable. Isotope data support differences between seasons and sexes. Nitrogen isotope values are higher during the rainy season when lemurs consume more arthropods, and higher in males than females, particularly during the dry season. However, differences among populations inferred from focal observations are not fully supported. Lemurs from riparian forest have lower isotope values than those in xeric scrub, but isotope data suggest that lemurs from the dry forest eat the least animal matter and that focal observations overestimated dry forest arthropod consumption. Overall, our results suggest that observational and isotopic data are complementary. Isotope data can be obtained from a larger number of individuals and can quantify ingestion of animal matter, but they apparently cannot quantify the relative consumption of different sugar-rich foods. Combined focal and isotope data provide valuable insight into the dietary constraints of reddish-grey mouse lemurs, with implications for their vulnerability to future habitat change.
Joly, Marine; Ammersdörfer, Sandra; Schmidtke, Daniel; Zimmermann, Elke
Mouse lemurs are suggested to represent promising novel non-human primate models for aging research. However, standardized and cross-taxa cognitive testing methods are still lacking. Touchscreen-based testing procedures have proven high stimulus control and reliability in humans and rodents. The aim of this study was to adapt these procedures to mouse lemurs, thereby exploring the effect of age. We measured appetitive learning and cognitive flexibility of two age groups by applying pairwise visual discrimination (PD) and reversal learning (PDR) tasks. On average, mouse lemurs needed 24 days of training before starting with the PD task. Individual performances in PD and PDR tasks correlate significantly, suggesting that individual learning performance is unrelated to the respective task. Compared to the young, aged mouse lemurs showed impairments in both PD and PDR tasks. They needed significantly more trials to reach the task criteria. A much higher inter-individual variation in old than in young adults was revealed. Furthermore, in the PDR task, we found a significantly higher perseverance in aged compared to young adults, indicating an age-related deficit in cognitive flexibility. This study presents the first touchscreen-based data on the cognitive skills and age-related dysfunction in mouse lemurs and provides a unique basis to study mechanisms of inter-individual variation. It furthermore opens exciting perspectives for comparative approaches in aging, personality, and evolutionary research.
Schäffler, Livia; Kappeler, Peter M
The distribution of most recently discovered or described lemur species remains poorly known, but many appear to have small geographical ranges, making them vulnerable to extinction. Research can contribute to future conservation actions on behalf of these species by providing accurate information on local distribution and abundance. The distribution of the world's smallest primate, the endangered Madame Berthe's mouse lemur (Microcebus berthae), is limited to the Menabe Central region of western Madagascar. This species was discovered in the 1990s, but many fundamental aspects of its ecology remain unknown. The aims of our study were therefore to determine the actual distribution of Microcebus berthae across the forests of this region, to estimate population density, and to examine the species' response to anthropogenic activities. We established 35 1-km line transects across Menabe Central, on which we surveyed mouse lemurs by distance sampling and live trapping. Microcebus berthae does not occur in all remaining forests of this small region and its population density is highly heterogeneous, both across its geographic range and locally. Within its area of occupancy, the population of Microcebus berthae not only was distributed according to spatial heterogeneities of the habitat, but also responded to anthropogenic disturbances and varied seasonally. Our results indicate that Microcebus berthae is susceptible to habitat degradation and avoids human environments spatially. As none of the forest remnants in which the species still occurs were officially protected until recently, immediate conservation actions should focus on effectively protecting Kirindy and Ambadira forests.
Rodriguez, Idalia A; Rasoazanabary, Emilienne; Godfrey, Laurie R
At Bezà Mahafaly Special Reserve (BMSR), Madagascar, mouse lemurs (Microcebus griseorufus) are parasitized by multiple species of haemaphysaline ticks. At present we know little about the role ticks play in wild lemur populations and how they can alter interspecies relationships within communities or impact host fitness. In order to better understand these dynamics at BMSR, we examined parasite-host interactions as well as the ecology of mouse lemurs and their infesting ticks, Haemaphysalis lemuris and H. sp. cf. simplex. We show that season, host sex, and habitat influence the relative abundance of ticks on mouse lemurs. Specifically, infestations occur only during the dry season (May-October), are higher in males, and are higher at the study site with the most ground cover and with greater density of large-bodied hosts. Microcebus likely experience decreased susceptibility to tick infestations during the wet season because at that time they rarely if ever descend to the ground. Similarly, male mouse lemurs have higher infestation rates than females because of the greater time they spend traveling and foraging on the ground. During the dry season, Microcebus likely serve as hosts for the tenrec tick, H. sp. cf. simplex, when tenrecs hibernate. In turn, during the wet season when mouse lemurs rarely descend to the ground, other small mammals at the reserve may serve as maintenance hosts for populations of immature ticks. The synchronous development of larvae and nymphs could present high risk for vector-borne disease in Microcebus. This study also provides a preliminary description of the ecology and life cycle of the most common lemur tick, H. lemuris.
Rodriguez, Idalia A.; Rasoazanabary, Emilienne; Godfrey, Laurie R.
At Bezà Mahafaly Special Reserve (BMSR), Madagascar, mouse lemurs (Microcebus griseorufus) are parasitized by multiple species of haemaphysaline ticks. At present we know little about the role ticks play in wild lemur populations and how they can alter interspecies relationships within communities or impact host fitness. In order to better understand these dynamics at BMSR, we examined parasite-host interactions as well as the ecology of mouse lemurs and their infesting ticks, Haemaphysalis lemuris and H. sp. cf. simplex. We show that season, host sex, and habitat influence the relative abundance of ticks on mouse lemurs. Specifically, infestations occur only during the dry season (May–October), are higher in males, and are higher at the study site with the most ground cover and with greater density of large-bodied hosts. Microcebus likely experience decreased susceptibility to tick infestations during the wet season because at that time they rarely if ever descend to the ground. Similarly, male mouse lemurs have higher infestation rates than females because of the greater time they spend traveling and foraging on the ground. During the dry season, Microcebus likely serve as hosts for the tenrec tick, H. sp. cf. simplex, when tenrecs hibernate. In turn, during the wet season when mouse lemurs rarely descend to the ground, other small mammals at the reserve may serve as maintenance hosts for populations of immature ticks. The synchronous development of larvae and nymphs could present high risk for vector-borne disease in Microcebus. This study also provides a preliminary description of the ecology and life cycle of the most common lemur tick, H. lemuris. PMID:26767168
Heckman, Kellie L; Rasoazanabary, Emilienne; Machlin, Erica; Godfrey, Laurie R; Yoder, Anne D
Background The past decade has seen a remarkable increase in the number of recognized mouse lemur species (genus Microcebus). As recently as 1994, only two species of mouse lemur were recognized according to the rules of zoological nomenclature. That number has now climbed to as many as fifteen proposed species. Indeed, increases in recognized species diversity have also characterized other nocturnal primates – galagos, sportive lemurs, and tarsiers. Presumably, the movement relates more to a previous lack of information than it does to any recent proclivity for taxonomic splitting. Due to their nocturnal habits, one can hypothesize that mouse lemurs will show only minimal variation in pelage coloration as such variation should be inconsequential for the purposes of mate and/or species recognition. Even so, current species descriptions for nocturnal strepsirrhines place a good deal of emphasis on relatively fine distinctions in pelage coloration. Results Here, we report results from a multi-year study of mouse lemur populations from Beza Mahafaly in southern Madagascar. On the basis of morphological and pelage variation, we initially hypothesized the presence of up to three species of mouse lemurs occurring sympatrically at this locality, one of which appeared to be undescribed. Genetic analysis reveals definitively, however, that all three color morphs belong to a single recognized species, Microcebus griseorufus. Indeed, in some cases, the three color morphs can be characterized by identical mitochondrial haplotypes. Conclusion Given these results, we conclude that investigators should always proceed with caution when using a single data source to identify novel species. A synthetic approach that combines morphological, genetic, geographic, and ecological data is most likely to reveal the true nature of species diversity. PMID:17109740
Heckman, Kellie L; Rasoazanabary, Emilienne; Machlin, Erica; Godfrey, Laurie R; Yoder, Anne D
The past decade has seen a remarkable increase in the number of recognized mouse lemur species (genus Microcebus). As recently as 1994, only two species of mouse lemur were recognized according to the rules of zoological nomenclature. That number has now climbed to as many as fifteen proposed species. Indeed, increases in recognized species diversity have also characterized other nocturnal primates--galagos, sportive lemurs, and tarsiers. Presumably, the movement relates more to a previous lack of information than it does to any recent proclivity for taxonomic splitting. Due to their nocturnal habits, one can hypothesize that mouse lemurs will show only minimal variation in pelage coloration as such variation should be inconsequential for the purposes of mate and/or species recognition. Even so, current species descriptions for nocturnal strepsirrhines place a good deal of emphasis on relatively fine distinctions in pelage coloration. Here, we report results from a multi-year study of mouse lemur populations from Beza Mahafaly in southern Madagascar. On the basis of morphological and pelage variation, we initially hypothesized the presence of up to three species of mouse lemurs occurring sympatrically at this locality, one of which appeared to be undescribed. Genetic analysis reveals definitively, however, that all three color morphs belong to a single recognized species, Microcebus griseorufus. Indeed, in some cases, the three color morphs can be characterized by identical mitochondrial haplotypes. Given these results, we conclude that investigators should always proceed with caution when using a single data source to identify novel species. A synthetic approach that combines morphological, genetic, geographic, and ecological data is most likely to reveal the true nature of species diversity.
Blanco, Marina B; Andriantsalohimisantatra, Andon'ny A; Rivoharison, Tahiry V; Andriambeloson, Jean-Basile
The small-bodied mouse lemurs of Madagascar (Microcebus) are capable of heterothermy (i.e., torpor or hibernation). The expression of these energy-saving strategies has been physiologically demonstrated in three species: M. berthae, the pygmy mouse lemur (daily torpor), M. murinus, the gray mouse lemur (daily torpor and hibernation), and M. griseorufus, the reddish-gray mouse lemur (daily, prolonged torpor and hibernation). Additional evidence, based on radiotracking and seasonal body mass changes, indicated that mouse lemur capabilities for heterothermy extended to M. lehilahytsara, the Goodman's mouse lemur. In this study, we confirm the use of hibernation in Goodman's mouse lemurs at a new location, a high-plateau forest fragment in Ankafobe, central Madagascar. Our evidence is based on sleeping site monitoring of radiocollared individuals and the retrieval of three mouse lemurs from inside a tree hole, all of which displayed a lethargic state. Though our data are preliminary and scant, we show that hibernation occurs in high-plateau mouse lemurs, and suggest that a buffered environment (i.e., tree holes instead of nests) may be crucial to avoiding potentially extreme ambient temperatures.
Background Studies of host-parasite interactions have the potential to provide insights into the ecology of both organisms involved. We monitored the movement of sucking lice (Lemurpediculus verruculosus), parasites that require direct host-host contact to be transferred, in their host population of wild mouse lemurs (Microcebus rufus). These lemurs live in the rainforests of Madagascar, are small (40 g), arboreal, nocturnal, solitary foraging primates for which data on population-wide interactions are difficult to obtain. We developed a simple, cost effective method exploiting the intimate relationship between louse and lemur, whereby individual lice were marked, without removal from their host, with an individualized code, and tracked throughout the lemur population. We then tested the hypotheses that 1) the frequency of louse transfers, and thus interactions, would decrease with increasing distance between paired individual lemurs; 2) due to host polygynandry, social interactions and hence louse transfers would increase during the onset of the breeding season; and 3) individual mouse lemurs would vary in their contributions to the spread of lice. Results We show that louse transfers involved 43.75% of the studied lemur population, exclusively males. Louse transfers peaked during the breeding season, perhaps due to increased social interactions between lemurs. Although trap-based individual lemur ranging patterns are restricted, louse transfer rate does not correlate with the distance between lemur trapping locales, indicating wider host ranging behavior and a greater risk of rapid population-wide pathogen transmission than predicted by standard trapping data alone. Furthermore, relatively few lemur individuals contributed disproportionately to the rapid spread of lice throughout the population. Conclusions Using a simple method, we were able to visualize exchanges of lice in a population of cryptic wild primates. This method not only provided insight into the
Schmid, J.; Ganzhorn, J. U.
Among the order of primates, torpor has been described only for the small Malagasy cheirogaleids Microcebus and Cheirogaleus. The nocturnal, gray mouse lemur, Microcebus murinus (approx. 60 g), is capable of entering into and spontaneously arousing from apparently daily torpor during the dry season in response to reduced temperatures and low food and water sources. Mark-recapture studies indicated that this primate species might also hibernate for several weeks, although physiological evidence is lacking. In the present study, we investigated patterns of body temperature in two free-ranging M. murinus during the austral winter using temperature-sensitive data loggers implanted subdermally. One lemur hibernated and remained inactive for 4 weeks. During this time, body temperature followed the ambient temperature passively with a minimum body temperature of 11.5°C, interrupted by irregular arousals to normothermic levels. Under the same conditions, the second individual displayed only short bouts of torpor in the early morning hours but maintained stable normothermic body temperatures throughout its nocturnal activity. Reduction of body temperature was less pronounced in the mouse lemur that utilized short bouts of torpor with a minimum value of 27°C. Despite the small sample size, our findings provide the first physiological confirmation that free-ranging individuals of M. murinus from the humid evergreen littoral rain forest have the option to utilize short torpor bouts or hibernation under the same conditions as two alternative energy-conserving physiological solutions to environmental constraints.
McLain, Adam T.; Meyer, Thomas J.; Faulk, Christopher; Herke, Scott W.; Oldenburg, J. Michael; Bourgeois, Matthew G.; Abshire, Camille F.
Lemurs (infraorder: Lemuriformes) are a radiation of strepsirrhine primates endemic to the island of Madagascar. As of 2012, 101 lemur species, divided among five families, have been described. Genetic and morphological evidence indicates all species are descended from a common ancestor that arrived in Madagascar ∼55–60 million years ago (mya). Phylogenetic relationships in this species-rich infraorder have been the subject of debate. Here we use Alu elements, a family of primate-specific Short INterspersed Elements (SINEs), to construct a phylogeny of infraorder Lemuriformes. Alu elements are particularly useful SINEs for the purpose of phylogeny reconstruction because they are identical by descent and confounding events between loci are easily resolved by sequencing. The genome of the grey mouse lemur (Microcebus murinus) was computationally assayed for synapomorphic Alu elements. Those that were identified as Lemuriformes-specific were analyzed against other available primate genomes for orthologous sequence in which to design primers for PCR (polymerase chain reaction) verification. A primate phylogenetic panel of 24 species, including 22 lemur species from all five families, was examined for the presence/absence of 138 Alu elements via PCR to establish relationships among species. Of these, 111 were phylogenetically informative. A phylogenetic tree was generated based on the results of this analysis. We demonstrate strong support for the monophyly of Lemuriformes to the exclusion of other primates, with Daubentoniidae, the aye-aye, as the basal lineage within the infraorder. Our results also suggest Lepilemuridae as a sister lineage to Cheirogaleidae, and Indriidae as sister to Lemuridae. Among the Cheirogaleidae, we show strong support for Microcebus and Mirza as sister genera, with Cheirogaleus the sister lineage to both. Our results also support the monophyly of the Lemuridae. Within Lemuridae we place Lemur and Hapalemur together to the exclusion of
Picq, Jean-Luc; Villain, Nicolas; Gary, Charlotte; Pifferi, Fabien; Dhenain, Marc
The mouse lemur (Microcebus murinus) is a promising primate model for investigating normal and pathological cerebral aging. The locomotor behavior of this arboreal primate is characterized by jumps to and from trunks and branches. Many reports indicate insufficient adaptation of the mouse lemur to experimental devices used to evaluate its cognition, which is an impediment to the efficient use of this animal in research. In order to develop cognitive testing methods appropriate to the behavioral and biological traits of this species, we adapted the Lashley jumping stand apparatus, initially designed for rats, to the mouse lemur. We used this jumping stand apparatus to compare performances of young (n = 12) and aged (n = 8) adults in acquisition and long-term retention of visual discriminations. All mouse lemurs completed the tasks and only 25 trials, on average, were needed to master the first discrimination problem with no age-related differences. A month later, all mouse lemurs made progress for acquiring the second discrimination problem but only the young group reached immediately the criterion in the retention test of the first discrimination problem. This study shows that the jumping stand apparatus allows rapid and efficient evaluation of cognition in mouse lemurs and demonstrates that about half of the old mouse lemurs display a specific deficit in long-term retention but not in acquisition of visual discrimination. PMID:26716699
Picq, Jean-Luc; Villain, Nicolas; Gary, Charlotte; Pifferi, Fabien; Dhenain, Marc
The mouse lemur (Microcebus murinus) is a promising primate model for investigating normal and pathological cerebral aging. The locomotor behavior of this arboreal primate is characterized by jumps to and from trunks and branches. Many reports indicate insufficient adaptation of the mouse lemur to experimental devices used to evaluate its cognition, which is an impediment to the efficient use of this animal in research. In order to develop cognitive testing methods appropriate to the behavioral and biological traits of this species, we adapted the Lashley jumping stand apparatus, initially designed for rats, to the mouse lemur. We used this jumping stand apparatus to compare performances of young (n = 12) and aged (n = 8) adults in acquisition and long-term retention of visual discriminations. All mouse lemurs completed the tasks and only 25 trials, on average, were needed to master the first discrimination problem with no age-related differences. A month later, all mouse lemurs made progress for acquiring the second discrimination problem but only the young group reached immediately the criterion in the retention test of the first discrimination problem. This study shows that the jumping stand apparatus allows rapid and efficient evaluation of cognition in mouse lemurs and demonstrates that about half of the old mouse lemurs display a specific deficit in long-term retention but not in acquisition of visual discrimination.
Bons, Noëlle; Lehmann, Sylvain; Nishida, Noriyuki; Mestre-Frances, Nadine; Dormont, Dominique; Belli, Patrick; Delacourte, Andre; Grassi, Jacques; Brown, Paul
Eleven Microcebus murinus (lemur) primates were intracerebrally or orally infected by bovine spongiform encephalopathy (BSE) or macaque-adapted BSE (MBSE) brain homogenates. In many BSE and MBSE infected lemurs, but not in animals inoculated with normal bovine brain, persistent behavioral changes occurred as early as 3 months, and neurological signs as early as 13 months after infection. Immunohistochemical examination of animals sacrificed during the incubation period revealed an abnormal accumulation of 'prion' protein (PrP) in the intestinal wall, intestinal nervous plexus, mesenteric lymph nodes and spleen, and in the clinical stage, also in the brain. In MBSE-inoculated animals, proteinase K resistance of the PrP (PrPres) was confirmed by Western blot in the spleen and the brain. Obvious signs of neurodegeneration were observed in all infected animals characterized by hyperaggregated and paired-helical filaments-immunoreactive Tau proteins, beta 42-amyloid plaques and astrogliosis. Additionally, PrPres was present in the ganglion cells of the retina in diseased animals after either intracerebrally or oral infection by the BSE or MBSE agent. These results show that the microcebe is susceptible to the BSE infectious agent via intracerebral and oral routes with comparatively short incubation periods compared to simians, and could be a useful animal model to study the pathophysiology of disease transmission in primates.
Gligor, M; Ganzhorn, J U; Rakotondravony, D; Ramilijaona, O R; Razafimahatratra, E; Zischler, H; Hapke, A
Hybrid zones in ecotones can be useful model systems for the study of evolutionary processes that shape the distribution and discreteness of species. Such studies could be important for an improved understanding of the complex biogeography of Madagascar, which is renowned for its outstanding degree of small-scale endemism. Certain forest remnants in central Madagascar indicate that transitional corridors across the island could have connected microendemics in different forest types in the past. Evolutionary processes in such corridors are difficult to study because most of these corridors have disappeared due to deforestation in central Madagascar. We studied a hybrid zone in one of the few remaining ecotonal corridors between dry and humid forests in Madagascar, which connects two species of mouse lemurs, Microcebus griseorufus in dry spiny forest and Microcebus murinus in humid littoral forest. We sampled 162 mouse lemurs at nine sites across this boundary. Morphometric analyses revealed intermediate morphotypes of many individuals in transitional habitat. Bayesian clustering of microsatellite genotypes and assignment tests yielded evidence for a mixed ancestry of mouse lemurs in the ecotone, where we also observed significant linkage disequilibria and heterozygote deficiency. In contrast to these observations, mitochondrial haplotypes displayed a sharply delimited boundary at the eastern edge of spiny forest, which was noncoincident with the signals from microsatellite data. Among several alternative scenarios, we propose asymmetric nuclear introgression due to male-biased dispersal, divergent environmental selection, and an expansion of dry spiny forest in the course of aridification as a probable explanation of our observations.
Crowley, B. E.; Blanco, M. B.; Arrigo-Nelson, S. J.; Irwin, M. T.
The future of Madagascar’s forests and their resident lemurs is precarious. Determining how species respond to forest fragmentation is essential for management efforts. We use stable isotope biogeochemistry to investigate how disturbance affects resource partitioning between two genera of cheirogaleid lemurs ( Cheirogaleus and Microcebus) from three humid forest sites: continuous and fragmented forest at Tsinjoarivo, and selectively logged forest at Ranomafana. We test three hypotheses: (H1) cheirogaleids are unaffected by forest fragmentation, (H2) species respond individually to disturbance and may exploit novel resources in fragmented habitat, and (H3) species alter their behavior to rely on the same key resource in disturbed forest. We find significant isotopic differences among species and localities. Carbon data suggest that Microcebus feed lower in the canopy than Cheirogaleus at all three localities and that sympatric Cheirogaleus crossleyi and C. sibreei feed at different canopy heights in the fragmented forest. Microcbus have higher nitrogen isotope values than Cheirogaleus at all localities, indicating more faunivory. After accounting for baseline isotope values in plants, our results provide the most support for H3. We find similar isotopic variations among localities for both genera. Small differences in carbon among localities may reflect shifts in diet or habitat use. Elevated nitrogen values for cheirogaleid lemurs in fragments may reflect increased arthropod consumption or nutritional stress. These results suggest that cheirogaleids are affected by forest disturbance in Eastern Madagascar and stress the importance of accounting for baseline isotopic differences in plants in any work comparing localities.
Stevens, Jeffrey R; Mühlhoff, Nelly
Different species vary in their ability to wait for delayed rewards in intertemporal choice tasks. Models of rate maximization account for part of this variation, but other factors such as social structure and feeding ecology seem to underly some species differences. Though studies have evaluated intertemporal choice in several primate species, including Old World monkeys, New World monkeys, and apes, prosimians have not been tested. This study investigated intertemporal choices in three species of lemur (black-and-white ruffed lemurs, Varecia variegata, red ruffed lemurs, Varecia rubra, and black lemurs, Eulemur macaco) to assess how they compare to other primate species and whether their choices are consistent with rate maximization. We offered lemurs a choice between two food items available immediately and six food items available after a delay. We found that by adjusting the delay to the larger reward, the lemurs were indifferent between the two options at a mean delay of 17 s, ranging from 9 to 25 s. These data are comparable to data collected from common marmosets (Callithrix jacchus). The lemur data were not consistent with models of rate maximization. The addition of lemurs to the list of species tested in these tasks will help uncover the role of life history and socio-ecological factors influencing intertemporal choices. Copyright © 2011 Elsevier B.V. All rights reserved.
Ezran, Camille; Karanewsky, Caitlin J.; Pendleton, Jozeph L.; Sholtz, Alex; Krasnow, Maya R.; Willick, Jason; Razafindrakoto, Andriamahery; Zohdy, Sarah; Albertelli, Megan A.; Krasnow, Mark A.
Systematic genetic studies of a handful of diverse organisms over the past 50 years have transformed our understanding of biology. However, many aspects of primate biology, behavior, and disease are absent or poorly modeled in any of the current genetic model organisms including mice. We surveyed the animal kingdom to find other animals with advantages similar to mice that might better exemplify primate biology, and identified mouse lemurs (Microcebus spp.) as the outstanding candidate. Mouse lemurs are prosimian primates, roughly half the genetic distance between mice and humans. They are the smallest, fastest developing, and among the most prolific and abundant primates in the world, distributed throughout the island of Madagascar, many in separate breeding populations due to habitat destruction. Their physiology, behavior, and phylogeny have been studied for decades in laboratory colonies in Europe and in field studies in Malagasy rainforests, and a high quality reference genome sequence has recently been completed. To initiate a classical genetic approach, we developed a deep phenotyping protocol and have screened hundreds of laboratory and wild mouse lemurs for interesting phenotypes and begun mapping the underlying mutations, in collaboration with leading mouse lemur biologists. We also seek to establish a mouse lemur gene “knockout” library by sequencing the genomes of thousands of mouse lemurs to identify null alleles in most genes from the large pool of natural genetic variants. As part of this effort, we have begun a citizen science project in which students across Madagascar explore the remarkable biology around their schools, including longitudinal studies of the local mouse lemurs. We hope this work spawns a new model organism and cultivates a deep genetic understanding of primate biology and health. We also hope it establishes a new and ethical method of genetics that bridges biological, behavioral, medical, and conservation disciplines, while
Ezran, Camille; Karanewsky, Caitlin J; Pendleton, Jozeph L; Sholtz, Alex; Krasnow, Maya R; Willick, Jason; Razafindrakoto, Andriamahery; Zohdy, Sarah; Albertelli, Megan A; Krasnow, Mark A
Systematic genetic studies of a handful of diverse organisms over the past 50 years have transformed our understanding of biology. However, many aspects of primate biology, behavior, and disease are absent or poorly modeled in any of the current genetic model organisms including mice. We surveyed the animal kingdom to find other animals with advantages similar to mice that might better exemplify primate biology, and identified mouse lemurs (Microcebus spp.) as the outstanding candidate. Mouse lemurs are prosimian primates, roughly half the genetic distance between mice and humans. They are the smallest, fastest developing, and among the most prolific and abundant primates in the world, distributed throughout the island of Madagascar, many in separate breeding populations due to habitat destruction. Their physiology, behavior, and phylogeny have been studied for decades in laboratory colonies in Europe and in field studies in Malagasy rainforests, and a high quality reference genome sequence has recently been completed. To initiate a classical genetic approach, we developed a deep phenotyping protocol and have screened hundreds of laboratory and wild mouse lemurs for interesting phenotypes and begun mapping the underlying mutations, in collaboration with leading mouse lemur biologists. We also seek to establish a mouse lemur gene "knockout" library by sequencing the genomes of thousands of mouse lemurs to identify null alleles in most genes from the large pool of natural genetic variants. As part of this effort, we have begun a citizen science project in which students across Madagascar explore the remarkable biology around their schools, including longitudinal studies of the local mouse lemurs. We hope this work spawns a new model organism and cultivates a deep genetic understanding of primate biology and health. We also hope it establishes a new and ethical method of genetics that bridges biological, behavioral, medical, and conservation disciplines, while
Lanzagorta, Marco; Jitrik, Oliverio; Uhlmann, Jeffrey; Venegas-Andraca, Salvador E.
In previous research we designed an interferometric quantum seismograph that uses entangled photon states to enhance sensitivity in an optomechanic device. However, a spatially-distributed array of such sensors, with each sensor measuring only nm-vibrations, may not provide sufficient sensitivity for the prediction of major earthquakes because it fails to exploit potentially critical phase information. We conjecture that relative phase information can explain the anecdotal observations that animals such as lemurs exhibit sensitivity to impending earthquakes earlier than can be done confidently with traditional seismic technology. More specifically, we propose that lemurs use their limbs as ground motion sensors and that relative phase differences are fused in the brain in a manner similar to a phased-array or synthetic-aperture radar. In this paper we will describe a lemur-inspired quantum sensor network for early warning of earthquakes. The system uses 4 interferometric quantum seismographs (e.g., analogous to a lemurs limbs) and then conducts phase and data fusion of the seismic information. Although we discuss a quantum-based technology, the principles described can also be applied to classical sensor arrays
Gilbert, Clément; Maxfield, David G.; Goodman, Steven M.; Feschotte, Cédric
Retroviruses normally infect the somatic cells of their host and are transmitted horizontally, i.e., in an exogenous way. Occasionally, however, some retroviruses can also infect and integrate into the genome of germ cells, which may allow for their vertical inheritance and fixation in a given species; a process known as endogenization. Lentiviruses, a group of mammalian retroviruses that includes HIV, are known to infect primates, ruminants, horses, and cats. Unlike many other retroviruses, these viruses have not been demonstrably successful at germline infiltration. Here, we report on the discovery of endogenous lentiviral insertions in seven species of Malagasy lemurs from two different genera—Cheirogaleus and Microcebus. Combining molecular clock analyses and cross-species screening of orthologous insertions, we show that the presence of this endogenous lentivirus in six species of Microcebus is the result of one endogenization event that occurred about 4.2 million years ago. In addition, we demonstrate that this lentivirus independently infiltrated the germline of Cheirogaleus and that the two endogenization events occurred quasi-simultaneously. Using multiple proviral copies, we derive and characterize an apparently full length and intact consensus for this lentivirus. These results provide evidence that lentiviruses have repeatedly infiltrated the germline of prosimian species and that primates have been exposed to lentiviruses for a much longer time than what can be inferred based on sequence comparison of circulating lentiviruses. The study sets the stage for an unprecedented opportunity to reconstruct an ancestral primate lentivirus and thereby advance our knowledge of host–virus interactions. PMID:19300488
Peichl, Leo; Kaiser, Alexander; Rakotondraparany, Felix; Dubielzig, Richard R; Goodman, Steven M; Kappeler, Peter M
The lemurs of Madagascar (Primates: Lemuriformes) are a monophyletic group that has lived in isolation from other primates for about 50 million years. Lemurs have diversified into species with diverse daily activity patterns and correspondingly different visual adaptations. We assessed the arrangements of retinal cone and rod photoreceptors in six nocturnal, three cathemeral and two diurnal lemur species and quantified different parameters in six of the species. The analysis revealed lower cone densities and higher rod densities in the nocturnal than in the cathemeral and diurnal species. The photoreceptor densities in the diurnal Propithecus verreauxi indicate a less "diurnal" retina than found in other diurnal primates. Immunolabeling for cone opsins showed the presence of both middle-to-longwave sensitive (M/L) and shortwave sensitive (S) cones in most species, indicating at least dichromatic color vision. S cones were absent in Allocebus trichotis and Cheirogaleus medius, indicating cone monochromacy. In the Microcebus species, the S cones had an inverse topography with very low densities in the central retina and highest densities in the peripheral retina. The S cones in the other species and the M/L cones in all species had a conventional topography with peak densities in the central area. With the exception of the cathemeral Eulemur species, the eyes of all studied taxa, including the diurnal Propithecus, possessed a tapetum lucidum, a feature only found among nocturnal and crepuscular mammals.
Rakotoniaina, Josué H.; Kappeler, Peter M.; Ravoniarimbinina, Pascaline; Pechouskova, Eva; Hämäläinen, Anni M.; Grass, Juliane; Kirschbaum, Clemens; Kraus, Cornelia
Understanding how animals react to human-induced changes in their environment is a key question in conservation biology. Owing to their potential correlation with fitness, several physiological parameters are commonly used to assess the effect of habitat disturbance on animals’ general health status. Here, we studied how two lemur species, the fat-tailed dwarf lemur (Cheirogaleus medius) and the grey mouse lemur (Microcebus murinus), respond to changing environmental conditions by comparing their stress levels (measured as hair cortisol concentration), parasitism and general body condition across four habitats ordered along a gradient of human disturbance at Kirindy Forest, Western Madagascar. These two species previously revealed contrasting responses to human disturbance; whereas M. murinus is known as a resilient species, C. medius is rarely encountered in highly disturbed habitats. However, neither hair cortisol concentrations nor parasitism patterns (prevalence, parasite species richness and rate of multiple infections) and body condition varied across the gradient of anthropogenic disturbance. Our results indicate that the effect of anthropogenic activities at Kirindy Forest is not reflected in the general health status of both species, which may have developed a range of behavioural adaptations to deal with suboptimal conditions. Nonetheless, a difference in relative density among sites suggests that the carrying capacity of disturbed habitat is lower, and both species respond differently to environmental changes, with C. medius being more negatively affected. Thus, even for behaviourally flexible species, extended habitat deterioration could hamper long-term viability of populations. PMID:27656285
Lehman, Shawn M; Rajaonson, Andry; Day, Sabine
Forest edges are dynamic zones characterized by the penetration (to varying depths and intensities) of conditions from the surrounding environment (matrix) into the forest interior. Although edge effects influence many tropical organisms, they have not been studied directly in primates. Edge effects are particularly relevant to lemurs because of the highly fragmented forest landscapes found in Madagascar. In this study, data are presented regarding how the densities of six lemur species (Avahi laniger, Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, Microcebus rufus, and Propithecus diadema edwardsi) varied between six 500-m interior transects and six 500-m edge transects in the Vohibola III Classified Forest in SE Madagascar. Diurnal (n = 433) and nocturnal (n = 128) lemur surveys were conducted during June-October 2003 and May-November 2004. A. laniger, E. rubriventer, and H. g. griseus exhibited a neutral edge response (no differences in densities between habitats). M. rufus and P. d. edwardsi had a positive edge response (higher densities in edge habitats), which may be related to edge-related variations in food abundance and quality. Positive edge responses by M. rufus and P. d. edwardsi may ultimately be detrimental due to edge-related anthropogenic factors (e.g., hunting by local people). The negative edge response exhibited by C. major (lower densities in edge habitats) may result from heightened ambient temperatures that inhibit torpor in edge habitats.
Sawyer, Rachel Mary; Fenosoa, Zo Samuel Ella; Andrianarimisa, Aristide; Donati, Giuseppe
Madagascar is one of the world's biodiversity hotspots. The island's past and current rates of deforestation and habitat disturbance threaten its plethora of endemic biodiversity. On Madagascar, tavy (slash and burn agriculture), land conversion for rice cultivation, illegal hardwood logging and bushmeat hunting are the major contributors to habitat disturbance. Understanding species-specific responses to habitat disturbance across different habitat types is crucial when designing conservation strategies. We surveyed three nocturnal lemur species in four forest types of varying habitat disturbance on the Masoala Peninsula, northeastern Madagascar. We present here updated abundance and density estimates for the Endangered Avahi mooreorum and Lepilemur scottorum, and Microcebus sp. Distance sampling surveys were conducted on 11 transects, covering a total of 33 km after repeated transect walks. We collected data on tree height, bole height, diameter at breast height, canopy cover and tree density using point-quarter sampling to characterise the four forest types (primary lowland, primary littoral, selectively logged and agricultural mosaic). Median encounter rates by forest type ranged from 1 to 1.5 individuals (ind.)/km (Microcebus sp.), 0-1 ind./km (A. mooreorum) and 0-1 ind./km (L. scottorum). Species density estimates were calculated at 232.31 ind./km(2) (Microcebus sp.) and 121.21 ind./km(2) (A. mooreorum), while no density estimate is provided for L. scottorum due to a small sample size. Microcebus sp. was most tolerant to habitat disturbance, exhibiting no significant effect of forest type on abundance. Its small body size, omnivorous diet and generalised locomotion appear to allow it to tolerate a variety of habitat disturbance. Both A. mooreorum and L. scottorum showed significant effects of forest type on their respective abundance. This study suggests that the specialist locomotion and diet of A. mooreorum and L. scottorum make them susceptible to the
Hotaling, Scott; Foley, Mary E; Lawrence, Nicolette M; Bocanegra, Jose; Blanco, Marina B; Rasoloarison, Rodin; Kappeler, Peter M; Barrett, Meredith A; Yoder, Anne D; Weisrock, David W
Implementation of the coalescent model in a Bayesian framework is an emerging strength in genetically based species delimitation studies. By providing an objective measure of species diagnosis, these methods represent a quantitative enhancement to the analysis of multilocus data, and complement more traditional methods based on phenotypic and ecological characteristics. Recognized as two species 20 years ago, mouse lemurs (genus Microcebus) now comprise more than 20 species, largely diagnosed from mtDNA sequence data. With each new species description, enthusiasm has been tempered with scientific scepticism. Here, we present a statistically justified and unbiased Bayesian approach towards mouse lemur species delimitation. We perform validation tests using multilocus sequence data and two methodologies: (i) reverse-jump Markov chain Monte Carlo sampling to assess the likelihood of different models defined a priori by a guide tree, and (ii) a Bayes factor delimitation test that compares different species-tree models without a guide tree. We assess the sensitivity of these methods using randomized individual assignments, which has been used in bpp studies, but not with Bayes factor delimitation tests. Our results validate previously diagnosed taxa, as well as new species hypotheses, resulting in support for three new mouse lemur species. As the challenge of multiple researchers using differing criteria to describe diversity is not unique to Microcebus, the methods used here have significant potential for clarifying diversity in other taxonomic groups. We echo previous studies in advocating that multiple lines of evidence, including use of the coalescent model, should be trusted to delimit new species.
Drucker, Caroline B; Baghdoyan, Talia; Brannon, Elizabeth M
Implicit learning involves picking up information from the environment without explicit instruction or conscious awareness of the learning process. In nonhuman animals, conscious awareness is impossible to assess, so we define implicit learning as occurring when animals acquire information beyond what is required for successful task performance. While implicit learning has been documented in some nonhuman species, it has not been explored in prosimian primates. Here we ask whether ring-tailed lemurs (Lemur catta) learn sequential information implicitly. We tested lemurs in a modified version of the serial reaction time task on a touch screen computer. Lemurs were required to respond to any picture within a 2 × 2 grid of pictures immediately after its surrounding border flickered. Over 20 training sessions, both the locations and the identities of the images remained constant and response times gradually decreased. Subsequently, the locations and/or the identities of the images were disrupted. Response times indicated that the lemurs had learned the physical location sequence required in original training but did not learn the identity of the images. Our results reveal that ring-tailed lemurs can implicitly learn spatial sequences, and raise questions about which scenarios and evolutionary pressures give rise to perceptual versus motor-implicit sequence learning.
Gardner, Charlie J
Despite an increasing recognition of the ecosystem services provided by mangroves, we know little about their role in maintaining terrestrial biodiversity, including primates. Madagascar's lemurs are a top global conservation priority, with 94 % of species threatened with extinction, but records of their occurrence in mangroves are scarce. I used a mixed-methods approach to collect published and unpublished observations of lemurs in mangroves: I carried out a systematic literature search and supplemented this with a targeted information request to 1243 researchers, conservation and tourism professionals, and others who may have visited mangroves in Madagascar. I found references to, or observations of, at least 23 species in 5 families using mangroves, representing >20% of lemur species and >50% of species whose distributions include mangrove areas. Lemurs used mangroves for foraging, sleeping, and traveling between terrestrial forest patches, and some were observed as much as 3 km from the nearest permanently dry land. However, most records were anecdotal and thus tell us little about lemur ecology in this habitat. Mangroves are more widely used by lemurs than has previously been recognized and merit greater attention from primate researchers and conservationists in Madagascar.
Kobbe, Susanne; Dausmann, Kathrin H.
The spiny forest of southwestern Madagascar is the driest and most unpredictable region of the island. It is characterized by a pronounced seasonality with high fluctuations in ambient temperature, low availability of food, and a lack of water during the cool dry season and, additionally, by changes in environmental conditions between years. One of the few mammalian species that manages to inhabit this challenging habitat is the reddish-gray mouse lemur ( Microcebus griseorufus). The aim of our study was to determine whether this small primate uses continuous hibernation as an energy saving strategy, and if so, to characterize its physiological properties. We measured skin temperature of 16 free-ranging individuals continuously over 3 months during the cool dry season using collar temperature data loggers. Prolonged hibernation was found in three mouse lemurs and was not sex dependent (one male, two females). Skin temperature of hibernating individuals tracked ambient temperature passively with a minimum skin temperature of 6.5°C and fluctuated strongly each day (up to 20°C), depending on the insulation capacity of the hibernacula. Individuals remained in continuous hibernation even at an ambient temperature of 37°C. The animals hibernated continuously during the dry season, and hibernation bouts were only interrupted by short spontaneous arousals. The study emphasizes that hibernation is an important measure to counter environmental challenge for more tropical species than previously thought, including primates. It furthermore provides evidence that tropical hibernation is functionally similar among tropical species.
Kobbe, Susanne; Dausmann, Kathrin H
The spiny forest of southwestern Madagascar is the driest and most unpredictable region of the island. It is characterized by a pronounced seasonality with high fluctuations in ambient temperature, low availability of food, and a lack of water during the cool dry season and, additionally, by changes in environmental conditions between years. One of the few mammalian species that manages to inhabit this challenging habitat is the reddish-gray mouse lemur (Microcebus griseorufus). The aim of our study was to determine whether this small primate uses continuous hibernation as an energy saving strategy, and if so, to characterize its physiological properties. We measured skin temperature of 16 free-ranging individuals continuously over 3 months during the cool dry season using collar temperature data loggers. Prolonged hibernation was found in three mouse lemurs and was not sex dependent (one male, two females). Skin temperature of hibernating individuals tracked ambient temperature passively with a minimum skin temperature of 6.5 degrees C and fluctuated strongly each day (up to 20 degrees C), depending on the insulation capacity of the hibernacula. Individuals remained in continuous hibernation even at an ambient temperature of 37 degrees C. The animals hibernated continuously during the dry season, and hibernation bouts were only interrupted by short spontaneous arousals. The study emphasizes that hibernation is an important measure to counter environmental challenge for more tropical species than previously thought, including primates. It furthermore provides evidence that tropical hibernation is functionally similar among tropical species.
Zordan, Martin; Tirado, Marcela; López, Claudia
A female ring-tailed lemur (Lemur catta) and her two cubs held in a zoo in Chile exhibited signs of severe hepatic insufficiency. In spite of supportive treatment, the three animals died a few days after the onset of signs. Postmortem examination revealed ascites and fibrotic lesions in the liver of all the individuals. Histologically, the liver of two of them showed a severe parasitic ova infection and lipidosis, the morphologic characteristics of the parasitic ovas were consistent with Capillaria hepatica (syn. Calodium hepatica) eggs. To the authors' knowledge, this is the first clinical case report of hepatic capillariasis in prosimians, and its implications are discussed.
Cuozzo, Frank P; Rasoazanabary, Emilienne; Godfrey, Laurie R; Sauther, Michelle L; Youssouf, Ibrahim Antho; LaFleur, Marni M
A thorough knowledge of biological variation in extant primates is imperative for interpreting variation, and for delineating species in primate biology and paleobiology. This is especially the case given the recent, rapid taxonomic expansion in many primate groups, notably among small-bodied nocturnal forms. Here we present data on dental, cranial, and pelage variation in a single-locality museum sample of mouse lemurs from Amboasary, Madagascar. To interpret these data, we include comparative information from other museum samples, and from a newly collected mouse lemur skeletal sample from the Beza Mahafaly Special Reserve (BMSR), Madagascar. We scored forty dental traits (n = 126) and three pelage variants (n = 19), and collected 21 cranial/dental measures. Most dental traits exhibit variable frequencies, with some only rarely present. Individual dental variants include misshapen and supernumerary teeth. All Amboasary pelage specimens display a "reversed V" on the cap, and a distinct dorsal median stripe on the back. All but two displayed the dominant gray-brown pelage coloration typical of Microcebus griseorufus. Cranial and dental metric variability are each quite low, and craniometric variation does not illustrate heteroscedasticity. To assess whether this sample represents a single species, we compared dental and pelage variation to a documented, single-species M. griseorufus sample from BMSR. As at Amboasary, BMSR mouse lemurs display limited odontometric variation and wide variation in non-metric dental traits. In contrast, BMSR mouse lemurs display diverse pelage, despite reported genetic homogeneity. Ranges of dental and pelage variation at BMSR and Amboasary overlap. Thus, we conclude that the Amboasary mouse lemurs represent a single species - most likely (in the absence of genetic data to the contrary) M. griseorufus, and we reject their previous allocation to Microcebus murinus. Patterns of variation in the Amboasary sample provide a comparative
Introduction Maternal kin selection is a driving force in the evolution of mammalian social complexity and it requires that kin are distinctive from nonkin. The transition from the ancestral state of asociality to the derived state of complex social groups is thought to have occurred via solitary foraging, in which individuals forage alone, but, unlike the asocial ancestors, maintain dispersed social networks via scent-marks and vocalizations. We hypothesize that matrilineal signatures in vocalizations were an important part of these networks. We used the solitary foraging gray mouse lemur (Microcebus murinus) as a model for ancestral solitary foragers and tested for matrilineal signatures in their calls, thus investigating whether such signatures are already present in solitary foragers and could have facilitated the kin selection thought to have driven the evolution of increased social complexity in mammals. Because agonism can be very costly, selection for matrilineal signatures in agonistic calls should help reduce agonism between unfamiliar matrilineal kin. We conducted this study on a well-studied population of wild mouse lemurs at Ankarafantsika National Park, Madagascar. We determined pairwise relatedness using seven microsatellite loci, matrilineal relatedness by sequencing the mitrochondrial D-loop, and sleeping group associations using radio-telemetry. We recorded agonistic calls during controlled social encounters and conducted a multi-parametric acoustic analysis to determine the spectral and temporal structure of the agonistic calls. We measured 10 calls for each of 16 females from six different matrilineal kin groups. Results Calls were assigned to their matriline at a rate significantly higher than chance (pDFA: correct = 47.1%, chance = 26.7%, p = 0.03). There was a statistical trend for a negative correlation between acoustic distance and relatedness (Mantel Test: g = -1.61, Z = 4.61, r = -0.13, p = 0.058). Conclusions
Reddy, Rachna B; MacLean, Evan L; Sandel, Aaron A; Hare, Brian
We tested five lemur species-ring-tailed lemurs, ruffed lemurs, mongoose lemurs, black lemurs, and Coquerel's sifakas-(N = 52) in an experiment that evaluated skills for inhibitory control in a social context. First, two human experimenters presented identical food rewards; the "generous" experimenter allowed the subject to eat from her hand, whereas the "competitive" experimenter always withheld the reward. Lemurs quickly learned to approach the generous experimenter and avoid the competitive one. In the inhibition test phase, we endowed the competitive experimenter with a more valuable food reward but the competitive experimenter continued to withhold food from the subject. Thus, lemurs were required to inhibit approaching the more desirable reward in favor of the lesser but obtainable reward presented by the generous experimenter. In test trials, lemurs' tendency to approach the competitive experimenter increased from the reputation phase, demonstrating sensitivity to the experimental manipulation. However, subjects approached the larger reward less frequently in test trials compared with pretest food-preference trials, evidencing some capacity for inhibitory control in this context. Despite differences in sociality and ecology, the five lemur species did not differ in this ability. Although the study did not uncover species differences, this experimental task may provide a useful measure of social inhibition in broader comparative studies.
Reuter, Kim E; Schaefer, Melissa S
Live extraction of wildlife is a threat to biodiversity and can compromise animal welfare standards. Studies of the captive environments and welfare of pet primates are known, but none has focused on Madagascar. We aimed to expand knowledge about the captive conditions of pet lemurs in Madagascar. We hypothesized that captive lemurs would often be kept in restrictive settings, including small cages, would be fed foods inconsistent with their natural diets and, as a result, would be in bad physical or psychological health. Data were collected via a web-based survey (n = 253 reports) and from the websites and social media pages of 25 hotels. Most lemurs seen by respondents were either kept on a rope/leash/chain or in a cage (67%), though some lemurs were habituated and were not restrained (28%). Most of the time (72%) cages were considered small, and lemurs were rarely kept in captivity together with other lemurs (81% of lemurs were caged alone). Pet lemurs were often fed foods inconsistent with their natural diets, and most (53%) were described as being in bad health. These findings point to a need to undertake outreach to pet lemur owners in Madagascar about the captivity requirements of primates.
Merritt, Dustin J.; MacLean, Evan L.; Crawford, Jeremy Chase; Brannon, Elizabeth M.
We investigated numerical discrimination and numerical rule-learning in ring-tailed lemurs (Lemur catta). Two ring-tailed lemurs were trained to respond to two visual arrays, each of which contained between one and four elements, in numerically ascending order. In Experiment 1, lemurs were trained with 36 exemplars of each of the numerosities 1–4 and then showed positive transfer to trial-unique novel exemplars of the values 1–4. In Experiments 2A and 2B, lemurs were tested on their ability to transfer an ascending numerical rule from the values 1–4 to novel values 5–9. Both lemurs successfully ordered the novel values with above chance accuracy. Accuracy was modulated by the ratio between the two numerical values suggesting that lemurs accessed the approximate number system when performing the task. PMID:21713071
Rakotondranary, S. Jacques; Struck, Ulrich; Knoblauch, Christian; Ganzhorn, Jörg U.
Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson's rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these "rules" and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses ( δ 15N and δ 13C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ 13C values, indicating that M. griseorufus feeds more on C4 and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ 15N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.
Hohenbrink, Philipp; Dempewolf, Silke; Zimmermann, Elke; Mundy, Nicholas I.; Radespiel, Ute
The vomeronasal organ (VNO) is functional in most terrestrial mammals, though progressively reduced in the primate lineage, and is used for intraspecific communication and predator recognition. Vomeronasal receptor (VR) genes comprise two families of chemosensory genes (V1R and V2R) that have been considered to be specific for the VNO. However, recently a large number of VRs were reported to be expressed in the main olfactory epithelium (MOE) of mice, but there is little knowledge of the expression of these genes outside of rodents. To explore the function of VR genes in mammalian evolution, we analyzed and compared the expression of 64 V1R and 2 V2R genes in the VNO and the MOE of the gray mouse lemur (Microcebus murinus), the primate with the largest known VR repertoire. We furthermore compared expression patterns in adults of both sexes and seasons, and in an infant. A large proportion (83–97%) of the VR loci was expressed in the VNO of all individuals. The repertoire in the infant was as rich as in adults, indicating reliance on olfactory communication from early postnatal development onwards. In concordance with mice, we also detected extensive expression of VRs in the MOE, with proportions of expressed loci in individuals ranging from 29 to 45%. TRPC2, which encodes a channel protein crucial for signal transduction via VRs, was co-expressed in the MOE in all individuals indicating likely functionality of expressed VR genes in the MOE. In summary, the large VR repertoire in mouse lemurs seems to be highly functional. Given the differences in the neural pathways of MOE and VNO signals, which project to higher cortical brain centers or the limbic system, respectively, this raises the intriguing possibility that the evolution of MOE-expression of VRs enabled mouse lemurs to adaptively diversify the processing of VR-encoded olfactory information. PMID:25309343
Hope, Katharine L; Boedeker, Nancy C; Gordon, Sebastian S; Walsh, Timothy F
A 20-y-old, male, ring-tailed lemur (Lemur catta) presented with a large, firm mass on the proximal caudolateral left femur. The animal displayed no clinical signs associated with the mass. Radiographs revealed a mineralized mass protruding from the femur, with an intact femoral cortex. Histopathology diagnosed osteochondroma in view of the presence of a peripheral layer of cartilage with progressive endochondral ossification and typical remodeling of bony trabeculae. The mass grew quickly after the initial biopsy, and a second surgery to debulk 95% of the tumor was performed. Histopathologic features of the larger samples were similar to those of the initial biopsies, with the cartilage layer being discontinuous and development of bone from some borders progressing directly from a periost-like layer. Nineteen months after the second surgery, the mass had regrown and extended further proximally on the femur toward the epiphysis, but the animal remained asymptomatic, and additional debulking was not attempted. This report is the first description of an osteochondroma in a prosimian and describes unique behavior of the tumor compared with osteochondromas found in humans, dogs, and cats. PMID:26310465
Kendal, Rachel L; Custance, Deborah M; Kendal, Jeremy R; Vale, Gillian; Stoinski, Tara S; Rakotomalala, Nirina Lalaina; Rasamimanana, Hantanirina
Interest in social learning has been fueled by claims of culture in wild animals. These remain controversial because alternative explanations to social learning, such as asocial learning or ecological differences, remain difficult to refute. Compared with laboratory-based research, the study of social learning in natural contexts is in its infancy. Here, for the first time, we apply two new statistical methods, option-bias analysis and network-based diffusion analysis, to data from the wild, complemented by standard inferential statistics. Contrary to common thought regarding the cognitive abilities of prosimian primates, our evidence is consistent with social learning within subgroups in the ring-tailed lemur (Lemur catta), supporting the theory of directed social learning (Coussi-Korbel & Fragaszy, 1995). We also caution that, as the toolbox for capturing social learning in natural contexts grows, care is required in ensuring that the methods employed are appropriate-in particular, regarding social dynamics among study subjects. Supplemental materials for this article may be downloaded from http://lb.psychonomic-journals.org/content/supplemental.
Hope, Katharine L; Boedeker, Nancy C; Gordon, Sebastian S; Walsh, Timothy F
A 20-y-old, male, ring-tailed lemur (Lemur catta) presented with a large, firm mass on the proximal caudolateral left femur. The animal displayed no clinical signs associated with the mass. Radiographs revealed a mineralized mass protruding from the femur, with an intact femoral cortex. Histopathology diagnosed osteochondroma in view of the presence of a peripheral layer of cartilage with progressive endochondral ossification and typical remodeling of bony trabeculae. The mass grew quickly after the initial biopsy, and a second surgery to debulk 95% of the tumor was performed. Histopathologic features of the larger samples were similar to those of the initial biopsies, with the cartilage layer being discontinuous and development of bone from some borders progressing directly from a periost-like layer. Nineteen months after the second surgery, the mass had regrown and extended further proximally on the femur toward the epiphysis, but the animal remained asymptomatic, and additional debulking was not attempted. This report is the first description of an osteochondroma in a prosimian and describes unique behavior of the tumor compared with osteochondromas found in humans, dogs, and cats.
Van Steenhouse, Jan L.; Bradley, Julie M.; Hancock, Susan I.; Hegarty, Barbara C.; Breitschwerdt, Edward B.
A naturally occurring infection of Ehrlichia chaffeensis in lemurs is described. DNA of Ehrlichia chaffeensis was identified by polymerase chain reaction in peripheral blood from six of eight clinically ill lemurs. Organisms were cultured from the blood of one lemur exhibiting clinical and hematologic abnormalities similar to those of humans infected with E. chaffeensis. PMID:12498671
Rahman, Anisur; Lamberty, Yves; Bordet, Regis; Richardson, Jill C.; Forloni, Gianluigi; Drinkenburg, Wilhelmus; Lopez, Susanna; Aujard, Fabienne; Babiloni, Claudio; Pifferi, Fabien
The gray mouse lemur (Microcebus murinus) is considered a useful primate model for translational research. In the framework of IMI PharmaCog project (Grant Agreement n°115009, www.pharmacog.org), we tested the hypothesis that spectral electroencephalographic (EEG) markers of motor and locomotor activity in gray mouse lemurs reflect typical movement-related desynchronization of alpha rhythms (about 8–12 Hz) in humans. To this aim, EEG (bipolar electrodes in frontal cortex) and electromyographic (EMG; bipolar electrodes sutured in neck muscles) data were recorded in 13 male adult (about 3 years) lemurs. Artifact-free EEG segments during active state (gross movements, exploratory movements or locomotor activity) and awake passive state (no sleep) were selected on the basis of instrumental measures of animal behavior, and were used as an input for EEG power density analysis. Results showed a clear peak of EEG power density at alpha range (7–9 Hz) during passive state. During active state, there was a reduction in alpha power density (8–12 Hz) and an increase of power density at slow frequencies (1–4 Hz). Relative EMG activity was related to EEG power density at 2–4 Hz (positive correlation) and at 8–12 Hz (negative correlation). These results suggest for the first time that the primate gray mouse lemurs and humans may share basic neurophysiologic mechanisms of synchronization of frontal alpha rhythms in awake passive state and their desynchronization during motor and locomotor activity. These EEG markers may be an ideal experimental model for translational basic (motor science) and applied (pharmacological and non-pharmacological interventions) research in Neurophysiology. PMID:26618512
Languille, Solène; Liévin-Bazin, Agatha; Picq, Jean-Luc; Louis, Caroline; Dix, Sophie; De Barry, Jean; Blin, Olivier; Richardson, Jill; Bordet, Régis; Schenker, Esther; Djelti, Fathia; Aujard, Fabienne
Owing to a similar cerebral neuro-anatomy, non-human primates are viewed as the most valid models for understanding cognitive deficits. This study evaluated psychomotor and mnesic functions of 41 young to old mouse lemurs (Microcebus murinus). Psychomotor capacities and anxiety-related behaviors decreased abruptly from middle to late adulthood. However, mnesic functions were not affected in the same way with increasing age. While results of the spontaneous alternation task point to a progressive and widespread age-related decline of spatial working memory, both spatial reference and novel object recognition (NOR) memory tasks did not reveal any tendency due to large inter-individual variability in the middle-aged and old animals. Indeed, some of the aged animals performed as well as younger ones, whereas some others had bad performances in the Barnes maze and in the object recognition test. Hierarchical cluster analysis revealed that declarative-like memory was strongly impaired only in 7 out of 25 middle-aged/old animals. These results suggest that this analysis allows to distinguish elder populations of good and bad performers in this non-human primate model and to closely compare this to human aging.
Languille, Solène; Liévin-Bazin, Agatha; Picq, Jean-Luc; Louis, Caroline; Dix, Sophie; De Barry, Jean; Blin, Olivier; Richardson, Jill; Bordet, Régis; Schenker, Esther; Djelti, Fathia; Aujard, Fabienne
Owing to a similar cerebral neuro-anatomy, non-human primates are viewed as the most valid models for understanding cognitive deficits. This study evaluated psychomotor and mnesic functions of 41 young to old mouse lemurs (Microcebus murinus). Psychomotor capacities and anxiety-related behaviors decreased abruptly from middle to late adulthood. However, mnesic functions were not affected in the same way with increasing age. While results of the spontaneous alternation task point to a progressive and widespread age-related decline of spatial working memory, both spatial reference and novel object recognition (NOR) memory tasks did not reveal any tendency due to large inter-individual variability in the middle-aged and old animals. Indeed, some of the aged animals performed as well as younger ones, whereas some others had bad performances in the Barnes maze and in the object recognition test. Hierarchical cluster analysis revealed that declarative-like memory was strongly impaired only in 7 out of 25 middle-aged/old animals. These results suggest that this analysis allows to distinguish elder populations of good and bad performers in this non-human primate model and to closely compare this to human aging. PMID:25620921
Huchard, Elise; Albrecht, Christina; Schliehe-Diecks, Susanne; Baniel, Alice; Roos, Christian; Kappeler, Peter M; Peter, Peter M Kappeler; Brameier, Markus
The critical role of major histocompatibility complex (MHC) genes in disease resistance, along with their putative function in sexual selection, reproduction and chemical ecology, make them an important genetic system in evolutionary ecology. Studying selective pressures acting on MHC genes in the wild nevertheless requires population-wide genotyping, which has long been challenging because of their extensive polymorphism. Here, we report on large-scale genotyping of the MHC class II loci of the grey mouse lemur (Microcebus murinus) from a wild population in western Madagascar. The second exons from MHC-DRB and -DQB of 772 and 672 individuals were sequenced, respectively, using a 454 sequencing platform, generating more than 800,000 reads. Sequence analysis, through a stepwise variant validation procedure, allowed reliable typing of more than 600 individuals. The quality of our genotyping was evaluated through three independent methods, namely genotyping the same individuals by both cloning and 454 sequencing, running duplicates, and comparing parent-offspring dyads; each displaying very high accuracy. A total of 61 (including 20 new) and 60 (including 53 new) alleles were detected at DRB and DQB genes, respectively. Both loci were non-duplicated, in tight linkage disequilibrium and in Hardy-Weinberg equilibrium, despite the fact that sequence analysis revealed clear evidence of historical selection. Our results highlight the potential of 454 sequencing technology in attempts to investigate patterns of selection shaping MHC variation in contemporary populations. The power of this approach will nevertheless be conditional upon strict quality control of the genotyping data.
Reddy, Rachna B; Krupenye, Christopher; MacLean, Evan L; Hare, Brian
Among some haplorhine primates, including humans, relaxed yawns spread contagiously. Such contagious yawning has been linked to social bonds and empathy in some species. However, no studies have investigated contagious yawning in strepsirhines. We conducted an experimental study of contagious yawning in strepsirhines, testing ring-tailed and ruffed lemurs (n = 24) in a paradigm similar to one that has induced contagious yawning in haplorhines. First, in a control experiment, we investigated whether lemurs responded to projected video content in general (experiment 1). We showed them two videos to which we expected differential responses: one featured a terrestrial predator and the other a caretaker holding food. Next, to test for yawn contagion, we showed individual lemurs life-size video projections of groupmates and conspecific strangers yawning, and control footage of the same individuals at rest (experiment 2). Then, to examine whether a group context might enhance or allow for contagion, we exposed subjects to the same videos in a group setting (experiment 3). Lemurs produced alarm vocalizations and moved upward while viewing the predator, but not the caretaker, demonstrating that they do perceive video content meaningfully. However, lemurs did not yawn in response to yawning stimuli when tested alone, or with their groupmates. This study provides preliminary evidence that lemurs do not respond to yawning stimuli similarly to haplorhines, and suggests that this behavior may have evolved or become more exaggerated in haplorhines after the two major primate lineages split.
Chinnadurai, Sathya K; Balko, Julie A; Williams, Cathy V
The goal of this study was to determine the minimum alveolar concentration (MAC) and cardiopulmonary effects of isoflurane in ring-tailed lemurs (Lemur catta). The MAC of isoflurane was determined by using a tail-clamp stimulus in adult ring-tailed lemurs (6 male, 4 female). Once MAC was determined, another group of 10 adult ring-tailed lemurs (5 male, 5 female) were anesthetized and instrumented similarly as the previous group and maintained at 0.5, 1, 1.5, and 2 times MAC for 15 min each with no external stimulation. Five lemurs were exposed to increasing concentrations (that is, 0.5 times MAC increasing to 2 times MAC), and the other 5 animals were exposed to decreasing concentrations. MAC of isoflurane for ringtailed lemurs was 1.9%. The animals became hypotensive, but no significant differences were found in heart rate or systolic, mean, and diastolic blood pressures at the different multiples of MAC examined. At 1 MAC, all lemurs developed a moderate respiratory acidosis, which became more severe at 2 MAC. Given these findings, isoflurane at 0.5 to 2 times MAC in ringtailed lemurs does not result in predictable depression of blood pressure, but hypoventilation occurs at 1 MAC or greater.
Larsen, R Scott; Sauther, Michelle L; Cuozzo, Frank P
Wild ring-tailed lemurs (Lemur catta) can be anesthetized with Telazol via blow dart, but improved techniques are needed so that each lemur is reliably induced with a single dart. Medetomidine-butorphanol (MB) is a good supplemental protocol to be administered once the lemurs are captured, but other protocols may provide longer periods of sedation and immobility. One possible way of increasing the efficacy of each dart is to increase the time it is retained in the leg. In this investigation, a "double-sleeve" technique was used to try to increase the time of dart retention. This technique used a standard silicone sleeve on the needle, along with a second sleeve at the needle hub. Induction values were compared between lemurs darted with double-sleeve needles and those induced with needles that each had a single silicone sleeve. Once the lemurs were induced, supplementation with MB (0.04 mg/kg and 0.2 mg/kg) was compared with supplementation with ketamine-medetomidine (KM) (10 mg/ kg and 0.04 mg/kg). Twenty-three lemurs were darted with Telazol by using single-sleeve needles, and 24 were darted with double-sleeve needles. The number of darts per lemur and number of escapes were not different between animals darted with a single sleeve compared with a double-sleeve; thus, there were no significant improvements in induction success with the double-sleeve technique. Adequate sedation and muscle relaxation were achieved with both MB and KM; however, lemurs that received MB were more relaxed and needed fewer additional supplements that those that received KM. Single-sleeve dart needles are recommended for Telazol induction of ring-tailed lemurs via blow dart and MB is preferable to KM for supplemental sedation and muscle relaxation.
LaFleur, Marni; Clarke, Tara A; Reuter, Kim; Schaeffer, Toby
Lemurs are the most threatened group of mammals on earth. Lemur catta (ring-tailed lemur) represents one of the most iconic lemur species and faces numerous anthropogenic threats in the wild. In this study, we present population estimates from 32 sites across the range of L. catta, collected from primary and secondary data sources, to assess the number of ring-tailed lemurs left in the wild. We estimate that there are approximately 2,220 individual L. catta remaining in the 32 sites considered. We note local extinctions of populations of L. catta in at least 12 of the 32 sites examined, and that significantly more extinctions occurred in areas without some form of protection. This decrease in extant populations could represent a decrease of more than 95% of all ring-tailed lemurs in Madagascar since the year 2000. While these results should be considered preliminary, we stress the rapid decline of the species and note that habitat loss, bushmeat hunting and the illegal pet trade are driving populations to local extinction. Based on the data presented here, urgent and immediate funding and conservation action are crucial to ensure the viability of the remaining wild populations of ring-tailed lemurs.
Pifferi, Fabien; Dorieux, Olène; Castellano, Christian-Alexandre; Croteau, Etienne; Masson, Marie; Guillermier, Martine; Van Camp, Nadja; Guesnet, Philippe; Alessandri, Jean-Marc; Cunnane, Stephen; Dhenain, Marc; Aujard, Fabienne
Decreased brain content of DHA, the most abundant long-chain n-3 polyunsaturated fatty acid (n-3 LCPUFA) in the brain, is accompanied by severe neurosensorial impairments linked to impaired neurotransmission and impaired brain glucose utilization. In the present study, we hypothesized that increasing n-3 LCPUFA intake at an early age may help to prevent or correct the glucose hypometabolism observed during aging and age-related cognitive decline. The effects of 12 months’ supplementation with n-3 LCPUFA on brain glucose utilization assessed by positron emission tomography was tested in young adult mouse lemurs (Microcebus murinus). Cognitive function was tested in parallel in the same animals. Lemurs supplemented with n-3 LCPUFA had higher brain glucose uptake and cerebral metabolic rate of glucose compared with controls in all brain regions. The n-3 LCPUFA-supplemented animals also had higher exploratory activity in an open-field task and lower evidence of anxiety in the Barnes maze.jlr Our results demonstrate for the first time in a nonhuman primate that n-3 LCPUFA supplementation increases brain glucose uptake and metabolism and concomitantly reduces anxiety. PMID:26063461
Hogg, Russell T.; Godfrey, Laurie R.; Schwartz, Gary T.; Dirks, Wendy; Bromage, Timothy G.
Skeletal histology supports the hypothesis that primate life histories are regulated by a neuroendocrine rhythm, the Havers-Halberg Oscillation (HHO). Interestingly, subfossil lemurs are outliers in HHO scaling relationships that have been discovered for haplorhine primates and other mammals. We present new data to determine whether these species represent the general lemur or strepsirrhine condition and to inform models about neuroendocrine-mediated life history evolution. We gathered the largest sample to date of HHO data from histological sections of primate teeth (including the subfossil lemurs) to assess the relationship of these chronobiological measures with life history-related variables including body mass, brain size, age at first female reproduction, and activity level. For anthropoids, these variables show strong correlations with HHO conforming to predictions, though body mass and endocranial volume are strongly correlated with HHO periodicity in this group. However, lemurs (possibly excepting Daubentonia) do not follow this pattern and show markedly less variability in HHO periodicity and lower correlation coefficients and slopes. Moreover, body mass is uncorrelated, and brain size and activity levels are more strongly correlated with HHO periodicity in these animals. We argue that lemurs evolved this pattern due to selection for risk-averse life histories driven by the unpredictability of the environment in Madagascar. These results reinforce the idea that HHO influences life history evolution differently in response to specific ecological selection regimes. PMID:26267241
Hogg, Russell T; Godfrey, Laurie R; Schwartz, Gary T; Dirks, Wendy; Bromage, Timothy G
Skeletal histology supports the hypothesis that primate life histories are regulated by a neuroendocrine rhythm, the Havers-Halberg Oscillation (HHO). Interestingly, subfossil lemurs are outliers in HHO scaling relationships that have been discovered for haplorhine primates and other mammals. We present new data to determine whether these species represent the general lemur or strepsirrhine condition and to inform models about neuroendocrine-mediated life history evolution. We gathered the largest sample to date of HHO data from histological sections of primate teeth (including the subfossil lemurs) to assess the relationship of these chronobiological measures with life history-related variables including body mass, brain size, age at first female reproduction, and activity level. For anthropoids, these variables show strong correlations with HHO conforming to predictions, though body mass and endocranial volume are strongly correlated with HHO periodicity in this group. However, lemurs (possibly excepting Daubentonia) do not follow this pattern and show markedly less variability in HHO periodicity and lower correlation coefficients and slopes. Moreover, body mass is uncorrelated, and brain size and activity levels are more strongly correlated with HHO periodicity in these animals. We argue that lemurs evolved this pattern due to selection for risk-averse life histories driven by the unpredictability of the environment in Madagascar. These results reinforce the idea that HHO influences life history evolution differently in response to specific ecological selection regimes.
Morelli, Toni Lyn; Hayes, R. Andrew; Nahrung, Helen F.; Goodwin, Thomas E.; Harelimana, Innocent H.; MacDonald, Laura J.; Wright, Patricia C.
Lemurs are the most olfactory-oriented of primates, yet there is still only a basic level of understanding of what their scent marks communicate. We analyzed scent secretions from Milne-Edwards' sifakas ( Propithecus edwardsi) collected in their natural habitat of Ranomafana National Park, Madagascar. We sought to test whether the scent mark could signal genetic relatedness in addition to species, sex, season, and individuality. We not only found correlations ( r 2 = 0.38, P = 0.017) between the total olfactory fingerprint and genetic relatedness but also between relatedness and specific components of the odor, despite the complex environmental signals from differences in diet and behavior in a natural setting. To the best of our knowledge, this is the first demonstration of an association between genetic relatedness and chemical communication in a wild primate population. Furthermore, we found a variety of compounds that were specific to each sex and each sampling period. This research shows that scent marks could act as a remote signal to avoid inbreeding, optimize mating opportunities, and potentially aid kin selection.
Morelli, Toni Lyn; Hayes, R Andrew; Nahrung, Helen F; Goodwin, Thomas E; Harelimana, Innocent H; Macdonald, Laura J; Wright, Patricia C
Lemurs are the most olfactory-oriented of primates, yet there is still only a basic level of understanding of what their scent marks communicate. We analyzed scent secretions from Milne-Edwards' sifakas (Propithecus edwardsi) collected in their natural habitat of Ranomafana National Park, Madagascar. We sought to test whether the scent mark could signal genetic relatedness in addition to species, sex, season, and individuality. We not only found correlations (r (2) = 0.38, P = 0.017) between the total olfactory fingerprint and genetic relatedness but also between relatedness and specific components of the odor, despite the complex environmental signals from differences in diet and behavior in a natural setting. To the best of our knowledge, this is the first demonstration of an association between genetic relatedness and chemical communication in a wild primate population. Furthermore, we found a variety of compounds that were specific to each sex and each sampling period. This research shows that scent marks could act as a remote signal to avoid inbreeding, optimize mating opportunities, and potentially aid kin selection.
Weisrock, David W.; Smith, Stacey D.; Chan, Lauren M.; Biebouw, Karla; Kappeler, Peter M.; Yoder, Anne D.
The systematics and speciation literature is rich with discussion relating to the potential for gene tree/species tree discordance. Numerous mechanisms have been proposed to generate discordance, including differential selection, long-branch attraction, gene duplication, genetic introgression, and/or incomplete lineage sorting. For speciose clades in which divergence has occurred recently and rapidly, recovering the true species tree can be particularly problematic due to incomplete lineage sorting. Unfortunately, the availability of multilocus or “phylogenomic” data sets does not simply solve the problem, particularly when the data are analyzed with standard concatenation techniques. In our study, we conduct a phylogenetic study for a nearly complete species sample of the dwarf and mouse lemur clade, Cheirogaleidae. Mouse lemurs (genus, Microcebus) have been intensively studied over the past decade for reasons relating to their high level of cryptic species diversity, and although there has been emerging consensus regarding the evolutionary diversity contained within the genus, there is no agreement as to the inter-specific relationships within the group. We attempt to resolve cheirogaleid phylogeny, focusing especially on the mouse lemurs, by employing a large multilocus data set. We compare the results of Bayesian concordance methods with those of standard gene concatenation, finding that though concatenation yields the strongest results as measured by statistical support, these results are found to be highly misleading. By employing an approach where individual alleles are treated as operational taxonomic units, we show that phylogenetic results are substantially influenced by the selection of alleles in the concatenation process. PMID:22319174
Boedeker, Nancy C; Guzzetta, Philip; Rosenthal, Steven L; Padilla, Luis R; Murray, Suzan; Newman, Kurt
A 10-y-old ovariohysterectomized ring-tailed lemur (Lemur catta) was presented for exacerbation of respiratory signs. The lemur had a history of multiple examinations for various problems, including traumatic lacerations and recurrent perivulvar dermatitis. Examination revealed abnormal lung sounds and a femoral arteriovenous fistula with a palpable thrill and auscultable bruit in the right inguinal area. A diagnosis of congestive heart failure was made on the basis of exam findings, radiography, abdominal ultrasonography, and echocardiography. The lemur was maintained on furosemide until surgical ligation of the fistula was performed. Postoperative examination confirmed successful closure of the fistula and resolution of the signs of heart failure. Arteriovenous fistulas are abnormal connections between an artery and a vein that bypass the capillary bed. Large arteriovenous fistulas may result in decreased peripheral resistance and an increase in cardiac output with consequent cardiomegaly and high output heart failure. This lemur's high-flow arteriovenous fistula with secondary heart failure may have been iatrogenically induced during blood collection by prior femoral venipuncture. To our knowledge, this report is the first description of an arteriovenous fistula in a prosimian. Successful surgical correction of suspected iatrogenic femoral arteriovenous fistulas in a cynomolgus monkey (Macaca fascicularis) and a rhesus macaque (Macaca mulatta) have been reported previously. Arteriovenous fistula formation should be considered as a rare potential complication of venipuncture and as a treatable cause of congestive heart failure in lemurs. PMID:24672831
Boedeker, Nancy C; Guzzetta, Philip; Rosenthal, Steven L; Padilla, Luis R; Murray, Suzan; Newman, Kurt
A 10-y-old ovariohysterectomized ring-tailed lemur (Lemur catta) was presented for exacerbation of respiratory signs. The lemur had a history of multiple examinations for various problems, including traumatic lacerations and recurrent perivulvar dermatitis. Examination revealed abnormal lung sounds and a femoral arteriovenous fistula with a palpable thrill and auscultable bruit in the right inguinal area. A diagnosis of congestive heart failure was made on the basis of exam findings, radiography, abdominal ultrasonography, and echocardiography. The lemur was maintained on furosemide until surgical ligation of the fistula was performed. Postoperative examination confirmed successful closure of the fistula and resolution of the signs of heart failure. Arteriovenous fistulas are abnormal connections between an artery and a vein that bypass the capillary bed. Large arteriovenous fistulas may result in decreased peripheral resistance and an increase in cardiac output with consequent cardiomegaly and high output heart failure. This lemur's high-flow arteriovenous fistula with secondary heart failure may have been iatrogenically induced during blood collection by prior femoral venipuncture. To our knowledge, this report is the first description of an arteriovenous fistula in a prosimian. Successful surgical correction of suspected iatrogenic femoral arteriovenous fistulas in a cynomolgus monkey (Macaca fascicularis) and a rhesus macaque (Macaca mulatta) have been reported previously. Arteriovenous fistula formation should be considered as a rare potential complication of venipuncture and as a treatable cause of congestive heart failure in lemurs.
Larsen, R Scott; Moresco, Anneke; Sauther, Michelle L; Cuozzo, Frank P
Telazol has been commonly used for field anesthesia of wild lemurs, including ring-tailed lemurs (Lemur catta). Telazol alone provides good induction, but doesn't cause adequate muscle relaxation and sedation for collecting consistent somatic measurements and high-quality dental impressions that are sometimes needed. Variability in induction response has been seen between individuals that have received similar dosages, with young lemurs seeming to need more anesthetic than mature lemurs. This investigation evaluated Telazol induction in young (2.0-4.9 yr) and mature (> or = 5.0 yr) ring-tailed lemurs and compared postinduction supplementation with medetomidine or medetomidine-butorphanol. Forty-eight lemurs were anesthetized with Telazol administered via blow dart; then, 20 min after darting, they were supplemented via hand injection with either medetomidine (0.04 mg/ kg) or medetomidine-butorphanol (0.04 mg/kg and 0.2 mg/kg, respectively). The odds ratio for young lemurs to need more than one dart for induction, relative to mature lemurs, was 3.8, even though the initial dose of Telazol received by young lemurs (19 +/- 7 mg/kg) was significantly higher than the initial dose administered to mature lemurs (12 +/- 5 mg/kg). The total Telazol dosage was also significantly different between young lemurs (33 +/- 15 mg/kg) and mature lemurs (18 +/- 9 mg/kg). Both medetomidine and medetomidine-butorphanol provided good muscle relaxation and sedation for all procedures. Physiologic values were similar between the two protocols. Oxygen saturation by pulse oximetry was generally good, although there were a few SaO2 values < 90%. Recoveries were smooth, but long. Time to head up was correlated with total Telazol dosage in mature lemurs. In young lemurs, time to standing was correlated with Telazol induction dosage and time of last Telazol administration. Lemurs that received hand injections of Telazol took longer to recover than those that did not. Further refinements are
Bolt, Laura M
In mammals, purring has been described in mostly affiliative contexts. In the ring-tailed lemur (Lemur catta), both males and females purr, but only males were observed purring in agonistic contexts. In order to determine whether male ring-tailed lemurs purr as aggressive displays during intrasexual agonistic encounters, 480 h of focal data were collected on 25 adult males from Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. The male purring rate increased during periods of male-male agonism when compared to times without intrasexual agonism, and the purring rate was positively correlated with male dominance rank. However, the purring rate was not significantly higher during winning agonistic interactions when compared with losing encounters. My results indicate that the male ring-tailed lemur purr is used most frequently as an agonistic vocalization in male-male encounters, in addition to being used less frequently in other social contexts, including during tail-waving at females, resting, scent-marking, feeding and copulation. Dominant males have higher purring rates across social situations, suggesting that the purring rate may be driven by intrinsic male qualities rather than functioning as a meaningful signal in each disparate social context. Male purring in intrasexual agonistic encounters can be added to previously described social contexts for ring-tailed lemur purring.
Adult strepsirrhines have been completely neglected in the study of animal play. I focused on adult play fighting and the role of tail-play as a signal in ringtailed lemurs (Lemur catta). Tail-play is performed during play fighting, when lemurs anoint or, more rarely, wave their tails toward the playmate. During the prereproductive period, male and female lemurs engaged in play fighting with comparable frequencies, as was expected to occur in monomorphic species such as L. catta. The dyads showing low aggression rates engaged most frequently in play fighting, and polyadic play was frequently performed. Signals seem to be important in avoiding escalation to real aggression, especially when the playfulness of performers can be misunderstood by recipients. Tail-play was most frequent (a) in the dyads with low grooming rates (low familiarity degree) and (b) during the most risky play sessions (polyadic ones). Thus, tail-play can be considered as a useful tool for play communication in ringtailed lemurs. Copyright 2009 APA, all rights reserved.
Muller, S; Oevermann, A; Wenker, C; Altermatt, H J; Robert, N
Primary renal tumors are rare neoplasms in nonhuman primates. This report describes a mixed epithelial and stromal tumor of the kidney (MESTK) in a 14.5-year-old female ringtail lemur. The well-demarcated, solid, and cystic mass was located in the pelvis of the left kidney and consisted histologically of both epithelial and mesenchymal components. The mesenchymal cells were arranged in fascicles around cysts lined by a well-differentiated epithelium. Neither the mesenchymal nor the epithelial parts showed significant nuclear atypia or mitotic figures. To our knowledge, only 1 similar case, classified as adenoleiomyofibromatous hamartoma, has been reported in a ringtail lemur. In humans this tumor affects predominantly perimenopausal women and can express estrogen and progesterone receptors. However, neither estrogen nor progesterone receptors could be identified by immunohistochemistry in the tumor of the present ringtail lemur. Therefore, a hormonal mechanism could not be demonstrated in this case.
Luzón, Mónica; de la Fuente-López, Concepción; Martínez-Nevado, Eva; Fernández-Morán, Jesús; Ponce-Gordo, Francisco
Subcutaneous and intraperitoneal cysticercosis due to Taenia crassiceps was diagnosed in a 5-yr-old male ring-tailed lemur (Lemur catta) in the Madrid Zoo-Aquarium (Madrid, Spain). Under laparoscopic examination, several septated fibrous cystic structures and numerous masses of small transparent vesicles (ca. 3 mm in diameter) were observed subcutaneously and inside the peritoneal cavity. Most of the structures were extirpated but, after 2 days of postsurgical intensive care, the animal died. The loss of body weight of the animal after surgical extirpation (566 g) represented 22% of the total weight (body weight before mass removal, 2582 g). The vesicles were identified under light microscopic examination as cysticerci and by molecular diagnosis as Cysticercus longicollis, the larval form of T. crassiceps. The present report represents the first detection of T. crassiceps in the prosimian genus Lemur.
Clarke, Tara A; Gray, Olivia; Gould, Lisa; Burrell, Andrew S
Madagascar's lemurs, now deemed the most endangered group of mammals, represent the highest primate conservation priority in the world. Due to anthropogenic disturbances, an estimated 10% of Malagasy forest cover remains. The endangered Lemur catta is endemic to the southern regions of Madagascar and now occupies primarily fragmented forest habitats. We examined the influence of habitat fragmentation and isolation on the genetic diversity of L. catta across 3 different forest fragments in south-central Madagascar. Our analysis revealed moderate levels of genetic diversity. Genetic differentiation among the sites ranged from 0.05 to 0.11. These data suggest that the L. catta populations within south-central Madagascar have not yet lost significant genetic variation. However, due to ongoing anthropogenic threats faced by ring-tailed lemurs, continued conservation and research initiatives are imperative for long-term viability of the species.
Jones, Sarah M.; Pearson, John; DeWind, Nicholas K.; Paulsen, David; Tenekedjieva, Ana-Maria; Brannon, Elizabeth M.
We investigated the precision of the approximate number system (ANS) in three lemur species (Lemur catta, Eulemur mongoz, and Eulemur macaco flavifrons), one Old World monkey species (Macaca mulatta) and humans (Homo sapiens). In Experiment 1, four individuals of each nonhuman primate species were trained to select the numerically larger of two visual arrays on a touchscreen. We estimated numerical acuity by modeling Weber fractions (w) and found quantitatively equivalent performance among all four nonhuman primate species. In Experiment 2, we tested adult humans in a similar procedure, and they outperformed the four nonhuman species but showed qualitatively similar performance. These results indicate that the ANS is conserved over the primate order. PMID:24068469
Godfrey, Laurie R; Winchester, Julia M; King, Stephen J; Boyer, Doug M; Jernvall, Jukka
Understanding the paleoecology of extinct subfossil lemurs requires reconstruction of dietary preferences. Tooth morphology is strongly correlated with diet in living primates and is appropriate for inferring dietary ecology. Recently, dental topographic analysis has shown great promise in reconstructing diet from molar tooth form. Compared with traditionally used shearing metrics, dental topography is better suited for the extraordinary diversity of tooth form among subfossil lemurs and has been shown to be less sensitive to phylogenetic sources of shape variation. Specifically, we computed orientation patch counts rotated (OPCR) and Dirichlet normal energy (DNE) of molar teeth belonging to 14 species of subfossil lemurs and compared these values to those of an extant lemur sample. The two metrics succeeded in separating species in a manner that provides insights into both food processing and diet. We used them to examine the changes in lemur community ecology in Southern and Southwestern Madagascar that accompanied the extinction of giant lemurs. We show that the poverty of Madagascar's frugivore community is a long-standing phenomenon and that extinction of large-bodied lemurs in the South and Southwest resulted not merely in a loss of guild elements but also, most likely, in changes in the ecology of extant lemurs. Copyright © 2012 Wiley Periodicals, Inc.
Ballhorn, Daniel J; Rakotoarivelo, Fanny Patrika; Kautz, Stefanie
Feeding strategies of specialist herbivores often originate from the coevolutionary arms race of plant defenses and counter-adaptations of herbivores. The interaction between bamboo lemurs and cyanogenic bamboos on Madagascar represents a unique system to study diffuse coevolutionary processes between mammalian herbivores and plant defenses. Bamboo lemurs have different degrees of dietary specialization while bamboos show different levels of chemical defense. In this study, we found variation in cyanogenic potential (HCNp) and nutritive characteristics among five sympatric bamboo species in the Ranomafana area, southeastern Madagascar. The HCNp ranged from 209±72 μmol cyanide*g-1 dwt in Cathariostachys madagascariensis to no cyanide in Bambusa madagascariensis. Among three sympatric bamboo lemur species, the greater bamboo lemur (Prolemur simus) has the narrowest food range as it almost exclusively feeds on the highly cyanogenic C. madagascariensis. Our data suggest that high HCNp is the derived state in bamboos. The ancestral state of lemurs is most likely "generalist" while the ancestral state of bamboo lemurs was determined as equivocal. Nevertheless, as recent bamboo lemurs comprise several "facultative specialists" and only one "obligate specialist" adaptive radiation due to increased flexibility is likely. We propose that escaping a strict food plant specialization enabled facultative specialist bamboo lemurs to inhabit diverse geographical areas.
Ballhorn, Daniel J.; Rakotoarivelo, Fanny Patrika; Kautz, Stefanie
Feeding strategies of specialist herbivores often originate from the coevolutionary arms race of plant defenses and counter-adaptations of herbivores. The interaction between bamboo lemurs and cyanogenic bamboos on Madagascar represents a unique system to study diffuse coevolutionary processes between mammalian herbivores and plant defenses. Bamboo lemurs have different degrees of dietary specialization while bamboos show different levels of chemical defense. In this study, we found variation in cyanogenic potential (HCNp) and nutritive characteristics among five sympatric bamboo species in the Ranomafana area, southeastern Madagascar. The HCNp ranged from 209±72 μmol cyanide*g-1 dwt in Cathariostachys madagascariensis to no cyanide in Bambusa madagascariensis. Among three sympatric bamboo lemur species, the greater bamboo lemur (Prolemur simus) has the narrowest food range as it almost exclusively feeds on the highly cyanogenic C. madagascariensis. Our data suggest that high HCNp is the derived state in bamboos. The ancestral state of lemurs is most likely "generalist" while the ancestral state of bamboo lemurs was determined as equivocal. Nevertheless, as recent bamboo lemurs comprise several "facultative specialists" and only one "obligate specialist" adaptive radiation due to increased flexibility is likely. We propose that escaping a strict food plant specialization enabled facultative specialist bamboo lemurs to inhabit diverse geographical areas. PMID:27532127
Lim, Efrem S.; Deem, Sharon L.; Porton, Ingrid J.; Cao, Song
ABSTRACT The roles of host genetics versus exposure and contact frequency in driving cross-species transmission remain the subject of debate. Here, we used a multitaxon lemur collection at the Saint Louis Zoo in the United States as a model to gain insight into viral transmission in a setting of high interspecies contact. Lemurs are a diverse and understudied group of primates that are highly endangered. The speciation of lemurs, which are endemic to the island of Madagascar, occurred in geographic isolation apart from that of continental African primates. Although evidence of endogenized viruses in lemur genomes exists, no exogenous viruses of lemurs have been described to date. Here we identified two novel picornaviruses in fecal specimens of ring-tailed lemurs (Lemur catta) and black-and-white ruffed lemurs (Varecia variegata). We found that the viruses were transmitted in a species-specific manner (lesavirus 1 was detected only in ring-tailed lemurs, while lesavirus 2 was detected only in black-and-white ruffed lemurs). Longitudinal sampling over a 1-year interval demonstrated ongoing infection in the collection. This was supported by evidence of viral clearance in some animals and new infections in previously uninfected animals, including a set of newly born triplets that acquired the infection. While the two virus strains were found to be cocirculating in a mixed-species exhibit of ring-tailed lemurs, black-and-white ruffed lemurs, and black lemurs, there was no evidence of cross-species transmission. This suggests that despite high-intensity contact, host species barriers can prevent cross-species transmissions of these viruses. IMPORTANCE Up to 75% of emerging infectious diseases in humans today are the result of zoonotic transmission. However, a challenge in understanding transmission dynamics has been the limited models of cross-species transmission. Zoos provide a unique opportunity to explore parameters defining viral transmission. We demonstrated that
Rosati, Alexandra G; Rodriguez, Kerri; Hare, Brian
Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel's sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks-especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.
Tuten, Holly C; Miller, Heather C; Ellis, Angela E
In September 2008, two ring-tailed lemurs (Lemur catta), comprising a mother-daughter pair, at the Greenville Zoo, Greenville, South Carolina, USA, were diagnosed with cuterebrid myiasis (Diptera: Oestridae) subsequent to sudden death of the adult lemur. On necropsy, a single bot warble was discovered in the subcutis of the axillary region. Histopathology revealed a severe eosinophilic bronchopneumonia. The juvenile lemur was inspected and found to have warbles on three separate dates in late September. One representative bot fly larva was identified as a Cuterebra sp. that normally infests lagomorphs in the southeastern United States. Cuterebrid myiasis is rarely reported in lemurs and has not been previously associated with pneumonia or death in these animals.
Makungu, Modesta; du Plessis, Wencke M; Barrows, Michelle; Groenewald, Hermanus B; Koeppel, Katja N
The ring-tailed lemur (Lemur catta) is a quadruped arboreal primate primarily distributed in south and south-western Madagascar. This study was carried out to describe the normal radiographic thoracic anatomy of the ring-tailed lemur as a reference for clinical use. Radiography of the thorax was performed in 15 captive ring-tailed lemurs during their annual health examinations. Normal radiographic reference ranges for thoracic structures were established and ratios were calculated, such as the vertebral heart score (VHS). The mean VHS on the right lateral and dorsoventral views was 8.92 ± 0.47 and 9.42 ± 0.52, respectively. Differences exist in the normal radiographic thoracic anatomy of primates. Knowledge of the normal radiographic thoracic anatomy of individual species is important and fundamental to assist in clinical cases and for accurate diagnosis of diseases. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Shepherd, Stephen V; Platt, Michael L
Both human and nonhuman primates preferentially orient toward other individuals and follow gaze in controlled environments. Precisely where any animal looks during natural behavior, however, remains unknown. We used a novel telemetric gaze-tracking system to record orienting behavior of ringtailed lemurs (Lemur catta) interacting with a naturalistic environment. We here provide the first evidence that ringtailed lemurs, group-living prosimian primates, preferentially gaze towards other individuals and, moreover, follow other lemurs' gaze while freely moving and interacting in naturalistic social and ecological environments. Our results support the hypothesis that stem primates were capable of orienting toward and following the attention of other individuals. Such abilities may have enabled the evolution of more complex social behavior and cognition, including theory of mind and language, which require spontaneous attention sharing. This is the first study to use telemetric eye-tracking to quantitatively monitor gaze in any nonhuman animal during locomotion, feeding, and social interaction. Moreover, this is the first demonstration of gaze following by a prosimian primate and the first to report gaze following during spontaneous interaction in naturalistic social environments.
Toh, Hidehiro; Matsubara, Takehiro; Tomida, Shuta; Mimura, Iyo; Arakawa, Kensuke; Kikusui, Takefumi
ABSTRACT Bifidobacterium lemurum DSM 28807T was isolated from the gastrointestinal tracts of ring-tailed lemurs (Lemur catta). Here, we report the first draft genome sequence of this organism. PMID:28232445
Toh, Hidehiro; Matsubara, Takehiro; Tomida, Shuta; Mimura, Iyo; Arakawa, Kensuke; Kikusui, Takefumi; Morita, Hidetoshi
Bifidobacterium lemurum DSM 28807(T) was isolated from the gastrointestinal tracts of ring-tailed lemurs (Lemur catta). Here, we report the first draft genome sequence of this organism. Copyright © 2017 Toh et al.
Makungu, Modesta; du Plessis, Wencke M; Barrows, Michelle; Groenewald, Hermanus B; Koeppel, Katja N
The ring-tailed lemur (Lemur catta) is primarily distributed in south and southwestern Madagascar. It is classified as an endangered species by the International Union for Conservation of Nature. Various abdominal diseases, such as hepatic lipidosis, intestinal ulcers, cystitis, urinary tract obstruction, and neoplasia (e.g., colonic adenocarcinoma and cholangiocarcinoma), have been reported in this species. The aim of this study was to describe the normal radiographic and ultrasonographic abdominal anatomy in captive ring-tailed lemurs to provide guidance for clinical use. Radiography of the abdomen and ultrasonography of the liver, spleen, kidneys, and urinary bladder were performed in 13 and 9 healthy captive ring-tailed lemurs, respectively, during their annual health examinations. Normal radiographic and ultrasonographic reference ranges for abdominal organs were established and ratios were calculated. The majority (12/13) of animals had seven lumbar vertebrae. The sacrum had mainly (12/13) three segments. Abdominal serosal detail was excellent in all animals, and hypaxial muscles were conspicuous in the majority (11/13) of animals. The spleen was frequently (12/13) seen on the ventrodorsal (VD) view and rarely (3/13) on the right lateral (RL) view. The liver was less prominent and well contained within the ribcage. The pylorus was mostly (11/13) located to the right of the midline. The right and left kidneys were visible on the RL and VD views, with the right kidney positioned more cranial and dorsal to the left kidney. On ultrasonography, the kidneys appeared ovoid on transverse and longitudinal views. The medulla was hypoechoic to the renal cortex. The renal cortex was frequently (8/9) isoechoic and rarely (1/9) hyperechoic to the splenic parenchyma. The liver parenchyma was hypoechoic (5/5) to the renal cortex. Knowledge of the normal radiographic and ultrasonographic abdominal anatomy of ring-tailed lemurs may be useful in the diagnosis of diseases and in
Anderson, Kadie M; Wolf, Karen N
A 16-year-old vasectomized male ring-tailed lemur (Lemur catta) with a history of suspected chronic renal failure was evaluated because of extreme lethargy, hyperpnea, and abscess of the right pectoral scent gland. Examination of the anesthetized patient revealed an impacted right pectoral scent gland with serosanguineous exudate. A CBC and serum biochemical analysis revealed severe anemia, marked azotemia, hyperphosphatemia, and hypocalcemia. Supportive care (including fluid therapy and phosphorus binder administration) was initiated for renal failure; the affected gland was cleaned, and antimicrobials were administered. The patient received 1 blood transfusion, and darbepoetin alfa was administered weekly to stimulate RBC production. Anemia and azotemia persisted. Three months after treatment started, serum iron analysis revealed that iron deficiency was the probable cause for the lack of a consistent regenerative response to darbepoetin injections. Iron dextran injections resulted in a marked regenerative response; however, serum biochemical analysis results after the second injection were consistent with hepatic injury. Hepatic enzyme activities normalized following discontinuation of iron dextran treatment, but the lemur's Hct declined rapidly despite supplementary iron administration PO. The patient developed severe mandibular osteomyelitis and was euthanized because of poor prognosis. Postmortem evaluation of hepatic iron concentration confirmed iron deficiency. The family Lemuridae is considered prone to hemosiderosis and hemochromatosis, which delayed rapid diagnosis and treatment of the lemur's disease. Apparent hepatic injury following iron dextran injections further complicated treatment. Findings for this lemur support the use of species-specific total iron binding capacity and total serum iron and ferritin concentrations in evaluation of an animal with suspected iron deficiency.
Drea, Christine M; Weil, Anne
The extravagance and diversity of external genitalia have been well characterized in male primates; however, much less is known about sex differences or variation in female form. Our study represents a departure from traditional investigations of primate reproductive anatomy because we 1) focus on external rather than internal genitalia, 2) measure both male and female structures, and 3) examine a strepsirrhine rather than an anthropoid primate. The subjects for morphological study were 21 reproductively intact, adult ring-tailed lemurs (Lemur catta), including 10 females and 11 males, two of which (one per sex) subsequently died of natural causes and also served as specimens for gross anatomical dissection. Male external genitalia presented a typical masculine configuration, with a complex distal penile morphology. In contrast, females were unusual among mammals, presenting an enlarged, pendulous external clitoris, tunneled by the urethra. Females had a shorter anogenital distance and a larger urethral meatus than did males, but organ diameter and circumference showed no sex differences. Dissection confirmed these characterizations. Noteworthy in the male were the presence of a "levator penis" muscle and discontinuity in the corpus spongiosum along the penile shaft; noteworthy in the female were an elongated clitoral shaft and glans clitoridis. The female urethra, while incorporated within the clitoral body, was not surrounded by erectile tissue, as we detected no corpus spongiosum. The os clitoridis was 43% the length and 24% the height of the os penis. On the basis of these first detailed descriptions of strepsirrhine external genitalia (for either sex), we characterize those of the female ring-tailed lemur as moderately "masculinized." Our results highlight certain morphological similarities and differences between ring-tailed lemurs and the most male-like of female mammals, the spotted hyena (Crocuta crocuta), and call attention to a potential hormonal
Słodkowicz-Kowalska, Anna; Majewska, Anna C; Trzesowska, Ewa; Skrzypczak, Łukasz
Encephalitozoon intestinalis is one of the most common microsporidial species found in humans worldwide but it has rarely been identified in animals. The presence of this pathogen has been detected in a few species of domestic, captive and wild mammals as well as in three species of birds. The aim of the present study was to examine fecal samples obtained from mammals housed in the Poznan Zoological Garden, Poland, for the presence of potentially human-infectious microsporidia. A total of 339 fresh fecal samples collected from 75 species of mammals belonging to 27 families and 8 orders were examined for the presence of microsporidian spores. Microsporidian spores were identified in 3 out of 339 (0.9%) examined fecal samples. All samples identified as positive by chromotrope 2R and calcofluor white M2R were also positive by the FISH assay. Using multiplex FISH in all 3 fecal samples, only spores of E. intestinalis were identified in 2 out of 14 Ring-tailed lemurs (Lemur catta) and in one out of 17 Red ruffed lemurs (Varecia variegata rubra). To our knowledge this is the first diagnosis of E. intestinalis in Ring-tailed and Red ruffed lemurs. It should be mentioned that both lemur species are listed by the IUCN Red List of Threatened Species. Although the lemurs were asymptomatically infected, the possibility of widespread infection or death of these animals remains in the event of an elevated stress or a decrease in their immunological functions.
Jacobs, Rachel L; MacFie, Tammie S; Spriggs, Amanda N; Baden, Andrea L; Morelli, Toni Lyn; Irwin, Mitchell T; Lawler, Richard R; Pastorini, Jennifer; Mayor, Mireya; Lei, Runhua; Culligan, Ryan; Hawkins, Melissa T R; Kappeler, Peter M; Wright, Patricia C; Louis, Edward E; Mundy, Nicholas I; Bradley, Brenda J
Some primate populations include both trichromatic and dichromatic (red-green colour blind) individuals due to allelic variation at the X-linked opsin locus. This polymorphic trichromacy is well described in day-active New World monkeys. Less is known about colour vision in Malagasy lemurs, but, unlike New World monkeys, only some day-active lemurs are polymorphic, while others are dichromatic. The evolutionary pressures underlying these differences in lemurs are unknown, but aspects of species ecology, including variation in activity pattern, are hypothesized to play a role. Limited data on X-linked opsin variation in lemurs make such hypotheses difficult to evaluate. We provide the first detailed examination of X-linked opsin variation across a lemur clade (Indriidae). We sequenced the X-linked opsin in the most strictly diurnal and largest extant lemur, Indri indri, and nine species of smaller, generally diurnal indriids (Propithecus). Although nocturnal Avahi (sister taxon to Propithecus) lacks a polymorphism, at least eight species of diurnal indriids have two or more X-linked opsin alleles. Four rainforest-living taxa-I. indri and the three largest Propithecus species-have alleles not previously documented in lemurs. Moreover, we identified at least three opsin alleles in Indri with peak spectral sensitivities similar to some New World monkeys. © 2017 The Author(s).
Lemurs, the diverse, endemic primates of Madagascar, are thought to represent a classic example of adaptive radiation. Based on the most complete phylogeny of living and extinct lemurs yet assembled, I tested predictions of adaptive radiation theory by estimating rates of speciation, extinction and adaptive phenotypic evolution. As predicted, lemur speciation rate exceeded that of their sister clade by nearly twofold, indicating the diversification dynamics of lemurs and mainland relatives may have been decoupled. Lemur diversification rates did not decline over time, however, as predicted by adaptive radiation theory. Optimal body masses diverged among dietary and activity pattern niches as lineages diversified into unique multidimensional ecospace. Based on these results, lemurs only partially fulfil the predictions of adaptive radiation theory, with phenotypic evolution corresponding to an ‘early burst’ of adaptive differentiation. The results must be interpreted with caution, however, because over the long evolutionary history of lemurs (approx. 50 million years), the ‘early burst’ signal of adaptive radiation may have been eroded by extinction. PMID:28280597
Kulahci, Ipek G.; Drea, Christine M.; Rubenstein, Daniel I.; Ghazanfar, Asif A.
Individual recognition can be facilitated by creating representations of familiar individuals, whereby information from signals in multiple sensory modalities become linked. Many vertebrate species use auditory–visual matching to recognize familiar conspecifics and heterospecifics, but we currently do not know whether representations of familiar individuals incorporate information from other modalities. Ring-tailed lemurs (Lemur catta) are highly visual, but also communicate via scents and vocalizations. To investigate the role of olfactory signals in multisensory recognition, we tested whether lemurs can recognize familiar individuals through matching scents and vocalizations. We presented lemurs with female scents that were paired with the contact call either of the female whose scent was presented or of another familiar female from the same social group. When the scent and the vocalization came from the same individual versus from different individuals, females showed greater interest in the scents, and males showed greater interest in both the scents and the vocalizations, suggesting that lemurs can recognize familiar females via olfactory–auditory matching. Because identity signals in lemur scents and vocalizations are produced by different effectors and often encountered at different times (uncoupled in space and time), this matching suggests lemurs form multisensory representations through a newly recognized sensory integration underlying individual recognition. PMID:24741013
BUBLITZ, DEANNA C.; WRIGHT, PATRICIA C.; RASAMBAINARIVO, FIDISOA T.; ARRIGO-NELSON, SUMMER J.; BODAGER, JONATHAN R.; GILLESPIE, THOMAS R.
As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitat, greater human-primate contact is inevitable, making higher rates of pathogen transmission likely. Anthropogenic effects are particularly evident in Madagascar, where a diversity of endemic lemur species are threatened by rapid habitat loss. Despite these risks, knowledge of how anthropogenic activities affect lemur exposure to pathogens is limited. To improve our understanding of this interplay, we non-invasively examined six species of wild lemurs in Ranomafana National Park for enteric bacterial pathogens commonly associated with diarrheal disease in human populations in Madagascar. Patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica and pseudotuberculosis) were compared between lemurs inhabiting intact forest and lemurs inhabiting degraded habitat with frequent exposure to tourism and other human activity. Fecal samples acquired from humans, livestock, and rodents living near the degraded habitat were also screened for these bacteria. Remarkably, only lemurs living in disturbed areas of the park tested positive for these pathogens. Moreover, all of these pathogens were present in the human, livestock, and/or rodent populations. These data suggest that lemurs residing in forests altered or frequented by people, livestock, or peridomestic rodents, are at risk for infection by these diarrhea-causing enterobacteria and other similarly transmitted pathogens. PMID:25328106
Herrera, James P
Lemurs, the diverse, endemic primates of Madagascar, are thought to represent a classic example of adaptive radiation. Based on the most complete phylogeny of living and extinct lemurs yet assembled, I tested predictions of adaptive radiation theory by estimating rates of speciation, extinction and adaptive phenotypic evolution. As predicted, lemur speciation rate exceeded that of their sister clade by nearly twofold, indicating the diversification dynamics of lemurs and mainland relatives may have been decoupled. Lemur diversification rates did not decline over time, however, as predicted by adaptive radiation theory. Optimal body masses diverged among dietary and activity pattern niches as lineages diversified into unique multidimensional ecospace. Based on these results, lemurs only partially fulfil the predictions of adaptive radiation theory, with phenotypic evolution corresponding to an 'early burst' of adaptive differentiation. The results must be interpreted with caution, however, because over the long evolutionary history of lemurs (approx. 50 million years), the 'early burst' signal of adaptive radiation may have been eroded by extinction.
Berta, Ágnes I; Kiss, Anna L; Lukáts, Ákos; Szabó, Arnold
The distribution of caveolin isoforms was previously evaluated in the retinas of different species, but has not yet been described in the primate retina. In this study, the distribution of caveolins was assessed via immunochemistry using isoform-specific antibodies in the retina of the black-and-white ruffed lemur. Here, we report the presence of a variety of caveolin isoforms in many layers of the lemur retina. As normal human retinas were not available for research and the retinas of primates are fairly similar to those of humans, the lemur retina can be utilized as a model for caveolin distribution in normal humans. PMID:17679778
Berta, Agnes I; Kiss, Anna L; Lukáts, Akos; Szabó, Arnold; Szél, Agoston
The distribution of caveolin isoforms was previously evaluated in the retinas of different species, but has not yet been described in the primate retina. In this study, the distribution of caveolins was assessed via immunochemistry using isoform-specific antibodies in the retina of the black-and-white ruffed lemur. Here, we report the presence of a variety of caveolin isoforms in many layers of the lemur retina. As normal human retinas were not available for research and the retinas of primates are fairly similar to those of humans, the lemur retina can be utilized as a model for caveolin distribution in normal humans.
Juan-Sallés, Carles; Mainez, Mireia; Marco, Alberto; Sanchís, Ana M Malabia
Localized, myocardial toxoplasmosis contributed to the death of a female ring-tailed lemur (Lemur catta) 1 week after the delivery of 4 stillborn offspring with disseminated toxoplasmosis; the diagnosis was obtained by histopathology and immunohistochemistry in all 5 lemurs. Varying degrees of placentitis and placental edema with intralesional Toxoplasma gondii immunolabeling were observed in the 3 available placentas. The dam had severe myocarditis, and T. gondii antigen was only detected in the myocardial lesions. Disseminated toxoplasmosis with mild encephalitis was noted in all 4 fetuses, and 2 of the fetuses had mild acute multifocal hepatic necrosis. Fetal death was attributed to placental insufficiency with subsequent hypoxia and amniotic fluid aspiration.
Smith, Timothy D; Muchlinski, Magdalena N; Bhatnagar, Kunwar P; Durham, Emily L; Bonar, Christopher J; Burrows, Anne M
The vomeronasal organ (VNO), also known as the Jacobson's organ, is a bilateral chemosensory organ found at the base of the nasal cavity specialized for the detection of higher-molecular weight (non-volatile) chemostimuli. It has been linked to pheromone detection. The VNO has been well studied in nocturnal lemurs and lorises, but poorly studied in diurnal/cathemeral species despite the large repertoire of olfactory behaviors noted in species such as Lemur catta. Here, the VNO and associated structures were studied microanatomically in one adult female and one adult male L. catta. Traditional and immunohistochemical procedures demonstrate the VNO epithelium consists of multiple rows of sensory neurons. Immunoreactivity to Growth-associated protein 43 (GAP43) indicates the VNO is postnatally neurogenic. In volume, the VNO neuroepithelium scales similarly to palatal length compared to nocturnal strepsirrhines. Numerous taste buds present at the oral opening to the nasopalatine duct, with which the VNO communicates, provide an additional (or alternative) explanation for the flehmen behavior that has been observed in this species. The VNO of L. catta is shown to be microanatomically comparable to that of nocturnal strepsirrhines. Like nocturnal strepsirrhines, the VNO of L. catta may be functional in the reception of high-molecular weight secretions.
Ethan Pride, R
Glucocorticoid levels are commonly used as measures of stress in wild animal populations, but their relevance to individual fitness in a wild population has not been demonstrated. In this study I followed 93 ring-tailed lemurs (Lemur catta) at Berenty Reserve in Madagascar, collecting 1089 faecal samples from individually recognized animals, and recording their survival over a 2 year period. I evaluated faecal glucocorticoid levels as predictors of individual survival to the end of the study. Animals with high glucocorticoid levels had a significantly higher mortality rate. This result suggests that glucocorticoid measures can be useful predictors of individual survival probabilities in wild populations. The ‘stress landscape’ indicated by glucocorticoid patterns may approximate the fitness landscape to which animals adapt. PMID:17148128
St Clair, John; Campbell-Palmer, Roisin; Lathe, Richard
Monozygotic (MZ) twinning is generally considered to be rare in species other than human. We inspected sex ratios in European zoo-bred ring-tailed lemurs (Lemur catta), revealing a significant excess of same-sex twins. Of 94 pairs, 60 (64%) were either both males or both females (p = .004). Application of the Weinberg differential rule argues that 27% of all twins in this species are MZ pairs. In this protected species, where twinning is commonplace (~50% of newborns are twins), the probable existence of frequent MZ twinning has ramifications for breeding programs aimed to maximize genetic diversity, and suggests that twin studies in a species other than human could have potential as a medical research tool.
Wright, P C
The last decade's lemur research includes successes in discovering new living and extinct species and learning about the distribution, biogeography, physiology, behavior, and ecology of previously little-studied species. In addition, in both the dry forest and rain forest, long-term studies of lemur demography, life history, and reproduction, have been completed in conjunction with data on tree productivity, phenology, and climate. Lemurs contrast with anthropoids in several behavioral features, including female dominance, targeted female-female aggression, lack of sexual dimorphism regardless of mating system, sperm competition coupled with male-male aggression, high infant mortality, cathemerality, and strict seasonal breeding. Hypotheses to explain these traits include the "energy conservation hypothesis" (ECH) suggesting that harsh and unpredictable climate factors on the island of Madagascar have affected the evolution of female dominance, and the "evolutionary disequilibrium hypotheses" (EVDH) suggesting that the recent megafauna extinctions have influenced lemurs to become diurnal. These hypotheses are compared and contrasted in light of recent empirical data on climate, subfossils, and lemur behavior. New data on life histories of the rain forest lemurs at Ranomafana National Park give further support to the ECH. Birth seasons are synchronized within each species, but there is a 6-month distribution of births among species. Gestation and lactation lengths vary among sympatric lemurs, but all lemur species in the rain forest wean in synchrony at the season most likely to have abundant resources. Across-species weaning synchrony seen in Ranomafana corroborates data from the dry forest that late lactation and weaning is the life history event that is the primary focus of the annual schedule. Lemur adaptations may assure maximum offspring survival in this environment with an unpredictable food supply and heavy predation. In conclusion, a more comprehensive
Giroud, Sylvain; Perret, Martine; Stein, Peter; Goudable, Joëlle; Aujard, Fabienne; Gilbert, Caroline; Robin, Jean Patrice; Le Maho, Yvon; Zahariev, Alexandre; Blanc, Stéphane; Momken, Iman
During moderate calorie restriction (CR) the heterotherm Microcebus murinus is able to maintain a stable energy balance whatever the season, even if only wintering animals enter into torpor. To understand its energy saving strategies to respond to food shortages, we assessed protein and energy metabolisms associated with wintering torpor expression or summering torpor avoidance. We investigated body composition, whole body protein turnover, and daily energy expenditure (DEE), during a graded (40 and 80%) 35-day CR in short-days (winter; SD40 and SD80, respectively) and long-days (summer; LD40 and LD80, respectively) acclimated animals. LD40 animals showed no change in fat mass (FM) but a 12% fat free mass (FFM) reduction. Protein balance being positive after CR, the FFM loss was early and rapid. The 25% DEE reduction, in LD40 group was mainly explained by FFM changes. LD80 animals showed a steady body mass loss and were excluded from the CR trial at day 22, reaching a survival-threatened body mass. No data were available for this group. SD40 animals significantly decreased their FM level by 21%, but maintained FFM. Protein sparing was achieved through a 35 and 39% decrease in protein synthesis and catabolism (protein turnover), respectively, overall maintaining nitrogen balance. The 21% reduction in energy requirement was explained by the 30% nitrogen flux drop but also by torpor as DEE FFM-adjusted remained 13% lower compared to ad-libitum. SD80 animals were unable to maintain energy and nitrogen balances, losing both FM and FFM. Thus summering mouse lemurs equilibrate energy balance by a rapid loss of active metabolic mass without using torpor, whereas wintering animals spare protein and energy through increased torpor expression. Both strategies have direct fitness implication: 1) to maintain activities at a lower body size during the mating season and 2) to preserve an optimal wintering muscle mass and function.
Crawford, Graham; Puschner, Birgit; Affolter, Verena; Stalis, Ilse; Davidson, Autumn; Baker, Tomas; Tahara, John; Jolly, Alison; Ostapak, Susan
Leucaena (Leucaena leucocephala) is a leguminous tree that is nutritious forage for domestic livestock when ingested in limited amounts. Unfortunately, leucaena contains mimosine, a plant amino acid, that can be toxic when ingested at higher concentrations. Reported toxic effects include alopecia (fur loss), poor body condition, infertility, low birth weight, thyroid gland dysfunction, and organ toxicity. Originally native to Mexico and Central America, leucaena has been introduced throughout the tropics, including Berenty Reserve, Madagascar where it was planted as supplemental browse for livestock. In Berenty, a seasonal syndrome of alopecia in ringtailed lemurs (Lemur catta) is associated with eating leucaena. Although much is known about the toxic effects of leucaena and mimosine on domestic animals and humans, the systemic effects on wildlife had not been studied. In a comparison of lemurs that include leucaena in their diet and those that do not, we found that animals that ingest leucaena absorb mimosine but that ingestion does not affect body condition, cause kidney or liver toxicity, or affect the intestinal tract. Alopecia is due to mimosine's interference of the hair follicle cycle. Leucaena ingestion is associated with higher serum albumin, α-tocopherol, and thyroxine concentrations, suggesting that leucaena may provide some nutritional benefit and that lemurs can detoxify and convert mimosine to a thyroid stimulating metabolite. The primary conservation consequence of leucaena ingestion at Berenty may be increased infant mortality due to the infants' inability cling to their alopecic mothers. The widespread introduction of leucaena throughout the tropics and its rapid spread in secondary forest conditions mean that many other leaf-eating mammals may be including this tree in their diet. Thus, exposure to leucaena should be considered when wildlife health is being evaluated, and the potential effects on wildlife health should be considered when
Parga, Joyce A; Sauther, Michelle L; Cuozzo, Frank P; Jacky, Ibrahim Antho Youssouf; Lawler, Richard R
In light of historical and recent anthropogenic influences on Malagasy primate populations, in this study ring-tailed lemur (Lemur catta) samples from two sites in southwestern Madagascar, Beza Mahafaly Special Reserve (BMSR) and Tsimanampetsotsa National Park (TNP), were evaluated for the genetic signature of a population bottleneck. A total of 45 individuals (20 from BMSR and 25 from TNP) were genotyped at seven microsatellite loci. Three methods were used to evaluate these populations for evidence of a historical bottleneck: M-ratio, mode-shift, and heterozygosity excess tests. Three mutation models were used for heterozygosity excess tests: the stepwise mutation model (SMM), two-phase model (TPM), and infinite allele model (IAM). M-ratio estimations indicated a potential bottleneck in both populations under some conditions. Although mode-shift tests did not strongly indicate a population bottleneck in the recent historical past when samples from all individuals were included, a female-only analysis indicated a potential bottleneck in TNP. Heterozygosity excess was indicated under two of the three mutation models (IAM and TPM), with TNP showing stronger evidence of heterozygosity excess than BMSR. Taken together, these results suggest that a bottleneck may have occurred among L. catta in southwestern Madagascar in the recent past. Given knowledge of how current major stochastic climatic events and human-induced change can negatively impact extant lemur populations, it is reasonable that comparable events in the historical past could have caused a population bottleneck. This evaluation additionally functions to highlight the continuing environmental and anthropogenic challenges faced by lemurs in southwestern Madagascar.
Suárez-Bonnet, A; Grau-Bassas, E Rodríguez; Herráez, P; Quesada-Canales, O; Priestnall, S L; de Los Monteros, A Espinosa
Naturally occurring mammary tumours are uncommon in prosimians. A 20-year-old female ring-tailed lemur (Lemur catta) developed bilateral enlargement of the mammary glands. Surgical removal revealed that both masses were comprised of multiple nodules and cystic areas that entirely replaced the normal glands. Histologically, a benign neoplastic biphasic cellular proliferation, composed of luminal-epithelial and basal-myoepithelial components, was identified. Immunohistochemical analysis for expression of cytokeratin (CK) AE1/AE3, CK7, CK5 + 8, CK14, vimentin, p63 and 14-3-3σ highlighted the biphasic nature of the neoplasm. A low mitotic count, low Ki67 labelling index, expression of oestrogen receptor-α, lack of expression of human epidermal growth factor receptor and a 3-year disease-free period without recurrence supported the benign nature of the tumour. Macroscopically, histologically and immunohistochemically this neoplasm resembled benign adenomyoepithelioma of the breast in women. This is the first complete report of a naturally occurring mammary tumour in a ring-tailed lemur. Copyright © 2017 Elsevier Ltd. All rights reserved.
Tennenhouse, Erica M; Putman, Sarah; Boisseau, Nicole P; Brown, Janine L
Relationships between the hypothalamic-pituitary adrenal and hypothalamic-pituitary gonadal axes and social behaviour in primates are complex. By using hair to quantify steroid hormones, one can obtain retrospective estimates of long-term free hormone levels from a single sample. In this study, hair was used to quantify long-term levels of cortisol, testosterone, and estradiol among members of a colony of ring-tailed lemurs (Lemur catta) to explore associations between intra- and intersexual levels of these hormones and social behaviour between the breeding and birthing seasons. Positive trends between hair cortisol and rates of receiving aggression approached significance for males and females after controlling for age. While there was no relationship between sex steroid concentrations and intrasexual social interactions, high rates of aggression in females over the study period coincided with females exhibiting the same average concentrations of testosterone as males. We, therefore, conclude that being the recipient of aggression might be more stressful than being aggressive in ring-tailed lemurs, and that testosterone potentially mediates female dominance in this species. We suggest that further investigation of hair hormones and behaviour in additional primate species could provide a useful comparative framework to guide interpretation of these novel findings.
Alić, Amer; Hodžić, Adnan; Škapur, Vedad; Alić, Alma Šeho; Prašović, Senad; Duscher, Georg G
Here we describe fatal pulmonary cysticercosis caused by Cysticercus longicollis, the larval stage of Taenia crassiceps in a 15-year-old female ring-tailed lemur (Lemur catta) from Sarajevo Zoo. After sudden death, the lemur was subjected to necropsy and large multicystic structure, subdivided with fibrous septa and filled with numerous translucent, oval to ellipsoid bladder-like cysts (cysticerci), almost completely replacing right lung lobe was observed. In addition, numerous free and encysted cysticerci were found in the thoracic cavity. Histopathology revealed connective tissue outlined cavities that compress lung parenchyma. Each cavity contained several thin walled cysticerci with single inverted protoscolex, one or more suckers and rostelum with two rows of hooks. In many of the cysticerci one or several exogenous buds of daughter cysticerci were observed. Based on morphology and microscopic appearance the parasite was identified as C. longicollis. Subsequent molecular analysis and sequencing confirmed presumptive diagnosis. To our knowledge, this case represents the first report of T. crassiceps and cysticercosis caused by C. longicollis in Bosnia and Herzegovina. Copyright © 2017 Elsevier B.V. All rights reserved.
Rea, Mark S; Figueiro, Mariana G; Jones, Geoffrey E; Glander, Kenneth E
Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24-hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light-dark exposure and activity-rest patterns in free-ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter-D pendant that contained light and accelerometer sensors. Our results reveal common as well as species-specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre-sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid-day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species-specific photic niches and behaviors. The eventual application of the Daysimeter-D in the wild may help to better understand the adaptive evolution of ancestral primates.
Fogel, Andrew T
Mammalian gut microbes are invaluable to the host's metabolism, but few researchers have examined gut microbial dynamics under natural conditions in wild mammals. This study aims to help fill this knowledge gap with a survey of the natural variation of the gut microbiome in 2 wild lemur species, Lemur catta and Propithecus verreauxi. The wild L. catta were also compared to a captive population to discern the effect of habitat within a species. Gut microbial DNA was extracted from fecal samples collected in Madagascar and the Vienna Zoo and sequenced. The wild and captive L. catta had distinct microbial communities, likely due to differences in diet and development between their populations. The wild L. catta and P. verreauxi also had distinct gut microbiomes, due to a change in microbial abundance, not composition. Within each lemur species, there was abundant variation between individuals and from the dry to the wet season. The intraspecific and temporal microbial variation requires more investigation, with changes in diet a likely contributor.
Nemeth, N M; Blas-Machado, U; Cazzini, P; Oguni, J; Camus, M S; Dockery, K K; Butler, A M
A 16-year-old male ring-tailed lemur (Lemur catta) was presented with severe cachexia and an abdominal mass. The encapsulated, multilobular mass replaced the right medial lobe of the liver and compressed the adjacent gall bladder. Multiple haemorrhages and necrotic foci were found within the mass. Microscopically, neoplastic cells formed cords of moderately pleomorphic, polygonal cells with mild to moderate anaplasia. Immunohistochemical markers used for diagnosis of hepatocellular carcinomas in man were used to characterize the neoplastic cells, which expressed hepatocyte-specific antigen, but not glypican-3 or polyclonal carcinoembryonic antigen. Gross, microscopical and immunohistochemical features of the tumour were most consistent with a well-differentiated hepatocellular carcinoma. Although this tumour is common among prosimians, to the authors' knowledge this is the first documented case in a ring-tailed lemur. Hepatocellular carcinomas have been associated with hepatitis virus infections and excessive hepatic iron in man; however, no association was established between this tumour and viral infection or hepatic iron storage disease in the present case.
Drea, Christine M
Female ring-tailed lemurs (Lemur catta) are Malagasy primates that are size monomorphic with males, socially dominate males, and exhibit a long, pendulous clitoris, channeled by the urethra. These masculine traits evoke certain attributes of female spotted hyenas (Crocuta crocuta) and draw attention to the potential role of androgens in lemur sexual differentiation. Here, hormonal correlates of prenatal development were assessed to explore the possibility that maternal androgens may shape the masculine morphological and behavioral features of developing female lemurs. Maternal serum 17α-hydroxyprogesterone, dehydroepiandrosterone sulphate (DHEA-S), ∆⁴ androstenedione (androst-4-ene-3,17,dione), testosterone, and 17β-estradiol were charted throughout the 19 pregnancies of 11 ring-tailed lemurs. As in spotted hyenas, lemur pregnancies were associated with an immediate increase in androgen concentrations (implicating early maternal derivation), followed by continued increases across stages of gestation. Pregnancies that produced singleton males, twin males, or mixed-sex twins were marked by greater androgen and estrogen concentrations than were pregnancies that produced singleton or twin females, especially in the third trimester, implicating the fetal testes in late-term steroid profiles. Concentrations of DHEA-S were mostly below detectable limits, suggesting a minor role for the adrenals in androgen biosynthesis. Androgen concentrations of pregnant lemurs bearing female fetuses, although less than those of pregnant hyenas, exceeded preconception and postpartum values and peaked in the third trimester. Although a maternal (and, on occasion, fraternal) source of androgen may exist for fetal lemurs, further research is required to confirm that these steroids would reach the developing female and contribute to her masculinization.
Rainwater, Thomas R; Sauther, Michelle L; Rainwater, Katherine A E; Mills, Rachel E; Cuozzo, Frank P; Zhang, Baohong; McDaniel, Les N; Abel, Michael T; Marsland, Eric J; Weber, Martha A; Youssouf Jacky, Ibrahim Antho; Platt, Steven G; Cobb, George P; Anderson, Todd A
Like most of Madagascar's endemic primates, ring-tailed lemurs (Lemur catta) face a number of threats to their survival. Although habitat loss is of greatest concern, other anthropogenic factors including environmental contamination may also affect lemur health and survival. In this study, we examined ring-tailed lemurs from the Beza Mahafaly Special Reserve (BMSR), southern Madagascar for exposure to organochlorine (OC) pesticides and metals and examined differences in contaminant concentrations between sexes and among age groups, troops, and habitats. A total of 14 pesticides and 13 metals was detected in lemur blood (24 individuals) and hair (65 individuals) samples, respectively. p,p'-DDT, heptachlor, aldrin, heptachlor epoxide, endrin aldehyde, and endrin were among the most prevalent pesticides detected. Surprisingly, the persistent metabolite of p,p'-DDT, p,p'-DDE, was not detected. The most commonly detected metals were aluminum, zinc, boron, phosphorus, silicon, and copper, whereas metals considered more hazardous to wildlife (e.g. arsenic, cadmium, lead, selenium, vanadium) were not found above detection limits. Overall, concentrations of OC pesticides and metals were low and similar to those considered to be background concentrations in other studies examining the ecotoxicology of wild mammals. Few inter-sex, -age, -troop, and -habitat differences in contaminant concentrations were observed, suggesting a uniform distribution of contaminants within the reserve. Several statistically significant relationships between lemur body size and contaminant concentrations were observed, but owing to the lack of supportive data regarding contaminant exposure in wild primates, the biological significance of these findings remains uncertain. Results of this study document exposure of ring-tailed lemurs at BMSR to multiple OC pesticides and metals and provide essential baseline data for future health and toxicological evaluations of lemurs and other wild primates
Bray, Joel; Samson, David R; Nunn, Charles L
Cathemerality, or activity throughout the 24-hr cycle, is rare in primates yet relatively common among lemurs. However, the diverse ecological conditions under which cathemerality is expressed complicates attempts to identify species-typical behavior. For example, Lemur catta and Varecia have historically been described as diurnal, yet recent studies suggest that they might exhibit cathemeral behavior under some conditions. To investigate this variation, we monitored activity patterns among lemurs that are exposed to similar captive environments. Using MotionWatch 8 ® actigraphy data loggers, we studied 88 lemurs across seven species at the Duke Lemur Center (DLC). Six species were members of the family Lemuridae (Eulemur coronatus, E. flavifrons, E. mongoz, L. catta, V. rubra, V. variegata), while a seventh was strictly diurnal and included as an out-group (Propithecus coquereli). For each 24-hr cycle (N = 503), we generated two estimates of cathemerality: mean night (MN) activity and day/night (DN) activity ratio (day and night cutoffs were based on astronomical twilights). As expected, P. coquereli engaged in the least amount of nocturnal activity according to both measures; their activity was also outside the 95% confidence intervals of all three cathemeral Eulemur species, which exhibited the greatest evidence of cathemerality. By these estimates, Varecia activity was most similar to Eulemur and exhibited substantial deviations from P. coquereli (β (MN) = 0.22 ± SE 0.12; β (DN) = -0.21 ± SE 0.12). L. catta activity patterns also deviated from P. coquereli (β (MN) = 0.12 ± SE 0.11; β (DN) = -0.15 ± SE 0.12) but to a lesser degree than either Varecia or Eulemur. Overall, L. catta displayed an intermediate activity pattern between Eulemur and P. coquereli, which is somewhat consistent with wild studies. Regarding Varecia, although additional observations in more diverse wild habitats are needed, our findings support
Bolt, Laura M
Squeals are sharp and forceful short-range vocalizations used as aggressive and submissive agonistic signals by many mammalian species. The ring-tailed lemur (Lemur catta), a female-dominant strepsirhine primate, has a male-specific squeal call with proposed male-male agonistic functions and male-female courtship functions that have never been empirically tested. The goal of my study is to clarify why ring-tailed lemur males squeal at other males and females by applying the handicap hypothesis to this male-specific vocalization. This hypothesis has rarely been tested in primates, and this study elucidates how the rate of a male-specific call relates to male-male and male-female behavior in a Malagasy strepsirhine. To test whether males squeal towards other males to assert dominance, I predict that male squealing rate is positively correlated with dominance rank. I further predict that male ring-tailed lemurs squeal at other males while engaged in agonistic interactions, and that squealing during an interaction is positively correlated with winning that encounter. To test whether males squeal towards females as a mate attraction signal, I predict that male squealing rate is higher on estrus days, and that estrous females indicate attraction by approaching squealing males. From March to July 2010, 480 hr of focal data were collected on 25 males aged three and older at Beza Mahafaly Special Reserve, Madagascar. I continuously observed each male for 30 min at a time and recorded all agonistic interactions and squeal vocalizations using 1-0 sampling at 2.5-min intervals. Squealing rate was higher during times of male-male agonism when compared to times without male-male agonism, and males with higher dominance ranks had higher squealing rates. In contrast, the mate attraction hypothesis was not supported. My results suggest that the male squeal is an agonistic signal when used in male-male interaction in ring-tailed lemurs, but does not specifically indicate aggression
Bray, Joel; Krupenye, Christopher; Hare, Brian
Studies suggest that haplorhine primates are sensitive to what others can see and hear. Using two experimental designs, we tested the hypothesis that ring-tailed lemurs (N = 16) are also sensitive to the visual and auditory perception of others. In the first task, we used a go/no-go design that required lemurs to exploit only auditory information. In the second task, we used a forced-choice design where lemurs competed against a human who would prevent them from obtaining food if their approaches were detected. Subjects were given the choice of obtaining food silently or noisily when the competitor's back was turned. They were also given the choice to obtain food when the competitor could either see them or not. Here, we replicate the findings of previous studies indicating that ring-tailed lemurs are sensitive to whether they can be seen; however, we found no evidence that subjects are sensitive to whether others can hear them. Our findings suggest that ring-tailed lemurs converge with haplorhine primates only in their sensitivity to the visual information of others. The results emphasize the importance of investigating social cognition across sensory domains in order to elucidate the cognitive mechanisms that underlie apparently complex social behavior. These findings also suggest that the social dynamics of haplorhine groups impose greater cognitive demands than lemur groups, despite similarities in total group size.
Hosey, Geoff; Hill, Sonya P; Lherbier, Mary L
Most zoos keep comprehensive records, which potentially form a database for use in answering some research questions, such as in veterinary and population management research. They have not, however, been widely used to answer questions about animal behavior and welfare. Here we try to assess the usefulness to behavioral research of two sorts of zoo records (ARKS, the Animal Records Keeping System, and student dissertations held on file) to test the hypothesis that ring-tailed lemurs with a left limb preference experience more negative social lives. We found that, as predicted, lemurs with a left limb preference (LH) received more aggression and were involved in less grooming than nonleft-preferent lemurs (NLH), though the differences were not statistically significant. Contrary to prediction, LH lemurs had fewer reported woundings than NLH lemurs, but again the difference was not statistically significant. We found that the ARKS reports did not contain sufficient quantified and systematic behavioral data for our purposes, although otherwise they provided an excellent context for interpreting results. The student dissertations were also of limited use, primarily because of the small time frame in which they were carried out. Because of these shortcomings we were unable to distinguish whether our inability to find significant effects was due to biological (perhaps hand preference had no consequences for the lemurs) or data reasons. We suggest that closer liaison between zoo research staff, zoo record keepers and academic supervisors could help to improve the usefulness of zoo records for behavioral research.
Chinnadurai, Sathya K; Williams, Cathy
To determine the minimum alveolar concentration (MAC) of sevoflurane for ring-tailed lemurs (Lemur catta) and aye-ayes (Daubentonia madagascariensis). Prospective experimental trial. Six adult ring-tailed lemurs, aged 1.3-11.2 years (median age: 8.26) and weighing a mean ± standard deviation (SD) of 2283 ± 254 g. Five adult aye-ayes, aged 4.4-19.3 years (median age: 8.0) and weighing 2712 ± 191 g. Minimum alveolar concentration of sevoflurane was determined using a tail-clamp stimulus. The end-tidal sevoflurane (Fe'Sevo) concentration was increased or decreased by approximately 10% after a positive or negative response to tail clamping, respectively. This procedure was repeated until a positive and negative result were seen on two consecutive trials (i.e. a negative result was achieved and a single 10% decrease in Fe'Sevo concentration resulted in a positive test). The MAC for that animal was determined to be the mean of the concentrations at the two consecutive trials. The mean ± SD MAC of sevoflurane for ring-tailed lemurs was 3.48 ± 0.55% and 1.84 ± 0.17 for aye-ayes. This represents a 47.1% higher MAC in ring-tailed lemurs compared to aye-ayes. The sevoflurane MAC was significantly higher in ring-tailed lemurs, compared to aye-ayes. The MAC of sevoflurane in aye-ayes is consistent with reported MAC values in other species. Extrapolation of sevoflurane anesthetic dose between different species of lemurs could lead to significant errors in anesthetic dosing. © 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia.
Parga, Joyce A
Cathemerality, an activity pattern comprised of distinct periods of diurnal and nocturnal activity, is a trait found among several of the Malagasy strepsirhines and one species of Aotus. Because occasional anecdotal reports suggest that some diurnal primates can be active at night, I investigated the possibility of nocturnal ranging behavior in the ring-tailed lemur (Lemur catta) by using global positioning system (GPS) collars programmed to collect data across a 24-h period. Five individuals in a provisioned, free-ranging L. catta colony on St. Catherines Island, Georgia, USA, wore GPS collars across 1 week of the mating season. Results revealed that night ranging behavior occurred between the h of 1900 and 0530. An evaluation of the effect of moonlight on nocturnal activity showed that a greater rate of travel occurred during moonlit periods as opposed to periods when the moon had not yet risen. Distance travelled at night decreased across the deployment period, likely because of a decrease in available moonlight over time, as the lemurs were collared during a waning moon. Fewer mating opportunities over time may have also been responsible for the decrease in night ranging, because the number of females in estrus declined across the deployment period. Future research is needed to separate the effects of moonlight and mating activity on night ranging in this species, as well as to evaluate whether L. catta in Madagascar show night ranging similar to L. catta on SCI. These data raise the possibility that L. catta may be cathemeral, with an activity pattern fluctuating between diurnality and cathemerality in accordance with shifts in environmental conditions.
Parga, J A; Lessnau, R G
Male dispersal patterns were analyzed across a nine-year period in a population of ring-tailed lemurs (Lemur catta) on St. Catherines Island (SCI), USA, to evaluate two ultimate explanations for male dispersal: inbreeding avoidance and intrasexual mating competition. As part of this analysis, we also compared patterns of dispersal at this site with data from wild populations. Overall, we found that patterns of male intertroop movement on SCI are similar to the wild with respect to the frequency and seasonality of male transfer. In Madagascar, males move between groups every 3.1-3.5 years [Sussman, International Journal of Primatol 13:395-413, 1992; Koyama et al., Primates 43:291-314, 2002] as compared with every 3.2 years on SCI. The majority of transfers on SCI occurred during the birth season, as occurs at one site in Madagascar, Berenty [Budnitz & Dainis, Lemur biology. New York: Plenum Press, p 219-235, 1975; Jones, Folia Primatologica 40:145-160, 1983]. One difference is that males perform natal transfers 1-2 years earlier on SCI than in the wild, which may be related to food provisioning on SCI. Males never transferred back into their natal troops, which is remarkable given the small number of groups on SCI. Although this pattern of movement can indicate inbreeding avoidance by males, the fact that male troop tenure was in many cases long enough to overlap with the sexual maturation of potential daughters did not support the inbreeding avoidance hypothesis for male secondary dispersal. Instead, the intrasexual competition hypothesis was strongly supported, because males were significantly more likely to transfer into groups having fewer adult males and a more favorable sex ratio than their pretransfer groups. Males therefore appear to be bypassing groups in which they would experience a greater degree of intrasexual mating competition during the breeding season.
Merritt, Dustin; MacLean, Evan L.; Jaffe, Sarah; Brannon, Elizabeth M.
Research over the last 25 years has demonstrated that animals are able to organize sequences in memory and retrieve ordered sequences without language. Qualitative differences have been found between the serial organization of behavior in pigeons and monkeys. Here the authors test serial ordering abilities in ring-tailed lemurs, a strepsirrhine primate whose ancestral lineage diverged from that of monkeys, apes, and humans approximately 63 million years ago. Lemurs’ accuracy and response times were similar to monkeys, thus suggesting that they may share mechanisms for serial organization that dates to a common primate ancestor. PMID:18085919
Kopera, D; Soyer, H P; Kerl, H
A 31-year-old woman presented with a clinically otherwise unsuspicious area of profuse sweating on her right forearm. Without triggering agents, sweating attacks producing a clear, serous fluid were observed daily. Histopathologic examination of a biopsy specimen showed hyperplastic eccrine glands with pale, stippled cytoplasm characteristic of eccrine hamartoma. No explanation, however, has been given for the fact that several authors observed eccrine hamartomas in the same anatomical location. Adolescent lemurs of the species catta (ringtailed lemur) are equipped with a pair of antebrachial cutaneous glands located on the volar surface of the wrist. They exude a clear secretion enabling them to "brachial branch mark" their territories. Histopathologic findings in the ringtailed lemur's antebrachial organ show characteristics of both apocrine and eccrine glands. In contrast to normal apocrine glands, however, the antebrachial organs of ringtailed lemurs reach the epidermis directly and are not connected to hair follicles. According to the "biogenetic law" of Ernst Haeckel, stating that ontogeny has to be seen as a short and incomplete repetition of phylogeny, a human fetus passes all evolutional stages from a single cell via amphibians and mammals to a human being. Thus, the antebrachial organ of the ringtailed lemur may be the "phylogenetic explanation" for eccrine hamartomas of the forearm in humans. The histopathologic findings of the antebrachial organ and of eccrine hamartomas are in accordance with this hypothesis.
Chatfield, Jenifer; Penfold, Linda
Lemurs are a diverse group of primates comprised of five families, all of which are found only on Madagascar and the Comoro Islands. Of the 60 known species, 17 are endangered and 5 of these are considered critically endangered. The effects of inbreeding on population health and viability have been well described; though negative inbreeding effects can be ameliorated through the introduction of new genetic material. Introduction of new individuals into a population can be extremely challenging because of the highly social nature of lemurs. Semen collection in lemur species is notoriously challenging, as the ejaculate forms a coagulum. During normal breeding, the coagulum forms a copulatory plug in the female. However, this coagulum can present a life-threatening situation when retained in the urethra abnormally following electroejaculation. This study investigates the use of ascorbic acid in preventing urethral blockage in two lemur species during semen collection, demonstrates successful collection of semen by electroejaculation from two species of lemur during the breeding season, and discusses removal of urethral plugs subsequent to semen collection. Semen was collected successfully from all animals. Urethral plugs formed during each collection and were abnormally retained in 2/11 collections. Both plugs were successfully and immediately removed with the use of retropulsion through a urethral catheter. Although the results of this study are encouraging, more investigation is required to establish whether or not this procedure can be safely performed in the field.
Singleton, Cora L; Norris, Aimee M; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho
The health of 36 wild, free-ranging ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve was assessed across 2 habitats of varied human impact: a reserve riverine gallery forest, and a degraded mixed dry deciduous and Alluaudia-dominated spiny forest. While there were no statistically significant differences in leukocyte count or differential between habitats, female lemurs in the reserve gallery forest had significantly higher percentages of monocytes and eosinophils than male lemurs in the gallery forest. Lemurs from the degraded spiny habitat had significantly higher mean packed cell volume, hematocrit, hemoglobin, total protein, blood urea nitrogen, chloride, ionized calcium and urine specific gravity than lemurs from the reserve gallery forest. These findings may reflect lower hydration levels in lemurs living in degraded habitat, providing evidence that environmental degradation has identifiable impacts on the physiology and health of wild, free-ranging ring-tailed lemurs living in nearby habitats. Given the greater evidence of human impact in the mixed dry deciduous/spiny forest habitat, a pattern seen throughout southern Madagascar, biomedical markers suggestive of decreased hydration can provide empirical data to inform new conservation policies facilitating the long-term survival of this lemur community.
Modesto, Monica; Michelini, Samanta; Stefanini, Ilaria; Sandri, Camillo; Spiezio, Caterina; Pisi, Annamaria; Filippini, Gianfranco; Biavati, Bruno; Mattarelli, Paola
Four Gram-positive-staining, microaerophilic, non-spore-forming, fructose-6-phosphate phosphoketolase-positive bacterial strains were isolated from a faecal sample of a 5-year-old ring-tailed lemur (Lemur catta). The strains showed a peculiar morphology, resembling a small coiled snake, a ring shape, or forming a little 'Y' shape. The isolated strains appeared identical, and LMC 13T was chosen as a representative strain and characterized further. Strain LMC 13T showed an A3β peptidoglycan type, similar to that found in Bifidobacterium longum. The DNA base composition was 57.2 mol% G+C. Almost-complete 16S rRNA, hsp60, rpoB, dnaJ, dnaG, purF, clpC and rpoC gene sequences were obtained, and phylogenetic relationships were determined. Comparative analysis of 16S rRNA gene sequences showed that strain LMC 13T showed the highest similarity to B. longum subsp. suis ATCC 27533T (96.65 %) and Bifidobacterium saguini DSM 23967T (96.64 %). Strain LMC 13T was located in an actinobacterial cluster and was more closely related to the genus Bifidobacteriumthan to other genera in the Bifidobacteriaceae. On the basis of these results, strain LMC 13T represents a novel species within the genus Bifidobacterium, for which the name Bifidobacterium lemurum sp. nov. is proposed; the type strain is LMC 13T ( = DSM 28807T = JCM 30168T).
Bolt, Laura M; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho
The ring-tailed lemur (Lemur catta) is a group-living strepsirrhine primate endemic to Madagascar that faces considerable predation pressure from aerial and terrestrial predators. This species engages in mobbing and vigilance behavior in response to predators, and has referential alarm vocalizations. Because L. catta is female dominant, less is known about the alarm calls of males. We tested 3 hypotheses for male antipredator vocalization behavior on L. catta at the Bezà Mahafaly Special Reserve in Madagascar: the predator confusion, group maintenance, and predation risk allocation hypotheses. We found support for 2 hypotheses. When a male L. catta made an antipredator call, other group members vocalized in response. Dominant males did not make alarm calls at higher rates than subordinate males. Predators were more abundant on the western side of Parcel 1, but an even greater number of antipredator vocalizations occurred in this area than predator abundance warranted. We show that male L. catta consistently participated in group-level antipredator vocalization usage in high-risk locations. Although female L. catta are known to hold the primary role in group defense, male L. catta are also key participants in group-wide behaviors that may confuse or drive away predators.
Eppley, Timothy M; Donati, Giuseppe; Ganzhorn, Jörg U
Selection of sleeping sites has consequences for individual fitness. Non-human primates often bias their selection towards arboreal sites, and the lemurs of Madagascar typically rest/sleep in trees, tree holes, and/or constructed nests. Three non-mutually exclusive hypotheses to explain sleeping site selection include protection from predators, avoidance of parasitic vectors, and improved thermoregulation. Here, we examine these hypotheses for the unusual sleeping site selections by the southern bamboo lemur (Hapalemur meridionalis). Within the Mandena littoral forest of southeast Madagascar, the southern bamboo lemur is known for its ecological flexibility compared to other bamboo lemur species, including a dietary niche expansion to feeding on the ground. Between October 2012 and December 2013, we observed bamboo lemurs from three social groups for 1778.67 h, conducting full-day focal follows on 11 adult individuals (five males, six females). During this period, all three groups were observed to sleep on the ground, with one of these groups also using an abandoned nest of a Madagascar crested ibis (Lophotibis cristata). We collected habitat and temperature data to examine whether selection was influenced by environmental variables. Terrestrial sleeping (N = 17) was observed in all individuals but one adult female, with individuals burrowing under thick vegetation more often during the hot austral summer. While difficult to rigorously test, it is possible that terrestrial sleep sites and/or sleeping in a bird nest may impair visual detection by some aerial and terrestrial predators. Neither of these sites (i.e., terrestrial sleeping or use of a bird nest), however, is likely to minimize exposure to parasites/vectors. Terrestrial sleeping appears to support a thermoregulatory strategy, whereas the use of a bird nest could not be empirically tested. Our observations of unique sleeping site locations used by southern bamboo lemurs further the complexity of their
MacLean, Evan L; Mandalaywala, Tara M; Brannon, Elizabeth M
Numerous studies have demonstrated that animals' tolerance for risk when foraging can be affected by changes in metabolic state. Specifically, animals on a negative energy budget increase their preferences for risk, while animals on a positive energy budget are typically risk-averse. The malleability of these preferences may be evolutionarily advantageous, and important for maximizing chances of survival during brief periods of energetic stress. However, animals adapted to living in unpredictable conditions are unlikely to benefit from risk-seeking strategies, and instead are expected to reduce energetic demands while maintaining risk-aversion. We measured risk preferences in lemurs, a group of primates restricted to the island of Madagascar. Lemurs have evolved diverse anatomical and behavioral traits for survival in a harsh and unpredictable ecology, and these traits have been explained as forms of anatomical and behavioral risk reduction. We therefore predicted that lemurs would also be risk-averse in a behavioral task that offered subjects a choice between a small certain reward, and an uncertain but potentially large reward. In Experiment 1, the average rewards associated with the constant and variable options were equal and lemurs exhibited high levels of risk-aversion, replicating a phenomenon that has been demonstrated in dozens of taxa. In Experiment 2, we gradually increased the average value of the variable option relative to the constant option. Lemurs' preferences tracked these changes and subjects became more risk-seeking as the risk premium increased. However, many subjects maintained high levels of risk-aversion even when the average payout of the variable option yielded double that of the constant option. These results are consistent with the notion that lemur cognition has evolved to minimize risk in an unpredictable island environment.
Pastorini, Jennifer; Zaramody, Alphonse; Curtis, Deborah J; Nievergelt, Caroline M; Mundy, Nicholas I
Hybrid zones generally represent areas of secondary contact after speciation. The nature of the interaction between genes of individuals in a hybrid zone is of interest in the study of evolutionary processes. In this study, data from nuclear microsatellites and mitochondrial DNA sequences were used to genetically characterize hybridization between wild mongoose lemurs (Eulemur mongoz) and brown lemurs (E. fulvus) at Anjamena in west Madagascar. Two segments of mtDNA have been sequenced and 12 microsatellite loci screened in 162 brown lemurs and mongoose lemurs. Among the mongoose lemur population at Anjamena, we identified two F1 hybrids (one also having the mtDNA haplotype of E. fulvus) and six other individuals with putative introgressed alleles in their genotype. Principal component analysis groups both hybrids as intermediate between E. mongoz and E. fulvus and admixture analyses revealed an admixed genotype for both animals. Paternity testing proved one F1 hybrid to be fertile. Of the eight brown lemurs genotyped, all have either putative introgressed microsatellite alleles and/or the mtDNA haplotype of E. mongoz. Introgression is bidirectional for the two species, with an indication that it is more frequent in brown lemurs than in mongoose lemurs. We conclude that this hybridization occurs because mongoose lemurs have expanded their range relatively recently. Introgressive hybridization may play an important role in the unique lemur radiation, as has already been shown in other rapidly evolving animals.
Pastorini, Jennifer; Zaramody, Alphonse; Curtis, Deborah J; Nievergelt, Caroline M; Mundy, Nicholas I
Background Hybrid zones generally represent areas of secondary contact after speciation. The nature of the interaction between genes of individuals in a hybrid zone is of interest in the study of evolutionary processes. In this study, data from nuclear microsatellites and mitochondrial DNA sequences were used to genetically characterize hybridization between wild mongoose lemurs (Eulemur mongoz) and brown lemurs (E. fulvus) at Anjamena in west Madagascar. Results Two segments of mtDNA have been sequenced and 12 microsatellite loci screened in 162 brown lemurs and mongoose lemurs. Among the mongoose lemur population at Anjamena, we identified two F1 hybrids (one also having the mtDNA haplotype of E. fulvus) and six other individuals with putative introgressed alleles in their genotype. Principal component analysis groups both hybrids as intermediate between E. mongoz and E. fulvus and admixture analyses revealed an admixed genotype for both animals. Paternity testing proved one F1 hybrid to be fertile. Of the eight brown lemurs genotyped, all have either putative introgressed microsatellite alleles and/or the mtDNA haplotype of E. mongoz. Conclusion Introgression is bidirectional for the two species, with an indication that it is more frequent in brown lemurs than in mongoose lemurs. We conclude that this hybridization occurs because mongoose lemurs have expanded their range relatively recently. Introgressive hybridization may play an important role in the unique lemur radiation, as has already been shown in other rapidly evolving animals. PMID:19196458
Seiler, Melanie; Schwitzer, Christoph; Gamba, Marco; Holderied, Marc W
As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This "eavesdropping" was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species' and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect
Petty, Joseph M. A.; Drea, Christine M.
Female social dominance (FSD) over males is unusual in mammals, yet characterizes most Malagasy lemurs, which represent almost 30% of all primates. Despite its prevalence in this suborder, both the evolutionary trajectory and proximate mechanism of FSD remain unclear. Potentially associated with FSD is a suite of behavioural, physiological and morphological traits in females that implicates (as a putative mechanism) ‘masculinization’ via androgen exposure; however, relative to conspecific males, female lemurs curiously show little evidence of raised androgen concentrations. By observing mixed‐sex pairs of related Eulemur species, we identified two key study groups ‐‐ one comprised of species expressing FSD and increased female scent marking, the other comprised of species (from a recently evolved clade) showing equal status between the sexes and the more traditional pattern of sexually dimorphic behaviour. Comparing females from these two groups, we show that FSD is associated with more masculine androgen profiles. Based on the widespread prevalence of male‐like features in female lemurs and a current phylogeny, we suggest that relaxation of hormonally mediated FSD emerged only recently and that female masculinization may be the ancestral lemur condition, an idea that could revolutionize our understanding of the ancient socioecology and evolution of primate social systems. PMID:25950904
Sauther, Michelle L; Cuozzo, Frank P
While understanding somatic variability among wild primates can provide insight into natural patterns of developmental plasticity, published data for living populations are rare. Here we provide such information for two distinct wild populations of Lemur catta. Variants observed include microtia, athelia, and female virilization. Dental variants observed include individuals with supernumerary teeth, rotated teeth, maxillary incisor agenesis, and severe malocclusion. There was a sex bias in incisor agenesis, with 5 of 7 examples (71%) found in males. The frequency of dental variants in our sample is lower than that seen in many other lemuriformes, as well as other primates. This may be a product of their less derived dental formula and/or their relatively fast dental development. Amassing such data is a critical first step to assess if wild primate populations are exhibiting normal variability or are being affected by potential inbreeding and/or environmental effects.
Berg, Wiebke; Jolly, Alison; Rambeloarivony, Hajarimanitra; Andrianome, Vonjy; Rasamimanana, Hantanirina
Coat condition can be influenced by a wide variety of disorders and thus provides a useful tool for noninvasive health and welfare assessments in wild and captive animals. Using Lemur catta as an exemplar, we offer a 6-step scoring system for coat and tail condition, ranging from perfectly fluffy to half or more of body and tail being hairless. The categories are described in detail and illustrated with sample pictures from a wild population in Berenty Reserve, Madagascar. Furthermore, we elaborate on intermediate conditions and discoloration of fur. Coat condition scoring allows the comparison between years, seasons, and the effect of toxin, disease or stress. Although this system was developed for wild L. catta, we believe it can also be of value for other species. We recommend scoring coat condition in healthy wild mammal populations to give a baseline on yearly and seasonal variations vs. deteriorating health conditions or pathology. (c) 2009 Wiley-Liss, Inc.
Sauther, Michelle L.; Cuozzo, Frank P.; Youssouf Jacky, Ibrahim Antho; Lawler, Richard R.; Sussman, Robert W.; Gould, Lisa; Pastorini, Jennifer
1 In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males. PMID:27391113
Parga, Joyce A; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho; Lawler, Richard R; Sussman, Robert W; Gould, Lisa; Pastorini, Jennifer
In group-living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single-male monopolization of paternity in groups. Ring-tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi-male, multi-female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra-group males-posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80-95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra-troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra-group mating is a viable strategy that can result in extra-group paternity for L. catta males. © 2016 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.
Starling, Anne P; Charpentier, Marie J E; Fitzpatrick, Courtney; Scordato, Elizabeth S; Drea, Christine M
Fecal glucocorticoid (fGC) concentrations are reliable, non-invasive indices of physiological stress that provide insight into an animal's energetic and social demands. To better characterize the long-term stressors in adult members of a female-dominant, seasonally breeding species - the ring-tailed lemur (Lemur catta) - we first validated fecal samples against serum samples and then examined the relationship between fGC concentrations and seasonal, social, demographic, genetic, and reproductive variables. Between 1999 and 2006, we collected 1386 fecal samples from 32 adult, semi-free-ranging animals of both sexes. In males and non-pregnant, non-lactating females, fGC concentrations were significantly elevated during the breeding season, specifically during periods surrounding known conceptions. Moreover, group composition (e.g., multi-male versus one-male) significantly predicted the fGC concentrations of males and females in all reproductive states. In particular, the social instability introduced by intra-male competition likely created a stressor for all animals. We found no relationship, however, between fGC and the sex, age, or heterozygosity of animals. In reproducing females, fGC concentrations were significantly greater during lactation than during the pre-breeding period. During pregnancy, fGC concentrations were elevated in mid-ranking dams, relative to dominant or subordinate dams, and significantly greater during the third trimester than during the first or second trimesters. Thus, in the absence of nutritional stressors, social dominance was a relatively poor predictor of fGC in this female-dominant species. Instead, the animals were maximally challenged by their social circumstances and reproductive events-males by competition for mating opportunities and females by late-term gestation and lactation.
The solar outer atmosphere is an extremely dynamic environment characterized by the continuous interplay between the plasma and the magnetic field that generates and permeates it. Such interactions play a fundamental role in hugely diverse astrophysical systems, but occur at scales that cannot be studied outside the solar system. Understanding this complex system requires concerted, simultaneous solar observations from the visible to the vacuum ultraviolet (VUV) and soft X-rays, at high spatial resolution (between 0.1'' and 0.3''), at high temporal resolution (on the order of 10 s, i.e., the time scale of chromospheric dynamics), with a wide temperature coverage (0.01 MK to 20 MK, from the chromosphere to the flaring corona), and the capability of measuring magnetic fields through spectropolarimetry at visible and near-infrared wavelengths. Simultaneous spectroscopic measurements sampling the entire temperature range are particularly important. These requirements are fulfilled by the Japanese Solar-C mission (Plan B), composed of a spacecraft in a geosynchronous orbit with a payload providing a significant improvement of imaging and spectropolarimetric capabilities in the UV, visible, and near-infrared with respect to what is available today and foreseen in the near future. The Large European Module for solar Ultraviolet Research (LEMUR), described in this paper, is a large VUV telescope feeding a scientific payload of high-resolution imaging spectrographs and cameras. LEMUR consists of two major components: a VUV solar telescope with a 30 cm diameter mirror and a focal length of 3.6 m, and a focal-plane package composed of VUV spectrometers covering six carefully chosen wavelength ranges between 170 Angstrom and 1270 Angstrom. The LEMUR slit covers 280'' on the Sun with 0.14'' per pixel sampling. In addition, LEMUR is capable of measuring mass flows velocities (line shifts) down to 2 km s - 1 or better. LEMUR has been proposed to ESA as the European contribution
MacLean, Evan L.; Mandalaywala, Tara M.; Brannon, Elizabeth M.
Numerous studies have demonstrated that animals’ tolerance for risk when foraging can be affected by changes in metabolic state. Specifically, animals on a negative energy budget increase their preferences for risk, while animals on a positive energy budget are typically risk averse. The malleability of these preferences may be evolutionarily advantageous, and important for maximizing chances of survival during brief periods of energetic stress. However, animals adapted to living in unpredictable conditions are unlikely to benefit from risk-seeking strategies and instead are expected to reduce energetic demands while maintaining risk aversion. We measured risk preferences in lemurs, a group of primates restricted to the island of Madagascar. Lemurs have evolved diverse anatomical and behavioral traits for survival in a harsh and unpredictable ecology, and these traits have been explained as forms of anatomical and behavioral risk reduction. We therefore predicted that lemurs would also be risk averse in a behavioral task that offered subjects a choice between a small certain reward, and an uncertain but potentially large reward. In Experiment 1, the average rewards associated with the constant and variable options were equal and lemurs exhibited high levels of risk aversion, replicating a phenomenon that has been demonstrated in dozens of taxa. In Experiment 2 we gradually increased the average value of the variable option relative to the constant option. Lemurs’ preferences tracked these changes and subjects became more risk seeking as the risk premium increased. However, many subjects maintained high levels of risk aversion even when the average payout of the variable option yielded double that of the constant option. These results are consistent with the notion that lemur cognition has evolved to minimize risk in an unpredictable island environment. PMID:21670948
Scordato, Elizabeth S; Dubay, George; Drea, Christine M
The apocrine and sebaceous scent glands of ringtailed lemurs (Lemur catta) appear to serve different social functions. In behavioral experiments, lemurs modulate their responses to scent marks based on the type of odorant, their own physiological state, the signaler's physiological state, and prior social experience. To examine variation in odorant chemistry relative to olfactory behavior, we used gas chromatography and mass spectrometry to analyze over 86 samples of glandular secretion collected over 2 years from 15 adult lemurs. Labial and scrotal secretions contained organic acids and esters, whereas male brachial secretions were composed almost entirely of squalene and cholesterol derivatives. Principal component and linear discriminant analyses revealed glandular, individual-specific, and seasonal variation in chemical profiles but no relationship to the signaler's social status. The chemical composition of the various secretions provides further clues about the function of the different glands: the higher molecular weight compounds in genital and brachial secretions may increase signal longevity and provide lasting information to conspecifics, consistent with a role in advertising resource ownership or reproductive state. Conversely, the lower molecular weight compounds of antebrachial secretions produce ephemeral signals used primarily in social dominance displays and require integration of multiple sensory modalities for effective signal transmission.
Makungu, M; Groenewald, H B; du Plessis, W M; Barrows, M; Koeppel, K N
There is limited information available on the morphology of the thoracic limb of the ring-tailed lemur (Lemur catta). This study describes the morphology of the thoracic limb of captive ring-tailed lemurs evidenced by gross osteology and radiography as a guide for clinical use. Radiographic findings of 12 captive ring-tailed lemurs are correlated with bone specimens of three adult animals. The clavicle is well developed. The scapula has a large area for the origin of the m. teres major. The coracoid and hamate processes are well developed. The lateral supracondylar crest and medial epicondyle are prominent. The metacarpal bones are widely spread, and the radial tuberosity is prominent. These features indicate the presence of strong flexor muscles and flexibility of thoracic limb joints, which are important in arboreal quadrupedal locomotion. Furthermore, an ovoid ossicle is always seen at the inter-phalangeal joint of the first digit. Areas of increased soft tissue opacity are superimposed over the proximal half of the humerus and distal half of the antebrachium in male animals as a result of the scent gland. Knowledge of the morphology of the thoracic limb of individual species is important for accurate interpretation and diagnosis of musculoskeletal diseases.
Umhang, Gérald; Lahoreau, Jennifer; Nicolier, Alexandra; Boué, Franck
Echinococcus multilocularis is a tapeworm responsible in its larval stage for alveolar echinococcosis, a disease which is lethal when left untreated. Multivesiculated parasitic lesions in the liver were diagnosed at necropsy in a captive-born nutria (Myocastor coypus) and in a ring-tailed lemur (Lemur catta) which had been in a French zoo for 16months. Molecular analyses confirmed the diagnosis of E. multilocularis obtained by histological analyses. These were the first cases of infection by E. multilocularis reported in lemurs in Europe, and the first case in nutria in European enclosures. Lemurs are confirmed to be particularly sensitive to E. multilocularis with a massive infection. In both cases, the infection appears to have been contracted in the zoo indirectly via environmental contamination by feces from roaming foxes. Due to the large endemic area for E. multilocularis, the increasing prevalence in foxes in France, and an increase in awareness of the disease, other cases of infection in captive animals will probably be recorded in France in the coming years.
Bennett, Genevieve; Malone, Matthew; Sauther, Michelle L; Cuozzo, Frank P; White, Bryan; Nelson, Karen E; Stumpf, Rebecca M; Knight, Rob; Leigh, Steven R; Amato, Katherine R
The gut microbiota contributes to host health by maintaining homeostasis, increasing digestive efficiency, and facilitating the development of the immune system. The composition of the gut microbiota can change dramatically within and between individuals of a species as a result of diet, age, or habitat. Therefore, understanding the factors determining gut microbiota diversity and composition can contribute to our knowledge of host ecology as well as to conservation efforts. Here we use high-throughput sequencing to describe variation in the gut microbiota of the endangered ring-tailed lemur (Lemur catta) at the Bezà Mahafaly Special Reserve (BMSR) in southwestern Madagascar. Specifically, we measured the diversity and composition of the gut microbiota in relation to social group, age, sex, tooth wear and loss, and habitat disturbance. While we found no significant variation in the diversity of the ring-tailed lemur gut microbiota in response to any variable tested, the taxonomic composition of the gut microbiota was influenced by social group, age, and habitat disturbance. However, effect sizes were small and appear to be driven by the presence or absence of relatively low abundance taxa. These results suggest that habitat disturbance may not impact the lemur gut microbiota as strongly as it impacts the gut microbiota of other primate species, highlighting the importance of distinct host ecological and physiological factors on host-gut microbe relationships. Am. J. Primatol. 78:883-892, 2016. © 2016 Wiley Periodicals, Inc.
Hämäläinen, Anni; Heistermann, Michael; Kraus, Cornelia
Chronic stress [i.e. long-term elevation of glucocorticoid (GC) levels] and aging have similar, negative effects on the functioning of an organism. Aged individuals' declining ability to regulate GC levels may therefore impair their ability to cope with stress, as found in humans. The coping of aged animals with long-term natural stressors is virtually unstudied, even though the ability to respond appropriately to stressors is likely integral to the reproduction and survival of wild animals. To assess the effect of age on coping with naturally fluctuating energetic demands, we measured stress hormone output via GC metabolites in faecal samples (fGCM) of wild grey mouse lemurs (Microcebus murinus) in different ecological seasons. Aged individuals were expected to exhibit elevated fGCM levels under energetically demanding conditions. In line with this prediction, we found a positive age effect in the dry season, when food and water availability are low and mating takes place, suggesting impaired coping of aged wild animals. The age effect was significantly stronger in females, the longer-lived sex. Body mass of males but not females correlated positively with fGCM in the dry season. Age or body mass did not influence fGCM significantly in the rainy season. The sex- and season-specific predictors of fGCM may reflect the differential investment of males and females into reproduction and longevity. A review of prior research indicates contradictory aging patterns in GC regulation across and even within species. The context of sampling may influence the likelihood of detecting senescent declines in GC functioning.
Miller, David S; Sauther, Michelle L; Hunter-Ishikawa, Mandala; Fish, Krista; Culbertson, Heather; Cuozzo, P Frank; Campbell, Terry W; Andrews, Gordon A; Chavey, Patricia Sue; Nachreiner, Raymond; Rumbeiha, Wilson; Stacewicz-Sapuntzakis, Maria; Lappin, Michael R
Complete physical examinations and biomedical sample collection were performed on 70 free-ranging ring-tailed lemurs (Lemur catta) from three different habitats in the Beza Mahfaly Special Reserve (BMSR), in southern Madagascar, to assess the impact of humans and habitat on lemur health. Lemurs were chemically immobilized with ketamine and diazepam administered via blow darts for concurrent biomedical, morphometric, and behavioral studies. Subsets of the animals had blood analyzed for hematology, serum chemistry, micronutrients, fat-soluble vitamins (vitamins A, D, and E), measures of iron metabolism, and polymerase chain reaction assays (PCR) for Toxoplasma gondii, Hemoplasma spp., Bartonella spp., Ehrlichia spp., Anaplasma phagocytophilum, and Neorickettsia risticii. Results were compared on the basis of gender and the habitats at the study site: reserve (intact gallery forest), degraded (human inhabited and altered), and marginal (dry didieracea forest with heavy grazing and tree cutting). Levels of vitamin D, triglycerides, and cholesterol, and measures of iron metabolism for BMSR lemurs were greater than those previously reported for a free-ranging lemur population (Tsimanampetsotsa Strict Nature Reserve, Madagascar) with less access to foods of anthropogenic origin. BMSR ring-tailed lemurs from a habitat with less water (marginal) had higher sodium (P = 0.051), chloride (P = 0.045), osmolality (P = 0.010), and amylase (P = 0.05) levels than lemurs from other BMSR habitats, suggesting that these lemurs were less hydrated. Vitamin D levels of male lemurs were higher (P = 0.011) than those of females at BMSR, possibly because of differences in sunning behavior or differential selection of food items. The biological significance is uncertain for other parameters with statistically significant differences. All samples tested (n = 20) were negative for the pathogens tested using PCR assays. Continued concurrent biomedical and ecological research is needed at BMSR
Cuozzo, Frank P; Sauther, Michelle L; Gould, Lisa; Sussman, Robert W; Villers, Lynne M; Lent, Cheryl
Tooth wear is generally an age-related phenomenon, often assumed to occur at similar rates within populations of primates and other mammals, and has been suggested as a correlate of reduced offspring survival among wild lemurs. Few long-term wild studies have combined detailed study of primate behavior and ecology with dental analyses. Here, we present data on dental wear and tooth loss in older (>10 years old) wild and captive ring-tailed lemurs (Lemur catta). Among older ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar (n=6), the percentage of severe dental wear and tooth loss ranges from 6 to 50%. Among these six individuals, the oldest (19 years old) exhibits the second lowest frequency of tooth loss (14%). The majority of captive lemurs at the Indianapolis Zoo (n=7) are older than the oldest BMSR lemur, yet display significantly less overall tooth wear for 19 of 36 tooth positions, with only two individuals exhibiting antemortem tooth loss. Among the captive lemurs, only one lemur (a nearly 29 year old male) has lost more than one tooth. This individual is only missing anterior teeth, in contrast to lemurs at BMSR, where the majority of lost teeth are postcanine teeth associated with processing specific fallback foods. Postcanine teeth also show significantly more overall wear at BMSR than in the captive sample. At BMSR, degree of severe wear and tooth loss varies in same aged, older individuals, likely reflecting differences in microhabitat, and thus the availability and use of different foods. This pattern becomes apparent before "old age," as seen in individuals as young as 7 years. Among the four "older" female lemurs at BMSR, severe wear and/or tooth loss do not predict offspring survival.
Seiler, Melanie; Schwitzer, Christoph; Gamba, Marco; Holderied, Marc W.
As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect
Rasambainarivo, Fidisoa T; Junge, Randall E
Infections with gastrointestinal parasites may be a major threat to lemurs kept in captivity, as they are a common cause of diarrhea. In this study, fecal egg count patterns and clinical signs associated with gastrointestinal nematodes were assessed for 12 mo in 40 lemurs kept under different husbandry and climatic conditions at two sites in Madagascar. Involved species were black-and-white ruffed lemurs (Varecia variegata), eastern grey bamboo lemurs (Hapalemur griseus), greater bamboo lemurs (Prolemur simus), red-bellied lemurs (Eulemur rubriventer), common brown lemurs (Eulemurfulvus), crowned lemurs (Eulemur coronatus), and Sclater's black lemurs (Eulemur macaco flavifrons). At site 1 (Tsimbazaza Zoological Park), lemurs were kept in small enclosures with daily cleaning of the cement soiling and without routine anthelmintic program, whereas at site 2 (Ivoloina Zoological Park), lemurs received routine anthelmintic prophylaxis and were housed in small enclosure with daily cleaning of sandy soil enclosures. A total of five genera of nematode eggs from the orders Strongylida, Oxyurida, and Enoplida were recovered and identified from 198 out of 240 samples (83%) at site 1 and 79% (189 out of 240) at site 2 with the use of a modified McMaster technique. Significant differences were found for parasites from the order Strongylida between the two sites. The differences may be due to climate conditions and the presumed life cycle of these parasites. No significant differences were found for parasites from the other orders. No significant differences were noted between sexes or between seasons. No clinical signs of parasitic gastroenteritis were seen in either lemur collection.
Elofsson, Rolf; Kröger, Ronald H H
The skin of the lemur nose tip (rhinarium) has arterioles in the outer vascular plexus that are endowed with an unusual coat of smooth muscle cells. Comparison with the arterioles of the same area in a number of unrelated mammalians shows that the lemur pattern is unique. The vascular smooth muscle cells belong to the synthetic type. The function of synthetic smooth muscles around the terminal vessels in the lemur rhinarium is unclear but may have additional functions beyond regulation of vessel diameter.
Regaiolli, Barbara; Spiezio, Caterina; Hopkins, William D
Assessing manual lateralization in non-human primates could be an optimal way to understand the adaptive value of this asymmetry in humans. Though many studies have investigated hand preferences in Old and New World monkeys and apes, fewer studies have considered manual lateralization in strepsirrhines, especially in experimental tasks. This study investigated hand preferences for a unimanual and a bimanual task of 17 captive ring-tailed lemurs (Lemur catta), housed at Parco Natura Viva (VR), Italy. The effect of age on handedness has been also investigated. The lemurs were tested on a unimanual task, in which subjects were restricted to using one hand to retrieve the food inside an apparatus, and on a bimanual task, in which lemurs had to use one hand to keep the apparatus door open while reaching with the other hand to retrieve the food inside it. At the population-level, our results revealed an asymmetrical hand use distribution, in particular a bias toward a right hand preference for food reaching in both the unimanual and the bimanual tasks. Furthermore, at the individual-level, the bimanual task seems to elicit a greater hand preference than the unimanual task. Results of this study underline the importance of experimental tasks in determining hand preference in strepsirrhines. Furthermore, as bimanual tasks elicited a stronger degree of lateralization, they appear to be more suited to investigate manual laterality. Finally, findings from this study highlight the presence of a right hand preference in ring-tailed lemurs, shedding new light on the evolution of human right handedness. Am. J. Primatol. 78:851-860, 2016. © 2016 Wiley Periodicals, Inc. © 2016 Wiley Periodicals, Inc.
Cuozzo, Frank P; Head, Brian R; Sauther, Michelle L; Ungar, Peter S; O'Mara, M Teague
Ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve (BMSR), Madagascar display a high frequency of individuals with notable and sometimes extreme tooth wear. Adult lemurs display a range of tooth wear even among individuals of the same age, but we do not know at what age this variation first appears. This study's goal was to determine whether wear variation occurs in younger wild lemurs. Based on the decade-long study of ring-tailed lemur feeding and dental ecology at BMSR, we hypothesized that younger, natal lemurs (under 5 years of age), would display variation in their degree of tooth wear that would correspond to microhabitat differences, given differences in food availability in different troops' home ranges. We also hypothesized that wear would differ between sexes at this young age, given differences in feeding between males and females in this population. Hypotheses were tested using dental topographic analyses using dental impressions collected from known-aged lemurs across 10 years at BMSR. Results illustrate significant differences in wear-related tooth topography (i.e., relief and slope, presented here as "occlusal lift") for microhabitat, sex and troop affiliation among lemurs under 5 years of age in this population. Although, all lemurs in this population consume mechanically challenging tamarind fruit, those in more disturbed habitats eat additional introduced foods, some of which are also mechanically challenging. Thus, dietary variation is the likely cause of variation in tooth wear. The wear variation we show at a young age suggests caution when assigning age based on tooth wear in living and fossil primates. These wear-related tooth shape changes early in life, which reflects sex, habitat variation and levels of anthropogenic disturbance, may potentially impact reproductive fitness later in life. © 2014 Wiley Periodicals, Inc.
Fish, Krista D; Sauther, Michelle L; Loudon, James E; Cuozzo, Frank P
Coprophagy occurs in a number of animal species, including nonhuman primates. During the 2003-2004 dry seasons at the Beza Mahafaly Special Reserve, Madagascar, we observed wild ring-tailed lemurs (Lemur catta) consuming dried fecal matter from three different species. Ring-tailed lemurs consumed human feces on 12 occasions, cattle feces twice, and feral dog feces once. Coprophagy in this population may be a behavioral adaptation that provides animals access to energy and nutrients and may be an important nutritional source for older, and/or dentally impaired individuals during the dry season. (c) 2007 Wiley-Liss, Inc.
Weisrock, David W.; Rasoloarison, Rodin M.; Fiorentino, Isabella; Ralison, José M.; Goodman, Steven M.; Kappeler, Peter M.; Yoder, Anne D.
Background Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters—including morphological differences, reproductive isolation, and gene tree monophyly—that are typically used as evidence for separately evolving lineages. Methodology In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed. Conclusions The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa
Kappeler, Peter M
Recent comparative analyses reached contradictory conclusions about the evolutionary origins of social monogamy in primates and other mammals, but they ignored variation in social bond quality between pair-partners. Recent field studies of Malagasy primates (lemurs) with variable intersexual bonds indicate independent evolutionary transitions to pair-living from solitary and group-living ancestors, respectively, as well as four cumulative steps in evolutionary transitions from a solitary life style to pair-living that resolve some contradictory results of previous studies.
Mertl-Millhollen, Anne S
Because ring-tailed lemurs (Lemur catta) are a female-dominant, female-philopatric species in which the females provide the majority of parental care and troop defense, resource defense is a possible function of female lemur scent marking. To test this hypothesis, I conducted three studies. First, I presented captive, individually housed females with a series of samples of female scent, each from a different female, to determine whether they would respond to those samples and discriminate between them. Second, I reanalyzed data from a focal animal study of four females in two adjacent troops in Berenty Reserve, Madagascar, to determine female marking rates before, during, and after the mating season, and to clarify the relationship among positions of feeding, intertroop defense, and scent marking. The third study was based on ad libitum observations of the sniffing and marking behavior of a troop in Berenty Reserve during a year when they traveled far out of their home range. The females in study 1 investigated female scent samples but provided no evidence that they discriminated between them. In study 2 the wild females marked throughout the study and did not limit their marking to the mating season. They deposited significantly more of their marks in a zone of confrontation with adjacent troops, where they also did the majority of their feeding, and they increased their rate of marking during agonistic intertroop confrontations. The females determined the positions of their scent marks and deposited the first mark in the majority of countermarking sequences. When the females traveled out of their defended range in study 3, they significantly decreased their rate of marking and increased their rate of sniffing spots but not marking them. All evidence gathered so far supports the hypothesis that one function of female ring-tailed lemur scent marking is to provide intergroup information that is then used to reinforce the border of the defended resource.
Gudde, Renske; Venditti, Chris
Conservation planning is important to protect species from going extinct now that natural habitats are decreasing owing to human activity and climate change. However, there is considerable controversy in choosing appropriate metrics to weigh the value of species and geographic regions. For example, the added value of phylogenetic conservation-selection criteria remains disputed because high correlations between them and the nonphylogenetic criteria of species richness have been reported. We evaluated the commonly used conservation metrics species richness, endemism, phylogenetic diversity (PD), and phylogenetic endemism (PE) in a case study on lemurs of Madagascar. This enabled us to identify the conservation target of each metric and consider how they may be used in future conservation planning. We also devised a novel metric that uses a phylogeny scaled according to the rate of phenotypic evolution as a proxy for a species' ability to adapt to change. High rates of evolution may indicate generalization or specialization. Both specialization and low rates of evolution may result in an inability to adapt to changing environments. We examined conservation priorities by using the inverse of the rate of body mass evolution to account for species with low rates of evolution. In line with previous work, we found high correlations among species richness and PD (r = 0.96), and endemism and PE (r = 0.82) in Malagasy lemurs. Phylogenetic endemism in combination with rates of evolution and their inverse prioritized grid cells containing highly endemic and specialized lemurs at risk of extinction, such as Avahi occidentalis and Lepilemur edwardsi, 2 endangered lemurs with high rates of phenotypic evolution and low-quality diets, and Hapalemur aureus, a critically endangered species with a low rate of body mass evolution and a diet consisting of very high doses of cyanide.
The lemurs of Madagascar represent a spectacular example of adaptive radiation among primates. Given the special setting under which they evolved (i.e. long isolation, geographical location, geological relief), they provide excellent models for study in many realms, and at different levels and scales, including diversity. At the same time, they occur in a 'hottest hot spot' region for biodiversity conservation. Although there is no single definition of biodiversity, the most commonly used units to measure biodiversity are species-species richness, species abundance and, for conservation purposes in particular, species endemism. However, what a species actually is or how, precisely, it should be defined are unresolved issues. Many species concepts have been proposed and several have been used in primatology in recent years. Nowadays, one of the more common approaches to measuring diversity, and eventually inferring species status, is to look at genetic diversity as reflected by mitochondrial DNA differences. Not enough attention has been paid, however, to the different levels at which genetic differences may occur. Lemurs provide instructive examples to highlight the questions involved in species recognition and definition. Using lemurs as examples, I will highlight the strengths and limitations of some analytical tools, including phylogeography and cladistic biogeography and, I will, in particular, emphasize the questions arising at the interface of scientific and conservation perceptions, both of which influence decisions in the field of biodiversity preservation. Copyright 2007 S. Karger AG, Basel.
Hayes, Corinne E.; Williams, Cathy V.; Junge, Randall E.; Razafindramanana, Josia; Mass, Vanessa; Rakotondrainibe, Hajanirina; Yoder, Anne D.
Zoonotic diseases are a looming threat to global populations, and nearly 75% of emerging infectious diseases can spread among wildlife, domestic animals and humans. A ‘One World, One Health’ perspective offers us an ideal framework for understanding and potentially mitigating the spread of zoonoses, and the island of Madagascar serves as a natural laboratory for conducting these studies. Rapid habitat degradation and climate change on the island are contributing to more frequent contact among humans, livestock and wildlife, increasing the potential for pathogen spillover events. Given Madagascar's long geographical isolation, coupled with recent and repeated introduction of agricultural and invasive species, it is likely that a number of circulating pathogens remain uncharacterized in lemur populations. Thus, it is imperative that new approaches be implemented for de novo pathogen discovery. To this end, we used non-targeted deep sequencing of blood transcriptomes from two species of critically endangered wild lemurs (Indri indri and Propithecus diadema) to characterize blood-borne pathogens. Our results show several undescribed vector-borne parasites circulating within lemurs, some of which may cause disease in wildlife, livestock and humans. We anticipate that advanced methods for de novo identification of unknown pathogens will have broad utility for characterizing other complex disease transmission systems. PMID:26814226
von Engelhardt, N; Kappeler, P M; Heistermann, M
Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are influenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and conflict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming effects for a complete understanding of this phenomenon. PMID:11007329
Li, Bo; Zhao, Bo; Yang, Guang-You; Wang, Qiang; Niu, Li-Li; Deng, Jia-Bo; Gu, Xiao-Bin; Wang, Shu-Xian
The present study was conducted to evaluate the effectiveness of mebendazole in the treatment of Hymenolepis nana infection in ring-tailed lemurs (Lemur catta). Ten (L. catta) from the Chengdu Zoological Garden in China, which were naturally infected with H. nana, were treated with mebendazole (10 mg/kg for 5 days). A posttreatment fecal examination was conducted 10 and 20 days after the start of treatment. All treatments resulted in a decrease in the number of eggs per gram in the posttreatment sample compared with the pretreatment sample. Reduction of mean egg count was 97.6% and 100% on days 10 and 20, respectively. The results indicated that mebendazole has marked efficacy against H. nana infections in L. catta.
O'Neill, Matthew C; Schmitt, Daniel
Most primates, including lemurs, have a broad range of locomotor capabilities, yet much of the time, they walk at slow speeds and amble, canter or gallop at intermediate and fast speeds. Although numerous studies have investigated limb function during primate quadrupedalism, how the center of mass (COM) moves is not well understood. Here, we examined COM energy, work and power during walking, cantering and galloping in ring-tailed lemurs, Lemur catta (N=5), over a broad speed range (0.43-2.91 m s(-1)). COM energy recoveries were substantial during walking (35-71%) but lower during canters and gallops (10-51%). COM work, power and collisional losses increased with speed. The positive COM works were 0.625 J kg(-1) m(-1) for walks and 1.661 J kg(-1) m(-1) for canters and gallops, which are in the middle range of published values for terrestrial animals. Although some discontinuities in COM mechanics were evident between walking and cantering, there was no apparent analog to the trot-gallop transition across the intermediate and fast speed range (dimensionless v>0.75, Fr>0.5). A phenomenological model of a lemur cantering and trotting at the same speed shows that canters ensure continuous contact of the body with the substrate while reducing peak vertical COM forces, COM stiffness and COM collisions. We suggest that cantering, rather than trotting, at intermediate speeds may be tied to the arboreal origins of the Order Primates. These data allow us to better understand the mechanics of primate gaits and shed new light on primate locomotor evolution.
Gardner, Charlie J; Jasper, Louise D
The species-level diversity of Madagascar's lemurs has increased hugely over the last two decades, growing from 32 species in 1994 to 102 species in 2014. This growth is primarily due to the application of molecular phylogenetic analyses and the phylogenetic species concept to known populations, and few previously unknown lemur populations have been discovered during this time. We report on a new population of dwarf lemurs (Cheirogaleus sp.) from Nosy Hara, a 312-ha island in far northern Madagascar, which constitutes the northernmost distribution record for the genus. The dwarf lemurs appeared to show two characteristics of island populations-insular dwarfism and predator naïveté-that suggest a long isolation, and may thus represent an undescribed taxon. If this is the case, the dwarf lemurs of Nosy Hara are probably one of the rarest primate taxa on Earth.
Makungu, M; Groenewald, H B; du Plessis, W M; Barrows, M; Koeppel, K N
In family Lemuridae, anatomical variations exist. Considering its conservation status (near threatened) and presence of similarities between strepsirrhines and primitive animals, it was thought to be beneficial to describe the gross osteology and radiographic anatomy of the pelvis and hind limb of ring-tailed lemurs (Lemur catta) as a reference for clinical use and species identification. Radiography was performed in 14 captive adult ring-tailed lemurs. The radiographic findings were correlated with bone specimens from two adult animals. Additionally, computed tomography of the hind limbs was performed in one animal. The pelvic bone has a well-developed caudal ventral iliac spine. The patella has a prominent tuberosity on the cranial surface. The first metatarsal bone and digit 1 are markedly stouter than the other metatarsal bones and digits with medial divergence from the rest of the metatarsal bones and digits. Ossicles were seen in the lateral meniscus, inter-phalangeal joint of digit 1 and in the infrapatellar fat pad. Areas of mineral opacity were seen within the external genitalia, which are believed to be the os penis and os clitoris. Variations exist in the normal osteology and radiographic appearance of the pelvis and hind limb of different animal species. The use of only atlases from domestic cats and dogs for interpretative purposes may be misleading. © 2013 Blackwell Verlag GmbH.
Kistler, Logan; Ratan, Aakrosh; Godfrey, Laurie R; Crowley, Brooke E; Hughes, Cris E; Lei, Runhua; Cui, Yinqiu; Wood, Mindy L; Muldoon, Kathleen M; Andriamialison, Haingoson; McGraw, John J; Tomsho, Lynn P; Schuster, Stephan C; Miller, Webb; Louis, Edward E; Yoder, Anne D; Malhi, Ripan S; Perry, George H
Humans first arrived on Madagascar only a few thousand years ago. Subsequent habitat destruction and hunting activities have had significant impacts on the island's biodiversity, including the extinction of megafauna. For example, we know of 17 recently extinct 'subfossil' lemur species, all of which were substantially larger (body mass ∼11-160 kg) than any living population of the ∼100 extant lemur species (largest body mass ∼6.8 kg). We used ancient DNA and genomic methods to study subfossil lemur extinction biology and update our understanding of extant lemur conservation risk factors by i) reconstructing a comprehensive phylogeny of extinct and extant lemurs, and ii) testing whether low genetic diversity is associated with body size and extinction risk. We recovered complete or near-complete mitochondrial genomes from five subfossil lemur taxa, and generated sequence data from population samples of two extinct and eight extant lemur species. Phylogenetic comparisons resolved prior taxonomic uncertainties and confirmed that the extinct subfossil species did not comprise a single clade. Genetic diversity estimates for the two sampled extinct species were relatively low, suggesting small historical population sizes. Low genetic diversity and small population sizes are both risk factors that would have rendered giant lemurs especially susceptible to extinction. Surprisingly, among the extant lemurs, we did not observe a relationship between body size and genetic diversity. The decoupling of these variables suggests that risk factors other than body size may have as much or more meaning for establishing future lemur conservation priorities. Copyright © 2014 Elsevier Ltd. All rights reserved.
Yabsley, Michael J; Jordan, Carly N; Mitchell, Sheila M; Norton, Terry M; Lindsay, David S
In the current study, we determined the seroprevalence of Toxoplasma gondii, Sarcocystis neurona, and Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, Georgia. Serum samples were tested from 52 ring-tailed lemurs (Lemur catta), six blue-eyed black lemurs (Eulemur macaco flavifrons), and four black and white ruffed lemurs (Varecia variegata variegata) using an agglutination assay. Three ring-tailed lemurs (5.8%) were positive for T. gondii (titer of 1:50); one ring-tailed lemur (1.9%) and one black and white ruffed lemur (25%) were positive for S. neurona (titers of 1:1000); and one ring-tailed lemur (1.9%) was positive for E. cuniculi (titer of 1:400). All blue-eyed black lemurs were negative for antibodies to T. gondii, S. neurona, and E. cuniculi. This is the first detection of antibodies to T. gondii in ring-tailed lemurs and antibodies to S. neurona and E. cuniculi in any species of prosimian.
Botting, Jennifer L; Wiper, Mallory L; Anderson, James R
Whilst the ability to follow human gaze has been demonstrated in monkeys and apes, there is little evidence that prosimians share this ability. The current study used a food choice paradigm to assess whether captive brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human gaze direction as a cue when choosing between an attending or non-attending human. Four experiments assessed the use of body, head and eye cues by the lemurs. In experiment 1, the non-attending human stood with her back to a food item; 3 of the 5 lemurs preferentially chose the attending human with an equivalent food item in view. In experiments 2 and 3, which used head angles of 90°, 4 out of 5 lemurs preferentially chose the attending human. In experiment 4, in which the humans differed only by whether their eyes were open or shut, no significant preferences were found. This study provides the first tentative evidence that lemurs are capable of discriminating human gaze direction and can use both body and head direction to do so. Copyright © 2011 S. Karger AG, Basel.
Lovegrove, Barry G; Canale, Cindy; Levesque, Danielle; Fluch, Gerhard; Reháková-Petrů, Milada; Ruf, Thomas
There is some urgency in the necessity to incorporate physiological data into mechanistic, trait-based, demographic climate change models. Physiological responses at the individual level provide the mechanistic link between environmental changes and individual performances and hence population dynamics. Here we consider the causal relationship between ambient temperature (Ta) and metabolic rate (MR), namely, the Arrhenius effect, which is directly affected by global warming through increases in average global air temperatures and the increase in the frequency and intensity of extreme climate events. We measured and collated data for several small, free-ranging tropical arboreal mammals and evaluated their vulnerability to Arrhenius effects and putative heat stress associated with climate change. Skin temperatures (Tskin) were obtained from free-ranging tarsiers (Tarsius syrichta) on Bohol Island, Philippines. Core body temperature (Tb) was obtained from the greater hedgehog tenrec (Setifer setosus) and the gray brown mouse lemur (Microcebus ravelobensis) from Ankarafantsika, Madagascar. Tskin for another mouse lemur, Microcebus griseorufus, was obtained from the literature. All four species showed evidence of hyperthermia during the daytime rest phase in the form of either Tskin or Tb that was higher than the normothermic Tb during the nighttime active phase. Potentially, tropical arboreal mammals with the lowest MRs and Tb, such as tarsiers, are the most vulnerable to sustained heat stress because their Tb is already close to Ta. Climate change may involve increases in MRs due to Arrhenius effects, especially during the rest phase or during torpor and hibernation. The most likely outcome of increased Arrhenius effects with climate change will be an increase in energy expenditure at the expense of other critical functions such as reproduction or growth and will thus affect fitness. However, we propose that these hypothetical Arrhenius costs can be, and in some
Lewis, Kerrie P; Jaffe, Sarah; Brannon, Elizabeth M
A wealth of data demonstrating that monkeys and apes represent number have been interpreted as suggesting that sensitivity to number emerged early in primate evolution, if not before. Here we examine the numerical capacities of the mongoose lemur (Eulemur mongoz), a member of the prosimian suborder of primates that split from the common ancestor of monkeys, apes and humans approximately 47-54 million years ago. Subjects observed as an experimenter sequentially placed grapes into an opaque bucket. On half of the trials the experimenter placed a subset of the grapes into a false bottom such that they were inaccessible to the lemur. The critical question was whether lemurs would spend more time searching the bucket when food should have remained in the bucket, compared to when they had retrieved all of the food. We found that the amount of time lemurs spent searching was indicative of whether grapes should have remained in the bucket, and furthermore that lemur search time reliably differentiated numerosities that differed by a 1:2 ratio, but not those that differed by a 2:3 or 3:4 ratio. Finally, two control conditions determined that lemurs represented the number of food items, and neither the odor of the grapes, nor the amount of grape (e.g., area) in the bucket. These results suggest that mongoose lemurs have numerical representations that are modulated by Weber's Law.
Tromp, D; Meunier, H; Roeder, J J
When confronted with tasks involving reasoning instead of simple learning through trial and error, lemurs appeared to be less competent than simians. Our study aims to investigate lemurs' capability for transitive inference, a form of deductive reasoning in which the subject deduces logical conclusions from preliminary information. Transitive inference may have an adaptative function, especially in species living in large, complex social groups and is proposed to play a major role in rank estimation and establishment of dominance hierarchies. We proposed to test the capacities of reasoning using transitive inference in two species of lemurs, the brown lemur (Eulemur fulvus) and the black lemur (Eulemur macaco), both living in multimale-multifemale societies. For that purpose, we designed an original setup providing, for the first time in this kind of cognitive task, pictures of conspecifics' faces as stimuli. Subjects were trained to differentiate six photographs of unknown conspecifics named randomly from A to F to establish the order A > B > C > D > E > F and select consistently the highest-ranking photograph in five adjacent pairs AB, BC, CD, DE, and EF. Then lemurs were presented with the same adjacent pairs and three new and non-adjacent pairs BD, BE, CE. The results showed that all subjects correctly selected the highest-ranking photograph in every non-adjacent pair, reflecting lemurs' capacity for transitive inference. Our results are discussed in the context of the still debated current theories about the mechanisms underlying this specific capacity.
Cuozzo, Frank P; Sauther, Michelle L; Yamashita, Nayuta; Lawler, Richard R; Brockman, Diane K; Godfrey, Laurie R; Gould, Lisa; Youssouf, Ibrahim Antho Jacky; Lent, Cheryl; Ratsirarson, Joelisoa; Richard, Alison F; Scott, Jessica R; Sussman, Robert W; Villers, Lynne M; Weber, Martha A; Willis, George
Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad
Sclafani, Valentina; Norscia, Ivan; Antonacci, Daniela; Palagi, Elisabetta
Scratching has been successfully used to detect anxiety, a proxy for stress, in primates, from strepsirrhines to Homo sapiens. Here, we investigated the fluctuation of scratching in Lemur catta during the mating season. In particular we evaluated whether scratching (1) varied according to sex and rank differences, (2) increased in the period of maximum stress (around the mating days), and (3) was reduced by grooming. At Berenty (South Madagascar), we followed two lemur groups (23 adult/subadult individuals) and gathered data on self-scratching, aggression, and grooming. Based on perineal area features, we recognized two periods: low swelling (LS), with no estrus female, and high swelling (HS), when at least one female was in estrus. We predicted that aggressive behaviors and anxiety-related scratching would covary. Indeed, scratching peaked in HS, when aggression was also highest. In agreement with previous literature, this result suggests that conflicts around estrus days may raise anxiety levels in the social group. We expected scratching levels to be highest in males because they aggressively compete for females and are subject to mate choice and repeated attacks by dominant females. Instead, the scratching rates were similar in males and females, probably because the high competition, which involves both sexes, dampened intersexual differences. In contrast to our prediction, scratching was not rank dependent, probably because animal ranking positions changed from LS to HS. Finally, we showed that, in ring-tailed lemurs, as well as in other primates, scratching decreases after reciprocal grooming in both periods. This finding provides the first evidence that grooming could assist in reducing anxiety in strepsirrhines.
Bradley, Brenda J; Pedersen, Anja; Mundy, Nicholas I
Almost all mammals have brown or darkly-pigmented eyes (irises), but among primates, there are some prominent blue-eyed exceptions. The blue eyes of some humans and lemurs are a striking example of convergent evolution of a rare phenotype on distant branches of the primate tree. Recent work on humans indicates that blue eye color is associated with, and likely caused by, a single nucleotide polymorphism (rs12913832) in an intron of the gene HERC2, which likely regulates expression of the neighboring pigmentation gene OCA2. This raises the immediate question of whether blue eyes in lemurs might have a similar genetic basis. We addressed this by sequencing the homologous genetic region in the blue-eyed black lemur (Eulemur macaco flavifrons; N = 4) and the closely-related black lemur (Eulemur macaco macaco; N = 4), which has brown eyes. We then compared a 166-bp segment corresponding to and flanking the human eye-color-associated region in these lemurs, as well as other primates (human, chimpanzee, orangutan, macaque, ring-tailed lemur, mouse lemur). Aligned sequences indicated that this region is strongly conserved in both Eulemur macaco subspecies as well as the other primates (except blue-eyed humans). Therefore, it is unlikely that this regulatory segment plays a major role in eye color differences among lemurs as it does in humans. Although convergent phenotypes can sometimes come about via the same or similar genetic changes occurring independently, this does not seem to be the case here, as we have shown that the genetic basis of blue eyes in lemurs differs from that of humans.
Elofsson, Rolf; Kröger, Ronald H H
The skin of the lemur nose tip (rhinarium) has arterioles in the outer vascular plexus that are endowed with an unusual coat of smooth muscle cells. Comparison with the arterioles of the same area in a number of unrelated mammalians shows that the lemur pattern is unique. The vascular smooth muscle cells belong to the synthetic type. The function of synthetic smooth muscles around the terminal vessels in the lemur rhinarium is unclear but may have additional functions beyond regulation of vessel diameter. PMID:28260706
Collins, Courtney; Corkery, Ilse; Haigh, Amy; McKeown, Sean; Quirke, Thomas; O'Riordan, Ruth
The effect of the zoo environment on captive animals is an increasingly studied area of zoo research, with visitor effects and exhibit design recognized as two of the factors that can contribute to animal welfare in captivity. It is known that in some situations, visitors may be stressful to zoo-housed primates, and this may be compounded by environmental factors such as the weather, the time of day, and zoo husbandry routines. Exhibit design and proximity of the public are also known to influence behavioral response of primates to visitors; however, there is minimal research on free-ranging zoo animals, even though they are potentially subjected to intense interactions with visitors. The current study explores the effect of the zoo environment, several visitor variables and specific animal-visitor interactions on the behavior of free-ranging ring-tailed lemurs (Lemur catta) at Fota Wildlife Park, Ireland. Data were obtained through scan samples collected over 18 months (n = 12,263) and analyzed using a range of statistical tests, including general estimating equations (GEE). Results demonstrate that the free-ranging lemurs' behavior at Fota Wildlife Park is affected by season, weather and time of day. Similarities in feeding behavior exist between the free-ranging group and lemurs in the wild when resources are plentiful. Visitor variables had a limited effect on lemur behavior and behavioral diversity level. Lemurs rarely reacted to visitors when specific interactions were considered. Generally, the results indicate that the ring-tailed lemurs in this study have adapted well to the zoo environment and habituated to visitors. © 2017 Wiley Periodicals, Inc.
Millette, James B; Sauther, Michelle L; Cuozzo, Frank P
Severe dental wear and tooth loss is often assumed to impede the processing, breakdown, and energetic conversion of food items, thereby negatively impacting individual health, reproduction, and survival. Ring-tailed lemurs at the Beza Mahafaly Special Reserve demonstrate exceptionally high frequencies of severe dental wear and antemortem tooth loss, yet often survive multiple years with these impairments. To test the hypothesis that these lemurs mitigate tooth loss through behavioral adjustments, we collected 191 h of observational data from 16 focal subjects, eight without tooth loss and eight with between 3% and 44% loss. These data indicate dentally-impaired ring-tailed lemurs show compensatory behaviors consistent with the demands of living in a social group. During early afternoon (12:00-14:30 h) individuals with loss showed trends towards higher frequencies of foraging and grooming, while individuals without loss rested significantly more often. Individuals with >10% loss (n = 7) showed higher frequencies of feeding, foraging, and grooming, and lower frequencies of resting during this period than individuals with <10% loss (n = 9). Individuals with tooth loss maintained relatively higher levels of feeding and foraging throughout the day. These individuals licked tamarind fruit at higher frequencies, likely spending more time softening it before ingestion. These individuals did not demonstrate longer feeding bouts overall, although bouts involving tamarinds were significantly longer. Individuals with marked toothcomb wear engaged in higher rates of certain types of allogrooming, demonstrating that social behaviors are used to compensate for reduced grooming efficiency. These data have implications for interpreting behavioral responses to dental impairment in the fossil record. Copyright 2009 Wiley-Liss, Inc.
Villers, Lynne M; Jang, Spencer S; Lent, Cheryl L; Lewin-Koh, Sock-Cheng; Norosoarinaivo, Jeanne Aimée
A survey to identify the major intestinal species of aerobic bacteria, protozoa and helminths was conducted on captive and wild populations of ring-tailed lemurs (Lemur catta). Samples were collected from 50 captive lemurs at 11 zoological institutions in the United States. In Madagascar, 98 aerobic bacteria samples and 99 parasite samples were collected from eight sites chosen to cover a variety of populations across the species range. Identical collection, preservation and lab techniques were used for captive and wild populations. The predominant types of aerobic bacteria flora were identified via five separate tests. The tests for parasites conducted included flotation, sedimentation and FA/GC. Twenty-seven bacteria unique to either the captive or wild populations were cultured with eight of these being statistically significantly different. Fourteen bacteria common to both populations were cultured, of which six differed significantly. Entamoeba coli was the only parasite common to both the captive and wild populations. Giardia spp., Isospora spp., strongyles-type ova, Entamoeba spp. and Entamoeba polecki were found only in captive samples. Cryptosporidium, Balantidium coli, pinworm-type ova, and two fluke-like ova were seen only in wild samples. In addition, samples were compared for both bacteria and parasites from three unique field sites in Madagascar. In this three-site comparison, six types of bacteria were statistically significantly different. No significant differences regarding parasites were seen. Significant differences were found between the captive and wild populations, whereas fewer differences were found between sites within Madagascar. Although we isolated Campylobacter and Giardia, all animals appeared clinically healthy. (c) 2007 Wiley-Liss, Inc.
Huebner, Franziska; Fichtel, Claudia
Innovations and problem-solving abilities can provide animals with important ecological advantages as they allow individuals to deal with novel social and ecological challenges. Innovation is a solution to a novel problem or a novel solution to an old problem, with the latter being especially difficult. Finding a new solution to an old problem requires individuals to inhibit previously applied solutions to invent new strategies and to behave flexibly. We examined the role of experience on cognitive flexibility to innovate and to find new problem-solving solutions with an artificial feeding task in wild redfronted lemurs (Eulemur rufifrons). Four groups of lemurs were tested with feeding boxes, each offering three different techniques to extract food, with only one technique being available at a time. After the subjects learned a technique, this solution was no longer successful and subjects had to invent a new technique. For the first transition between task 1 and 2, subjects had to rely on their experience of the previous technique to solve task 2. For the second transition, subjects had to inhibit the previously learned technique to learn the new task 3. Tasks 1 and 2 were solved by most subjects, whereas task 3 was solved by only a few subjects. In this task, besides behavioral flexibility, especially persistence, i.e., constant trying, was important for individual success during innovation. Thus, wild strepsirrhine primates are able to innovate flexibly, suggesting a general ecological relevance of behavioral flexibility and persistence during innovation and problem solving across all primates.
Loudon, James E; Sponheimer, Matt; Sauther, Michelle L; Cuozzo, Frank P
Stable carbon and nitrogen isotope compositions were analyzed from hair samples of 30 sympatric ring-tailed lemurs (Lemur catta) inhabiting the Beza Mahafaly Special Reserve, Madagascar. All lemurs were known individuals involved in a longitudinal study, which allowed us to explore the degree to which group membership, sex, health status, and migration influenced their stable isotope compositions. The differences in delta(13)C and delta(15)N values between groups were small (<1.5 per thousand) but highly significant. In fact, each group was tightly clustered, and discriminant function analysis of the stable isotope data assigned individuals to the group in which they were originally collared with over 90% accuracy. In general, the differences between groups reflected the degree to which they utilized forested versus open habitats. As open habitats at Beza Mahafaly often correspond to areas of anthropogenic disturbance, these data suggest that isotopic data can be useful for addressing questions of lemur conservation. There were few sex differences, but significant differences did occur between individuals of normal and suboptimal health, with those in poor health (especially those in the worst condition) being enriched in (15)N and to a lesser degree (13)C compared with healthy individuals. Moreover, lemurs that had emigrated between 2003 and 2004 had different delta(13)C and delta(15)N compositions than their original groups. (c) 2007 Wiley-Liss, Inc.
Sasaki, E; Tokiwa, T; Tsugo, K; Higashi, Y; Hori, H; Une, Y
We describe the development of neurological signs in four juvenile black-and-white ruffed lemurs (Varecia variegate), housed at a petting zoo in Japan. The clinical course was severe, with three lemurs dying within 1 day of the appearance of clinical signs. The other lemur was treated and survived. Pathological analyses demonstrated meningitis and the presence of gram-negative bacilli in the cerebrum, cerebellum, palatine tonsil and liver. Klebsiella pneumoniae was isolated from the brain of all of the dead lemurs. Multilocus sequence typing analysis showed that all the isolates were sequence type 86 (ST86). To our knowledge, this is the first determination of K. pneumoniae infection in ruffed lemurs of this genus. K. pneumoniae infection may represent a risk to lemurs and people who come into contact with infected animals. Copyright © 2017 Elsevier Ltd. All rights reserved.
Raharison, Fidiniaina; Bourges Abella, Nathalie; Sautet, Jean; Deviers, Alexandra; Mogicato, Giovanni
The medical care currently to brown lemurs (Eulemur fulvus) is limited by a lack of knowledge of their anatomy. The aim of this study was to describe the anatomy and histology and obtain ultrasonographic measurements of normal adrenal glands in these animals. The adrenal glands of four lemurs cadavers were used for the anatomical and histological studies, and those of 15 anesthetized lemurs were examined by ultrasonography. Anatomically, the adrenal glands of brown lemurs are comparable to those of other species. The histological findings showed that the cortex is organized into three distinct layers, whereas most domestic mammals have an additional zone. The surface area of the adrenal glands increased with body weight, and the area of the right adrenal was slightly larger than the left. We suggest using ultrasonography to aid the etiological diagnosis of behavioral abnormalities that might be due to dysfunctions of the adrenal gland. © 2017 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
A functional analysis was conducted to assess the antecedent and reinforcing conditions underlying aggressive behavior in a female lemur in captivity. Results showed that her aggression was primarily the result of human attention. A replacement behavior-training program was introduced, and the lemur's aggression was successfully eliminated. These results demonstrate the utility of using functional assessment and analyses in zoos with captive wild nonhuman animals.
Donati, Giuseppe; Kesch, Kristina; Ndremifidy, Kelard; Schmidt, Stacey L.; Ramanamanjato, Jean-Baptiste; Borgognini-Tarli, Silvana M.; Ganzhorn, Joerg U.
Background Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce. Methodology/Principal Findings Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees. Conclusions/Significance Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for
De Liberato, Claudio; Berrilli, Federica; Meoli, Roberta; Friedrich, Klaus G; Di Cerbo, Pilar; Cocumelli, Cristiano; Eleni, Claudia
A case of fatal infection caused by larval forms of Taenia martis in a ring-tailed lemur (Lemur catta) living in the Rome zoological garden is described. The animal, living in a semi-natural pen with other 15 conspecific individuals and being fed with fresh fruit and vegetables, yoghurt and eggs, was transported to the Istituto Zooprofilattico of Rome for post-mortem examination. The anamnesis included, ten days before the death, apathy, lack of appetite, abdominal distension and diarrhoea. A severe exudative fibrinous-purulent peritonitis with numerous adhesions between the abdominal wall and the bowel loops was detected. After intestine removal, two free and viable, 4 cm long, whitish, leaf-like parasitic forms were pinpointed. Macroscopic examination of the two parasites allowed their identification as larval stages of cestodes, identified via molecular analysis as T. martis metacestodes. This report represents the first record of T. martis infection in the host species and in a zoological garden and for the pathological relevance of the infection.
Distinctive cues are predicted to evolve when the benefits obtained by the recognition process overcome its costs. When individual recognition is particularly beneficial for both senders and receivers, the expression of strongly distinctive signals is predicted to evolve. On the other hand, it could be predicted that each individual should show a very stable individual signature. In the same perspective, a great stability of the individual signatures could be expected. Lemur catta is the first non-human primate in which olfactory individual recognition has been demonstrated on the basis of the specialized brachial gland secretions. In this paper, I performed gas chromatograph analyses of right and left gland samples collected in two different periods (breeding and non-breeding seasons) from seven males. The aim was to verify if a diversification in such cues, already demonstrated at the inter-individual level, also occurs at the intra-individual level between left and right glands. I verified, by discriminant analysis and chemical distance comparisons, that each gland of each lemur has its particular signature that is maintained through time. Moreover, such diversification resulted so marked to make the overall intra-individual chemical differences similar to/as strong as the inter-individual ones. Since in rodents several odors from different glands may be integrated in individual recognition, I suggest that bilateral diversification in L. catta scents may offer an enhanced distinctiveness that could provide benefits in mate choice and social relationships.
Distinctive cues are predicted to evolve when the benefits obtained by the recognition process overcome its costs. When individual recognition is particularly beneficial for both senders and receivers, the expression of strongly distinctive signals is predicted to evolve. On the other hand, it could be predicted that each individual should show a very stable individual signature. In the same perspective, a great stability of the individual signatures could be expected. Lemur catta is the first non-human primate in which olfactory individual recognition has been demonstrated on the basis of the specialized brachial gland secretions. In this paper, I performed gas chromatograph analyses of right and left gland samples collected in two different periods (breeding and non-breeding seasons) from seven males. The aim was to verify if a diversification in such cues, already demonstrated at the inter-individual level, also occurs at the intra-individual level between left and right glands. I verified, by discriminant analysis and chemical distance comparisons, that each gland of each lemur has its particular signature that is maintained through time. Moreover, such diversification resulted so marked to make the overall intra-individual chemical differences similar to/as strong as the inter-individual ones. Since in rodents several odors from different glands may be integrated in individual recognition, I suggest that bilateral diversification in L. catta scents may offer an enhanced distinctiveness that could provide benefits in mate choice and social relationships.
Ichino, Shinichiro; Soma, Takayo; Miyamoto, Naomi; Chatani, Kaoru; Sato, Hiroki; Koyama, Naoki; Takahata, Yukio
The lifespan and age-specific fecundity of female ring-tailed lemurs (Lemur catta) were estimated from a 24-year longitudinal dataset based on individual identification at Berenty Reserve, Madagascar. The mean lifespan of females in 10-year (1989-1998) birth cohorts was 4.9 ± 4.9 years (n = 77), and the longest recorded lifespan in the population was 20 years. The mortality rate of adult females increased to ≥20% at 10-11 years old and reached 33-50% at 12-15 years old. Although the birth rate of old females (12-17 years old) was 72.0%, slightly lower than that of prime adult females (4-11 years old), i.e. 80.2%, no significant difference was found between them. Half of the females who reached the age of 12 years gave birth in the last year of their life. The oldest mother to give birth was 17 years old. These results suggest that most females can maintain reproductive performance in their later life and that there is no evidence for a postreproductive lifespan in this species.
Wischusen, E W; Ingle, N; Richmond, M E
The rate of digesta passage was measured in five captive Philippine flying lemurs (Cynocephalus volans). These animals were force fed capsules containing known quantities of either particulate or soluble markers. The volumes of the gastrointestinal tracts of three flying lemurs were determined based on the wet weight of the contents of each section of the gut. The mean rate of digesta passage was 14.37 +/- 3.31 h when determined using the particulate marker and 21.9 +/- 0.03 h when determined using the soluble marker. The values based on the particulate marker are between 2% and 10% of similar values for other arboreal folivores. The morphology of the gastrointestinal system of the Philippine flying lemur is similar to that of other hindgut fermenters. Flying lemurs have a simple stomach and a large caecum. The total gut capacity of the Philippine flying lemur is similar to that of other herbivores, but is slightly smaller than that of either the koala (Phascolarctos cinereus), a hindgut fermenter, or the three-toed sloth (Bradypus variegatus), a foregut fermenter. These data suggest that flying lemurs deal with the problems of a folivorous diet very differently than some other arboreal mammals. Phascolarctos cinereus and Bradypus variegatus may represent one extreme with Cynocephalus volans representing the other extreme along a continuum of foraging strategies that are compatible with the arboreal folivore lifestyle.
Rosser, Michael F; Lindemann, Dana M; Barger, Anne M; Allender, Matthew C; Hsiao, Shih-Hsuan; Howes, Mark E
A 5-yr-old, intact male red ruffed lemur ( Varecia rubra ) presented for evaluation as the result of a 1-wk history of lethargy and hyporexia. Physical examination findings included thin body condition, muffled heart sounds, harsh lung sounds, and liquid brown diarrhea. Complete blood count and serum biochemistry showed an inflammatory leukogram, mild hyponatremia, and mild hypochloremia. Orthogonal trunk radiographs revealed a severe alveolar pattern in the right cranial lung lobes with cardiac silhouette effacement. Thoracic ultrasound confirmed a large, hypoechoic mass in the right lung lobes. Fine-needle aspiration of the lung mass and cytology revealed fungal yeast organisms, consistent with Blastomyces dermatitidis. Blastomyces Quantitative EIA Test on urine was positive. Postmortem examination confirmed systemic blastomycosis involving the lung, tracheobronchial lymph nodes, spleen, kidney, liver, cerebrum, and eye. To the authors' knowledge, this is the first report of blastomycosis in a prosimian species.
Kaesler, Eva; Kappeler, Peter M; Brameier, Markus; Demeler, Janina; Kraus, Cornelia; Rakotoniaina, Josué H; Hämäläinen, Anni M; Huchard, Elise
Genes of the Major Histocompatibility Complex (MHC) play a central role in adaptive immune responses of vertebrates. They exhibit remarkable polymorphism, often crossing species boundaries with similar alleles or allelic motifs shared across species. This pattern may reflect parallel parasite-mediated selective pressures, either favouring the long maintenance of ancestral MHC allelic lineages across successive speciation events by balancing selection ('trans-species polymorphism'), or alternatively favouring the independent emergence of functionally similar alleles post-speciation via convergent evolution. Here we investigate the origins of MHC similarity across several species of dwarf and mouse lemurs (Cheirogaleidae). We examined MHC class II variation in two highly polymorphic loci (DRB, DQB) and evaluated the overlap of gut-parasite communities in four sympatric lemurs. We tested for parasite-MHC associations across species to determine whether similar parasite pressures may select for similar MHC alleles in different species. Next, we integrated our MHC data with those previously obtained from other Cheirogaleidae to investigate the relative contribution of convergent evolution and co-ancestry to shared MHC polymorphism by contrasting patterns of codon usage at functional versus neutral sites. Our results indicate that parasites shared across species may select for functionally similar MHC alleles, implying that the dynamics of MHC-parasite co-evolution should be envisaged at the community level. We further show that balancing selection maintaining trans-species polymorphism, rather than convergent evolution, is the primary mechanism explaining shared MHC sequence motifs between species that diverged up to 30 million years ago. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Yamashita, Nayuta; Cuozzo, Frank P; Sauther, Michelle L
Knowledge of dietary mechanical properties can be informative about physical consequences to consumers during ingestion and mastication. In this article, we examine how Tamarindus indica fruits can affect dental morphology in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly special reserve in southwestern Madagascar. Ring-tailed lemurs in tamarind dominated gallery forests exhibit extreme wear and tooth loss on their postcanine dentition that has been related to processing T. indica fruits. We measured and compared mechanical properties of individual food parts in the diet of ring-tailed lemurs in different seasons in 1999-2000, 2008, and 2010. Fracture toughness, hardness, and modulus of foods were measured with a portable mechanical tester. The ripe fruits of T. indica are indeed the toughest and hardest foods ingested by the lemurs. In addition, they are among the largest foods consumed, require high numbers of ingestive bites to process, and are the most frequently eaten by volume. During controlled cutting tests of the ripe fruit shell, multiple runaway side cracks form alongside the cut. Similarly, the lemurs repeatedly bite the ripe shell during feeding and thereby introduce multiple cracks that eventually fragment the shell. Studies of enamel microstructure (e.g., Lucas et al.: BioEssays 30 (2008) 374-385; Campbell et al., 2011) advance the idea that the thin enamel of ring-tailed lemur teeth is susceptible to substantial micro-cracking that rapidly erodes the teeth. We conclude that micro-cracking from repeated loads, in combination with the mechanical and physical properties of the fruit, is primarily responsible for the observed dental damage.
Simmen, Bruno; Bayart, Françoise; Rasamimanana, Hanta; Zahariev, Alexandre; Blanc, Stéphane; Pasquet, Patrick
Background Evolutionary theories that account for the unusual socio-ecological traits and life history features of group-living prosimians, compared with other primates, predict behavioral and physiological mechanisms to conserve energy. Low energy output and possible fattening mechanisms are expected, as either an adaptive response to drastic seasonal fluctuations of food supplies in Madagascar, or persisting traits from previously nocturnal hypometabolic ancestors. Free ranging ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur sp.) of southern Madagascar have different socio-ecological characteristics which allow a test of these theories: Both gregarious primates have a phytophagous diet but different circadian activity rhythms, degree of arboreality, social systems, and slightly different body size. Methodology and Results Daily total energy expenditure and body composition were measured in the field with the doubly labeled water procedure. High body fat content was observed at the end of the rainy season, which supports the notion that individuals need to attain a sufficient physical condition prior to the long dry season. However, ring-tailed lemurs exhibited lower water flux rates and energy expenditure than brown lemurs after controlling for body mass differences. The difference was interpreted to reflect higher efficiency for coping with seasonally low quality foods and water scarcity. Daily energy expenditure of both species was much less than the field metabolic rates predicted by various scaling relationships found across mammals. Discussion We argue that low energy output in these species is mainly accounted for by low basal metabolic rate and reflects adaptation to harsh, unpredictable environments. The absence of observed sex differences in body weight, fat content, and daily energy expenditure converge with earlier investigations of physical activity levels in ring-tailed lemurs to suggest the absence of a relationship between energy
LaFleur, Marni; Sauther, Michelle; Cuozzo, Frank; Yamashita, Nayuta; Jacky Youssouf, Ibrahim Antho; Bender, Richard
Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered "strictly diurnal". We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010-April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25% of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5% of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53% nighttime, 43% daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.
Smith, Tessa E; McCusker, Cara M; Stevens, Jeroen M G; Elwood, Robert W
In ring-tailed lemurs, Lemur catta, the factors modulating hypothalamic-pituitary-adrenal (HPA) activity differ between wild and semi-free-ranging populations. Here we assess factors modulating HPA activity in ring-tailed lemurs housed in a third environment: the zoo. First we validate an enzyme immunoassay to quantify levels of glucocorticoid (GC) metabolites in the faeces of L. catta. We determine the nature of the female-female dominance hierarchies within each group by computing David's scores and examining these in relation to faecal GC (fGC). Relationships between female age and fGC are assessed to evaluate potential age-related confounds. The associations between fGC, numbers of males in a group and reproductive status are explored. Finally, we investigate the value of 7 behaviours in predicting levels of fGC. The study revealed stable linear dominance hierarchies in females within each group. The number of males in a social group together with reproductive status, but not age, influenced fGC. The 7 behavioural variables accounted for 68% of the variance in fGC. The amounts of time an animal spent locomoting and in the inside enclosure were both negative predictors of fGC. The study highlights the flexibility and adaptability of the HPA system in ring-tailed lemurs.
Schnoell, Anna Viktoria; Dittmann, Marie T; Fichtel, Claudia
Behavioural traditions have only been described for a small subset of species, and the factors responsible for the maintenance of traditions over time are unclear. Redfronted lemurs are known to learn socially but traditions have not been described in the wild. We conducted a social diffusion experiment over three experimental years with artificial feeding boxes that could be opened in two different ways (pushing or pulling a door). Six out of 14 individuals that participated in at least 2 years exhibited a stable preference: five lemurs maintained a pull and one lemur a push preference, suggesting that habit formation and reinforcement learning may have lead to preferences over time. The remaining individuals exhibited fluctuating preferences and switched between showing a preference or no preference, but never switched between preferences. This instability might have been due to the low level of difficulty and/or the low object specificity of the task. The majority of lemurs additionally scrounged. Scrounging was not influenced by age, sex or success in manipulating the boxes. Thus, redfronted lemurs appear to use the two techniques flexibly but also scrounged opportunistically to get access to the rewards, indicating that traditions might be stabilized by multiple factors.
Donati, Giuseppe; Ricci, Eva; Baldi, Nicoletta; Morelli, Valentina; Borgognini-Tarli, Silvana M
Primates deal with fluctuations of the thermal environment by both physiological and behavioral mechanisms of thermoregulation. In this article we focus on non-hibernating lemurs, which are hypometabolic and have to cope with a seasonal environment. Behavioral thermoregulation has received little attention compared with specific physiological adaptations to seasonality, i.e., hibernation and torpor, which characterize a number of lemurs. We investigated the role of seasonality and dietary-related factors in determining frequencies of resting, social and postural thermoregulation, and microhabitat selection in collared lemurs, Eulemur collaris. We observed two groups of collared lemurs over a 14-month period in the littoral forest of Sainte Luce, Southern Madagascar. Frequencies of total resting and time spent in huddling, prone, and curled postures were collected via 5-min instantaneous sampling. Microhabitat selection was evaluated as the proportion of time spent in the upper canopy as compared with other layers. Climatic variables were recorded by automatic data loggers, while dietary variables were derived from phenological data and nutritional analyses of the ingested food items. We weighted the combined effects of climatic and dietary variables on the different types of behavioral thermoregulation by means of canonical correlation analysis. The model with the strongest canonical correlation included a first root representing mainly feeding time, day length, and ambient temperature and a second root representing diet quality and height of feeding trees. The output indicated that collared lemurs adapt to thermal and dietary-related metabolic stress by adjusting resting time, social, and postural thermoregulation.
O'Neill, Matthew C
Metabolic costs of resting and locomotion have been used to gain novel insights into the behavioral ecology and evolution of a wide range of primates; however, most previous studies have not considered gait-specific effects. Here, metabolic costs of ring-tailed lemurs (Lemur catta) walking, cantering and galloping are used to test for gait-specific effects and a potential correspondence between costs and preferred speeds. Metabolic costs, including the net cost of locomotion (COL) and net cost of transport (COT), change as a curvilinear function of walking speed and (at least provisionally) as a linear function of cantering and galloping speeds. The baseline quantity used to calculate net costs had a significant effect on the magnitude of speed-specific estimates of COL and COT, especially for walking. This is because non-locomotor metabolism constitutes a substantial fraction (41-61%, on average) of gross metabolic rate at slow speeds. The slope-based estimate of the COT was 5.26 J kg(-1) m(-1) for all gaits and speeds, while the gait-specific estimates differed between walking (0.5 m s(-1) : 6.69 J kg(-1) m(-1) ) and cantering/galloping (2.0 m s(-1) : 5.61 J kg(-1) m(-1) ). During laboratory-based overground locomotion, ring-tailed lemurs preferred to walk at ~0.5 m s(-1) and canter/gallop at ~2.0 m s(-1) , with the preferred walking speed corresponding well to the COT minima. Compared with birds and other mammals, ring-tailed lemurs are relatively economical in walking, cantering, and galloping. These results support the view that energetic optima are an important movement criterion for locomotion in ring-tailed lemurs, and other terrestrial animals.
Kelley, Elizabeth A; Jablonski, Nina G; Chaplin, George; Sussman, Robert W; Kamilar, Jason M
Regulation of body temperature poses significant problems for organisms that inhabit environments with extreme and seasonally fluctuating ambient temperatures. To help alleviate the energetic costs of autonomic responses, these organisms often thermoregulate through behavioral mechanisms. Among primates, lemurs in Madagascar experience uncharacteristically seasonal and unpredictable climates relative to other primate-rich regions. Malagasy primates are physiologically flexible, but different species use different mechanisms to influence their body temperatures. Lemur catta, the ring-tailed lemur, experiences particularly acute diurnal temperature fluctuations in its mostly open-canopy habitat in south and southwest Madagascar. Ring-tailed lemurs are also atypical among lemurs in that they appear to use both sun basking postures and huddling to maintain body temperature when ambient temperatures are cold. To our knowledge, however, no one has systematically tested whether these behaviors function in thermoregulation. We present evidence that ring-tailed lemurs use these postures as behavioral thermoregulation strategies, and that different environmental variables are associated with the use of each posture. Major predictors of sunning included ambient temperature, time of day, and season. Specifically, L. catta consistently assumed sunning postures early after daybreak when ambient temperatures were <13°C, and ceased sunning around 10:00a.m., after ambient temperatures approached 26°C. Sunning occurred more often during austral winter months. Huddling was associated with time of day, but not with ambient temperature or season. We conclude that L. catta tend to sun, rather than huddle, under cold weather conditions when sunning is possible. However, both sunning and huddling are important behavioral adaptations of L. catta that augment chemical thermoregulation and the absence of a dynamic, insulating pelage. Sunning and huddling help to account for the great
Catlett, Kierstin K; Schwartz, Gary T; Godfrey, Laurie R; Jungers, William L
Studies of primate life history variation are constrained by the fact that all large-bodied extant primates are haplorhines. However, large-bodied strepsirrhines recently existed. If we can extract life history information from their skeletons, these species can contribute to our understanding of primate life history variation. This is particularly important in light of new critiques of the classic "fast-slow continuum" as a descriptor of variation in life history profiles across mammals in general. We use established dental histological methods to estimate gestation length and age at weaning for five extinct lemur species. On the basis of these estimates, we reconstruct minimum interbirth intervals and maximum reproductive rates. We utilize principal components analysis to create a multivariate "life history space" that captures the relationships among reproductive parameters and brain and body size in extinct and extant lemurs. Our data show that, whereas large-bodied extinct lemurs can be described as "slow" in some fashion, they also varied greatly in their life history profiles. Those with relatively large brains also weaned their offspring late and had long interbirth intervals. These were not the largest of extinct lemurs. Thus, we distinguish size-related life history variation from variation that linked more strongly to ecological factors. Because all lemur species larger than 10 kg, regardless of life history profile, succumbed to extinction after humans arrived in Madagascar, we argue that large body size increased the probability of extinction independently of reproductive rate. We also provide some evidence that, among lemurs, brain size predicts reproductive rate better than body size. (c) 2010 Wiley-Liss, Inc.
Bleier, T; Hetzel, U; Bauer, C; Behlert, O; Burkhardt, E
This report describes the morphologic and histologic features of a case of esophageal Gongylonema pulchrum infection and esophageal squamous cell carcinoma in a 17-yr-old, female vari (Lemur macaco variegates). The lemur had lived in a German zoo and had a clinical history of dyspnea, vomiting, and anorexia. At necropsy, a whitish, soft, nodular, centrally necrotic mass was found in the caudal third of the esophagus. In addition, numerous intraepithelial nematodes (G. pulchrum) were observed in the entire esophagus. Results suggest a relation between infection with G. pulchrum and development of an esophageal squamous cell carcinoma.
Yamashita, Nayuta; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho
Ring-tailed lemurs have been studied intensively in the Parcel 1 gallery forest of Bezà Mahafaly Special Reserve. Here, we report on lemur groups in a mixture of deciduous dry forest and spiny forest just 5 km to the west. Compared to Parcel 1, Parcel 2 (P2) has a lower density of Tamarindus indica, a major dietary plant species for gallery forest lemurs. Recent studies in drier habitats have called into question the association of lemur density and tamarind presence. In order to address this question, we measured forest structure and composition of plant plots between parcels and conducted lemur feeding observations. The trees and shrubs within the parcels did not differ in height or diameter at breast height, but the frequencies of plant species that were common between parcels were significantly different. Numbers of feeding observations on foods common to both parcels did not differ, but their relative rankings within parcels did. Frequencies of food plants corresponded to earlier reports of lemur population densities. However, we found that the ring-tailed lemur diet is a mixture of plants that are eaten in abundance regardless of frequency and those that are locally available. In terms of their reliance on Tamarindus, P2 animals appear intermediate between those in gallery forests and nontamarind sites.
Blanco, Marina B; Rahalinarivo, Vololonirina
The nocturnal dwarf lemurs of Madagascar (genus Cheirogaleus) are the only primates known to be obligate hibernators. Although the physiology of hibernation has been studied widely in the western, small-bodied species, Cheirogaleus medius, no direct evidence of hibernation, i.e., body temperature recordings, has been reported for any of the three recognized eastern dwarf lemur species. We present skin temperature data collected by external collar transmitters from two eastern dwarf lemur individuals (Cheirogaleus crossleyi) captured in the high-altitude forest of Tsinjoarivo, central-eastern Madagascar. Our study species is larger in body size than western dwarf lemurs and inhabits much colder environments. We present the first evidence of hibernation in an eastern dwarf lemur species, and we compare the results with data available for the western species. Although the hibernation period is shorter in dwarf lemurs from Tsinjoarivo, minimum body temperatures are lower than those reported for C. medius. Both individuals at Tsinjoarivo showed limited passive and extended deep hibernation during which they did not track ambient temperature as observed in most western dwarf lemurs. Because ambient temperatures at Tsinjoarivo never exceed 30°C, dwarf lemurs have to experience arousals to maintain homeostasis during periods of hibernation. We show that large dwarf lemurs (>400 g) are capable of undergoing deep hibernation and suggest that cold, high-altitude forests may render hibernation highly advantageous during periods of food scarcity. This study has implications for understanding the physiology of hibernation in small-bodied lemurs.
Blanco, Marina B.; Rahalinarivo, Vololonirina
The nocturnal dwarf lemurs of Madagascar (genus Cheirogaleus) are the only primates known to be obligate hibernators. Although the physiology of hibernation has been studied widely in the western, small-bodied species, Cheirogaleus medius, no direct evidence of hibernation, i.e., body temperature recordings, has been reported for any of the three recognized eastern dwarf lemur species. We present skin temperature data collected by external collar transmitters from two eastern dwarf lemur individuals ( Cheirogaleus crossleyi) captured in the high-altitude forest of Tsinjoarivo, central-eastern Madagascar. Our study species is larger in body size than western dwarf lemurs and inhabits much colder environments. We present the first evidence of hibernation in an eastern dwarf lemur species, and we compare the results with data available for the western species. Although the hibernation period is shorter in dwarf lemurs from Tsinjoarivo, minimum body temperatures are lower than those reported for C. medius. Both individuals at Tsinjoarivo showed limited passive and extended deep hibernation during which they did not track ambient temperature as observed in most western dwarf lemurs. Because ambient temperatures at Tsinjoarivo never exceed 30°C, dwarf lemurs have to experience arousals to maintain homeostasis during periods of hibernation. We show that large dwarf lemurs (>400 g) are capable of undergoing deep hibernation and suggest that cold, high-altitude forests may render hibernation highly advantageous during periods of food scarcity. This study has implications for understanding the physiology of hibernation in small-bodied lemurs.
An index of coat condition can be a non-invasive tool for tracking health and stress at population level. Coat condition in ringtailed lemurs, Lemur catta, was recorded during September-November birth seasons of 1996, 1997, 1999, and 2001-2006 at Berenty Reserve, Madagascar. Condition was scored on a scale from 0: full, fluffy coat with guard hairs present, to 5: half or more of body hairless. Adult males did not differ overall from adult females. Coats were worse in adults than in 2-year-old subadults; 1-year-old juveniles were intermediate. Mothers and adult males lost coat condition as the season progressed: non-mother females maintained condition. Years 1999-2002 scored better coats than either 1996-1997 or 2003-2006. Lemurs in high population density areas had worse coats than in natural forest, but tourist presence had less effect than density. Monitoring coat condition in an apparently healthy population reveals differences between population segments, and in a forest fragment with limited immigration or emigration it can track progressive changes, correcting impressions of progressive improvement or degradation over time. Above all it gives a baseline for response to climate changes or eventual pathology. (c) 2008 Wiley-Liss, Inc.
Fur condition in wild ringtailed lemurs, Lemur catta, was recorded during September-November birth seasons 2001-2006 at Berenty Reserve, Madagascar. Body coat condition was scored on a scale from BS 0: full, smooth coat with guard hairs, to BS5: half or more of back and limbs hairless. Tail condition was scored from TS 0: full, to TS 5: half or more hairless. Where troop core areas included stands of Leucaena leucocephala, alopecia was dramatically more frequent than in similar areas without leucaena, including many animals with score BS5 or TS5, "bald lemur syndrome." Females' coats were worse than males', possibly related to female dominance and access to this preferred food. Tails in non-leucaena-feeding females tend to remain full, even if coats deteriorate, but with leucaena-feeding female tails are highly correlated with coat condition and equally bare. Coat and tail condition in L. catta reflected not only the dietary toxin but individual differences as well as differences between adjacent troops that may result from territorially mediated access to the environment. Leucaena contains the non-protein amino acid mimosine, a known cause of alopecia, wasting, and organ damage in livestock, although the effects are usually reversible. This is the first case of its effect in wildlife. Leucaena is an agroforestry tree introduced throughout the tropics. In high dietary concentrations leucaena might potentially affect any browsing mammal.
Durden, Lance A; Blanco, Marina B; Seabolt, Matthew H
Lemurpediculus robbinsi sp. nov. is described from Crossley's dwarf lemur, Cheirogaleus crossleyi A. Grandidier, and Lemurpediculus claytoni sp. nov. is described from Sibree's dwarf lemur, Cheirogaleus sibreei Forsyth Major, from Madagascar. Both sexes of each new louse species are illustrated and distinguished from the two previously known species of Lemurpediculus: L. verruculosus (Ward) and L. petterorum Paulian. With the addition of two new species to the genus, an amended description of Lemurpediculus is provided. The two hosts of the new louse species are morphologically similar, endangered, obligately hibernating lemurs. These two species of lemurs are sometimes sympatric in rainforests in eastern Madagascar. Despite the morphological similarity of the two host species, their lice are morphologically distinct and are easiest to identify based on the shape of the subgenital plate of the female and the shape of the genitalia in the male. Both new species of lice should be considered to be endangered because their hosts are endangered. It is not known if either of the new species of lice are vectors of pathogens or parasites to their hosts. © The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: email@example.com Version of Record, first published online February 15, 2017 with fixed content and layout in compliance with Art. 188.8.131.52 ICZN.
Horvath, Julie E; Weisrock, David W; Embry, Stephanie L; Fiorentino, Isabella; Balhoff, James P; Kappeler, Peter; Wray, Gregory A; Willard, Huntington F; Yoder, Anne D
Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing approximately 9 kb of nuclear sequence data. In combination with previously published nuclear and mitochondrial loci, this yields a data set of more than 16 kb and adds approximately 275 kb of DNA sequence to current databases. Our phylogenetic analyses confirm hypotheses of lemuriform monophyly and provide robust resolution of the phylogenetic relationships among the five lemuriform families. We verify that the genus Daubentonia is the sister lineage to all other lemurs. The Cheirogaleidae and Lepilemuridae are sister taxa and together form the sister lineage to the Indriidae; this clade is the sister lineage to the Lemuridae. Divergence time estimates indicate that lemurs are an ancient group, with their initial diversification occurring around the Cretaceous-Tertiary boundary. Given the power of this data set to resolve branches in a notoriously problematic area of primate phylogeny, we anticipate that our phylogenomic toolkit will be of value to other studies of primate phylogeny and diversification. Moreover, the methods applied will be broadly applicable to other taxonomic groups where phylogenetic relationships have been notoriously difficult to resolve.
Markolf, Matthias; Brameier, Markus; Kappeler, Peter M
Although most taxonomists agree that species are independently evolving metapopulation lineages that should be delimited with several kinds of data, the taxonomic practice in Malagasy primates (Lemuriformes) looks quite different. Several recently described lemur species are based solely on evidence of genetic distance and diagnostic characters of mitochondrial DNA sequences sampled from a few individuals per location. Here we explore the validity of this procedure for species delimitation in lemurs using published sequence data. We show that genetic distance estimates and Population Aggregation Analysis (PAA) are inappropriate for species delimitation in this group of primates. Intra- and interspecific genetic distances overlapped in 14 of 17 cases independent of the genetic marker used. A simulation of a fictive taxonomic study indicated that for the mitochondrial D-loop the minimum required number of individuals sampled per location is 10 in order to avoid false positives via PAA. Genetic distances estimates and PAA alone should not be used for species delimitation in lemurs. Instead, several nuclear and sex-specific loci should be considered and combined with other data sets from morphology, ecology or behavior. Independent of the data source, sampling should be done in a way to ensure a quantitative comparison of intra- and interspecific variation of the taxa in question. The results of our study also indicate that several of the recently described lemur species should be reevaluated with additional data and that the number of good species among the currently known taxa is probably lower than currently assumed.
Background Although most taxonomists agree that species are independently evolving metapopulation lineages that should be delimited with several kinds of data, the taxonomic practice in Malagasy primates (Lemuriformes) looks quite different. Several recently described lemur species are based solely on evidence of genetic distance and diagnostic characters of mitochondrial DNA sequences sampled from a few individuals per location. Here we explore the validity of this procedure for species delimitation in lemurs using published sequence data. Results We show that genetic distance estimates and Population Aggregation Analysis (PAA) are inappropriate for species delimitation in this group of primates. Intra- and interspecific genetic distances overlapped in 14 of 17 cases independent of the genetic marker used. A simulation of a fictive taxonomic study indicated that for the mitochondrial D-loop the minimum required number of individuals sampled per location is 10 in order to avoid false positives via PAA. Conclusions Genetic distances estimates and PAA alone should not be used for species delimitation in lemurs. Instead, several nuclear and sex-specific loci should be considered and combined with other data sets from morphology, ecology or behavior. Independent of the data source, sampling should be done in a way to ensure a quantitative comparison of intra- and interspecific variation of the taxa in question. The results of our study also indicate that several of the recently described lemur species should be reevaluated with additional data and that the number of good species among the currently known taxa is probably lower than currently assumed. PMID:21777472
Horvath, Julie E.; Weisrock, David W.; Embry, Stephanie L.; Fiorentino, Isabella; Balhoff, James P.; Kappeler, Peter; Wray, Gregory A.; Willard, Huntington F.; Yoder, Anne D.
Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing ∼9 kb of nuclear sequence data. In combination with previously published nuclear and mitochondrial loci, this yields a data set of more than 16 kb and adds ∼275 kb of DNA sequence to current databases. Our phylogenetic analyses confirm hypotheses of lemuriform monophyly and provide robust resolution of the phylogenetic relationships among the five lemuriform families. We verify that the genus Daubentonia is the sister lineage to all other lemurs. The Cheirogaleidae and Lepilemuridae are sister taxa and together form the sister lineage to the Indriidae; this clade is the sister lineage to the Lemuridae. Divergence time estimates indicate that lemurs are an ancient group, with their initial diversification occurring around the Cretaceous-Tertiary boundary. Given the power of this data set to resolve branches in a notoriously problematic area of primate phylogeny, we anticipate that our phylogenomic toolkit will be of value to other studies of primate phylogeny and diversification. Moreover, the methods applied will be broadly applicable to other taxonomic groups where phylogenetic relationships have been notoriously difficult to resolve. PMID:18245770
Herrera, James P; Dávalos, Liliana M
Paleontological and neontological systematics seek to answer evolutionary questions with different data sets. Phylogenies inferred for combined extant and extinct taxa provide novel insights into the evolutionary history of life. Primates have an extensive, diverse fossil record and molecular data for living and extinct taxa are rapidly becoming available. We used two models to infer the phylogeny and divergence times for living and fossil primates, the tip-dating (TD) and fossilized birth-death process (FBD). We collected new morphological data, especially on the living and extinct endemic lemurs of Madagascar. We combined the morphological data with published DNA sequences to infer near-complete (88% of lemurs) time-calibrated phylogenies. The results suggest that primates originated around the Cretaceous-Tertiary boundary, slightly earlier than indicated by the fossil record and later than previously inferred from molecular data alone. We infer novel relationships among extinct lemurs, and strong support for relationships that were previously unresolved. Dates inferred with TD were significantly older than those inferred with FBD, most likely related to an assumption of a uniform branching process in the TD compared with a birth-death process assumed in the FBD. This is the first study to combine morphological and DNA sequence data from extinct and extant primates to infer evolutionary relationships and divergence times, and our results shed new light on the tempo of lemur evolution and the efficacy of combined phylogenetic analyses.
Decreased activity has been reported in both nocturnal and diurnal primates during the prolonged dry season in western Madagascar, and this has been interpreted as a reaction to the severe environment, with its food scarcity and/or thermal stress. Several day-active lemurs rest more as trees defoliate, although the reason for this is unclear. To understand the mechanism underpinning the diurnal resting of lemurs in seasonal deciduous forests, I observed common brown lemurs (Eulemur fulvus fulvus) for one year in Ankarafantsika National Park, northwestern Madagascar. In Ankarafantsika, despite high fruit availability during the dry season, brown lemurs are known to engage in diurnal resting. To examine the effects of thermal factors and defoliation on lemur inactivity, I recorded the activity of a troop at 1 min intervals, hourly ambient temperature, daily rainfall, and weather during observations (06:00-18:00). I quantified the amount of leaves biweekly for 680 trees. I tested correlations between percentages of resting time and each factor across hours during the day and across seasons. During the rainy season, resting time did not differ between sunny and cloudy days, and lemurs were active throughout the daytime. At the hourly level during the dry season, lemurs rested exclusively at midday, apparently at peak sunlight intensity rather than at peak ambient temperature. At seasonal level, percentages of total resting time from 08:00 to 16:00 were greater during dry season (81.9%) than during rainy season (62.6%), and percentages increased as ambient temperatures increased. Defoliation was related to seasonal decrease in weekly rainfall, which served as an index of water retained in the forest. Defoliation probably reflected aridification as well as the penetration of sunlight into the forest. Diurnal resting increased as both the amount of leaves and weekly rainfall decreased seasonally. These results suggest that heat stress under dry conditions may promote
Rushmore, Julie; Leonhardt, Sara D.; Drea, Christine M.
Visual and olfactory cues provide important information to foragers, yet we know little about species differences in sensory reliance during food selection. In a series of experimental foraging studies, we examined the relative reliance on vision versus olfaction in three diurnal, primate species with diverse feeding ecologies, including folivorous Coquerel's sifakas (Propithecus coquereli), frugivorous ruffed lemurs (Varecia variegata spp), and generalist ring-tailed lemurs (Lemur catta). We used animals with known color-vision status and foods for which different maturation stages (and hence quality) produce distinct visual and olfactory cues (the latter determined chemically). We first showed that lemurs preferentially selected high-quality foods over low-quality foods when visual and olfactory cues were simultaneously available for both food types. Next, using a novel apparatus in a series of discrimination trials, we either manipulated food quality (while holding sensory cues constant) or manipulated sensory cues (while holding food quality constant). Among our study subjects that showed relatively strong preferences for high-quality foods, folivores required both sensory cues combined to reliably identify their preferred foods, whereas generalists could identify their preferred foods using either cue alone, and frugivores could identify their preferred foods using olfactory, but not visual, cues alone. Moreover, when only high-quality foods were available, folivores and generalists used visual rather than olfactory cues to select food, whereas frugivores used both cue types equally. Lastly, individuals in all three of the study species predominantly relied on sight when choosing between low-quality foods, but species differed in the strength of their sensory biases. Our results generally emphasize visual over olfactory reliance in foraging lemurs, but we suggest that the relative sensory reliance of animals may vary with their feeding ecology. PMID:22870229
Ganzhorn, Jörg U
This study examines segregation of seven lemur species in an eastern rainforest of Madagascar by a numerical analysis of microhabitats using structural and phenological data. These data are combined with the results of a previous study on food selection by these species in relation to plant chemistry. Description of some 441 10×10 m(2) microhabitats yields clear separation of the frugivorous from the more folivorous guild of lemurs. Within each guild there are subgroups of two species each, which use similar microhabitats. The two species of the subgroups are separated by their different reactions towards food chemicals. Thus food chemistry and microhabitat structure are two complementary axes sufficient to separate lemur species in the Malagasy rainforest. Species using the same microhabitats choose food items with different chemical properties and species eating the same food differ in their utilization of microhabitats. Only Cheirogaleus major can not be separated from the other lemur species based on habitat utilization and the chemical composition of their food. This species, however, is active only at times of food abundance and reduces its activity at times of scarcity thus avoiding potential competition. The folivorous species Avahi laniger and Indri indri use similar micro habitats for feeding and for resting, reflecting the strategy of low energy cost and fow energy return. A more folivorous species, Lemur fulvus, discriminates between feeding and resting sites based on phenological and structural variables, representing an example for behavior shaped by high cost and high energy return. Feeding sites of this species are linked to fruit abundance but the need to see but not to be seen seems to determine their choice of resting sites. This discrimination is similar to habitat choices of frugivorous primates in other tropical rainforests which have been linked to anti-predator behavior and suggests convergent evolution due to similar evolutionary selection
Rushmore, Julie; Leonhardt, Sara D; Drea, Christine M
Visual and olfactory cues provide important information to foragers, yet we know little about species differences in sensory reliance during food selection. In a series of experimental foraging studies, we examined the relative reliance on vision versus olfaction in three diurnal, primate species with diverse feeding ecologies, including folivorous Coquerel's sifakas (Propithecus coquereli), frugivorous ruffed lemurs (Varecia variegata spp), and generalist ring-tailed lemurs (Lemur catta). We used animals with known color-vision status and foods for which different maturation stages (and hence quality) produce distinct visual and olfactory cues (the latter determined chemically). We first showed that lemurs preferentially selected high-quality foods over low-quality foods when visual and olfactory cues were simultaneously available for both food types. Next, using a novel apparatus in a series of discrimination trials, we either manipulated food quality (while holding sensory cues constant) or manipulated sensory cues (while holding food quality constant). Among our study subjects that showed relatively strong preferences for high-quality foods, folivores required both sensory cues combined to reliably identify their preferred foods, whereas generalists could identify their preferred foods using either cue alone, and frugivores could identify their preferred foods using olfactory, but not visual, cues alone. Moreover, when only high-quality foods were available, folivores and generalists used visual rather than olfactory cues to select food, whereas frugivores used both cue types equally. Lastly, individuals in all three of the study species predominantly relied on sight when choosing between low-quality foods, but species differed in the strength of their sensory biases. Our results generally emphasize visual over olfactory reliance in foraging lemurs, but we suggest that the relative sensory reliance of animals may vary with their feeding ecology.
Teriaca, Luca; Andretta, Vincenzo; Auchère, Frédéric; Brown, Charles M.; Buchlin, Eric; Cauzzi, Gianna; Culhane, J. Len; Curdt, Werner; Davila, Joseph M.; Del Zanna, Giulio; Doschek, George A.; Fineschi, Silvano; Fludra, Andrzej; Gallagher, Peter T.; Green, Lucie; Harra, Louise K.; Imada, Shinsuke; Innes, Davina; Kliem, Bernhard; Korendyke, Clarence; Mariska, John T.; Martínez-Pillet, Valentin; Parenti, Susanna; Patsourakos, Spiros; Peter, Hardi; Poletto, Luca; Rutten, Robert J.; Schühle, Udo; Siemer, Martin; Shimizu, Toshifumi; Socas-Navarro, Hector; Solanki, Sami K.; Spadaro, Daniele; Trujillo-Bueno, Javier; Tsuneta, Saku; Dominguez, Santiago Vargas; Vial, Jean-Claude; Walsh, Robert; Warren, Harry P.; Wiegelmann, Thomas; Winter, Berend; Young, Peter
The solar outer atmosphere is an extremely dynamic environment characterized by the continuous interplay between the plasma and the magnetic field that generates and permeates it. Such interactions play a fundamental role in hugely diverse astrophysical systems, but occur at scales that cannot be studied outside the solar system. Understanding this complex system requires concerted, simultaneous solar observations from the visible to the vacuum ultraviolet (VUV) and soft X-rays, at high spatial resolution (between 0.1'' and 0.3''), at high temporal resolution (on the order of 10 s, i.e., the time scale of chromospheric dynamics), with a wide temperature coverage (0.01 MK to 20 MK, from the chromosphere to the flaring corona), and the capability of measuring magnetic fields through spectropolarimetry at visible and near-infrared wavelengths. Simultaneous spectroscopic measurements sampling the entire temperature range are particularly important. These requirements are fulfilled by the Japanese Solar-C mission (Plan B), composed of a spacecraft in a geosynchronous orbit with a payload providing a significant improvement of imaging and spectropolarimetric capabilities in the UV, visible, and near-infrared with respect to what is available today and foreseen in the near future. The Large European Module for solar Ultraviolet Research (LEMUR), described in this paper, is a large VUV telescope feeding a scientific payload of high-resolution imaging spectrographs and cameras. LEMUR consists of two major components: a VUV solar telescope with a 30 cm diameter mirror and a focal length of 3.6 m, and a focal-plane package composed of VUV spectrometers covering six carefully chosen wavelength ranges between 170 Å and 1270 Å. The LEMUR slit covers 280'' on the Sun with 0.14'' per pixel sampling. In addition, LEMUR is capable of measuring mass flows velocities (line shifts) down to 2 km s - 1 or better. LEMUR has been proposed to ESA as the European contribution to the Solar
Schmidt, Debra A; Iambana, R Bernard; Britt, Adam; Junge, Randall E; Welch, Charles R; Porton, Ingrid J; Kerley, Monty S
The purpose of this study was to quantify the concentrations of crude protein, fat, ash, neutral detergent fiber, acid detergent fiber, lignin, nonstructural carbohydrates, and gross energy in plant foods consumed by wild black and white ruffed lemurs (Varecia variegata). Calcium, phosphorous, magnesium, potassium, sodium, iron, zinc, copper, manganese, molybdenum, and selenium concentrations were also determined. A total of 122 samples from 33 plant families and more than 60 species were collected and analyzed for their nutritional content. The specific nutrient needs of black and white ruffed lemurs are unknown, but quantifying the nutritional composition of the foods they consume in the wild will help nutritionists and veterinarians formulate more appropriate diets for captive ruffed lemurs. This information will also supply information on how man-induced habitat changes affect the nutritional composition of foods consumed by free-ranging lemurs.
Meyer, Wynn K; Venkat, Aarti; Kermany, Amir R; van de Geijn, Bryce; Zhang, Sidi; Przeworski, Molly
Lemurs, the living primates most distantly related to humans, demonstrate incredible diversity in behaviour, life history patterns and adaptive traits. Although many lemur species are endangered within their native Madagascar, there is no high-quality genome assembly from this taxon, limiting population and conservation genetic studies. One critically endangered lemur is the blue-eyed black lemur Eulemur flavifrons. This species is fixed for blue irises, a convergent trait that evolved at least four times in primates and was subject to positive selection in humans, where 5′ regulatory variation of OCA2 explains most of the brown/blue eye colour differences. We built a de novo genome assembly for E. flavifrons, providing the most complete lemur genome to date, and a high confidence consensus sequence for close sister species E. macaco, the (brown-eyed) black lemur. From diversity and divergence patterns across the genomes, we estimated a recent split time of the two species (160 Kya) and temporal fluctuations in effective population sizes that accord with known environmental changes. By looking for regions of unusually low diversity, we identified potential signals of directional selection in E. flavifrons at MITF, a melanocyte development gene that regulates OCA2 and has previously been associated with variation in human iris colour, as well as at several other genes involved in melanin biosynthesis in mammals. Our study thus illustrates how whole-genome sequencing of a few individuals can illuminate the demographic and selection history of nonmodel species. PMID:26198179
Sauther, Michelle L; Cuozzo, Frank P
Fallback foods are often viewed as central in shaping primate morphology, and influencing adaptive shifts in hominin and other primate evolution. Here we argue that fruit of the tamarind tree (Tamarindus indica) qualifies as a fallback food of ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve (BMSR), Madagascar. Contrary to predictions that fallback foods may select for dental and masticatory morphologies adapted to processing these foods, consumption of tamarind fruit by these lemurs leaves a distinct pattern of dental pathology among ring-tailed lemurs at BMSR. Specifically, the physical and mechanical properties of tamarind fruit likely result in a high frequency of severe tooth wear, and subsequent antemortem tooth loss, in this lemur population. This pattern of dental pathology is amplified among lemurs living in disturbed areas at Beza Mahafaly, resulting from a disproportionate emphasis on challenging tamarind fruit, due to few other fruits being available. This is in part caused by a reduction in ground cover and other plants due to livestock grazing. As such, tamarind trees remain one of the few food resources in many areas. Dental pathologies are also associated with the use of a nonendemic leaf resource Argemone mexicana, an important food during the latter part of the dry season when overall food availability is reduced. Such dental pathologies at Beza Mahafaly, resulting from the use or overemphasis of fallback foods for which they are not biologically adapted, indicate that anthropogenic factors must be considered when examining fallback foods.
Meyer, Wynn K; Venkat, Aarti; Kermany, Amir R; van de Geijn, Bryce; Zhang, Sidi; Przeworski, Molly
Lemurs, the living primates most distantly related to humans, demonstrate incredible diversity in behaviour, life history patterns and adaptive traits. Although many lemur species are endangered within their native Madagascar, there is no high-quality genome assembly from this taxon, limiting population and conservation genetic studies. One critically endangered lemur is the blue-eyed black lemur Eulemur flavifrons. This species is fixed for blue irises, a convergent trait that evolved at least four times in primates and was subject to positive selection in humans, where 5' regulatory variation of OCA2 explains most of the brown/blue eye colour differences. We built a de novo genome assembly for E. flavifrons, providing the most complete lemur genome to date, and a high confidence consensus sequence for close sister species E. macaco, the (brown-eyed) black lemur. From diversity and divergence patterns across the genomes, we estimated a recent split time of the two species (160 Kya) and temporal fluctuations in effective population sizes that accord with known environmental changes. By looking for regions of unusually low diversity, we identified potential signals of directional selection in E. flavifrons at MITF, a melanocyte development gene that regulates OCA2 and has previously been associated with variation in human iris colour, as well as at several other genes involved in melanin biosynthesis in mammals. Our study thus illustrates how whole-genome sequencing of a few individuals can illuminate the demographic and selection history of nonmodel species.
Crowley, Brooke E; Godfrey, Laurie R; Irwin, Mitchell T
The Spiny Thicket Ecoregion (STE) of Southern and southwestern Madagascar was recently home to numerous giant lemurs and other "megafauna," including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores. Following the arrival of humans more than 2,000 years ago, dramatic extinctions occurred. Only one-third of the lemur species which earlier occupied the STE survive today; other taxa suffered even greater losses. We use stable isotope biogeochemistry to reconstruct past diets and habitat preferences of the recently extinct lemurs of the STE. We show that the extinct lemurs occupied a wide range of niches, often distinct from those filled by coeval non-primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Most fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets. These new data suggest that the recent extinctions have likely had significant ecological ramifications for the communities and ecosystems of Southern and southwestern Madagascar. © 2010 Wiley-Liss, Inc.
Sato, Hiroki; Ichino, Shinichiro; Hanya, Goro
Primates often modify dietary composition in relation to seasonal changes in food availability or climate conditions. We studied the feeding patterns of a troop of common brown lemurs (Eulemur fulvus), a semi-frugivorous strepsirhine, in a dry forest in northwestern Madagascar. To understand the mechanism of dietary modification, we recorded daily feeding times of diet items during 101 full-day observations over 1 year, and then conducted a linear model analysis to examine the effects of fruiting tree density in the forest, daily ambient temperature, and weekly rainfall (index of water retained in the forest) on the lemurs' daily feeding time. The lemurs spent dramatically more time on leaf-eating as well as total feeding time, and less time on fruit-eating during the late dry season (total 152 min/day, frugivory 56 min/day, folivory 77 min/day), as compared with other seasons when the diet was highly frugivorous (total 96 min/day, frugivory 81 min/day, folivory 8 min/day). Folivory increased as temperatures rose under the condition of low weekly rainfall, whereas frugivory was unrelated to fruiting tree density. Most (97.4%) diurnal folivory during the late dry season was spent consuming Lissochilus rutenbergianus, chewing the succulent leaves and licking the juice. Because the nutritional analysis showed that L. rutenbergianus is rich in water (80.1% of fresh weight) but poor in protein and nonstructural carbohydrates, its increased use was probably for rehydration. We conducted 13 full-night observations, because brown lemurs increase nocturnal activities during the dry season. At nighttime, the lemurs tended to spend more time eating fruit in the late dry season (32 min/night) than in the early dry season (14 min/night), and never consumed L. rutenbergianus. Fruits rich in nonstructural carbohydrates can be energy sources for Eulemur. They likely engaged in additional nocturnal frugivory for energy compensation. Brown lemurs have a flexible strategy of
Reuter, Kim E; Schaefer, Melissa S
Although it is illegal to capture, sell, and trade lemurs, the live capture of lemurs in Madagascar is ongoing and may have impacted over 28,000 lemurs between 2010 and 2013. Only one study has examined this trade and did so using in-person interviews in northern Madagascar. The current study sought to expand this existing dataset and examine the comparability of online surveys to more traditional on-location data collection methods. In this study, we collected data through a web-based survey resulting in 302 sightings of 685 captive lemurs. We also collected data from 171 hotel and 43 restaurant websites and social media profiles. Survey submissions included sightings of 30 species from 10 genera, nearly twice as many species as identified via the in-person interviews. Lemur catta, Varecia variegata, and Eulemur fulvus were the most common species sighted in captivity. Captive lemurs were reported in 19 of Madagascar's 22 administrative regions and most were seen in urban areas near their habitat ranges. This represents a wider geographic distribution of captive lemurs than previously found through in-person interviews. The online survey results were broadly similar to those of the in-person surveys though greater in species and geographic diversity demonstrating advantages to the use of online surveys. The online research methods were low in cost (USD $100) compared to on-location data collection (USD $12,000). Identified disadvantages included sample bias; most of the respondents to the online survey were researchers and many captive sightings were near study sites. The results illustrate the benefits of incorporating a social science approach using online surveys as a complement to traditional fieldwork. Am. J. Primatol. © 2016 Wiley Periodicals, Inc. © 2016 Wiley Periodicals, Inc.
Backues, K A; Hoover, J P; Bahr, R J; Confer, A W; Chalman, J A; Larry, M L
Chronic recurrent multifocal osteomyelitis is a rare inflammatory bone disease of children and adolescents that is characterized by localized swelling and pain in the clavicles and long bones of the limbs. Diagnosis of chronic recurrent multifocal osteomyelitis is made from clinical signs, characteristic radiographic and histopathologic findings, and negative results of microbial cultures. Treatment of chronic recurrent multifocal osteomyelitis in humans includes administration of nonsteroidal anti-inflammatory drugs or immune modulators, which may be effective in lemurs.
Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners. (c) 2007 Wiley-Liss, Inc.
Brown, Jason L; Yoder, Anne D
Geospatial modeling is one of the most powerful tools available to conservation biologists for estimating current species ranges of Earth's biodiversity. Now, with the advantage of predictive climate models, these methods can be deployed for understanding future impacts on threatened biota. Here, we employ predictive modeling under a conservative estimate of future climate change to examine impacts on the future abundance and geographic distributions of Malagasy lemurs. Using distribution data from the primary literature, we employed ensemble species distribution models and geospatial analyses to predict future changes in species distributions. Current species distribution models (SDMs) were created within the BIOMOD2 framework that capitalizes on ten widely used modeling techniques. Future and current SDMs were then subtracted from each other, and areas of contraction, expansion, and stability were calculated. Model overprediction is a common issue associated Malagasy taxa. Accordingly, we introduce novel methods for incorporating biological data on dispersal potential to better inform the selection of pseudo-absence points. This study predicts that 60% of the 57 species examined will experience a considerable range of reductions in the next seventy years entirely due to future climate change. Of these species, range sizes are predicted to decrease by an average of 59.6%. Nine lemur species (16%) are predicted to expand their ranges, and 13 species (22.8%) distribution sizes were predicted to be stable through time. Species ranges will experience severe shifts, typically contractions, and for the majority of lemur species, geographic distributions will be considerably altered. We identify three areas in dire need of protection, concluding that strategically managed forest corridors must be a key component of lemur and other biodiversity conservation strategies. This recommendation is all the more urgent given that the results presented here do not take into
Palagi, Elisabetta; Norscia, Ivan; Spada, Giulia
Play signals are commonly used by animals to communicate their playful motivation and to limit the risk that rough acts are misunderstood by playmates. The relaxed open mouth is the most common facial expression performed during play in many mammals and represents the ritualized version of the movement anticipating a play bite. The signaling nature of this expression has been proven in many haplorrhine species but never demonstrated in strepsirrhines. Our purpose was assessing whether, also in strepsirrhines, the relaxed open mouth has an actual communicative function. We studied wild ring-tailed lemurs (Lemur catta), characterized by highly social habits including intense playful interactions. They largely use playful signals, mostly performed with the black and white tail. The signaling function of the tail (tail play) has been widely demonstrated. We analyzed both tail play and the relaxed open mouth to verify how their distribution is affected by different play variables (e.g., play session symmetry, number of play mates, previous use of the same pattern). Indeed, ring-tailed lemurs use the relaxed open mouth as a communicative signal during play. Relaxed open mouth was more frequent during unbalanced interactions showing the highest asymmetry in the patterns performed by the two players (offensive/neutral). Compared to tail play, relaxed open mouth was more frequent during dyadic than polyadic interactions and, as a highly directional signal, it was more frequently replicated by the play mate. Therefore, the relaxed open mouth needs to be performed face-to-face so that signal detection can be optimized. Similar to previous findings in monkeys and apes, the relaxed open mouth in lemurs seems to be a ritualized signal used to engage and, perhaps, sustain playful interaction. © 2014 Wiley Periodicals, Inc.
Greene, Lydia K.; Grogan, Kathleen E.; Smyth, Kendra N.; Adams, Christine A.; Klager, Skylar A.; Drea, Christine M.
Animals communicating via scent often deposit composite signals that incorporate odorants from multiple sources; however, the function of mixing chemical signals remains understudied. We tested both a ‘multiple-messages’ and a ‘fixative’ hypothesis of composite olfactory signalling, which, respectively, posit that mixing scents functions to increase information content or prolong signal longevity. Our subjects—adult, male ring-tailed lemurs (Lemur catta)—have a complex scent-marking repertoire, involving volatile antebrachial (A) secretions, deposited pure or after being mixed with a squalene-rich paste exuded from brachial (B) glands. Using behavioural bioassays, we examined recipient responses to odorants collected from conspecific strangers. We concurrently presented pure A, pure B and mixed A + B secretions, in fresh or decayed conditions. Lemurs preferentially responded to mixed over pure secretions, their interest increasing and shifting over time, from sniffing and countermarking fresh mixtures, to licking and countermarking decayed mixtures. Substituting synthetic squalene (S)—a well-known fixative—for B secretions did not replicate prior results: B secretions, which contain additional chemicals that probably encode salient information, were preferred over pure S. Whereas support for the ‘multiple-messages’ hypothesis underscores the unique contribution from each of an animal's various secretions, support for the ‘fixative’ hypothesis highlights the synergistic benefits of composite signals. PMID:27152222
Andriaholinirina, Nicole; Fausser, Jean-Luc; Roos, Christian; Zinner, Dietmar; Thalmann, Urs; Rabarivola, Clément; Ravoarimanana, Iary; Ganzhorn, Jörg U; Meier, Bernhard; Hilgartner, Roland; Walter, Lutz; Zaramody, Alphonse; Langer, Christoph; Hahn, Thomas; Zimmermann, Elke; Radespiel, Ute; Craul, Mathias; Tomiuk, Jürgen; Tattersall, Ian; Rumpler, Yves
Background The number of species within the Malagasy genus Lepilemur and their phylogenetic relationships is disputed and controversial. In order to establish their evolutionary relationships, a comparative cytogenetic and molecular study was performed. We sequenced the complete mitochondrial cytochrome b gene (1140 bp) from 68 individuals representing all eight sportive lemur species and most major populations, and compared the results with those obtained from cytogenetic studies derived from 99 specimens. Results Interspecific genetic variation, diagnostic characters and significantly supported phylogenetic relationships were obtained from the mitochondrial sequence data and are in agreement with cytogenetic information. The results confirm the distinctiveness of Lepilemur ankaranensis, L. dorsalis, L. edwardsi, L. leucopus, L. microdon, L. mustelinus, L. ruficaudatus and L. septentrionalis on species level. Additionally, within L. ruficaudatus large genetic differences were observed among different geographic populations. L. dorsalis from Sahamalaza Peninsula and from the Ambanja/Nosy Be region are paraphyletic, with the latter forming a sister group to L. ankaranensis. Conclusion Our results support the classification of the eight major sportive lemur taxa as independent species. Moreover, our data indicate further cryptic speciation events within L. ruficaudatus and L. dorsalis. Based on molecular data we propose to recognize the sportive lemur populations from north of the Tsiribihina River, south of the Betsiboka River, and from the Sahamalaza Peninsula, as distinct species. PMID:16504080
Trochet, Delphine; Mergui, Xénia; Ivkovic, Ivana; Porreca, Rosa Maria; Gerbault-Seureau, Michèle; Sidibe, Assitan; Richard, Florence; Londono-Vallejo, Arturo; Perret, Martine; Aujard, Fabienne; Riou, Jean-François
Telomere erosion leading to replicative senescence has been well documented in human and anthropoid primates, and provides a clue against tumorigenesis. In contrast, other mammals, such as laboratory mice, with short lifespan and low body weight mass have different telomere biology without replicative senescence. We analyzed telomere biology in the grey mouse lemur, a small prosimian model with a relative long lifespan currently used in ageing research. We report an average telomere length by telomere restriction fragment (TRF) among the longest reported so far for a primate species (25-30 kb), but without detectable overall telomere shortening with ageing on blood samples. However, we demonstrate using universal STELA (Single Telomere Length Amplification) the existence of short telomeres, the increase of which, while correlating with ageing might be related to another mechanism than replicative senescence. We also found a low stringency of telomerase restriction in tissues and an ease to immortalize fibroblasts in vitro upon spontaneous telomerase activation. Finally, we describe the first grey mouse lemur cancer cell line showing a dramatic telomere shortening and high telomerase activity associated with polyploidy. Our overall results suggest that telomere biology in grey mouse lemur is an exception among primates, with at best a physiologically limited replicative telomere ageing and closest to that observed in small rodents.
Simons, Elwyn L.; Burney, David A.; Chatrath, Prithijit S.; Godfrey, Laurie R.; Jungers, William L.; Rakotosamimanana, Berthe
An extensive late Quaternary fauna, including many extinct giant lemurs, has been collected recently in a 110+-km system of caves in the Ankarana Massif of northern Madagascar. AMS 14C dates for the acid-insoluble (collagen/gelatin) fraction of bones of the giant lemur Megaladapis (26,150 ± 400 and 12,760 ± 70 yr B.P.) confirm its presence in the area during the late Pleistocene and provide the first Pleistocene 14 C ages from bones of the extinct megafauna of the island. The first date from bones of the recently described extinct Babakotia radofilai (4400 ± 60 yr B.P.) shows that it was present in northern Madagascar in mid-Holocene times. A comparatively recent age of 1020 ± 50 yr B.P. for the extinct Archaeolemur indicates survival of this genus for at least a millennium after the first direct evidence for humans in Madagascar. This suggests that the island's "extinction window" may have represented a longer time span than would have been expected under the Blitzkrieg model of late Quaternary extinctions. A mid-Holocene age (4560 ± 70 yr B.P.) for a bone sample of the small extant lemur Hapalemur simus indicates that the disappearance of this now-restricted species from the Ankarana occurred after this date. New data from the Ankarana and other sites on the island add to the consensus that major biotic changes occurred on Madagascar in the late Holocene.
O'Mara, M Teague
The extended primate juvenile period has been linked to interactions between feeding ecology and sociality. However, accumulating field data on juvenile primates suggest variation in the linkages between foraging efficiency, group foraging and social behaviour. In many non-human primates, juvenile ability (strength, coordination and motor skills) does not limit foraging success. If predicted limitations in feeding are not found in juvenile monkeys, it is possible that the gregarious strepsirrhines may show foraging patterns similar to those implicated in the evolution of a life history where long juvenile periods are advantageous. To test these behavioural predictions, I present a mixed longitudinal sample of observations on feeding and foraging behaviour from ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve, Madagascar. Like several platyrrhine species, close proximity during foraging, low feeding efficiency and low dietary diversity are not typical of ring-tailed lemurs. The lack of ecological trade-offs in these species may indicate stronger common roles of sociality and social complexity in structuring the elongation of the primate juvenile period.
Curtis, Deborah J
Data collected on the feeding behavior, food intake, and chemical analyses of plant foods were used to document seasonal variation in diet and nutrition in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with a predominantly frugivorous diet supplemented mainly by leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods; mature fruit and flowers contained the most water-soluble carbohydrates; immature leaves were richest in protein and essential amino acids; the limiting amino acids in all plant foods were methionine and cystine; ash (mineral) content was highest in petioles and mature leaves; crude lipid content was highest in seeds; and crude fiber content was indistinguishable between immature and mature fruit and leaves. High-fiber foods were eaten during both seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles). However, nutrient intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These results suggest we draw more conservative conclusions when interpreting dietary variability in the absence of chemical analysis, and also draw into question the idea that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs.
Hartstone-Rose, Adam; Parkinson, Jennifer A; Criste, Taylor; Perry, Jonathan M G
Previously we found that Maximum Ingested Bite Size (Vb )-the largest piece of food that an animal will ingest whole without biting first-scales isometrically with body size in 17 species of strepsirrhines at the Duke Lemur Center (DLC). However, because this earlier study focused on only three food types (two with similar mechanical properties), it did not yield results that were easily applied to describing the broad diets of these taxa. Expressing Vb in terms of food mechanical properties allows us to compare data across food types, including foods of wild lemurs, to better understand dietary adaptations in lemurs. To this end, we quantified Vb in five species of lemurs at the DLC representing large and small frugivores and folivores using ten types of food that vary widely in stiffness and toughness to determine how these properties relate to bite sizes. We found that although most species take smaller bites of stiffer foods, this negative relationship was not statistically significant across the whole sample. However, there is a significant relationship between bite size and toughness. All three of the more frugivorous taxa in our sample take significantly smaller bites of tougher foods. However, the two more folivorous lemurs do not. They take small bites for all foods. This suggests that the species most adapted to the consumption of tough foods do not modulate their ingestive sizes to accommodate larger pieces of weak foods. © 2015 Wiley Periodicals, Inc.
Background Comprehensive explanations of behavioral adaptations rarely invoke all levels famously admonished by Niko Tinbergen. The role of developmental processes and plasticity, in particular, has often been neglected. In this paper, we combine ecological, physiological and developmental perspectives in developing a hypothesis to account for the evolution of ‘the lemur syndrome’, a combination of reduced sexual dimorphism, even adult sex ratios, female dominance and mild genital masculinization characterizing group-living species in two families of Malagasy primates. Results We review the different components of the lemur syndrome and compare it with similar adaptations reported for other mammals. We find support for the assertion that the lemur syndrome represents a unique set of integrated behavioral, demographic and morphological traits. We combine existing hypotheses about underlying adaptive function and proximate causation by adding a potential developmental mechanism linking maternal stress and filial masculinization, and outline an evolutionary scenario for its canalization. Conclusions We propose a new hypothesis linking ecological, physiological, developmental and evolutionary processes to adumbrate a comprehensive explanation for the evolution of the lemur syndrome, whose assumptions and predictions can guide diverse future research on lemurs. This hypothesis should also encourage students of other behavioral phenomena to consider the potential role of developmental plasticity in evolutionary innovation. PMID:26816515
Drea, Christine M
Female social dominance characterizes many strepsirrhine primates endemic to Madagascar, but currently there is no comprehensive explanation for how or why female lemurs routinely dominate males. Reconstructing the evolutionary pressures that may have shaped female dominance depends on better understanding the mechanism of inheritance, variation in trait expression, and correlating variables. Indeed, relative to males, many female lemurs also display delayed puberty, size monomorphism, and 'masculinized' external genitalia. As in the spotted hyena (Crocuta crocuta), a species characterized by extreme masculinization of the female, this array of traits focuses attention on the role of androgens in female development. Consequently, I examined endocrine profiles and social interaction in the ringtailed lemur (Lemur catta) to search for a potential source of circulating androgen in adult females and an endocrine correlate of female dominance or its proxy, aggression. I measured serum androstenedione (A(4)), testosterone (T), and estradiol (E(2)) in reproductively intact, adult lemurs (10 females; 12 males) over four annual cycles. Whereas T concentrations in males far exceeded those in females, A(4) concentrations were only slightly greater in males than in females. In both sexes, A(4) and T were positively correlated, implicating the Delta(4)-biosynthetic pathway. Moreover, seasonal changes in reproductive function in both sexes coincided with seasonal changes in behavior, with A(4) and T in males versus A(4) and E(2) in females increasing during periods marked by heightened aggression. Therefore, A(4) and/or E(2) may be potentially important steroidal sources in female lemurs that could modulate aggression and underlie a suite of masculinized features.
Knapp, Leslie A; Robson, Julie; Waterhouse, John S
The major histocompatibility complex (MHC) is the most polymorphic genetic system known in vertebrates. Decades of research demonstrate that it plays a critical role in immune response and disease resistance. It has also been suggested that MHC genes influence social behavior and reproductive phenomena. Studies in laboratory mice and rats report that kin recognition and mate choice are influenced by olfactory cues determined at least in part by an individual's MHC genes. This issue has stimulated intense but controversial research. However, work in this field has only been carried out in rodents and humans. Thus far, no study has directly investigated the relationship between olfactory cues and MHC genotype in nonhuman primates. Furthermore, other genetic loci, including those linked to the MHC, have not been ruled out as the primary influence on odor profiles. To explore the relationship between individual odor profiles and MHC alleles, we are studying ring-tailed lemurs (Lemur catta). These animals are an ideal model species because they are extremely scent-oriented and their behaviors suggest that olfactory signals form an important part of their intra- and intergroup communication systems. Individual odor profiles from tail and scent gland samples were generated for six males using gas chromatography mass spectrometry (GC-MS). MHC genotypes were identified using polymerase chain reaction (PCR) and denaturing gradient gel electrophoresis (DGGE). The GC-MS analyses demonstrated a difference between profiles obtained from tail and scent gland samples. Although our sample size is relatively small and statistical significance could not be obtained, our analyses suggest a relationship between MHC and concentrations of volatile compounds. While these results are preliminary, they support the need for further studies of the MHC and olfactory signals in lemurs and other primates. Copyright 2006 Wiley-Liss, Inc.
Rakotonirina, Hanitriniaina; Kappeler, Peter M; Fichtel, Claudia
Signals are essential for communication and play a fundamental role in the evolution and diversification of species. Olfactory, visual and acoustic species-specific signals have been shown to function for species recognition in non-human primates, but the relative contributions of selection for species recognition driven by sexual selection, natural selection, or genetic drift for the diversification of these signals remain largely unexplored. This study investigates the importance of acoustic signals for species recognition in redfronted lemurs (Eulemur rufifrons). We conducted playback experiments in both major populations of this species separated by several hundred kilometers: Kirindy Forest in the west and Ranomafana National Park in the east of Madagascar. The playback stimuli were composed of species-specific loud calls of E. rufifrons, three closely related species (E. albifrons, E. fulvus and E. rufus) and one genetically more distant species (E. rubriventer) that occurs in sympatry with eastern redfronted lemurs. We tested the ability of redfronted lemurs to discriminate conspecific from heterospecific loud calls by measuring the time spent looking towards the speaker after presentation of each loud call. We also tested the difference between female and male responses because loud calls may play a role in mate choice and the avoidance of heterospecific mating. Redfronted lemurs in Kirindy Forest did not discriminate their own loud calls from those of E. albifrons, E. fulvus and E. rufus, but they discriminated loud calls of E. rubriventer from their own. The Ranomafana population was tested only with three playback stimuli (E. rufifrons, E. albifrons, E. rubriventer) and did not discriminate between their own loud calls and those of E. albifrons and E. rubriventer. The response of females and males to playbacks did not differ in both populations. However, subjects in Ranomafana National Park responded more strongly to playback stimuli from E. rubriventer
Bertoncini, Stefania; D'Ercole, Jacopo; Brisighelli, Francesca; Ramanamanjato, Jean-Baptiste; Capelli, Cristian; Tofanelli, Sergio; Donati, Giuseppe
The Endangered collared brown lemur (Eulemur collaris) is the largest primate living in the littoral forest of southeastern Madagascar, a top priority habitat for biodiversity conservation on the island. Because this lemur is a key seed-disperser, an evaluation of the structure and connectivity of the populations surviving in the forest fragments is urgently needed to guide conservation plans. Genetic variability at autosomal microsatellites and mitochondrial DNA was investigated in a total of 49 collared brown lemurs sampled by non-invasive methods in three littoral forest fragments and in the nearby lowland humid forest. The overall genetic diversity of E. collaris in the southeastern coastal region of Madagascar was lower than in other populations, as well as in other lemur species. The population appears highly structured, with less variable and more inbred groups inhabiting the littoral forest fragments compared to the inland area. Major barriers to gene flow were identified isolating littoral forest fragments from each other and from the inland lowland humid forest. Medium to long-term drift and scarce gene flow is the scenario that best explains the current genetic distribution. Habitat discontinuities such as rivers and grassland between forest fragments played a major role in structuring the population. A common history of size contraction is pointed out by several genetic estimators, indicating a possible ecological crisis triggered around 1,300 years ago. The adoption of strategies aimed at facilitating gene flow and population growth appears crucial to delay further loss of genetic diversity. © 2017 Wiley Periodicals, Inc.
Dutton, Christopher J; Junge, Randall E; Louis, Edward E
Complete health assessments were performed on 22 adult red ruffed lemurs (Varecia rubra), comprising nine males and 13 females, found within the Masoala National Park in northeast Madagascar. Each animal was anesthetized using tiletamine and zolazepam and underwent a thorough physical examination, including measurement of its weight and vital signs; blood collection for hematology, plasma total protein concentration, serum chemistries, fat-soluble vitamins, trace minerals, assessment of iron metabolism, toxoplasmosis serology, viral serologies, and examination for hemoparasites; fecal collection for bacterial culture and parasite examination; and collection of a representative number of any ectoparasites. Comparison of blood values with those of captive lemurs demonstrated a number of significant differences thought to be associated with physiologic state (e.g., reproductive stage and stress), hydration, and diet. There was no evidence of serious infectious diseases, and hemoparasites were not detected. The enteric flora appeared unremarkable; however, results may have been skewed toward more cold-tolerant bacteria. The fecal parasite burden was low. Lemurostrongylus spp. was identified in two of the lemurs, and there were moderate numbers of Laelapidae mites present on approximately one third of the lemurs. This study demonstrated the substantial amount of data that can be collected from free-ranging populations, considered invaluable in the management of captive populations, in reducing the incidence of captivity-related diseases, and in the risk assessment associated with reintroduction programs.
Gould, Lisa; Power, Michael L; Ellwanger, Nicholas; Rambeloarivony, Hajamanitra
Strong resource seasonality in Madagascar has led to the evolution of female feeding priority and weaning synchrony in most lemur species. For these taxa, pregnancy/early lactation periods coincide with low food availability, and weaning of infants is timed with increased resources at the onset of the rainy season. Reproductive females experience high metabolic requirements, which they must accommodate, particularly when food resources are scarce. Female ring-tailed lemurs (Lemur catta) residing in spiny forest habitat must deal with resource scarcity, high temperatures (∼36-40°C) and little shade in early to mid-lactation periods. Considered "income breeders," these females must use resources obtained from the environment instead of relying on fat stores; thus, we expected they would differ from same-sized males in time spent on feeding and in the intake of food and nutrients. We investigated these variables in two groups (N = 11 and 12) of Lemur catta residing in spiny forest habitat during early gestation and early to mid-lactation periods. Focal animal data and food plant samples were collected, and plants were analyzed for protein, kcal, and fiber. We found no sex differences for any feeding or nutrient intake variable for the top five food species consumed. Females in early gestation spent more time feeding compared with early/mid-lactation. Physiological compensation for spiny forest-dwelling females may be tied to greater time spent resting compared with gallery forest conspecifics, consuming foods high in protein, calories, and water, reduced home range defense in a sparsely populated habitat, and for Lemur catta females in general, production of relatively dilute milk compared with many strepsirrhines.
Elofsson, Rolf; Tuminaite, Inga; Kröger, Ronald H H
Most mammals have nose tips covered by glabrous skin, a labronasal area, or rhinarium. The surface of the rhinarium of Lemur catta has a dermatoglyphic pattern consisting of epidermal domes. Below the domes, epidermal pegs dip down into the dermis. In and below the tip of the epidermal peg, a complex sensory organ is found. It consists of an association of innervated Merkel cells, lamellate (Pacini-like) bodies with a central nerve, and a ring of unmyelinated nerve endings in the epidermis. The Merkel cells are situated basally in the epidermis and the lamellated bodies just below the epidermis. The unmyelinated nerve endings related to the organ ascend in a circle straight through the epidermis ending below the corneal layer. From these nerve terminals, horizontal spikes enter the keratinocytes. The three components occur together forming an organ and are innervated from a common nerve plexus. The morphology of the complex sensory organ of the lemur shares most crucial components with Eimer's organs in moles, echidna, and platypus, while some structures are lacking, for example, the specific central pillar of keratinocytes, the cuticular cap, and a central unmyelinated fiber. The presence of the essentials of an Eimer's organ in many mammals suggests that a wider definition is motivated.
Ferrie, Gina M; Becker, Kris K; Wheaton, Catharine J; Fontenot, Deidre; Bettinger, Tammie
To reduce male-male aggression in collared lemurs (Eulemur collaris) at Disney's Animal Kingdom, a clinical trial of leuprolide acetate (Depo-Lupron) injections through one breeding season (24 wk), followed by surgical castration after the breeding season was implemented. Daily behavioral observations to record occurrences of aggression were conducted before and during the injection period, as well as after castration. Fecal sample collection began 2 wk before the first injection and continued throughout the clinical trial to determine testosterone metabolite concentration. Samples were collected 3 times per week. Fecal collection and behavioral observation continued for 5 mo after castration. Fecal samples from 3 intact males from other institutions were obtained to compare testosterone values. While the lemurs were treated with Depo-Lupron, testosterone concentrations spiked immediately after injection, and then returned to pretreatment, nonbreeding-season levels after varying lengths of time. Analysis of the behavioral data indicated that aggression was not significantly reduced with Depo-Lupron treatment. However, after castration, contact aggression and wounding decreased to zero. Although the sample is small, this study presents the first documented data on the effects that chemical treatment with Depo-Lupron and surgical castration have upon hormone levels and aggressive behavior in eulemurs.
Lei, Runhua; Frasier, Cynthia L; Hawkins, Melissa T R; Engberg, Shannon E; Bailey, Carolyn A; Johnson, Steig E; McLain, Adam T; Groves, Colin P; Perry, George H; Nash, Stephen D; Mittermeier, Russell A; Louis, Edward E
The family Lepilemuridae includes 26 species of sportive lemurs, most of which were recently described. The cryptic morphological differences confounded taxonomy until recent molecular studies; however, some species' boundaries remain uncertain. To better understand the genus Lepilemur, we analyzed 35 complete mitochondrial genomes representing all recognized 26 sportive lemur taxa and estimated divergence dates. With our dataset we recovered 25 reciprocally monophyletic lineages, as well as an admixed clade containing Lepilemur mittermeieri and Lepilemur dorsalis Using modern distribution data, an ancestral area reconstruction and an ecological vicariance analysis were performed to trace the history of diversification and to test biogeographic hypotheses. We estimated the initial split between the eastern and western Lepilemur clades to have occurred in the Miocene. Divergence of most species occurred from the Pliocene to the Pleistocene. The biogeographic patterns recovered in this study were better addressed with a combinatorial approach including climate, watersheds, and rivers. Generally, current climate and watershed hypotheses performed better for western and eastern clades, while speciation of northern clades was not adequately supported using the ecological factors incorporated in this study. Thus, multiple mechanisms likely contributed to the speciation and distribution patterns in Lepilemur.
Campbell, Sara E; Cuozzo, Frank P; Sauther, Michelle L; Sponheimer, Matt; Ferguson, Virginia L
The common morphological metrics of size, shape, and enamel thickness of teeth are believed to reflect the functional requirements of a primate's diet. However, the mechanical and material properties of enamel also contribute to tooth function, yet are rarely studied. Substantial wear and tooth loss previously documented in Lemur catta at the Beza Mahafaly Special Reserve suggests that their dental morphology, structure, and possibly their enamel are not adapted for their current fallback food (the mechanically challenging tamarind fruit). In this study, we investigate the nanomechanical properties, mineralization, and microstructure of the enamel of three sympatric lemur species to provide insight into their dietary functional adaptations. Mechanical properties measured by nanoindentation were compared to measurements of mineral content, prism orientation, prism size, and enamel thickness using electron microscopy. Mechanical properties of all species were similar near the enamel dentin junction and variations correlated with changes in microstructure (e.g., prism size) and mineral content. Severe wear and microcracking within L. catta's enamel were associated with up to a 43% reduction in nanomechanical properties in regions of cracking versus intact enamel. The mechanical and material properties of L. catta's enamel are similar to those of sympatric folivores and suggest that they are not uniquely mechanically adapted to consume the physically challenging tamarind fruit. An understanding of the material and mechanical properties of enamel is required to fully elucidate the functional and ecological adaptations of primate teeth. Copyright © 2012 Wiley Periodicals, Inc.
Schnoell, Anna Viktoria; Fichtel, Claudia
Reports on behavioural innovations in wild primate populations as well as on their transmission are rare. Here, we report observations suggesting that redfronted lemurs (Eulemur rufifrons) invent new behaviours in the wild. We observed a novel feeding behaviour in redfronted lemurs in Kirindy Forest, western Madagascar. The feeding behaviour consisted of depletion of nests of a social spider species (Stegodyphus sp.). The behaviour was observed in only one out of four study groups, although spider nests were present in the home ranges of all four groups. The behaviour was exhibited in three different years (2009, 2011, 2012) and appears to be re-invented from time to time. Interestingly, in 2011 this behaviour was shown by four individuals and probably spread within the group. This feeding behaviour has only been observed between the middle of June and early August (i.e. the early dry season), and nests were found to be empty later on, suggesting that these nests are available as a food source only seasonally. Our observation contributes a rare case of behavioural innovations in a wild primate population.
Crawford, Jeremy Chase; Boulet, Marylène; Drea, Christine M.
Animals, including humans, use olfaction to assess potential social and sexual partners. Although hormones modulate olfactory cues, we know little about whether contraception affects semiochemical signals and, ultimately, mate choice. We examined the effects of a common contraceptive, medroxyprogesterone acetate (MPA), on the olfactory cues of female ring-tailed lemurs (Lemur catta), and the behavioural response these cues generated in male conspecifics. The genital odorants of contracepted females were dramatically altered, falling well outside the range of normal female variation: MPA decreased the richness and modified the relative abundances of volatile chemicals expressed in labial secretions. Comparisons between treatment groups revealed several indicator compounds that could reliably signal female reproductive status to conspecifics. MPA also changed a female's individual chemical ‘signature’, while minimizing her chemical distinctiveness relative to other contracepted females. Most remarkably, MPA degraded the chemical patterns that encode honest information about genetic constitution, including individual diversity (heterozygosity) and pairwise relatedness to conspecifics. Lastly, males preferentially investigated the odorants of intact over contracepted females, clearly distinguishing those with immediate reproductive potential. By altering the olfactory cues that signal fertility, individuality, genetic quality and relatedness, contraceptives may disrupt intraspecific interactions in primates, including those relevant to kin recognition and mate choice. PMID:20667870
Zannella, Alessandra; Norscia, Ivan; Stanyon, Roscoe; Palagi, Elisabetta
Yawning, although easily recognized, is difficult to explain. Traditional explanations stressed physiological mechanisms, but more recently, behavioral processes have received increasing attention. This is the first study to test a range of hypotheses on yawning in wild primate populations. We studied two sympatric strepsirrhine species, Lemur catta, and Propithecus verreauxi, of the Ankoba forest (24.99°S, 46.29°E, Berenty reserve) in southern Madagascar. Sexual dimorphism is lacking in both species. However, their differences in ecological and behavioral characteristics facilitate comparative tests of hypotheses on yawning. Our results show that within each species males and females yawned with similar frequencies supporting the Dimorphism Hypothesis, which predicts that low sexual dimorphism leads to little inter-sexual differences in yawning. In support of the State Changing Hypothesis yawning frequencies was linked to the sleep-wake cycle and punctuated transitions from one behavior to another. Accordingly, yawning frequencies were significantly higher in L. catta than in P. verreauxi, because L. catta has a higher basal level of activity and consequently a higher number of behavioral transitions. In agreement with the Anxiety Hypothesis, yawning increased significantly in the 10 min following predatory attacks or aggression. Our findings provide the first empirical evidence of a direct connection between anxiety and yawning in lemurs. Our results show that yawning in these two strepsirrhines occurs in different contexts, but more research will be necessary to determine if yawns are a single, unitary behavior. © 2015 Wiley Periodicals, Inc.
Jones, H; McGregor, P K; Farmer, H L A; Baker, K R
Research suggests that zoo visitors can have positive, negative, and neutral impacts on captive primate welfare; however, research investigating the implications of visitor-animal feeding experiences is extremely limited. In the UK, a large proportion of BIAZA zoos that house lemur species offer visitor interaction experiences (16 out of 33). This study investigated the impact on the behavior of a family group of crowned lemurs (Eulemur coronatus) housed at Newquay Zoo, UK of visitors, accompanied by a keeper, entering the enclosure to feed the lemurs. Behavior was observed under four conditions: (i) during visitor feed; (ii) 30 min post-visitor feed; (iii) during a keeper feed; and (iv) 30 min post-keeper feed. Keeper feeds were conducted by keepers only, on the day after visitor feeds. The lemur group spent significantly less time performing aggressive behavior and was also significantly more interactive with keepers during visitor feeds compared with keeper-only feeds. There was no significant difference in behaviors performed immediately after interacting with visitors. Over the study period, there was a tendency for interactions with visitors to increase, and for interactions with keepers during visitor feeds to decrease. After a 28-day interval without visitor interaction, the lemurs' interaction with visitors had returned to the level recorded at the start of the study. In conclusion, visitor interaction did not compromise the welfare of the study subjects in either the short- or long-term, while an increase in visitor interactions over time has interesting implications for the enrichment properties of, or habituation to, unfamiliar humans. Zoo Biol. 35:222-227, 2016. © 2016 Wiley Periodicals, Inc.
Donati, Giuseppe; Santini, Luca; Razafindramanana, Josia; Boitani, Luigi; Borgognini-Tarli, Silvana
The ability to operate during the day and at night (i.e., cathemerality) is common among mammals but has rarely been identified in primates. Adaptive hypotheses assume that cathemerality represents a stable adaptation in primates, while nonadaptive hypotheses propose that it is the result of an evolutionary disequilibrium arising from human impacts on natural habitats. Madagascar offers a unique opportunity to study the evolution of activity patterns as there we find a monophyletic primate radiation that shows nocturnal, diurnal, and cathemeral patterns. However, when and why cathemeral activity evolved in lemurs is the subject of intense debate. Thus far, this activity pattern has been regularly observed in only three lemurid genera but the actual number of lemur species exhibiting this activity is as yet unknown. Here we show that the ring-tailed lemur, Lemur catta, a species previously considered to be diurnal, can in fact be cathemeral in the wild. In neighboring but distinct forest areas these lemurs exhibited either mainly diurnal or cathemeral activity. We found that, as in other cathemeral lemurs, activity was entrained by photoperiod and masked by nocturnal luminosity. Our results confirm the relationship between transitional eye anatomy and physiology and 24-h activity, thus supporting the adaptive scenario. Also, on the basis of the most recent strepsirrhine phylogenetic reconstruction, using parsimony criterion, our findings suggest pushing back the emergence of cathemerality to stem lemurids. Flexible activity over 24-h could thus have been one of the key adaptations of the early lemurid radiation possibly driven by Madagascar's island ecology.
Killick, Rowena; Saunders, Richard; Redrobe, Sharon P
Serum samples were collected from 18 lemurs of four diurnal/cathemeral species housed with outdoor access at Bristol Zoo Gardens (United Kingdom) to test 25-hydroxy-vitamin D3 (25OHD3) levels as part of the veterinary department's preventative health care program. Samples were collected from each lemur in August 2008 (summer) and January 2009 (winter) to examine the effect of season on 25OHD3 levels. The lemurs were fed commercial primate food and a range of fruit and vegetables, and dietary levels of vitamin D3 remained the same throughout the study period. Statistical analysis showed that the lemurs' summer 25OHD3 values (range 26.7 to >150.0 μg/L) were significantly higher than their winter 25OHD3 values (range 11.4-87.1 μg/L). UVB measurements taken during the study period confirmed that UVB levels were significantly higher in summer (mean reading for 1200-1300 GMT time period 153.8 μW/cm2) compared to winter (mean reading for 1200-1300 GMT time period 19.4 μW/cm2). The 25OHD3 levels measured were generally found to be high compared to previously published values from wild (free-ranging) lemurs in Madagascar. The most likely explanation for this was the higher vitamin D3 content of the captive lemurs' diet, as UVB levels at the zoo (latitude 51° north) are substantially lower than those that occur in Madagascar (latitude 12°-26° south). No evidence of vitamin D toxicity or deficiency was found in any of the captive lemurs. The results indicate that vitamin D3 levels in lemurs housed with outdoor access in the United Kingdom and by extension, other regions of similar latitude, vary with seasonal environmental UVB levels, in a similar way to the seasonal variations in vitamin D3 observed in humans living in these regions, but that vitamin D levels in this captive lemur population were adequate compared to wild lemur levels, even in winter.
Delmore, Kira E; Louis, Edward E; Johnson, Steig E
Hybridization has recently been identified as a pervasive force in the evolution of primates. In this study, we characterized a hybrid zone between two species of brown lemur (Eulemur rufifrons and E. cinereiceps) in the Andringitra region of southeastern Madagascar using morphological traits. We immobilized animals along a north-south transect (∼80 km), scored them for their degree of hybridity using pelage traits and measured standard morphometric variables. Results from our study suggest that hybridization between E. rufifrons and E. cinereiceps is extensive, with the hybrid zone extending over 42.6 km and being composed mostly of later generation hybrids. We also identified significant variation between ancestral groups in our study: hybrid males exhibited longer tails than both parental species and sexual dimorphism in upper canine height favoring males was documented in E. rufifrons. These patterns could suggest that gene flow between parental and hybrid populations is relatively limited. Finally, significant differences between ancestral groups in relative body mass and skin-fold thickness were absent in our study, indicating that, as measured by these proxies, hybrids are equally as fit as parental forms. Based on these preliminary findings, the Andringitra hybrid zone could conform to the bounded superiority model of hybrid zone stability (i.e., it could be being maintained by selection favoring hybrids within transitional habitats). Accordingly, hybrids in Andringitra may be an unusual case among primates, representing a stable recombinant but distinct lineage. This conclusion has important implications for evolutionary processes within the brown lemur species complex. Copyright © 2011 Wiley-Liss, Inc.
Hilgartner, Roland; Fichtel, Claudia; Kappeler, Peter M; Zinner, Dietmar
Pair-living and a monogamous mating strategy are rare and theoretically unexpected among mammals. Nevertheless, about 10% of primate species exhibit such a social system, which is difficult to explain in the absence of paternal care. In this study, we investigated the two major hypotheses proposed to explain the evolution of monogamy in mammals, the female defence hypothesis (FDH) and the resource defence hypothesis (RDH), in red-tailed sportive lemurs (Lepilemur ruficaudatus), a nocturnal primate from Madagascar. We analysed behavioural data from eight male–female pairs collected during a 24-mo field study to illuminate the determinants of pair-living in this species. Male and female L. ruficaudatus were found to live in dispersed pairs, which are characterised by low cohesion and low encounter rates within a common home range. Social interactions between pair partners were mainly agonistic and characterised by a complete absence of affiliative interactions – body contact was only observed during mating. During the short annual mating season, males exhibited elevated levels of aggression towards mates, as well as extensive mate guarding and increased locomotor activity. In addition, males were exclusively responsible for the maintenance of proximity between pair partners during this period, and they defended their territories against neighbouring males but not against females. Together, these results point towards the importance of female defence in explaining pair-living in L. ruficaudatus. We discuss the spatial and temporal distribution of receptive females in relation to the female defence strategies of males and suggest possible costs that prevent male red-tailed sportive lemurs from defending more than one female. PMID:23144523
Dominance hierarchy influences the life quality of social animals, and its definition should in principle be based on the outcome of agonistic interactions. However, defining and comparing the dominance profile of social groups is difficult due to the different dominance measures used and because no one measure explains it all. We applied different analytical methods to winner-loser sociomatrices to determine the dominance profile of five groups of wild lemurs (species: Lemur catta, Propithecus verreauxi, and Eulemur rufus x collaris) from the Berenty forest (Madagascar). They are an excellent study model because they share the same habitat and an apparently similar dominance profile: linear hierarchy and female dominance. Data were collected over more than 1200 h of observation. Our approach included four steps: (1) by applying the binary dyadic dominance relationship method (I&SI) on either aggressions or supplant sociomatrices we verified whether hierarchy was aggression or submission based; (2) by calculating normalized David’s scores and measuring steepness from aggression sociomatrices we evaluated whether hierarchy was shallow or steep; (3) by comparing the ranking orders obtained with methods 1 and 2 we assessed whether hierarchy was consistent or not; and (4) by assessing triangle transitivity and comparing it with the linearity index and the level of group cohesion we determined if hierarchy was more or less cohesive. Our results show that L. catta groups have got a steep, consistent, highly transitive and cohesive hierarchy. P. verreauxi groups are characterized by a moderately steep and consistent hierarchy, with variable levels of triangle transitivity and cohesion. E. rufus x collaris group possesses a shallow and inconsistent hierarchy, with lower (but not lowest) levels of transitivity and cohesion. A multiple analytical approach on winner-loser sociomatrices other than leading to an in-depth description of the dominance profile, allows intergroup
Campbell, J L; Williams, C V; Eisemann, J H
Differences in dietary profiles and gastrointestinal (GI) morphologies observed across lemur species suggest that there may be variation in patterns of digesta flow through the GI tract related to the method of digesta processing. Using radio-opaque barium-impregnated polyethylene spheres (BIPS), we characterized such patterns in four lemur species: Varecia variegata (VV), Eulemur fulvus (EF), Propithecus verreauxi (PV), and Hapalemur griseus (HG) (n = 2 per species). After an initial radiograph was taken under light sedation, the animals were fed the BIPS together with a small meal. A combination of 30 small (1.5 mm) and 10 large (5 mm) BIPS was administered. Radiographs were then taken on a species-dependent basis up to 48 hr post-dosage. For small BIPS, the gastric transit time (GTT; time of first exit of BIPS from stomach) was 0.25-2 hr for VV, EF, and HG, and approximately 10 hr for PV. The oro-rectal transit time (ORTT; time of first appearance in the rectum) was < 2 hr for VV and EF, and 24.0 hr for PV and HG. The intestinal transit time (ITT, measured as ORTT - GTT) was < 1.5 hr for VV and EF, and approximately 14 hr and 22 hr for PV and HG, respectively. These data suggest that the GTT of digesta as measured with BIPS was rapid for VV, EF, and HG. For VV and EF, the ORTT and ITT were also rapid, while for HG they were much slower. PV was characterized by delayed GTT, and a more rapid ITT compared to HG. Thus, patterns of flow for PV and HG, despite similar ORTT, differed in that HG emptied BIPS more rapidly and ITT was slower. The flow of BIPS did not differ for VV and EF. These data reveal new information in addition to the total tract transit time, and complement existing knowledge regarding anatomy and diet.
Perry, George H; Reeves, Darryl; Melsted, Páll; Ratan, Aakrosh; Miller, Webb; Michelini, Katelyn; Louis, Edward E; Pritchard, Jonathan K; Mason, Christopher E; Gilad, Yoav
We present a high-coverage draft genome assembly of the aye-aye (Daubentonia madagascariensis), a highly unusual nocturnal primate from Madagascar. Our assembly totals ~3.0 billion bp (3.0 Gb), roughly the size of the human genome, comprised of ~2.6 million scaffolds (N50 scaffold size = 13,597 bp) based on short paired-end sequencing reads. We compared the aye-aye genome sequence data with four other published primate genomes (human, chimpanzee, orangutan, and rhesus macaque) as well as with the mouse and dog genomes as nonprimate outgroups. Unexpectedly, we observed strong evidence for a relatively slow substitution rate in the aye-aye lineage compared with these and other primates. In fact, the aye-aye branch length is estimated to be ~10% shorter than that of the human lineage, which is known for its low substitution rate. This finding may be explained, in part, by the protracted aye-aye life-history pattern, including late weaning and age of first reproduction relative to other lemurs. Additionally, the availability of this draft lemur genome sequence allowed us to polarize nucleotide and protein sequence changes to the ancestral primate lineage-a critical period in primate evolution, for which the relevant fossil record is sparse. Finally, we identified 293,800 high-confidence single nucleotide polymorphisms in the donor individual for our aye-aye genome sequence, a captive-born individual from two wild-born parents. The resulting heterozygosity estimate of 0.051% is the lowest of any primate studied to date, which is understandable considering the aye-aye's extensive home-range size and relatively low population densities. Yet this level of genetic diversity also suggests that conservation efforts benefiting this unusual species should be prioritized, especially in the face of the accelerating degradation and fragmentation of Madagascar's forests.
Perry, George H.; Reeves, Darryl; Melsted, Páll; Ratan, Aakrosh; Miller, Webb; Michelini, Katelyn; Louis, Edward E.; Pritchard, Jonathan K.; Mason, Christopher E.; Gilad, Yoav
We present a high-coverage draft genome assembly of the aye-aye (Daubentonia madagascariensis), a highly unusual nocturnal primate from Madagascar. Our assembly totals ∼3.0 billion bp (3.0 Gb), roughly the size of the human genome, comprised of ∼2.6 million scaffolds (N50 scaffold size = 13,597 bp) based on short paired-end sequencing reads. We compared the aye-aye genome sequence data with four other published primate genomes (human, chimpanzee, orangutan, and rhesus macaque) as well as with the mouse and dog genomes as nonprimate outgroups. Unexpectedly, we observed strong evidence for a relatively slow substitution rate in the aye-aye lineage compared with these and other primates. In fact, the aye-aye branch length is estimated to be ∼10% shorter than that of the human lineage, which is known for its low substitution rate. This finding may be explained, in part, by the protracted aye-aye life-history pattern, including late weaning and age of first reproduction relative to other lemurs. Additionally, the availability of this draft lemur genome sequence allowed us to polarize nucleotide and protein sequence changes to the ancestral primate lineage—a critical period in primate evolution, for which the relevant fossil record is sparse. Finally, we identified 293,800 high-confidence single nucleotide polymorphisms in the donor individual for our aye-aye genome sequence, a captive-born individual from two wild-born parents. The resulting heterozygosity estimate of 0.051% is the lowest of any primate studied to date, which is understandable considering the aye-aye's extensive home-range size and relatively low population densities. Yet this level of genetic diversity also suggests that conservation efforts benefiting this unusual species should be prioritized, especially in the face of the accelerating degradation and fragmentation of Madagascar's forests. PMID:22155688
Norscia, Ivan; Palagi, Elisabetta
Dominance hierarchy influences the life quality of social animals, and its definition should in principle be based on the outcome of agonistic interactions. However, defining and comparing the dominance profile of social groups is difficult due to the different dominance measures used and because no one measure explains it all. We applied different analytical methods to winner-loser sociomatrices to determine the dominance profile of five groups of wild lemurs (species: Lemur catta, Propithecus verreauxi, and Eulemur rufus x collaris) from the Berenty forest (Madagascar). They are an excellent study model because they share the same habitat and an apparently similar dominance profile: linear hierarchy and female dominance. Data were collected over more than 1200 h of observation. Our approach included four steps: (1) by applying the binary dyadic dominance relationship method (I&SI) on either aggressions or supplant sociomatrices we verified whether hierarchy was aggression or submission based; (2) by calculating normalized David's scores and measuring steepness from aggression sociomatrices we evaluated whether hierarchy was shallow or steep; (3) by comparing the ranking orders obtained with methods 1 and 2 we assessed whether hierarchy was consistent or not; and (4) by assessing triangle transitivity and comparing it with the linearity index and the level of group cohesion we determined if hierarchy was more or less cohesive. Our results show that L. catta groups have got a steep, consistent, highly transitive and cohesive hierarchy. P. verreauxi groups are characterized by a moderately steep and consistent hierarchy, with variable levels of triangle transitivity and cohesion. E. rufus x collaris group possesses a shallow and inconsistent hierarchy, with lower (but not lowest) levels of transitivity and cohesion. A multiple analytical approach on winner-loser sociomatrices other than leading to an in-depth description of the dominance profile, allows intergroup
Gaide, N; Pelandakis, M; Robveille, C; Albaric, O; Jouvion, G; Souchon, M; Risler, A; Abadie, J
A mature male, black and white ruffed lemur (Varecia variegata variegata) died in a zoological garden after a 4-day history of lethargy and non-responsive convulsions. Necropsy and histopathological examinations revealed acute necrotizing and haemorrhagic meningoencephalitis with intralesional amoebas confirmed by immunohistochemistry. Acanthamoeba T4 genotype was identified as the causative agent of the brain lesion, based on amplification and sequencing of 18S ribosomal RNA genes. The presence of free-living amoebas in water and mud from the lemur's environment was investigated by morphological and molecular analyses. The two predominant genera, representing 80% of isolated amoebas, were Naegleria spp. and Acanthamoeba spp. All Acanthamoeba isolates belonged to the T4 genotype. To the author's knowledge, this is the first report of a meningoencephalitis due to Acanthamoeba T4 genotype in Lemuridae with concurrent analysis of pathological tissues and environment. Copyright © 2015 Elsevier Ltd. All rights reserved.
Junge, Randall E; Dutton, Christopher J; Knightly, Felicia; Williams, Cathy V; Rasambainarivo, Fidisoa T; Louis, Edward E
Health and nutritional assessments of wildlife are important management tools and can provide a means to evaluate ecosystem health. Such examinations were performed on 37 white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. Comparison of health parameters between sites revealed statistically significant differences in body weight, body temperature, respiratory rate, hematology parameters (white cell count, hematocrit, segmented neutrophil count, and lymphocyte count), serum chemistry parameters (aspartate aminotransferase, alanine aminotransferase, serum alkaline phosphatase, total protein, albumin, phosphorus, calcium, sodium, chloride, and creatinine phosphokinase), and nutrition parameters (copper, zinc, ferritin, retinol, tocopherol, and 25-hydroxycholecalciferol). Two of 10 lemurs tested were positive for toxoplasmosis; none of 10 were positive for Cryptosporidium or Giardia. Enteric bacteria and endo- and ectoparasites were typical. Statistically different values in hematology and chemistry values probably do not reflect clinically significant differences, whereas nutrition parameter differences are likely related to season, soil, and forage availability.
Zehr, Sarah M; Roach, Richard G; Haring, David; Taylor, Julie; Cameron, Freda H; Yoder, Anne D
Since its establishment in 1966, the Duke Lemur Center (DLC) has accumulated detailed records for nearly 4,200 individuals from over 40 strepsirrhine primate taxa-the lemurs, lorises, and galagos. Here we present verified data for 3,627 individuals of 27 taxa in the form of a life history table containing summarized species values for variables relating to ancestry, reproduction, longevity, and body mass, as well as the two raw data files containing direct and calculated variables from which this summary table is built. Large sample sizes, longitudinal data that in many cases span an animal's entire life, exact dates of events, and large numbers of individuals from closely related yet biologically diverse primate taxa make these datasets unique. This single source for verified raw data and systematically compiled species values, particularly in combination with the availability of associated biological samples and the current live colony for research, will support future studies from an enormous spectrum of disciplines.
Baden, Andrea L; Webster, Timothy H; Kamilar, Jason M
Ruffed lemurs (genus Varecia) are often described as having a flexible social organization, such that both cohesive (low fission-fusion dynamics) and fluid (high fission-fusion dynamics) grouping patterns have been observed. In ruffed lemur communities with high fission-fusion dynamics, group members vary in their temporal and spatial dispersion throughout a communally defended territory. These patterns have been likened to those observed in several haplorrhine species that exhibit the most fluid types of fission-fusion social organization (e.g., Pan and Ateles). To substantiate and further refine these claims, we describe the fission-fusion dynamics of a black-and-white ruffed lemur (Varecia variegata) community at Mangevo, an undisturbed primary rainforest site in Ranomafana National Park, Madagascar. We collected instantaneous group scan samples from August 2007-December 2008 (4,044 observation hours) to study and characterize patterns of subgroup size, composition, cohesion, and social association. In 16 consecutive months, we never found all members of the community together. In fact, individuals spent nearly half of their time alone. Subgroups were small, cohesive, and typically of mixed-sex composition. Mixed-sex subgroups were significantly larger, less cohesive, and more common than either male-only or female-only subgroups. Subgroup dynamics were related to shifts in climate, phenology of preferred fruit species, and female reproductive state. On average, association indices were low. Males and females were equally gregarious; however, adult male-male associations were significantly weaker than any other association type. Results presented herein document striking differences in fission-fusion dynamics between black-and-white ruffed lemurs and haplorrhines, while also demonstrating many broad-scale similarities to haplorrhine taxa that possess the most fluid fission-fusion societies. © 2015 Wiley Periodicals, Inc.
Donati, G; Lunardini, A; Kappeler, P M; Borgognini Tarli, S M
Several ecological and physiological factors have been suggested to structure circadian activity in cathemeral primates, i.e., those that are regularly active both day and night, but their relative importance remains controversial. We studied the nocturnal activity of a group of cathemeral redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest in Western Madagascar to examine its relationship with one environmental factor, ambient light levels, in detail. To this end, nightly travel distances and moon luminosity were determined between March and June 1996. During this transitional period between the wet and dry seasons these red-fronted lemurs were regularly active at night, and traveled significantly larger distances during full-moon nights compared to new-moon nights. The importance of ambient luminosity for nocturnal activity was highlighted by observations during a total lunar eclipse (i.e., during a full-moon night), which caused abrupt cessation of the animal's activity. Our results support the hypothesis that nocturnal activity of these cathemeral lemurs is regulated also by changes in ambient light levels.
Eppley, Timothy M.; Donati, Giuseppe; Ramanamanjato, Jean-Baptiste; Randriatafika, Faly; Andriamandimbiarisoa, Laza N.; Rabehevitra, David; Ravelomanantsoa, Robertin; Ganzhorn, Jörg U.
The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations. PMID:26536667
Mason, G A; Buettner-Janusch, J
Red cell acid phosphatase phenotypes of 207 captive animals of the genera Lemur, Hapalemur, and Prophithecus were determined by starch gel electrophoresis and phosphatase-specific staining. In Lemur fulvus, three phenotypes, designated A, B, and AB, were observed. In each of the species L. catta, L. macaco, L. mongoz, and L. variegatus, a single phenotype was observed, In Hapalemur griseus, three phenotypes were found: A,B, and AB. In Propithecus verreauxi, a single phenotype was found. Examination of breeding records in conjunction with the results of the electrophoretic analyses supports the conclusion that the erythrocytic acid phosphatases in this group of nonhuman primates are the products of at least two codominant autosomal alleles. There is a wide range of specific activities of the acid phosphatases as determined by colorimetric assays. The values range from 60.6 micronmoles of p-nitrophenol released per gram of hemoglobin per 30 min in Lemur catta to 429.1 micronmoles in Propithecus verreauxi. The enzymes of L. fulvus and P. vereauxi were purified approximately 400-fold, and Michaelis-Menten constants were determined on the purified preparations. For L. fulvus phenotype A, Km = 0.8 mM; for L. fulvus phenotype B, Km = 0.8 mM; and for P. verreauxi, Km = 0.6 mM; the substrate in each case was p-nitrophenylphosphate.
Rasoloharijaona, Solofonirina; Randrianambinina, Blanchard; Zimmermann, Elke
Suitable sleeping sites as potentially restricted resources are suggested to shape sociality in primates. We investigated sleeping site ecology of a rain-forest dwelling sportive lemur in eastern Madagascar for the first time. Using radiotelemetry, we characterized the type, quality and usage of sleeping sites as well as social sleeping habits of 11 focal individuals of the weasel sportive lemur (Lepilemur mustelinus) during the dry and the onset of the rainy season. Morphometric measurements provided additional information. The sexes showed an unusual sexual dimorphism for primates. Males and females did not differ in body length, but females surpassed males in body mass suggesting female dominance. Both sexes used dense vegetation and holes in hollow trees high above the ground as shelters for sleeping during the day. No sex difference in the quality of tree holes was found, but focal individuals used tree holes more often than open sleeping sites in dense vegetation. Both sexes showed high sleeping site fidelity limited to two to six different sites that they used primarily solitarily. The results imply that suitable sleeping sites are limited and survival of this species will strongly depend on the availability of mature rain forests with suitable hollow trees. Furthermore, these findings provide evidence of a solitary sleeping and ranging system in this rain-forest dwelling sportive lemur with suitable sleeping sites as defendable resources.
Eppley, Timothy M; Donati, Giuseppe; Ramanamanjato, Jean-Baptiste; Randriatafika, Faly; Andriamandimbiarisoa, Laza N; Rabehevitra, David; Ravelomanantsoa, Robertin; Ganzhorn, Jörg U
The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations.
Jacobs, A; Maumy, M; Petit, O
Studies on leadership during group movements in several lemur species showed that females were responsible for the travelling choices concerning time and direction. Interestingly, in these species females are dominant over males. We investigated the influence of social organisation upon leadership processes by studying a lemur species in which social organisation is characterized by the absence of female dominance: the brown lemur (Eulemur fulvus fulvus). The study was conducted on a semi-free ranging group of 11 individuals and the analysis performed on 69 group movements showed that all the individuals could initiate a group movement. In 34 cases, the whole group moved. There was no significant difference in the number of start attempts or in the number of group members involved from one initiator to another. Moreover, there was no effect of sex or age of the initiator on the number of individuals following it or on the speed of the joining process. Therefore, the leadership observed is widely distributed to all group members. These results support the hypothesis of an influence of social organisation upon the decision-making processes but still remain to be studied in a more relevant ecological context.
Blanco, Marina B.; Godfrey, Laurie R.; Rakotondratsima, Mamihasimbola; Rahalinarivo, Vololonirina; Samonds, Karen E.; Raharison, Jean-Luc; Irwin, Mitchell T.
The number of species within the Malagasy lemur genus Cheirogaleus is currently under debate. Museum collections are spotty, and field work, supplemented by morphometric and genetic analysis, is essential for documenting geographic distributions, ecological characteristics and species boundaries. We report here field evidence for 2 dwarf lemur species at Tsinjoarivo, an eastern-central high-altitude rain forest: one, from a forest fragment, displaying coat and dental characteristics similar to C. sibreei (previously described only from museum specimens) and the other, from the continuous forest, resembling individuals of Cheirogaleus found today at Ranomafana National Park, further to the south. This study represents the first confirmation of a living population of grey-fawn, C.-sibreei-like, dwarf lemurs in Madagascar. PMID:19023214
Nelson, Eliza L; O'Karma, Jaime M; Ruperti, Felicia S; Novak, Melinda A
Previous studies in human and chimpanzee infants have identified a predictive relationship between early rightward head orientation and later right hand use. Data from lemurs suggest a leftward bias in hand preference, but there are no data on head positioning. The purpose of this study was to examine the relationship between head and hand preferences in the black and white ruffed lemur (Varecia variegata variegata). Ruffed lemurs rotate the head vertically during chewing in a behavior called head-tilting. Frequency of head-tilting and bouts of unimanual hand use were measured during normal feeding in a semi-free-ranging population of lemurs. Subjects were provisioned at feeding platforms twice daily with fresh fruits, vegetables, and other food items. Sampling was spontaneous and all observations were videotaped. No group-level bias was found for head-tilting, but a left hand bias emerged for hand use. A positive relationship was found between direction of head-tilting preference and direction of hand use preference such that left head-tilts increased as left hand use increased. Furthermore, left head-tilts increased as the degree of hand preference lateralization increased. When the hand used to bring food to the mouth just before head-tilting was examined, there was a strong bias for the left hand to precede left head-tilts. For right head-tilts, however, lemurs were equally likely to use either hand before head-tilting. Overall a strong relationship was found between the left hand and left head-tilting in black and white ruffed lemurs, suggesting a common link between these behaviors. However, the direction of bias was different from that seen in human and chimpanzee studies. Additional studies on patterns of laterality would be informative for understanding how laterality has changed across the primate order and the adaptive significance of laterality in primates.
Terrien, Jeremy; Zizzari, Philippe; Epelbaum, Jacques; Perret, Martine; Aujard, Fabienne
Daily variations in core temperature (Tc) within the normothermic range imply thermoregulatory processes that are essential for optimal function and survival. Higher susceptibility towards cold exposure in older animals suggests that these processes are disturbed with age. In the mouse lemur, a long-day breeder, we tested whether aging affected circadian rhythmicity of Tc, locomotor activity (LA), and energy balance under long-day conditions when exposed to cold. Adult (N = 7) and aged (N = 5) mouse lemurs acclimated to LD14/10 were exposed to 10-day periods at 25 and 12 degrees C. Tc and LA rhythms were recorded by telemetry, and caloric intake (CI), body mass changes, and plasma IGF-1 were measured. During exposure to 25 degrees C, both adult and aged mouse lemurs exhibited strong daily variations in Tc. Aged animals exhibited lower levels of nocturnal LA and nocturnal and diurnal Tc levels in comparison to adults. Body mass and IGF-1 levels remained unchanged with aging. Under cold exposure, torpor bout occurrence was never observed whatever the age category. Adult and aged mouse lemurs maintained their Tc in the normothermic range and a positive energy balance. All animals exhibited increase in CI and decrease in IGF-1 in response to cold. The decrease in IGF-1 was delayed in aged mouse lemurs compared to adults. Moreover, both adult and aged animals responded to cold exposure by increasing their diurnal LA compared to those under Ta = 25 degrees C. However, aged animals exhibited a strong decrease in nocturnal LA and Tc, whereas cold effects were only slight in adults. The temporal organization and amplitude of the daily phase of low Tc were particularly well preserved under cold exposure in both age groups. Sexually active mouse lemurs exposed to cold thus seemed to prevent torpor exhibition and temporal disorganization of daily rhythms of Tc, even during aging. However, although energy balance was not impaired with age in mouse lemurs after cold exposure
Background Species are the fundamental units in evolutionary biology. However, defining them as evolutionary independent lineages requires integration of several independent sources of information in order to develop robust hypotheses for taxonomic classification. Here, we exemplarily propose an integrative framework for species delimitation in the “brown lemur complex” (BLC) of Madagascar, which consists of seven allopatric populations of the genus Eulemur (Primates: Lemuridae), which were sampled extensively across northern, eastern and western Madagascar to collect fecal samples for DNA extraction as well as recordings of vocalizations. Our data base was extended by including museum specimens with reliable identification and locality information for skull shape and pelage color analysis. Results Between-group analyses of principal components revealed significant heterogeneity in skull shape, pelage color variation and loud calls across all seven populations. Furthermore, post-hoc statistical tests between pairs of populations revealed considerable discordance among different data sets for different dyads. Despite a high degree of incomplete lineage sorting among nuclear loci, significant exclusive ancestry was found for all populations, except for E. cinereiceps, based on one mitochondrial and three nuclear genetic loci. Conclusions Using several independent lines of evidence, our results confirm the species status of the members of the BLC under the general lineage concept of species. More generally, the present analyses demonstrate the importance and value of integrating different kinds of data in delimiting recently evolved radiations. PMID:24159931
Shah, Kalpit; Bradbury, Neil A.
Progression from early forms of prostate cancer to castration-resistant disease is associated with an increase in signal transduction activity. The majority of castration-resistance cancers persist in the expression of the androgen receptor (AR), as well as androgen-dependent genes. The AR is regulated not only by it associated steroid hormone, but also by manifold regulatory and signaling molecules, including several kinases. We undertook evaluation of the role of Lemur Tyrosine Kinase 2 (LMTK2) in modulating AR activity, as several Genome Wide Association Studies (GWAS) have shown a marked association of LMTK2 activity with the development of prostate cancer. We confirm that not only is LMTK2 mRNA reduced in prostate cancer tissue, but also LMTK2 protein levels are markedly diminished. Knockdown of LMTK2 protein in prostate cell lines greatly increased the transcription of androgen-responsive genes. In addition, LMTK2 knockdown led to an increase in prostate cancer stem cell populations in LNCaP cells, indicative of increased tumorogenicity. Using multiple approaches, we also demonstrate that LMTK2 interacts with the AR, thus putting LMTK2 as a component of a signaling complex modulating AR activity. Our finding that LMTK2 is a negative regulator of AR activity defines a novel cellular pathway for activation of AR-responsive genes in castrate resistant-prostate cancer. Moreover, pharmacologic manipulation of LMTK2 activity will provide a novel therapeutic target for more effective treatments for patients with castrate-resistant prostate cancer. PMID:26008968
Markolf, Matthias; Rakotonirina, Hanitriniaina; Fichtel, Claudia; von Grumbkow, Phillip; Brameier, Markus; Kappeler, Peter M
Species are the fundamental units in evolutionary biology. However, defining them as evolutionary independent lineages requires integration of several independent sources of information in order to develop robust hypotheses for taxonomic classification. Here, we exemplarily propose an integrative framework for species delimitation in the "brown lemur complex" (BLC) of Madagascar, which consists of seven allopatric populations of the genus Eulemur (Primates: Lemuridae), which were sampled extensively across northern, eastern and western Madagascar to collect fecal samples for DNA extraction as well as recordings of vocalizations. Our data base was extended by including museum specimens with reliable identification and locality information for skull shape and pelage color analysis. Between-group analyses of principal components revealed significant heterogeneity in skull shape, pelage color variation and loud calls across all seven populations. Furthermore, post-hoc statistical tests between pairs of populations revealed considerable discordance among different data sets for different dyads. Despite a high degree of incomplete lineage sorting among nuclear loci, significant exclusive ancestry was found for all populations, except for E. cinereiceps, based on one mitochondrial and three nuclear genetic loci. Using several independent lines of evidence, our results confirm the species status of the members of the BLC under the general lineage concept of species. More generally, the present analyses demonstrate the importance and value of integrating different kinds of data in delimiting recently evolved radiations.
Biebouw, Karla; Bearder, Simon; Nekaris, Anna
In this study we describe tree hole characteristics and use by the hairy-eared dwarf lemur (Allocebus trichotis) to determine habitat needs, potential functions of tree holes and sleeping group composition. We radio-tracked 6 adult individuals between April and November 2007 in the Analamazaotra Special Reserve. Tree holes were 1-9 m high (median: 7 m), in living trees measuring 26-54 cm in diameter at breast height (median: 32 cm), and could be a limiting resource. Each individual used 4 or 5 tree holes and had high nest fidelity. Animals most often slept socially in mixed-sex groups of 2-6 individuals and occasionally shared a tree hole with white-tailed tree rats (Brachytarsomys albicauda). We identified two sleeping groups: one composed of 2 adult males, 2 adult females and 2 juveniles; one composed of at least 2 adult females and 2 juveniles. Although tree holes were generally group exclusive, some intergroup sleeping was observed. Tree holes could have antipredator and thermoregulatory functions. Further research into sleeping hole availability, nest use and the degree of niche separation or competition between sympatric Cheirogaleidae and other tree hole users (e.g. endemic rodents) is needed to assess better the conservation needs of these species. Copyright 2009 S. Karger AG, Basel.
Hohenbrink, Sarah; Zimmermann, Elke; Radespiel, Ute
The life history of mammals underlies a fast-slow continuum, ranging from "slow" species with large body size, delayed sexual maturation, low fertility, and long lifespan, to "fast" species showing the opposite traits. Primates fall into the "slow" category, considering their relatively low offspring numbers and delayed juvenile development. However, social and sexual maturation processes do not necessarily have to be completed simultaneously. The comparison of the timeframes for sexual and social maturation is largely lacking for primates, with the prominent exception of humans. Here, we compare both maturation processes in a basal primate, the gray mouse lemur, which ranges in many aspects at the fast end of the slow-fast life history continuum among primates. We compared the patterns and frequencies of various social and solitary behaviors in young adults (YA, 12-13 months old) and older individuals (A, ≥2 years) of both sexes outside estrus. Observations were conducted during mix-sexed dyadic encounter experiments under controlled captive conditions (eight dyads per age class). Results indicate that although all young adults were sexually mature, social maturation was not yet completed in all behavioral domains: Age-dependent differences were found in the number of playing dyads, female marking behavior, female aggression, and social tolerance. Thus, this study provides a first indication that social maturation lags behind sexual maturation in an ancestral nocturnal primate model, indicating that these two developmental schemes may have been decoupled early and throughout the primate lineage.
Blair, M E; Sterling, E J; Dusch, M; Raxworthy, C J; Pearson, R G
Understanding ecological niche evolution over evolutionary timescales is crucial to elucidating the biogeographic history of organisms. Here, we used, for the first time, climate-based ecological niche models (ENMs) to test hypotheses about ecological divergence and speciation processes between sister species pairs of lemurs (genus Eulemur) in Madagascar. We produced ENMs for eight species, all of which had significant validation support. Among the four sister species pairs, we found nonequivalent niches between sisters, varying degrees of niche overlap in ecological and geographic space, and support for multiple divergence processes. Specifically, three sister-pair comparisons supported the null model that niches are no more divergent than the available background region. These findings are consistent with an allopatric speciation model, and for two sister pairs (E. collaris-E. cinereiceps and E. rufus-E. rufifrons), a riverine barrier has been previously proposed for driving allopatric speciation. However, for the fourth sister pair E. flavifrons-E. macaco, we found support for significant niche divergence, and consistent with their parapatric distribution on an ecotone and the lack of obvious geographic barriers, these findings most strongly support a parapatric model of speciation. These analyses thus suggest that various speciation processes have led to diversification among closely related Eulemur species.
delBarco-Trillo, Javier; Sacha, Caitlin R; Dubay, George R; Drea, Christine M
Signal complexity has been linked to social complexity in vocal, but not chemical, communication. To address this gap, we examined the chemical complexity of male and female glandular secretions in eight species of Eulemur. In this diverse clade of macrosmatic primates, species differ by social or mating system and dominance structure. We applied principal component and linear discriminate analyses to data obtained by gas chromatography/mass spectrometry. Beyond the significant effects on chemical signals of gland type, sex, season and species, we found effects of social variables and phylogeny. Notably, female odours were more chemically complex in multimale-multifemale species than pair-bonded species, whereas male odours were more chemically complex in codominant species than female-dominant species. Also, the traditional sexual dimorphism, whereby male signal complexity exceeds that of females, was present in codominant species, but reversed in female-dominant species. Lastly, a positive relationship between the species' pairwise chemical distances and their pairwise phylogenetic distances supported a gradual, but relatively fast mode of signal evolution. We suggest that the comparative method can be a powerful tool in olfactory research, revealing species differences relevant to the understanding of current signal utility and evolutionary processes. In particular, social complexity in lemurs may have selected for olfactory complexity.
Shah, Kalpit; Bradbury, Neil A
Progression from early forms of prostate cancer to castration-resistant disease is associated with an increase in signal transduction activity. The majority of castration-resistance cancers persist in the expression of the androgen receptor (AR), as well as androgen-dependent genes. The AR is regulated not only by it associated steroid hormone, but also by manifold regulatory and signaling molecules, including several kinases. We undertook evaluation of the role of Lemur Tyrosine Kinase 2 (LMTK2) in modulating AR activity, as several Genome Wide Association Studies (GWAS) have shown a marked association of LMTK2 activity with the development of prostate cancer. We confirm that not only is LMTK2 mRNA reduced in prostate cancer tissue, but also LMTK2 protein levels are markedly diminished. Knockdown of LMTK2 protein in prostate cell lines greatly increased the transcription of androgen-responsive genes. In addition, LMTK2 knockdown led to an increase in prostate cancer stem cell populations in LNCaP cells, indicative of increased tumorogenicity. Using multiple approaches, we also demonstrate that LMTK2 interacts with the AR, thus putting LMTK2 as a component of a signaling complex modulating AR activity. Our finding that LMTK2 is a negative regulator of AR activity defines a novel cellular pathway for activation of AR-responsive genes in castrate resistant-prostate cancer. Moreover, pharmacologic manipulation of LMTK2 activity will provide a novel therapeutic target for more effective treatments for patients with castrate-resistant prostate cancer.
Parga, Joyce A; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho; Gould, Lisa; Sussman, Robert W; Lawler, Richard R; Pastorini, Jennifer
Lemur catta has traditionally been considered a species with male-biased dispersal; however, occasional female dispersal occurs. Using molecular data, we evaluated dispersal patterns in 2 L. catta populations in southwestern Madagascar: Tsimanampesotse National Park (TNP) and Bezà Mahafaly Special Reserve (BMSR). We also investigated the genetic differentiation between the populations and dispersal partner relatedness. Results showed minor genetic differentiation between the populations (ϴ(ST) = 0.039), which may indicate gene flow historically occurring in this region, made possible by the presence of L. catta groups between the sites. Different patterns of sex-biased dispersal were found between the sites using corrected assignment indices: male-biased dispersal in TNP, and a lack of sex-biased dispersal in BMSR. Observational evidence of female dispersal in BMSR supports these results and may imply intense female resource competition in and around BMSR, because small groups of 2-3 females have been observed dispersing within BMSR and entering the reserve from outside. These dispersing groups largely consisted of mothers transferring with daughters, although we have an aunt-niece pair transferring together. Genetic data suggest that males also transfer with relatives. Our data demonstrate that dispersal partners consist of same-sexed kin for L. catta males and females, highlighting the importance of kin selection.
Groeneveld, Linn F; Weisrock, David W; Rasoloarison, Rodin M; Yoder, Anne D; Kappeler, Peter M
Background Species are viewed as the fundamental unit in most subdisciplines of biology. To conservationists this unit represents the currency for global biodiversity assessments. Even though Madagascar belongs to one of the top eight biodiversity hotspots of the world, the taxonomy of its charismatic lemuriform primates is not stable. Within the last 25 years, the number of described lemur species has more than doubled, with many newly described species identified among the nocturnal and small-bodied cheirogaleids. Here, we characterize the diversity of the dwarf lemurs (genus Cheirogaleus) and assess the status of the seven described species, based on phylogenetic and population genetic analysis of mtDNA (cytb + cox2) and three nuclear markers (adora3, fiba and vWF). Results This study identified three distinct evolutionary lineages within the genus Cheirogaleus. Population genetic cluster analyses revealed a further layer of population divergence with six distinct genotypic clusters. Conclusion Based on the general metapopulation lineage concept and multiple concordant data sets, we identify three exclusive groups of dwarf lemur populations that correspond to three of the seven named species: C. major, C. medius and C. crossleyi. These three species were found to be genealogically exclusive in both mtDNA and nDNA loci and are morphologically distinguishable. The molecular and morphometric data indicate that C. adipicaudatus and C. ravus are synonymous with C. medius and C. major, respectively. Cheirogaleus sibreei falls into the C. medius mtDNA clade, but in morphological analyses the membership is not clearly resolved. We do not have sufficient data to assess the status of C. minusculus. Although additional patterns of population differentiation are evident, there are no clear subdivisions that would warrant additional specific status. We propose that ecological and more geographic data should be collected to confirm these results. PMID:19193227
Ramsier, Marissa A; Dominy, Nathaniel J
Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost-effective alternative-the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring-tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally-derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high-frequency limits were comparable. However, at frequencies < or =2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10-dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR- and behaviorally-derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising
Yamashita, Nayuta; Cuozzo, Frank P; Sauther, Michelle L; Fitzgerald, Emily; Riemenschneider, Andrea; Ungar, Peter S
Determining the proximate causes of tooth wear remains a major focus of dental study. Here we compare the diets of three ring-tailed lemur (Lemur catta) populations and examine how different dietary components may contribute to patterns of wear-related tooth shape. Casts were made from dental impressions collected between 2003 and 2010 from lemurs in the gallery and spiny/mixed forests of the Bezá Mahafaly Special Reserve (BMSR; Parcels 1 and 2) and the spiny/mixed forests of Tsimanampesotse National Park (TNP), Madagascar. Tooth shape variables (occlusal relief and slope, angularity) were analyzed using dental topographic analysis. Focal observations and food mechanical properties (FMPs: toughness, hardness, elastic modulus) were conducted and tested, respectively, during wet and dry seasons from 2008 to 2012. We found that FMPs correlate with patterns of dental topography in these three populations. Specifically, food toughness and elastic modulus correlate with the dental variables, but hardness does not. Average food toughness and elastic modulus, but not hardness, are highest in BMSR Parcel 2, followed by BMSR Parcel 1 and TNP. Occlusal relief and slope, which serve as proxies for tooth wear, show the greatest wear in Parcel 2 and the least in TNP. Angularity is also more pronounced in TNP. Further, dental topographic patterns correspond to reliance on Tamarindus indica (tamarind) fruit. Both BMSR populations consume tamarind at high frequencies in the dry season, but the fruits are rare at TNP and only occasionally consumed. Thus, high seasonal tamarind consumption and its mechanical values help explain the low dental relief and slope among BMSR lemurs. By investigating the ecology of a single widespread species across a variety of habitats, we have been able to link specific components of diet to patterns of dental topography in this species. This provides a context for interpreting wear-related tooth shape changes more generally, illustrating that
Gjeltema, Jenessa; Stoskopf, Michael; Shea, Damian; De Voe, Ryan
Habitat preservation and management may play an important role in the conservation of the Puerto Rican crested toad, Peltophryne lemur, due to this species' small geographic range and declining native wild population. Bioavailable water concentrations of Polycyclic Aromatic Hydrocarbon (PAH) contaminants within breeding pools at 3 sites were established using Passive Sampling Devices (PSDs) and gas chromatography-mass spectrometry (GC/MS). A more diverse population of PAH analytes were found in higher concentrations at the breeding site that allowed direct vehicular access, but calculated risk quotients indicated low risk to toad reproduction associated with the current PAH analyte levels. PMID:23762634
Palagi, Elisabetta; Norscia, Ivan
However despotic a social group may be, managing conflicts of interest is crucial to preserve group living benefits, mainly based on cooperation. In despotic groups, post-conflict management via reconciliation (the first post-conflict reunion between former opponents) can occur, even if conciliatory rates are considerably different. Lemur catta is defined as a despotic species because groups are characterized by a strict linear hierarchy maintained by the adult females (the dominant sex) mainly via aggression. Reconciliation was reported in one out of four captive groups of L. catta. Here we investigate which variables influence the occurrence of reconciliation in these despotic groups. We analyzed 2339 Post Conflict (PC)-Matched Control (MC) observation pairs, collected on eight groups (five in the Berenty forest, Madagascar; three hosted at the Pistoia Zoo, Italy). Since L. catta is characterized by steep female dominance but shows female-female coalitionary support, we expected to confirm the presence of reconciliation in the study species. Consistently, we found reconciliation in one captive group and two wild groups, thus providing the first evidence of the presence of this phenomenon in wild L. catta. Moreover, because this species is a seasonal breeder (with mating occurring once a year), we expected seasonal fluctuations in reconciliation levels. Via a GLMM analysis using data from all wild groups and on a captive group followed for more than one year, we found that season (but not rank; individuals’ identity, sex, and age; or group identity) significantly affected individual reconciliation rates, and such rates were lowest during the mating period. Thus, reconciliation can be present in groups in which dominants strongly influence and limit social relationships (steep dominance hierarchy) except when the advantages of intra-group cooperation are overcome by competition, as occurs in seasonal breeders when reproduction is at stake. We conclude that in
Palagi, Elisabetta; Norscia, Ivan
Urine marking has been neglected in prosimian primates. Captive studies showed that the Malagasy prosimian Lemur catta scent marks with urine, as well as via specialized depositions. L. catta urine mark, a multimodal signal, differs from simple urination in terms of different design features, including tail configuration: the tail is held up during marking (UT-up) and down during urination (UT-down). We explore economy and function of UT-up in the female dominant L. catta. We collected 240 h of observations on one group at Berenty (south Madagascar) during the nonmating period via all occurrences sampling. We gathered behavioral bouts/contexts (marking, traveling, feeding, resting, and fights) and recorded 191 UT-ups and 79 UT-downs. Via Global Positioning System we established the location of the places frequented i) by extragroup individuals and ii) by group members, in this case recording also behavioral context and time spent in each place. We found that L. catta UT-up is not an artifact of captivity. Moreover, UT-up in the nonmating period plays a role in territorial defense, which is mostly performed by females in L. catta society. Female UT-ups were the most investigated and UT-ups were performed/investigated more by females. Finally, signal use is parsimonious, in that urine is economically placed where and when detection probability by competitors is higher. UT-ups were performed in places most frequented by extragroup individuals and in presence of extragroup competitors (nonrandom topography and timing). In conclusion, we suggest that UT-up is an economical signal with a primarily territorial function. Copyright 2009 Wiley-Liss, Inc.
Kelley, Elizabeth A
Large home ranges and extreme flexibility in ranging behaviors characterize most subarid dwelling haplorhines. However, the most comparable extant strepsirhine, Lemur catta, is characterized as having small home ranges with consistent boundaries. Since ranging studies on this species have been limited to gallery forest habitat, the author's goal is to identify ecological factors that affect range use of L. catta in one of the most resource-limited environments of its distribution. To conduct this study, ranging and behavioral data were collected on two nonoverlapping groups through all-day follows in the semidesert scrub environment of Cap Sainte-Marie (CSM), Madagascar. Data were collected from August 2007 through July 2008. Home range areas and day range lengths were generated using ArcGIS(®) 9.3. Other variables measured were habitat composition, diet richness, daily activity, and microclimate. Home range areas of CSM L. catta were very large relative to those of gallery forest L. catta, and there was great monthly variation. In contrast, day range lengths at CSM were either smaller than or approximated the size of comparative gallery forest groups. Temperature, sunning, and diet richness were associated with day range length for one but not for both groups and appear to be related to energy management needs. Based on these findings, the author suggests that L. catta is capable of extensive behavioral and ranging flexibility in the extremes of its environment. However, physiological constraints impose limitations that can interfere with its ability to adapt to even seemingly minor variations in microclimate and habitat structure within the same site.
Palagi, Elisabetta; Norscia, Ivan
However despotic a social group may be, managing conflicts of interest is crucial to preserve group living benefits, mainly based on cooperation. In despotic groups, post-conflict management via reconciliation (the first post-conflict reunion between former opponents) can occur, even if conciliatory rates are considerably different. Lemur catta is defined as a despotic species because groups are characterized by a strict linear hierarchy maintained by the adult females (the dominant sex) mainly via aggression. Reconciliation was reported in one out of four captive groups of L. catta. Here we investigate which variables influence the occurrence of reconciliation in these despotic groups. We analyzed 2339 Post Conflict (PC)-Matched Control (MC) observation pairs, collected on eight groups (five in the Berenty forest, Madagascar; three hosted at the Pistoia Zoo, Italy). Since L. catta is characterized by steep female dominance but shows female-female coalitionary support, we expected to confirm the presence of reconciliation in the study species. Consistently, we found reconciliation in one captive group and two wild groups, thus providing the first evidence of the presence of this phenomenon in wild L. catta. Moreover, because this species is a seasonal breeder (with mating occurring once a year), we expected seasonal fluctuations in reconciliation levels. Via a GLMM analysis using data from all wild groups and on a captive group followed for more than one year, we found that season (but not rank; individuals' identity, sex, and age; or group identity) significantly affected individual reconciliation rates, and such rates were lowest during the mating period. Thus, reconciliation can be present in groups in which dominants strongly influence and limit social relationships (steep dominance hierarchy) except when the advantages of intra-group cooperation are overcome by competition, as occurs in seasonal breeders when reproduction is at stake. We conclude that in
Millette, James B; Sauther, Michelle L; Cuozzo, Frank P; Ness, Jenifer L
During mastication, foods are reduced into particles suitable for swallowing and digestion. Smaller particles possess a greater surface area per unit of volume on which digestive enzymes and bacteria may work than relatively larger particles, and are thus more readily digested. As dental morphology facilitates the breakdown of diets with specific mechanical properties, extensive dental wear and/or tooth loss may impede an individual's ability to break down and exploit foods. We present data demonstrating a relationship between dental impairment and particle size in 43 fecal samples from 33 ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar. All fecal samples were sifted through three sieves of decreasing size (11.2 mm, 4.75 mm, and 1.0 mm). The resulting fraction in each sieve was then weighed and assessed in relation to individual dental impairment status. With increasing wear, the percentage of each sample within the 1.0 mm sieve decreases, whereas that in the 11.2 mm sieve increases with increasing postcanine wear, although these effects are not present when limited to individuals without tooth loss. Individuals with tooth loss also demonstrate larger proportions of fecal material 1.0-4.75 mm in size. Dental impairment results in larger food particles and potentially less efficient utilization of foods. When fecal material was examined by leaf vs. fruit content, individuals with tooth loss demonstrated reduced proportions of fruit in the 1.0 mm and 11.2 mm sieves. These data suggest individuals with tooth loss consume less fruit than those without loss, potentially reflecting a reduced ability to process tamarind fruit, a key fallback resource at BMSR.
Hosey, Geoff; Melfi, Vicky; Formella, Isabel; Ward, Samantha J; Tokarski, Marina; Brunger, Dave; Brice, Sara; Hill, Sonya P
Chimpanzees in laboratory colonies experience more wounds on weekdays than on weekends, which has been attributed to the increased number of people present during the week; thus, the presence of more people was interpreted as stressful. If this were also true for primates in zoos, where high human presence is a regular feature, this would clearly be of concern. Here we examine wounding rates in two primate species (chimpanzees Pan troglodytes and ring-tailed lemurs Lemur catta) at three different zoos, to determine whether they correlate with mean number of visitors to the zoo. Wounding data were obtained from a zoo electronic record keeping system (ZIMS™). The pattern of wounds did not correlate with mean gate numbers for those days for either species in any group. We conclude that there is no evidence that high visitor numbers result in increased woundings in these two species when housed in zoos. Zoo Biol. 35:205-209, 2016. © 2016 Wiley Periodicals, Inc. © 2016 Wiley Periodicals, Inc.
Gould, L; Constabel, P; Mellway, R; Rambeloarivony, H
Primates vary in their choice or avoidance of plant foods high in condensed tannins (CT). Our study focused on CT intake in two groups of Lemur catta residing in spiny forest habitat during two reproductive periods. We examined whether L. catta in this habitat avoided plant foods high in CT, and whether reproductive females ingested lower concentrations of CT compared with males, since CT consumption compromises protein absorption. Feeding data and plant food samples were collected during reproductive periods in 2006 (early/mid-lactation) and 2007 (early gestation). Food samples were assayed for CT content, and average CT intake was determined for all focal animals. No significant difference was found in CT content of the most commonly consumed foods compared with other foods in each season or between seasons. No sex differences occurred in CT consumption in either reproductive period. These L. catta did not avoid plant foods high in CT, and three strategies - ingesting small amounts of CT regularly, high amounts only over short periods, and geophagy - may assist these lemurs in coping with CT content in their highly seasonal diet. L. catta may also be somewhat physiologically adapted to cope with CT concentrations in their plant foods. Copyright 2009 S. Karger AG, Basel.
Zehr, Sarah M; Roach, Richard G; Haring, David; Taylor, Julie; Cameron, Freda H; Yoder, Anne D
Since its establishment in 1966, the Duke Lemur Center (DLC) has accumulated detailed records for nearly 4,200 individuals from over 40 strepsirrhine primate taxa—the lemurs, lorises, and galagos. Here we present verified data for 3,627 individuals of 27 taxa in the form of a life history table containing summarized species values for variables relating to ancestry, reproduction, longevity, and body mass, as well as the two raw data files containing direct and calculated variables from which this summary table is built. Large sample sizes, longitudinal data that in many cases span an animal’s entire life, exact dates of events, and large numbers of individuals from closely related yet biologically diverse primate taxa make these datasets unique. This single source for verified raw data and systematically compiled species values, particularly in combination with the availability of associated biological samples and the current live colony for research, will support future studies from an enormous spectrum of disciplines. PMID:25977776
Cuozzo, Frank P; Sauther, Michelle L
The Ankilitelo cave site, Madagascar, contains a large collection of extant and recently extinct subfossil lemurs including the extant taxa Lemur catta and Eulemur rufifrons, which today are rarely found in sympatry. Dates for this assemblage range from 300 to 13,000 BP, though known dates for extinct primate specimens range between ∼500 and ∼600 BP. Data from Ankilitelo L. catta and E. rufifrons were compared to assess tooth wear in sympatric, related forms. Wear was scored using an ordinal scale from 0 to 5. For P4, M1 and M2, E. rufifrons displays significantly more wear than L. catta. Ankilitelo represents one of the most southerly samples of E. rufifrons, and wear data suggest that in the recent (i.e. Holocene) past, their diet near the edges of their geographic range included mechanically challenging foods. In contrast, sympatric L. catta was using foods in this transitional humid-dry forest with succulent woodlands that were not significantly impacted by recent human actions, and for which they were dentally adapted. Results also suggest that this non-gallery forest habitat may be the 'adaptive home' of L. catta, given the lack of notable tooth wear when compared to populations currently living in tamarind-dominated riverine gallery forests.
Junge, Randall E; Williams, Cathy V; Rakotondrainibe, Hajanirina; Mahefarisoa, Karine L; Rajaonarivelo, Tsiky; Faulkner, Charles; Mass, Vanessa
Extractive industries can have significant impacts on ecosystems through loss of habitat, degradation of water quality, and direct impact on floral and faunal biodiversity. When operations are located in sensitive regions with high biodiversity containing endangered or threatened species, it is possible to minimize impact on the environment by developing programs to scientifically monitor the impact on resident flora and fauna species in the early phases of operation so that effects can be mitigated whenever possible. This report presents the baseline health, nutrition, and trace mineral evaluation for 33 Avahi laniger (Eastern wooly lemur) and 15 Lepilemur mustelinus (greater sportive lemur) captured and given complete health evaluations that included the measurement of fat-soluble vitamins and trace minerals in addition to routine complete blood counts, serum chemistries, and parasite evaluations. All lemurs appeared healthy on physical examination despite the presence of minor wounds consistent with interspecies aggression in some individuals. Serum chemistry values were within expected ranges for other lemur species; however, A. laniger erythrocytes were significantly smaller than those of L. mustelinus. Serum nickel values were markedly higher than expected in both species, and selenium, copper, and cobalt levels were higher in L. mustelinus compared with A. laniger at the study site, as well as values for I. indri or P. diadema reported from other locations. Endoparasites and ectoparasites were typical of those reported in other wild lemur species, but load and diversity varied between A. laniger and L. mustelinus despite inhabiting the same forest ecosystem. This baseline assessment provides the foundation for ongoing monitoring.
Wright, Patricia; King, Stephen J; Baden, Andrea; Jernvall, Jukka
Understanding the way prosimian primates age can be helpful in inferring what the 'basal primate mode' of senescence may have been. Even though prosimians are known to be long-lived in captivity, relatively little is known about their reproductive senescence, and even less is known about how prosimians age in their natural habitats. Twenty years of observational data in Madagascar for four Propithecus edwardsi sifaka groups were used to analyze reproductive and behavioral trends of aging in the wild. Techniques using tooth wear were developed to establish ages of wild sifakas and to estimate the onset of their 'dental senescence', a proxy for the onset of decline in the ability to obtain nutrition. Estimated maximum longevity was 32 years for female sifakas. Based on the loss of dental functional morphology, and changes in tooth wear patterns and in chewing efficiency, dental senescence was estimated to set in at approximately 18 years of age. Of the adult females in the study groups, the yearly average of the number of dentally senescent females was 24%. There was no indication of a decline in fertility in the dentally senescent females (aged >18 years) compared to younger adult females (aged 4-18 years). The field data showed, however, that in years when rain was decreased during months of prime lactation, infants of dentally senescent mothers died before weaning. This may be because the nursing mother's worn teeth could not shear leaves and extract moisture, nor nutrition, both essential for successful lactation. Old females showed no clear signs of social disengagement, further suggesting that drought-induced stress plays a direct role in increased infant mortality. These data support earlier findings that prosimian females continue to cycle and give birth until death. The effect of environmental variation on infant survival, however, indicates an incipient age-linked decline in reproductive fitness. Therefore, whereas lemurs represent the condition of no
Korendyke, Clarence M.; Teriaca, Luca; Doschek, George A.; Harra, Louise K.; Schühle, Udo H.; Shimizu, Toshifumi
LEMUR is a VUV imaging spectrograph with 0.28" resolution. Incident solar radiation is imaged onto the spectrograph slit by a single mirror telescope consisting of a 30-cm steerable f/12 off-axis paraboloid mirror. The spectrograph slit is imaged and dispersed by a highly corrected grating that focuses the solar spectrum over the detectors. The mirror is coated with a suitable multilayer with B4C top-coating providing a reflectance peak around 18.5 nm besides the usual B4C range above 500Å. The grating is formed by two halves, one optimized for performances around 185Å and the other above 500Å. Three intensified CCD cameras will record spectra above 50 nm while a large format CCD array with an aluminum filter will be used around 185Å.
Jacobs, Rachel L; Spriggs, Amanda N; MacFie, Tammie S; Baden, Andrea L; Irwin, Mitchell T; Wright, Patricia C; Louis, Edward E; Lawler, Richard R; Mundy, Nicholas I; Bradley, Brenda J
Analyses of genetic polymorphisms can aid our understanding of intra- and interspecific variation in primate sociality, ecology, and behavior. Studies of primate opsin genes are prime examples of this, as single nucleotide variants (SNVs) in the X-linked opsin gene underlie variation in color vision. For primate species with polymorphic trichromacy, genotyping opsin SNVs can generally indicate whether individual primates are red-green color-blind (denoted homozygous M or homozygous L) or have full trichromatic color vision (heterozygous ML). Given the potential influence of color vision on behavior and fitness, characterizing the color vision status of study subjects is becoming commonplace for many primate field projects. Such studies traditionally involve a multi-step sequencing-based method that can be costly and time-consuming. Here we present a new reliable, rapid, and relatively inexpensive method for characterizing color vision in primate populations using high resolution melt analysis (HRMA). Using lemurs as a case study, we characterized variation at exons 3 and/or 5 of the X-linked opsin gene for 87 individuals representing nine species. We scored opsin genotypes and color vision status using both traditional sequencing-based methods as well as our novel melting-curve based HRMA protocol. For each species, the melting curves of varying genotypes (homozygous M, homozygous L, heterozygous ML) differed in melting temperature and/or shape. Melting curves for each sample were consistent across replicates, and genotype-specific melting curves were consistent across DNA sources (blood vs. feces). We show that opsin genotypes can be quickly and reliably scored using HRMA once lab-specific reference curves have been developed based on known genotypes. Although the protocol presented here focuses on genotyping lemur opsin loci, we also consider the larger potential for applying this approach to various types of genetic studies of primate populations.
Feeding outside the forest: the importance of crop raiding and an invasive weed in the diet of gallery forest ring-tailed lemurs (Lemur catta) following a cyclone at the Beza Mahafaly special reserve, Madagascar.
LaFleur, M; Gould, L
In January 2005, a cyclone hit southern Madagascar, including the Beza Mahafaly Special Reserve, disrupting the flowering/fruiting cycle of Tamarindus indica, leaving Lemur catta without its major food resource during reproductive periods. We studied two adjacent groups of L. catta during the late gestation period, and both groups ventured outside the reserve to feed. The Red group (RG) fed daily on cultivated sweet potato (Ipomoea batatas) leaves in a nearby field, and both groups consumed leaves and stems of the invasive terrestrial flowering herb Mexican prickly poppy (Argemone mexicana), growing outside the reserve. The Green group (GG) spent significantly more time feeding than did RG, and more time feeding inside the forest compared to outside. The members of RG spent half of their time feeding in the crops, and nearly half of their diet consisted of easy-to-process sweet potato leaves. Additionally, RG defended and restricted GG's access to the crop territory. Of the two non-forest foods, A. mexicana leaves were higher in protein and most minerals (P, Mg, K and Na, but not Ca) and lower in fiber than sweet potato leaves, but sweet potato leaves were preferred by RG. L. catta is a markedly flexible primate with respect to diet, and switches to fallback foods from outside the forest during periods of low food availability. In the highly seasonal and unpredictable climate of southern Madagascar, such behavioral adaptations are important to the survival of this species.
Delmore, K E; Brenneman, R A; Lei, R; Bailey, C A; Brelsford, A; Louis, E E; Johnson, S E
Studies of hybrid zones can inform our understanding of reproductive isolation and speciation. Two species of brown lemur (Eulemur rufifrons and E. cinereiceps) form an apparently stable hybrid zone in the Andringitra region of southeastern Madagascar. The aim of this study was to identify factors that contribute to this stability. We sampled animals at 11 sites along a 90-km transect through the hybrid zone and examined variation in 26 microsatellites, the D-loop region of mitochondrial DNA, six pelage and nine morphological traits; we also included samples collected in more distant allopatric sites. Clines in these traits were noncoincident, and there was no increase in either inbreeding coefficients or linkage disequilibrium at the centre of the zone. These results could suggest that the hybrid zone is maintained by weak selection against hybrids, conforming to either the tension zone or geographical selection-gradient model. However, a closer examination of clines in pelage and microsatellites indicates that these clines are not sigmoid or stepped in shape but instead plateau at their centre. Sites within the hybrid zone also occur in a distinct habitat, characterized by greater seasonality in precipitation and lower seasonality in temperature. Together, these findings suggest that the hybrid zone may follow the bounded superiority model, with exogenous selection favouring hybrids within the transitional zone. These findings are noteworthy, as examples supporting the bounded superiority model are rare and may indicate a process of ecologically driven speciation without geographical isolation.
Junge, Randall E; Louis, Edward E
Complete medical examinations were performed on 20 wild Decken's sifaka (Propithecus verreauxi deckeni) and 20 wild red-fronted brown lemurs (Eulemurfulvus rufus) from western Madagascar. Each animal received a complete physical examination, and weight, body temperature, heart rate, and respiratory rate were recorded and ectoparasites collected. Blood samples were collected for complete blood cell count, differential white blood cell count, hemoparasite examination, serum biochemical profile, fat-soluble vitamin analysis, trace mineral analysis, and toxoplasmosis and viral serology. Fecal samples were collected for bacterial culture and endoparasite examination. Significant differences exist between the species for serum chemistry values for creatine phosphokinase, glucose, total protein, albumin, globulin, blood urea nitrogen, creatinine, phosphorus, potassium, and chloride; for fat-soluble vitamins 25-hydroxycholecalciferol, retinol, retinyl palmitate, gamma-tocopherol, alpha-tocopherol, and lutein + zeaxanthin; and serum copper. Parasites detected include Lemurostrongylus spp., Lemuricola spp., Trichurus spp., and ectoparasites Haemaphysalis lemuris, Psoroptes, and mites identified to the family Laelapidae. Enteric bacterial flora included Escherichia coli, Citrobacter ssp., Enterococcus faecalis, Bacillus cereus, Klebsiella ozaenae, Acinetobacter lwofii, and Enterobacter amnigenus.
Palagi, Elisabetta; Dapporto, Leonardo
In this paper, we aim at demonstrating individual recognition of female genital marking in Lemur catta. By gas chromatography and behavioural trials we verified the occurrence of the three components of recognition systems. We showed that each female has a unique chemical signature (expression component), and males and females perceive female individuality (perception component). To verify the presence of the action component (the last component of recognition systems), we designed a bioassay based on territorial competition to verify the functional response to female odours. Only females identified other females on the basis of their scents. The lack of a territorial functional response by males to female secretions may not indicate a male inability to identify females by their scents. In fact, sexual dimorphism in motivation and territorial defence may explain the response by males in the functional experiment. Actually, game theory predicts that males defend their own territories more vigorously against males compared with females. Therefore, the result of individual recognition bioassays of female odours may open interesting scenarios in the evaluation of the territorial defence investment across the different sex combinations.
Manser, Catherine; Vagnoni, Alessio; Guillot, Florence; Davies, Jennifer; Miller, Christopher C J
Cyclin-dependent kinase-5 (cdk5)/p35 and protein phosphatase-1 (PP1) are two major enzymes that control a variety of physiological processes within the nervous system including neuronal differentiation, synaptic plasticity and axonal transport. Defective cdk5/p35 and PP1 function are also implicated in several major human neurodegenerative diseases. Cdk5/p35 and the catalytic subunit of PP1 (PP1C) both bind to the brain-enriched, serine-threonine kinase lemur tyrosine kinase-2 (LMTK2). Moreover, LMTK2 phosphorylates PP1C on threonine-320 (PP1Cthr³²⁰) to inhibit its activity. Here, we demonstrate that LMTK2 is phosphorylated on serine-1418 (LMTK2ser¹⁴¹⁸) by cdk5/p35 and present evidence that this regulates its ability to phosphorylate PP1Cthr³²⁰. We thus describe a new signalling pathway within the nervous system that links cdk5/p35 with PP1C and which has implications for a number of neuronal functions and neuronal dysfunction.
Gould, L; Ziegler, T E
In primate species exhibiting seasonal reproduction, patterns of testosterone excretion in adult males are variable: in some species, peaks correlate with female receptivity periods and heightened male-male aggression over access to estrous females, in others, neither heightened aggression nor marked elevations in testosterone have been noted. In this study, we examined mean fecal testosterone ( f T) levels and intermale aggression in wild adult male ring-tailed lemurs residing in three groups at Beza Mahafaly Reserve, Madagascar. Results obtained from mating and post-mating season 2003 were compared to test Wingfield et al. [1990. Am Nat 136:829-846] "challenge hypothesis", which predicts a strong positive relationship between male testosterone levels and male-male competition for access to receptive females during breeding season. f T levels and rates of intermale aggression were significantly higher during mating season compared to the post-mating period. Mean f T levels and aggression rates were also higher in the first half of the mating season compared with the second half. Number of males in a group affected rates of intermale agonism, but not mean f T levels. The highest-ranking males in two of the groups exhibited higher mean f T levels than did lower-ranking males, and young males exhibited lower f T levels compared to prime-aged and old males. In the post-mating period, mean male f T levels did not differ between groups, nor were there rank or age effects. Thus, although male testosterone levels rose in relation to mating and heightened male-male aggression, f T levels fell to baseline breeding levels shortly after the early mating period, and to baseline non-breeding levels immediately after mating season had ended, offsetting the high cost of maintaining both high testosterone and high levels of male-male aggression in the early breeding period. (c) 2007 Wiley-Liss, Inc.
Dausmann, K H; Glos, J; Linsenmair, K E; Ganzhorn, J U
The objective of this study was to examine how the processes of seed dispersal and seed predation were altered in forest fragments of the dry forest of Madagascar, where the usual seed dispersers and vertebrate seed predators were absent, using a lemur-dispersed tree species (Strychnos madagascariensis; Loganiaceae) as an example. We then assessed how the changes in vertebrate community composition alter the regeneration pattern and establishment of this tree species and thus, ultimately, the species composition of the forest fragments. By using size-selective exclosures, data from forest fragments were compared with results from continuous forest where vertebrate dispersers and predators were abundant. Visits to the exclosures by mammalian seed predators were monitored with hair traps. In the continuous forest up to 100% of the seeds were removed within the 7 days of the experiments. A substantial proportion of them was lost to seed predation by native rodents. In contrast, practically no predation took place in the forest fragments and almost all seeds removed were dispersed into the safety of ant nests by Aphaenogaster swammerdami, which improves chances of seedling establishment. In congruence with these findings, the abundance of S. madagascariensis in the forest fragments exceeded that of the continuous forest. Thus, the lack of vertebrate seed dispersers in these forest fragments did not lead to a decline in regeneration of this animal-dispersed tree species as would have been expected, but rather was counterbalanced by the concomitant demise of vertebrate seed predators and an increased activity of ants taking over the role of seed dispersers, and possibly even out-doing the original candidates. This study provides an example of a native vertebrate-dispersed species apparently profiting from fragmentation due to flexible animal-plant interactions in different facets, possibly resulting in an impoverished tree species community.
Dröscher, Iris; Rothman, Jessica M; Ganzhorn, Jörg U; Kappeler, Peter M
Small-bodied folivores are rare because processing leaves often requires extensive gut adaptations and lengthy retention times for fiber fermentation. However, the <1 kg nocturnal white-footed sportive lemurs (Lepilemur leucopus) persist on a leaf-based diet. We investigated how extrinsic (i.e., seasonality in temperature and food availability) and intrinsic factors (i.e., reproductive state) influence nutrient intake and explored how nutrient and energy needs are met in this species. We conducted full night focal follows across all seasons and analyzed nutrients in all items eaten by adults of both sexes to investigate nutrient intake and nutritional priorities in L. leucopus. We estimated digestible protein content, as this is a biologically more meaningful measure than crude protein. Protein intake was constant across seasons, while non-protein energy and dry matter intake increased from the hot wet to the cold dry season. Males and females did not differ in their nutrient or apparent energy intake irrespective of female reproductive state. We conclude that these animals prioritize protein over non-protein energy intake as dietary protein is in limited supply, and that thermoregulation poses higher energetic costs than reproduction in this species. While protein intake did not differ across female reproductive states, the relative protein content of the diet was highest during the lactation period, indicating that the balance of non-protein to protein intake may be more important than absolute intake. Dry matter intake was high compared to other folivorous primates, indicating that L. leucopus follows an intake rather than an efficiency strategy to meet its energy requirements. Am J Phys Anthropol 160:197-207, 2016. © 2016 Wiley Periodicals, Inc. © 2016 Wiley Periodicals, Inc.
Eppley, Timothy M; Donati, Giuseppe; Ganzhorn, Jörg U
The proximate and ultimate determinants that may have prompted some primates to shift from an arboreal to terrestrial feeding niche, whether due to environmental change, seasonality, and/or predation pressure, are poorly understood. Within a fragmented littoral forest in southeast Madagascar, an arboreal strepsirrhine population spends a large proportion of time on the ground, thus we aimed to identify which factors influence terrestrial feeding. From January to December 2013, we conducted 103 full-day focal follows on three social groups of southern bamboo lemurs H. meridionalis. We continuously recorded feeding time on all arboreal and terrestrial items, as well as whether the focal individual was under the canopy or exposed, and the distance to their nearest conspecific neighbor. All observed food items were collected and analyzed for macronutrient content. Daily climatic variables (temperature, precipitation), resource seasonality, daily path length (DPL), along with dietary and predation risk proxies, were used as fixed effects in a linear mixed model, with the daily proportion of terrestrial feeding as the dependent variable. Our model indicated that daily terrestrial feeding increased at cooler temperature, was associated with reduced DPL, and the intake of dietary metabolizable energy increased as terrestrial feeding increased. All other fixed effects were not significant predictors. Our study provides a window into the ultimate determinants of niche expansion: ancestral primates, in absence of their primary resources, may have initially descended to the ground in peripheral population range areas where the benefits (e g., nutritional pay-off) out-weighed the costs. © 2016 Wiley Periodicals, Inc.
Wakatsuki, Takeru; LaBonte, Melissa J; Bohanes, Pierre O; Zhang, Wu; Yang, Dongyun; Azuma, Mizutomo; Barzi, Afsaneh; Ning, Yan; Loupakis, Fotios; Saadat, Siamak; Volz, Nico; Stintzing, Sebastian; El-Khoueiry, Rita; Koizumi, Wasaburo; Watanabe, Masahiko; Shah, Manish; Stebbing, Justin; Giamas, Georgios; Lenz, Heinz-Josef
Lemur tyrosine kinase-3 (LMTK3) was recently identified as an estrogen receptor (ER)-α modulator related to endocrine therapy resistance, and its polymorphisms rs9989661 (T>C) T/T genotype and rs8108419 (G>A) G/G or A/G genotype predicted improved outcomes in breast cancer. Because different predominant ER distributions link to breast and gastric cancer and little is known of the prognostic role of LMTK3 in gastric cancer, this study was carried out to clarify the prognostic role of these polymorphisms in gastric cancer. One-hundred and sixty-nine Japanese and 137 U.S. patients with localized gastric adenocarcinoma were enrolled. Genomic DNA was extracted from blood or tissue, and all samples were analyzed by PCR-based direct DNA sequencing. Overall, these polymorphisms were not associated with survival in both cohorts. When gender was considered, in multivariate analysis, harboring rs9989661 T/T genotype was associated with disease-free survival [HR, 4.37; 95% confidence interval (CI), 2.08-9.18; P < 0.0001] and overall survival (OS; HR, 3.69; 95% CI, 1.65-8.24; P = 0.0014) in the Japanese males and time to recurrence (HR, 7.29; 95% CI, 1.07-49.80; P = 0.043) in the U.S. females. Meanwhile, harboring rs8108419 G/G genotype was associated with OS in the Japanese females (HR, 3.04; 95% CI, 1.08-8.56; P = 0.035) and the U.S. males (HR, 3.39; 95% CI, 1.31-8.80; P = 0.012). The prognostic role of these polymorphisms may be negative in gastric cancer. These findings suggest that the estrogen pathway may play a prognostic role in patients with gastric cancer but this may be dependent on the regional differences both in physiology and genetic alterations of gastric cancer. ©2013 AACR.
Parga, Joyce A
In this study, dominance rank instability among male Lemur catta during mating was investigated. Also, data on agonism and sexual behavior across five consecutive mating seasons in a population of L. catta on St. Catherines Island, USA, were collected. Instances of male rank instability were categorized into three types. Type 1 consisted of a temporary switch in the dominance ranks of two males, which lasted for a period of minutes or hours. Type 2 dyadic male agonistic interactions showed highly variable outcomes for a period of time during which wins and losses were neither predictable nor consistent. Type 3 interactions consisted of a single agonistic win by a lower-ranked male over a more dominant male. More Type 2 interactions (indicating greater dominance instability) occurred when males had not spent the previous mating season in the same group, but this trend was not statistically significant. The majority of periods of male rank instability were preceded by female proceptivity or receptivity directed to a lower-ranked male. As such, exhibition of female mate choice for a lower-ranking male appeared to incite male-male competition. Following receipt of female proceptivity or receptivity, males who were lower-ranking took significantly longer to achieve their first agonistic win over a more dominant male than did males who were higher-ranked. Ejaculation frequently preceded loss of dominance. In conclusion, temporary rank reversals and overall dominance rank instability commonly occur among male L. catta in mating contexts, and these temporary increases in dominance status appear to positively affect male mating success.
Introduction Due to its remarkable species diversity and micro-endemism, Madagascar has recently been suggested to serve as a biogeographic model region. However, hypothesis-based tests of various diversification mechanisms that have been proposed for the evolution of the island’s micro-endemic lineages are still limited. Here, we test the fit of several diversification hypotheses with new data on the broadly distributed genus Eulemur using coalescent-based phylogeographic analyses. Results Time-calibrated species tree analyses and population genetic clustering resolved the previously polytomic species relationships among eulemurs. The most recent common ancestor of eulemurs was estimated to have lived about 4.45 million years ago (mya). Divergence date estimates furthermore suggested a very recent diversification among the members of the “brown lemur complex”, i.e. former subspecies of E. fulvus, during the Pleistocene (0.33-1.43 mya). Phylogeographic model comparisons of past migration rates showed significant levels of gene flow between lineages of neighboring river catchments as well as between eastern and western populations of the redfronted lemur (E. rufifrons). Conclusions Together, our results are concordant with the centers of endemism hypothesis (Wilmé et al. 2006, Science 312:1063–1065), highlight the importance of river catchments for the evolution of Madagascar’s micro-endemic biota, and they underline the usefulness of testing diversification mechanisms using coalescent-based phylogeographic methods. PMID:24228694
Markolf, Matthias; Kappeler, Peter M
Due to its remarkable species diversity and micro-endemism, Madagascar has recently been suggested to serve as a biogeographic model region. However, hypothesis-based tests of various diversification mechanisms that have been proposed for the evolution of the island's micro-endemic lineages are still limited. Here, we test the fit of several diversification hypotheses with new data on the broadly distributed genus Eulemur using coalescent-based phylogeographic analyses. Time-calibrated species tree analyses and population genetic clustering resolved the previously polytomic species relationships among eulemurs. The most recent common ancestor of eulemurs was estimated to have lived about 4.45 million years ago (mya). Divergence date estimates furthermore suggested a very recent diversification among the members of the "brown lemur complex", i.e. former subspecies of E. fulvus, during the Pleistocene (0.33-1.43 mya). Phylogeographic model comparisons of past migration rates showed significant levels of gene flow between lineages of neighboring river catchments as well as between eastern and western populations of the redfronted lemur (E. rufifrons). Together, our results are concordant with the centers of endemism hypothesis (Wilmé et al. 2006, Science 312:1063-1065), highlight the importance of river catchments for the evolution of Madagascar's micro-endemic biota, and they underline the usefulness of testing diversification mechanisms using coalescent-based phylogeographic methods.
Jimenez Martinez, Maria-Angeles; Valderrabano Cano, Esther; Rois, Jose L
Baylisascaris procyonis is a well-known ascaridoid nematode that causes larva migrans in humans and many other animal species. The North American raccoon (Procyon lotor) is the definitive host, which has been successfully introduced in the past decades to other geographical regions around the world. Two white-headed lemurs (Eulemuralbifrons) from a Zoological Park in Lugo, Spain, developed severe neurological signs within a brief period after being transferred from exhibit and placed in close contact with three captive raccoons from the same zoo. One lemur was euthanized due to the severity of disease progression and histopathology revealed granulomatous inflammation and ascaridoid larvae in kidneys, lung, spleen and brain. Larvae were identified as B. procyonis larvae by real time PCR. In light of the results, the cage mate with similar neurological signs was put on an albendazole treatment regimen adapted from a human pediatric protocol. The aggressive anthelmintic treatment likely contributed to the arrest of clinical signs and recovery of some motor skills. Importantly, Baylisascaris procyonis infection might occur in wild raccoon populations in Spain. Copyright © 2015 Elsevier B.V. All rights reserved.
Dröscher, Iris; Kappeler, Peter M
Whereas other species of sportive lemurs (genus Lepilemur) have been described as living in dispersed pairs, which are characterized by spatial overlap but a lack of affinity or affiliation between one adult male and female, existing reports on the social organization of the white-footed sportive lemur (Lepilemur leucopus) are conflicting, describing them as either living in dispersed one-male multifemale systems or pairs. We conducted this study in the spiny forest of Berenty Reserve, southern Madagascar, to clarify the social organization and to characterize the level of social complexity of this species. We combined 1530 h of radio-telemetry and behavioral observations over a period of 1 yr to describe the spatiotemporal stability, size, and interindividual overlap of individual home ranges as well as interindividual cohesiveness. Results revealed low intra- and high intersexual home range overlap. Although most of the social units identified consisted of dispersed pairs (N = 5), males were associated with two adult females in two cases. Furthermore, members of a social unit were never observed to groom each other or to share a daytime sleeping site, and Hutchinson's and Doncaster's dynamic interaction tests indicated active avoidance between pair partners. Low cohesiveness together with extremely low rates of social interactions therefore arguably places Lepilemur leucopus at the low end of primate social complexity.
Taufik, Epi; Fukuda, Kenji; Senda, Akitsugu; Saito, Tadao; Williams, Cathy; Tilden, Chris; Eisert, Regina; Oftedal, Olav; Urashima, Tadasu
The structures of milk oligosaccharides were characterized for four strepsirrhine primates to examine the extent to which they resemble milk oligosaccharides in other primates. Neutral and acidic oligosaccharides were isolated from milk of the greater galago (Galagidae: Otolemur crassicaudatus), aye-aye (Daubentoniidae: Daubentonia madagascariensis), Coquerel's sifaka (Indriidae: Propithecus coquereli) and mongoose lemur (Lemuridae: Eulemur mongoz), and their chemical structures were characterized by (1)H-NMR spectroscopy. The oligosaccharide patterns observed among strepsirrhines did not appear to correlate to phylogeny, sociality or pattern of infant care. Both type I and type II neutral oligosaccharides were found in the milk of the aye-aye, but type II predominate over type I. Only type II oligosaccharides were identified in other strepsirrhine milks. α3'-GL (isoglobotriose, Gal(α1-3)Gal(β1-4)Glc) was found in the milks of Coquerel's sifaka and mongoose lemur, which is the first report of this oligosaccharide in the milk of any primate species. 2'-FL (Fuc(α1-2)Gal(β1-4)Glc) was found in the milk of an aye-aye with an ill infant. Oligosaccharides containing the Lewis x epitope were found in aye-aye and mongoose lemur milk. Among acidic oligosaccharides, 3'-N-acetylneuraminyllactose (3'-SL-NAc, Neu5Ac(α2-3)Gal(β1-4)Glc) was found in all studied species, whereas 6'-N-acetylneuraminyllactose (6'-SL-NAc, Neu5Ac(α2-6)Gal(β1-4)Glc) was found in all species except greater galago. Greater galago milk also contained 3'-N-glycolylneuraminyllactose (3'-SL-NGc, Neu5Gc(α2-3)Gal(β1-4)Glc). The finding of a variety of neutral and acidic oligosaccharides in the milks of strepsirrhines, as previously reported for haplorhines, suggests that such constituents are ancient rather than derived features, and are as characteristic of primate lactation is the classic disaccharide, lactose.
Abdel-Wahab, Yasser H A; Power, Gavin J; Flatt, Peter R; Woodhams, Douglas C; Rollins-Smith, Louise A; Conlon, J Michael
A peptide with the ability to release insulin from the rat BRIN-BD11 clonal beta cell line was isolated from norepinephrine-stimulated skin secretions of the Lemur leaf frog Hylomantis lemur Boulenger,1882. Determination of the primary structure (FLSLIPHVISALSSL.NH(2)) demonstrated that the peptide belongs to the phylloseptin family whose members have previously been identified in other Phyllomedusinae species. A synthetic replicate of the peptide, termed phylloseptin-L2, produced a significant stimulation of insulin release (134% of basal rate, P<0.01) from BRIN-BD11 cells at a concentration of 30 nM, with a maximum response (301% of basal rate, P<0.001) at a concentration of 3 microM. Phylloseptin-L2 did not stimulate release of the cytosolic enzyme, lactate dehydrogenase at concentrations up to 3 microM, indicating that the integrity of the plasma membrane had been preserved. The stimulatory action was maintained in the absence of extracellular Ca(2+) and in the presence of verapamil (50 microM) and diazoxide (300 microM) suggesting that mechanism of action of the peptide did not primarily involve influx of Ca(2+) or closure of ATP-sensitive K(+) channels. Administration of phylloseptin-L2 (50 nmol/kgbody weight) into mice significantly (P<0.05) increased total release of insulin and improved glucose tolerance during the 60 min period following an intraperitoneal injection of glucose (18 mmol/kgbody weight). It is concluded that the peptide shows potential for development into a therapeutically valuable agent for the treatment of Type 2 diabetes.
Martinez, Barbara T; Razafindratsima, Onja H
Frugivorous primates can play a critical role in the regeneration of degraded habitats by dispersing seeds of their food plants. We studied the diet and seed dispersal patterns of 3 groups of habituated red-ruffed lemurs (Varecia rubra) in a rain forest restoration site in Masoala National Park, Madagascar, to assess the species' seed dispersal effectiveness. Fruits accounted for 61% of the diet, with an average foraging time of 10 min per fruit patch per day. Seeds from 75% of the consumed fruit species were recovered in the collected V. rubra feces. We traced the potential parent plants of 20 dispersed-seed species to calculate a gut passage range (63-423 min; mean = 225, n = 35). The median seed dispersal distance from the potential parent plant was 48 m (mean = 83 m, range 0-568 m, n = 194). The home ranges of 2 of the 3 groups overlapped with the regenerating forest parcels. Although 92% of fecal samples with seeds were dispersed into the undisturbed forest, V. rubra fed on the fruits of the non-native pioneer shrub Clidemia hirta, while also dispersing native and non-native seed species into the regenerating forest parcels.
Simmen, Bruno; Tarnaud, Laurent; Marez, André; Hladik, Annette
Folivorous primate biomass has been shown to positively correlate with the average protein-to-fiber ratio in mature leaves of tropical forests. However, studies have failed to explain the mismatch between dietary selection and the role of the protein-to-fiber ratio on primate biomass; why do not folivores always favor mature leaves or leaves with the highest protein-to-fiber ratio? We examined the effect of leaf chemical characteristics and plant abundance (using transect censuses; 0.37 ha, 233 trees) on food choices and nutrient/toxin consumption in a folivorous lemur (Propithecus verreauxi) in a gallery forest in southern Madagascar. To assess the nutritional quality of the habitat, we calculated an abundance-weighted chemical index for each chemical variable. Food intake was quantified using a continuous count of mouthfuls during individual full-day follows across three seasons. We found a significant positive correlation between food ranking in the diet and plant abundance. The protein-to-fiber ratio and most other chemical variables tested had no statistical effect on dietary selection. Numerous chemical characteristics of the sifaka's diet were essentially by-products of generalist feeding and "low energy input/low energy crop" strategy. The examination of feeding behavior and plant chemistry in Old World colobines and folivorous prosimians in Madagascar suggests that relative lack of feeding selectivity and high primate biomass occur when the average protein-to-fiber ratio of mature leaves in the habitat exceeds a threshold at 0.4.
Gould, Lisa; Kelley, Elizabeth A; LaFleur, Marni
The spiny forest ecoregion of southern and southwestern Madagascar is characterized by low annual rainfall, high temperatures, short-stature xeric vegetation and lack of canopy. Lemur catta is often the only diurnal primate persisting in this habitat. For reproductive females living in spiny forests, gestation and early-to-mid lactation periods occur during the dry season when food resources are limited. We conducted a between-site comparison of variables important to the feeding ecology of reproductive female L. catta inhabiting spiny forest at 3 sites: Berenty spiny forest (BSF), Cap Sainte-Marie (CSM) and Tsimanampesotse National Park (TNP). We hypothesize that the ability for pregnant and lactating females to adequately obtain plant foods high in protein, low in fiber and with a high water content is crucial to their survival and successful reproduction in spiny habitat. We found favorable or relatively equal protein-to-fiber ratios in plant foods most frequently consumed by reproductive females, and preferred foods contained high water content. Some overlap in preferred plant species at the 3 sites suggests important plant foods for reproductive females inhabiting spiny forests. We suggest that choosing foods high in protein, relatively low in fiber and with high water content are behavioral adaptations allowing female L. catta to reproduce and survive in this habitat.
Fecal inoculum can be used to determine the rate and extent of in vitro fermentation of dietary fiber sources across three lemur species that differ in dietary profile: Varecia variegata, Eulemur fulvus and Hapalemur griseus.
Campbell, J L; Williams, C V; Eisemann, J H
To estimate fermentative capacity among lemur species, four fiber substrates were tested across three species, Eulemur fulvus, Hapalemur griseus and Varecia variegata. The substrates, cellulose, beet pulp, citrus pulp and citrus pectin, ranged in composition from completely insoluble fiber (IF) to completely soluble fiber (SF), respectively. The lemurs consumed a nutritionally complete biscuit formulated for primates [85 g/100 g diet dry matter (DM)] and locally available produce (15 g/100 g diet DM). Feces were then collected and used to inoculate fermentation tubes prefilled with fiber substrates and an anaerobic growth medium. Dry matter disappearance (DMD), and acetate, propionate, butyrate, and total short-chain fatty acid (SCFA) production were measured in tubes subjected to 6, 12, 24 or 48 h of fermentation. Results were fitted to a logistic growth model. The maximal production (MP) time at which production or disappearance is at one-half maximum (t(50)) and the fermentation rate at 3 h were calculated. The maximal disappearance of DM differed among substrates (citrus pectin > citrus pulp > beet pulp; P < 0.0001) and species (E. fulvus > H. griseus > V. variegata; P < 0.001). V. variegata reached t(50) for acetate and total SCFA production faster than H. griseus or E. fulvus (P < 0.02). Three-hour production rates of acetate and total SCFA were also greater for V. variegata for citrus pulp and citrus pectin (P < 0.01). Few species differences were observed for beet pulp. Results provide evidence for differences in fermentative capacity and suggest that fiber solubility and fermentability should be considered when assessing the nutritional management of lemurs.
Of lemurs and louse flies: The biogeochemical and biotic effects of forest disturbance on Propithecus edwardsi and its obligate ectoparasite Allobosca crassipes in Ranomafana National Park, southeastern Madagascar.
McGee, Elizabeth; Vaughn, Stanley
From alleles to ecosystems and landscapes, anthropogenic activity continues to affect the environment, with particularly adverse effects on biodiversity hotspots such as Madagascar. Selective logging has been proposed as a "win-win" conservation strategy, yet its effects on different components of biodiversity are still not fully understood. Here we examine biotic factors (i.e., dietary differences) that may be driving differences in biogeochemical stocks between disturbed and undisturbed forests. We present the stable nitrogen (δ(15) N) and carbon (δ(13) C) isotope composition of hair from the lemur Propithecus edwardsi and of whole bodies of its obligate ectoparasite, the louse-fly Allobosca crassipes, from sites in Ranomafana National Park (RNP) that are comparable except for the history of logging and subsequent forest regeneration. P. edwardsi and A. crassipes from the disturbed (i.e., heavily selectively logged) site are lower in (15) N and (13) C relative to P. edwardsi and A. crassipes from sites that were minimally selectively logged or not commercially logged at all. There is a ∼3‰ decrease in (15) N between disturbed and undisturbed sites that corresponds to a difference of nearly a full trophic level. Flowers from Bakerella clavata, a staple food source for P. edwardsi in disturbed habitats and a fallback food for P. edwardsi in primary forests, were also analyzed isotopically. B. clavata is δ(15) N-depleted in both disturbed and undisturbed sites. Data from longitudinal behavioral surveys of P. edwardsi in RNP and other forests in eastern Madagascar point to significant differences in consumption patterns of B. clavata, with P. edwardsi in disturbed forests consuming almost twice as much of this plant. Depletion of (15) N in animal tissues is a complex issue, but likely the result of the interaction of physiological and ecological factors. Anthropogenic disturbance in RNP from selective logging has had both biotic and biogeochemical effects that
Dutton, Christopher; Lentini, Andrew; Berkvens, Charlene; Crawshaw, Graham
"Brown skin disease" (BSD) is a clinical syndrome of dysecdysis, chronic weight loss and death, previously reported in Puerto Rican crested toads (Peltophryne lemur). Although vitamin A deficiency has been suggested, its cause remains unknown and multiple treatments have failed to prevent or reverse the condition. This study compared the efficacy of vitamin A supplementation, administered in different forms and by different routes, in 48 captive born Puerto Rican crested toads fed from metamorphosis on gut-loaded, dusted, commercially raised crickets. Forty-five toads started to show clinical signs of BSD at 9 months of age; all toads were treated orally with an oil-based vitamin A formulation twice weekly for 2 months but continued to deteriorate. Two treatment groups were then compared: Animals in one group (n=19) received 2 IU injectable vitamin A (Aquasol-A) per gram bodyweight subcutaneously twice weekly for 3 months with no change in diet. Toads in the other group (n=22) received a single oral dose of vitamins A, D3 , and E, and were fed on earthworms and crickets gut-loaded with produce and a finely-ground alfalfa-based pellet, dusted with the same vitamin/mineral supplement. All affected animals developed severe BSD equally and died during, or were euthanized at the end of, the treatment regimen, with no clinical improvement. Animals supplemented with Aquasol-A had significantly higher liver vitamin A concentrations compared with the other treatment group, whereas serum retinol concentrations showed no significant difference. Vitamin A supplementation does not appear a successful treatment once BSD symptoms have developed.
Zohdy, Sarah; Gerber, Brian D.; Tecot, Stacey; Blanco, Marina B.; Winchester, Julia M.; Wright, Patricia C.; Jernvall, Jukka
Mouse lemurs (Microcebus spp.) are an exciting new primate model for understanding human aging and disease. In captivity, Microcebus murinus develops human-like ailments of old age after five years (e.g., neurodegeneration analogous to Alzheimer's disease) but can live beyond 12 years. It is believed that wild Microcebus follow a similar pattern of senescence observed in captive animals, but that predation limits their lifespan to four years, thus preventing observance of these diseases in the wild. Testing whether this assumption is true is informative about both Microcebus natural history and environmental influences on senescence, leading to interpretation of findings for models of human aging. Additionally, the study of Microcebus longevity provides an opportunity to better understand mechanisms of sex-biased longevity. Longevity is often shorter in males of species with high male-male competition, such as Microcebus, but mouse lemurs are sexually monomorphic, suggesting similar lifespans. We collected individual-based observations of wild brown mouse lemurs (Microcebus rufus) from 2003–2010 to investigate sex-differences in survival and longevity. Fecal testosterone was measured as a potential mechanism of sex-based differences in survival. We used a combination of high-resolution tooth wear techniques, mark-recapture, and hormone enzyme immunoassays. We found no dental or physical signs of senescence in M. rufus as old as eight years (N = 189, ages 1–8, mean = 2.59±1.63 SE), three years older than captive, senescent congeners (M. murinus). Unlike other polygynandrous vertebrates, we found no sex difference in age-dependent survival, nor sex or age differences in testosterone levels. While elevated male testosterone levels have been implicated in shorter lifespans in several species, this is one of the first studies to show equivalent testosterone levels accompanying equivalent lifespans. Future research on captive aged individuals can determine
The anatomy and ontogeny of the head, neck, pectoral, and upper limb muscles of Lemur catta and Propithecus coquereli (primates): discussion on the parallelism between ontogeny and phylogeny and implications for evolutionary and developmental biology.
Diogo, Rui; Molnar, Julia L; Smith, Timothy D
Most anatomical studies of primates focus on skeletal tissues, but muscular anatomy can provide valuable information about phylogeny, functional specializations, and evolution. Herein, we present the first detailed description of the head, neck, pectoral, and upper limb muscles of the fetal lemuriforms Lemur catta (Lemuridae) and Propithecus coquereli (Indriidae). These two species belong to the suborder Strepsirrhini, which is often presumed to possess some plesiomorphic anatomical features within primates. We compare the muscular anatomy of the fetuses with that of infants and adults and discuss the evolutionary and developmental implications. The fetal anatomy reflects a phylogenetically more plesiomorphic condition in nine of the muscles we studied and a more derived condition in only two, supporting a parallel between ontogeny and phylogeny. The derived exceptions concern muscles with additional insertions in the fetus which are lost in adults of the same species, that is, flexor carpi radialis inserts on metacarpal III and levator claviculae inserts on the clavicle. Interestingly, these two muscles are involved in movements of the pectoral girdle and upper limb, which are mainly important for activities in later stages of life, such as locomotion and prey capture, rather than activities in fetal life. Accordingly, our findings suggest that some exceptions to the "ontogeny parallels phylogeny" rule are probably driven more by ontogenetic constraints than by adaptive plasticity. © 2014 Wiley Periodicals, Inc.
Kobbe, Susanne; Nowack, Julia; Dausmann, Kathrin H
The reddish-gray mouse lemur (Microcebus griseorufus) is one of only a few small mammals inhabiting the spiny forest of southwestern Madagascar. In this study we investigated the physiological adjustments which allow these small primates to persist under the challenging climatic conditions of their habitat. To this end we measured energy expenditure (metabolic rate) and body temperature of 24 naturally acclimatized mouse lemurs, kept in outdoor enclosures, during different seasons (summer, winter, and the transition period between the two seasons). Mouse lemurs displayed two main physiological strategies to compensate seasonal and diurnal fluctuations of ambient temperature. On the one hand, individuals entered hypometabolism with decreasing ambient temperature (T a) during the transition period and winter, enabling them to save up to 21 % energy per day (92 % per hour) compared with the normal resting metabolic rate at comparable T a. On the other hand, euthermic mouse lemurs also showed physiological adjustments to seasonality when resting: the lower critical temperature of the thermoneutral zone decreased from summer to winter by 7.5 °C, which allowed mouse lemurs to keep energy demands constant despite colder T as during winter. In addition, the basal metabolic rate was substantially lowered prior to the winter period, which facilitated accumulation of fat reserves. The combination of physiological modifications during euthermia in addition to hypometabolism, which can be individually adjusted according to external parameters and respective body condition, is important as it allows M. griseorufus to cope with the environmental variability of an energetically challenging habitat.
Schopf, Christian; Schmidt, Sabine
When exposed to enhanced background noise, humans avoid signal masking by increasing the amplitude of the voice, a phenomenon termed the Lombard effect. This auditory feedback-mediated voice control has also been found in monkeys, bats, cetaceans, fish and some frogs and birds. We studied the Lombard effect for the first time in a phylogenetically basal primate, the grey mouse lemur, Microcebus murinus. When background noise was increased, mouse lemurs were able to raise the amplitude of the voice, comparable to monkeys, but they did not show this effect consistently across context/individuals. The Lombard effect, even if representing a generic vocal communication system property of mammals, may thus be affected by more complex mechanisms. The present findings emphasize an effect of context, and individual, and the need for further standardized approaches to disentangle the multiple system properties of mammalian vocal communication, important for understanding the evolution of the unique human faculty of speech and language. PMID:27602292
Laakkonen, Juha; Jernvall, Jukka
ABSTRACT Longitudinal sampling for intestinal microbiota in wild animals is difficult, leading to a lack of information on bacterial dynamics occurring in nature. We studied how the composition of microbiota communities changed temporally in free-ranging small primates, rufous mouse lemurs (Microcebus rufus). We marked and recaptured mouse lemurs during their mating season in Ranomafana National Park in southeastern mountainous rainforests of Madagascar for 2 years and determined the fecal microbiota compositions of these mouse lemurs with MiSeq sequencing. We collected 160 fecal samples from 71 animals and had two or more samples from 39 individuals. We found small, but statistically significant, effects of site and age on microbiota richness and diversity and effects of sex, year, and site on microbiota composition, while the within-year temporal trends were less clear. Within-host microbiota showed pervasive variation in intestinal bacterial community composition, especially during the second study year. We hypothesize that the biological properties of mouse lemurs, including their small body size and fast metabolism, may contribute to the temporal intraindividual-level variation, something that should be testable with more-extensive sampling regimes. IMPORTANCE While microbiome research has blossomed in recent years, there is a lack of longitudinal studies on microbiome dynamics on free-ranging hosts. To fill this gap, we followed mouse lemurs, which are small heterothermic primates, for 2 years. Most studied animals have shown microbiota to be stable over the life span of host individuals, but some previous research also found ample within-host variation in microbiota composition. Our study used a larger sample size than previous studies and a study setting well suited to track within-host variation in free-ranging mammals. Despite the overall microbiota stability at the population level, the microbiota of individual mouse lemurs can show large-scale changes
Kennedy, B.; Aghazarian, H.; Cheng, Y.; Garrett, M.; Hutsberger, T.; Magnone, L.; Okon, A.; Robinson, M.
The assembly inspection, and maintenance requirements of permanent installations in space demand robotic agents that provide a high level of operational flexibility relative to the mass and volume of the robotic system.
Veilleux, Carrie C; Kirk, E Christopher
Studies of visual acuity in primates have shown that diurnal haplorhines have higher acuity (30-75 cycles per degree (c/deg)) than most other mammals. However, relatively little is known about visual acuity in non-haplorhine primates, and published estimates are only available for four strepsirrhine genera (Microcebus, Otolemur, Galago, and Lemur). We present here the first measurements of visual acuity in a cathemeral strepsirrhine species, the blue-eyed black lemur (Eulemur macaco flavifrons). Acuity in two subjects, a 3-year-old male and a 16-year-old female, was assessed behaviorally using a two-alternative forced choice discrimination task. Visual stimuli consisted of high contrast square wave gratings of seven spatial frequencies. Acuity threshold was determined using a 70% correct response criterion. Results indicate a maximum visual acuity of 5.1 c/deg for the female (1718 trials) and 3.8 c/deg for the male (846 trials). These values for E. macaco are slightly lower than those reported for diurnal Lemur catta, and are generally comparable to those reported for nocturnal Microcebus murinus and Otolemur crassicaudatus. To examine ecological sources of variation in primate visual acuity, we also calculated maximum theoretical acuity for Cheirogaleus medius (2.8 c/deg) and Tarsius syrichta (8.9 c/deg) using published data on retinal ganglion cell density and eye morphology. These data suggest that visual acuity in primates may be influenced by activity pattern, diet, and phylogenetic history. In particular, the relatively high acuity of T. syrichta and Galago senegalensis suggests that visual predation may be an important selective factor favoring high visual acuity in primates.
... period. Species: Ring-tailed lemur (Lemur catta) Black and white ruffed lemur (Varecia variegata) Red ruffed lemur (Varecia rubra) Crowned lemur (Eulemur coronatus) Black lemur (Eulemur macaco) Brown lemur... (Bettongia penicillata) Ring-tailed lemur (Lemur catta) Black and white ruffed lemur (Varecia variegata)...
Gifford, Robert J.; Katzourakis, Aris; Tristem, Michael; Pybus, Oliver G.; Winters, Mark; Shafer, Robert W.
Lentiviruses chronically infect a broad range of mammalian species and have been transmitted from primates to humans, giving rise to multiple outbreaks of HIV infection over the past century. Although the circumstances surrounding these recent zoonoses are becoming clearer, the nature and timescale of interaction between lentiviruses and primates remains unknown. Here, we report the discovery of an endogenous lentivirus in the genome of the gray mouse lemur (Microcebus murinus), a strepsirrhine primate from Madagascar, demonstrating that lentiviruses are capable of invading the primate germ line. Phylogenetic analysis places gray mouse lemur prosimian immunodeficiency virus (pSIVgml) basal to all known primate lentiviruses and, consistent with this, its genomic organization is intermediate between the nonprimate lentiviruses and their more derived primate counterparts. Thus, pSIVgml represents the first unambiguous example of a viral transitional form, revealing the acquisition and loss of genomic features during lentiviral evolution. Furthermore, because terrestrial mammal populations in Madagascar and Africa are likely to have been isolated from one another for at least 14 million years, the presence of pSIVgml in the gray mouse lemur genome indicates that lentiviruses must have been infecting primates for at least this period of time, or have been transmitted between Malagasy and African primate populations by a vector species capable of traversing the Mozambique channel. The discovery of pSIVgml illustrates the utility of endogenous sequences for the study of contemporary retroviruses and indicates that primate lentiviruses may be considerably older and more broadly distributed than previously thought. PMID:19075221
Djelti, Fathia; Dhenain, Marc; Terrien, Jérémy; Picq, Jean-Luc; Hardy, Isabelle; Champeval, Delphine; Perret, Martine; Schenker, Esther; Epelbaum, Jacques; Aujard, Fabienne
Age-associated cognitive impairment is a major health and social issue because of increasing aged population. Cognitive decline is not homogeneous in humans and the determinants leading to differences between subjects are not fully understood. In middle-aged healthy humans, fasting blood glucose levels in the upper normal range are associated with memory impairment and cerebral atrophy. Due to a close evolutional similarity to Man, non-human primates may be useful to investigate the relationships between glucose homeostasis, cognitive deficits and structural brain alterations. In the grey mouse lemur, Microcebus murinus, spatial memory deficits have been associated with age and cerebral atrophy but the origin of these alterations have not been clearly identified. Herein, we showed that, on 28 female grey mouse lemurs (age range 2.4-6.1 years-old), age correlated with impaired fasting blood glucose (rs=0.37) but not with impaired glucose tolerance or insulin resistance. In middle-aged animals (4.1-6.1 years-old), fasting blood glucose was inversely and closely linked with spatial memory performance (rs=0.56) and hippocampus (rs=−0.62) or septum (rs=−0.55) volumes. These findings corroborate observations in humans and further support the grey mouse lemur as a natural model to unravel mechanisms which link impaired glucose homeostasis, brain atrophy and cognitive processes. PMID:28039490
Schliehe-Diecks, S.; Kappeler, P. M.; Langrock, R.
Analysing behavioural sequences and quantifying the likelihood of occurrences of different behaviours is a difficult task as motivational states are not observable. Furthermore, it is ecologically highly relevant and yet more complicated to scale an appropriate model for one individual up to the population level. In this manuscript (mixed) hidden Markov models (HMMs) are used to model the feeding behaviour of 54 subadult grey mouse lemurs (Microcebus murinus), small nocturnal primates endemic to Madagascar that forage solitarily. Our primary aim is to introduce ecologists and other users to various HMM methods, many of which have been developed only recently, and which in this form have not previously been synthesized in the ecological literature. Our specific application of mixed HMMs aims at gaining a better understanding of mouse lemur behaviour, in particular concerning sex-specific differences. The model we consider incorporates random effects for accommodating heterogeneity across animals, i.e. accounts for different personalities of the animals. Additional subject- and time-specific covariates in the model describe the influence of sex, body mass and time of night. PMID:23565332
Despite increasing interest, animal personality is still a puzzling phenomenon. Several theoretical models have been proposed to explain intraindividual consistency and interindividual variation in behaviour, which have been primarily supported by qualitative data and simulations. Using an empirical approach, I tested predictions of one main life-history hypothesis, which posits that consistent individual differences in behaviour are favoured by a trade-off between current and future reproduction. Data on life-history were collected for individuals of a natural population of grey mouse lemurs (Microcebus murinus). Using open-field and novel-object tests, I quantified variation in activity, exploration and boldness for 117 individuals over 3 years. I found systematic variation in boldness between individuals of different residual reproductive value. Young males with low current but high expected future fitness were less bold than older males with high current fecundity, and males might increase in boldness with age. Females have low variation in assets and in boldness with age. Body condition was not related to boldness and only explained marginal variation in exploration. Overall, these data indicate that a trade-off between current and future reproduction might maintain personality variation in mouse lemurs, and thus provide empirical support of this life-history trade-off hypothesis.
Le Tallec, Thomas; Perret, Martine; Théry, Marc
Among anthropogenic pressures, light pollution altering light/dark cycles and changing the nocturnal component of the environment constitutes a threat for biodiversity. Light pollution is widely spread across the world and continuously growing. However, despite the efforts realized to describe and understand the effects of artificial lighting on fauna, few studies have documented its consequences on biological rhythms, behavioral and physiological functions in nocturnal mammals. To determine the impacts of light pollution on nocturnal mammals an experimental study was conducted on a nocturnal primate, the grey mouse lemur Microcebus murinus. Male mouse lemurs (N = 8) were exposed 14 nights to moonlight treatment and then exposed 14 nights to light pollution treatment. For both treatments, chronobiological parameters related to locomotor activity and core temperature were recorded using telemetric transmitters. In addition, at the end of each treatment, the 14th night, nocturnal and feeding behaviors were explored using an infrared camera. Finally, throughout the study, body mass and daily caloric food intake were recorded. For the first time in a nocturnal primate, light pollution was demonstrated to modify daily rhythms of locomotor activity and core temperature especially through phase delays and increases in core temperature. Moreover, nocturnal activity and feeding behaviors patterns were modified negatively. This study suggests that light pollution induces daily desynchronization of biological rhythms and could lead to seasonal desynchronization with potential deleterious consequences for animals in terms of adaptation and anticipation of environmental changes. PMID:24236115
Despite increasing interest, animal personality is still a puzzling phenomenon. Several theoretical models have been proposed to explain intraindividual consistency and interindividual variation in behaviour, which have been primarily supported by qualitative data and simulations. Using an empirical approach, I tested predictions of one main life-history hypothesis, which posits that consistent individual differences in behaviour are favoured by a trade-off between current and future reproduction. Data on life-history were collected for individuals of a natural population of grey mouse lemurs (Microcebus murinus). Using open-field and novel-object tests, I quantified variation in activity, exploration and boldness for 117 individuals over 3 years. I found systematic variation in boldness between individuals of different residual reproductive value. Young males with low current but high expected future fitness were less bold than older males with high current fecundity, and males might increase in boldness with age. Females have low variation in assets and in boldness with age. Body condition was not related to boldness and only explained marginal variation in exploration. Overall, these data indicate that a trade-off between current and future reproduction might maintain personality variation in mouse lemurs, and thus provide empirical support of this life-history trade-off hypothesis. PMID:22398164
Le Tallec, Thomas; Perret, Martine; Théry, Marc
Among anthropogenic pressures, light pollution altering light/dark cycles and changing the nocturnal component of the environment constitutes a threat for biodiversity. Light pollution is widely spread across the world and continuously growing. However, despite the efforts realized to describe and understand the effects of artificial lighting on fauna, few studies have documented its consequences on biological rhythms, behavioral and physiological functions in nocturnal mammals. To determine the impacts of light pollution on nocturnal mammals an experimental study was conducted on a nocturnal primate, the grey mouse lemur Microcebus murinus. Male mouse lemurs (N = 8) were exposed 14 nights to moonlight treatment and then exposed 14 nights to light pollution treatment. For both treatments, chronobiological parameters related to locomotor activity and core temperature were recorded using telemetric transmitters. In addition, at the end of each treatment, the 14(th) night, nocturnal and feeding behaviors were explored using an infrared camera. Finally, throughout the study, body mass and daily caloric food intake were recorded. For the first time in a nocturnal primate, light pollution was demonstrated to modify daily rhythms of locomotor activity and core temperature especially through phase delays and increases in core temperature. Moreover, nocturnal activity and feeding behaviors patterns were modified negatively. This study suggests that light pollution induces daily desynchronization of biological rhythms and could lead to seasonal desynchronization with potential deleterious consequences for animals in terms of adaptation and anticipation of environmental changes.
Background Timing the origin of human malarias has been a focus of great interest. Previous studies on the mitochondrial genome concluded that Plasmodium in primates, including those parasitic to humans, radiated relatively recently during a process where host switches were common. Those investigations, however, assumed constant rate of evolution and tightly bound (fixed) calibration points based on host fossils or host distribution. We investigate the effect of such assumptions using different molecular dating methods. We include parasites from Lemuroidea since their distribution provides an external validation to time estimates allowing us to disregard scenarios that cannot explain their introduction in Madagascar. Results We reject the assumption that the Plasmodium mitochondrial genome, as a unit or each gene separately, evolves at a constant rate. Our analyses show that Lemuroidea parasites are a monophyletic group that shares a common ancestor with all Catarrhini malarias except those related to P. falciparum. However, we found no evidence that this group of parasites branched with their hosts early in the evolution of primates. We applied relaxed clock methods and different calibrations points to explore the origin of primate malarias including those found in African apes. We showed that previous studies likely underestimated the origin of malarial parasites in primates. Conclusions The use of fossils from the host as absolute calibration and the assumption of a strict clock likely underestimate time when performing molecular dating analyses on malarial parasites. Indeed, by exploring different calibration points, we found that the time for the radiation of primate parasites may have taken place in the Eocene, a time consistent with the radiation of African anthropoids. The radiation of the four human parasite lineages was part of such events. The time frame estimated in this investigation, together with our phylogenetic analyses, made plausible a scenario where gorillas and humans acquired malaria from a Pan lineage. PMID:21992100
Canale, Cindy I; Huchard, Elise; Perret, Martine; Henry, Pierre-Yves
The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive
Perret, Martine; Henry, Pierre-Yves
The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive
Terrien, Jeremy; Zahariev, Alexandre; Blanc, Stephane; Aujard, Fabienne
Daily heterothermia is used by small mammals for energy and water savings, and seems to be preferentially exhibited during winter rather than during summer. This feature induces a trade-off between the energy saved during daily heterothermia and the energy cost of arousal, which can impact energy balance and survival under harsh environmental conditions. Especially, aging may significantly affect such trade off during cold-induced energy stress, but direct evidences are still lacking. We hypothesized that aging could alter the energetics of daily heterothermia, and that the effects could differ according to season. In the gray mouse lemur (Microcebus murinus), a non-human primate species which exhibits daily heterothermia, we investigated the effects of exposures to 25 and 12 degrees C on body composition, energy balance, patterns of heterothermia and water turnover in adult (N = 8) and aged animals (N = 7) acclimated to winter-like or summer-like photoperiods. Acclimation to summer prevented animals from deep heterothermia, even during aging. During winter, adult animals at 12 degrees C and aged animals at 25 degrees C exhibited low levels of energy expenditure with minor modulations of heterothermia. The major effects of cold were observed during winter, and were particularly pronounced in aged mouse lemurs which exhibited deep heterothermia phases. Body composition was not significantly affected by age and could not explain the age-related differences in heterothermia patterns. However, aging was associated with increased levels of energy expenditure during cold exposure, in concomitance with impaired energy balance. Interestingly, increased energy expenditure and depth of heterothermia phases were strongly correlated. In conclusion, it appeared that the exhibition of shallow heterothermia allowed energy savings during winter in adult animals only. Aged animals exhibited deep heterothermia and increased levels of energy expenditure, impairing energy balance
Marchal, Julia; Picq, Jean-Luc; Aujard, Fabienne
Effects of an 18-month treatment with a moderate, chronic caloric restriction (CR) or an oral supplementation with resveratrol (RSV), a potential CR mimetic, on cognitive and motor performances were studied in non-human primates, grey mouse lemurs (Microcebus murinus). Thirty-three adult male mouse lemurs were assigned to three different groups: a control (CTL) group fed ad libitum, a CR group fed 70% of the CTL caloric intake, and an RSV group (RSV supplementation of 200 mg.kg−1.day−1) fed ad libitum. Three different cognitive tests, two motor tests, one emotional test and an analysis of cortisol level were performed in each group. Compared to CTL animals, CR or RSV animals did not show any change in motor performances evaluated by rotarod and jump tests, but an increase in spontaneous locomotor activity was observed in both groups. Working memory was improved by both treatments in the spontaneous alternation task. Despite a trend for CR group, only RSV supplementation increased spatial memory performances in the circular platform task. Finally, none of these treatments induced additional stress to the animals as reflected by similar results in the open field test and cortisol analyses compared to CTL animals. The present data provided the earliest evidence for a beneficial effect of CR or RSV supplementation on specific cognitive functions in a primate. Taken together, these results suggest that RSV could be a good candidate to mimic long-term CR effects and support the growing evidences that nutritional interventions can have beneficial effects on brain functions even in adults. PMID:21304942
Vuarin, Pauline; Henry, Pierre-Yves; Guesnet, Philippe; Alessandri, Jean-Marc; Aujard, Fabienne; Perret, Martine; Pifferi, Fabien
Optimal levels of unsaturated fatty acids have positive impacts on the use of prolonged bouts of hypothermia in mammalian hibernators, which generally have to face low winter ambient temperatures. Unsaturated fatty acids can maintain the fluidity of fat and membrane phospholipids at low body temperatures. However, less attention has been paid to their role in the regulation of shallow hypothermia, and in tropical species, which may be challenged more by seasonal energetic and/or water shortages than by low temperatures. The present study assessed the relationship between the fatty acids content of white adipose and liver tissues and the expression of shallow hypothermia in a tropical heterothermic primate, the gray mouse lemur (Microcebus murinus). The adipose tissue is the main tissue for fat storage and the liver is involved in lipid metabolism, so both tissues were expected to influence hypothermia dependence on fatty acids. As mouse lemurs largely avoid deep hypothermia (i.e. torpor) use under standard captive conditions, the expression of hypothermia was triggered by food-restricting experimental animals. Hypothermia depth increased with time, with a stronger increase for individuals that exhibited higher contents of unsaturated fatty acids suggesting that they were more flexible in their use of hypothermia. However these same animals delayed the use of long hypothermia bouts relative to individuals with a higher level of saturated fatty acids. This study evidences for the first time that body fatty acids unsaturation levels influence the regulation of body temperature not only in cold-exposed hibernators but also in tropical, facultative heterotherms. Copyright © 2014 Elsevier Ltd. All rights reserved.
Background Kin selection is a driving force in the evolution of mammalian social complexity. Recognition of paternal kin using vocalizations occurs in taxa with cohesive, complex social groups. This is the first investigation of paternal kin recognition via vocalizations in a small-brained, solitary foraging mammal, the grey mouse lemur (Microcebus murinus), a frequent model for ancestral primates. We analyzed the high frequency/ultrasonic male advertisement (courtship) call and alarm call. Results Multi-parametric analyses of the calls’ acoustic parameters and discriminant function analyses showed that advertisement calls, but not alarm calls, contain patrilineal signatures. Playback experiments controlling for familiarity showed that females paid more attention to advertisement calls from unrelated males than from their fathers. Reactions to alarm calls from unrelated males and fathers did not differ. Conclusions 1) Findings provide the first evidence of paternal kin recognition via vocalizations in a small-brained, solitarily foraging mammal. 2) High predation, small body size, and dispersed social systems may select for acoustic paternal kin recognition in the high frequency/ultrasonic ranges, thus limiting risks of inbreeding and eavesdropping by predators or conspecific competitors. 3) Paternal kin recognition via vocalizations in mammals is not dependent upon a large brain and high social complexity, but may already have been an integral part of the dispersed social networks from which more complex, kin-based sociality emerged. PMID:23198727
Schwensow, Nina; Eberle, Manfred; Sommer, Simone
The mechanisms and temporal aspects of mate choice according to genetic constitution are still puzzling. Recent studies indicate that fitness is positively related to diversity in immune genes (MHC). Both sexes should therefore choose mates of high genetic quality and/or compatibility. However, studies addressing the role of MHC diversity in pre- and post-copulatory mate choice decisions in wild-living animals are few. We investigated the impact of MHC constitution and of neutral microsatellite variability on pre- and post-copulatory mate choice in both sexes in a wild population of a promiscuous primate, the grey mouse lemur (Microcebus murinus). There was no support for pre-copulatory male or female mate choice, but our data indicate post-copulatory mate choice that is associated with genetic constitution. Fathers had a higher number of MHC supertypes different from those of the mother than randomly assigned males. Fathers also had a higher amino acid distance to the females' MHC as well as a higher total number of MHC supertypes and a higher degree of microsatellite heterozygosity than randomly assigned males. Female cryptic choice may be the underlying mechanism that operates towards an optimization of the genetic constitution of offspring. This is the first study that provides support for the importance of the MHC constitution in post-copulatory mate choice in non-human primates. PMID:18089539
Vuarin, Pauline; Dammhahn, Melanie; Kappeler, Peter M; Henry, Pierre-Yves
Timing of winter phenotype expression determines individual chances of survival until the next reproductive season. Environmental cues triggering this seasonal phenotypic transition have rarely been investigated, although they play a central role in the compensation of climatic fluctuations via plastic phenotypic adjustments. Initiation of winter daily torpor use-a widespread energy-saving phenotype-could be primarily timed according to anticipatory seasonal cues (anticipatory cues hypothesis), or flexibly fine-tuned according to actual energy availability (food shortage hypothesis). We conducted a food supplementation experiment on wild heterothermic primates (grey mouse lemurs, Microcebus murinus) at the transition to the food-limited dry season, i.e. the austral winter. As expected under the food shortage hypothesis, food-supplemented individuals postponed the seasonal transition to normal torpor use by 1-2 month(s), spent four times less torpid, and exhibited minimal skin temperature 6 °C higher than control animals. This study provides the first in situ experimental evidence that food availability, rather than abiotic cues, times the launching of torpor use. Fine-tuning of the timing of seasonal phenotypic transitions according to actual food shortage should provide heterotherms with a flexible adaptive mechanism to survive unexpected environmental fluctuations.
Canale, Cindy I; Perret, Martine; Théry, Marc; Henry, Pierre-Yves
As ecosystems undergo changes worldwide, physiological flexibility is likely to be an important adaptive response to increased climate instability. Extreme weather fluctuations impose energetical constraints such as unpredictable food shortage. We tested how grey mouse lemurs (Microcebus murinus) could adjust their daily heterothermy and locomotor activity to these 'energetic accidents' with a food restriction experiment. The experimental design consisted of acute calorie restriction (2 weeks, 80% restriction) in the middle of winter, after a fattening season with low (11 weeks, 40% restriction) versus high (ad libitum) food availability. This design aimed at simulating the combined effects of the quality of the fattening season (acclimation effect) and a sudden, severe food shortage during the lean season. Hour of start and duration of torpor were the most flexible components of energy savings, increasing in response to the acute food shortage with facilitation by chronic restriction (acclimation effect). Modulations of locomotor activity did not support the hypothesis of energy savings, as total locomotor activity was not reduced. Nonetheless, acutely restricted individuals modified their temporal pattern of locomotor activity according to former food availability. We provide the first experimental evidence of different temporal levels of flexibility of energy-saving mechanisms in a heterotherm exposed to food shortage. The acclimation effect of past food scarcity suggests that heterothermic organisms are better able to respond to unpredicted food scarcity during the lean season. The flexible control of energy expenditure conferred by heterothermy may facilitate the plastic response of heterothermic species to more frequent climatic hazards.
Kraus, Cornelia; Eberle, Manfred; Kappeler, Peter M
Male excess mortality is widespread among mammals and frequently interpreted as a cost of sexually selected traits that enhance male reproductive success. Sex differences in the propensity to engage in risky behaviours are often invoked to explain the sex gap in survival. Here, we aim to isolate and quantify the survival consequences of two potentially risky male behavioural strategies in a small sexually monomorphic primate, the grey mouse lemur Microcebus murinus: (i) most females hibernate during a large part of the austral winter, whereas most males remain active and (ii) during the brief annual mating season males roam widely in search of receptive females. Using a 10-year capture–mark–recapture dataset from a population of M. murinus in Kirindy Forest, western Madagascar, we statistically modelled sex-specific seasonal survival probabilities. Surprisingly, we did not find any evidence for direct survival benefits of hibernation—winter survival did not differ between males and females. By contrast, during the breeding season males survived less well than females (sex gap: 16%). Consistent with the ‘risky male behaviour’ hypothesis, the period for lowered male survival was restricted to the short mating season. Thus, sex differences in survival in a promiscuous mammal can be substantial even in the absence of sexual dimorphism. PMID:18426751
Canale, Cindy I.; Perret, Martine; Henry, Pierre-Yves
Torpor is an energy-saving mechanism that allows endotherms to overcome energetic challenges. Torpor should be avoided during reproduction because of potential incompatibility with offspring growth. To test if torpor can be used during gestation and lactation to compensate for food shortage, we exposed reproductive female grey mouse lemurs ( Microcebus murinus), a heterothermic primate, to different levels of food availability. Torpor use was characterised by daily skin temperature profiles, and its energetic outcome was assessed from changes in body mass. Food shortage triggered torpor during the end of the gestation period ( n = 1), ranging from shallow in response to 40% food restriction to deep daily torpor in response to 80% restriction. During the early period of lactation, females fed ad libitum ( n = 2) or exposed to a 40% restriction ( n = 4) remained normothermic; but 80% food restricted females ( n = 5) gave priority to energy saving, increasing the frequency and depth of torpor bouts. The use of torpor was insufficient to compensate for 80% energetic shortage during lactation resulting in loss of mass from the mother and delayed growth in the pups. This study provides the first evidence that a heterothermic primate can use torpor to compensate for food shortages even during reproduction. This physiological flexibility likely evolved as a response to climate-driven fluctuations in food availability in Madagascar.
Schwensow, Nina; Eberle, Manfred; Sommer, Simone
The mechanisms and temporal aspects of mate choice according to genetic constitution are still puzzling. Recent studies indicate that fitness is positively related to diversity in immune genes (MHC). Both sexes should therefore choose mates of high genetic quality and/or compatibility. However, studies addressing the role of MHC diversity in pre- and post-copulatory mate choice decisions in wild-living animals are few. We investigated the impact of MHC constitution and of neutral microsatellite variability on pre- and post-copulatory mate choice in both sexes in a wild population of a promiscuous primate, the grey mouse lemur (Microcebus murinus). There was no support for pre-copulatory male or female mate choice, but our data indicate post-copulatory mate choice that is associated with genetic constitution. Fathers had a higher number of MHC supertypes different from those of the mother than randomly assigned males. Fathers also had a higher amino acid distance to the females' MHC as well as a higher total number of MHC supertypes and a higher degree of microsatellite heterozygosity than randomly assigned males. Female cryptic choice may be the underlying mechanism that operates towards an optimization of the genetic constitution of offspring. This is the first study that provides support for the importance of the MHC constitution in post-copulatory mate choice in non-human primates.
Yoder, Anne D.; Chan, Lauren M.; dos Reis, Mario; Larsen, Peter A.; Campbell, C. Ryan; Rasoloarison, Rodin; Barrett, Meredith; Roos, Christian; Kappeler, Peter; Bielawski, Joseph; Yang, Ziheng
Vomeronasal receptor genes have frequently been invoked as integral to the establishment and maintenance of species boundaries among mammals due to the elaborate one-to-one correspondence between semiochemical signals and neuronal sensory inputs. Here, we report the most extensive sample of vomeronasal receptor class 1 (V1R) sequences ever generated for a diverse yet phylogenetically coherent group of mammals, the tooth-combed primates (suborder Strepsirrhini). Phylogenetic analysis confirms our intensive sampling from a single V1R subfamily, apparently unique to the strepsirrhine primates. We designate this subfamily as V1Rstrep. The subfamily retains extensive repertoires of gene copies that descend from an ancestral gene duplication that appears to have occurred prior to the diversification of all lemuriform primates excluding the basal genus Daubentonia (the aye-aye). We refer to the descendent clades as V1Rstrep-α and V1Rstrep-β. Comparison of the two clades reveals different amino acid compositions corresponding to the predicted ligand-binding site and thus potentially to altered functional profiles between the two. In agreement with previous studies of the mouse lemur (genus, Microcebus), the majority of V1Rstrep gene copies appear to be intact and under strong positive selection, particularly within transmembrane regions. Finally, despite the surprisingly high number of gene copies identified in this study, it is nonetheless probable that V1R diversity remains underestimated in these nonmodel primates and that complete characterization will be limited until high-coverage assembled genomes are available. PMID:24398377
Canale, Cindy I; Perret, Martine; Henry, Pierre-Yves
Torpor is an energy-saving mechanism that allows endotherms to overcome energetic challenges. Torpor should be avoided during reproduction because of potential incompatibility with offspring growth. To test if torpor can be used during gestation and lactation to compensate for food shortage, we exposed reproductive female grey mouse lemurs (Microcebus murinus), a heterothermic primate, to different levels of food availability. Torpor use was characterised by daily skin temperature profiles, and its energetic outcome was assessed from changes in body mass. Food shortage triggered torpor during the end of the gestation period (n = 1), ranging from shallow in response to 40% food restriction to deep daily torpor in response to 80% restriction. During the early period of lactation, females fed ad libitum (n = 2) or exposed to a 40% restriction (n = 4) remained normothermic; but 80% food restricted females (n = 5) gave priority to energy saving, increasing the frequency and depth of torpor bouts. The use of torpor was insufficient to compensate for 80% energetic shortage during lactation resulting in loss of mass from the mother and delayed growth in the pups. This study provides the first evidence that a heterothermic primate can use torpor to compensate for food shortages even during reproduction. This physiological flexibility likely evolved as a response to climate-driven fluctuations in food availability in Madagascar.
Hämäläinen, Anni; Dammhahn, Melanie; Aujard, Fabienne; Eberle, Manfred; Hardy, Isabelle; Kappeler, Peter M.; Perret, Martine; Schliehe-Diecks, Susanne; Kraus, Cornelia
Classic theories of ageing consider extrinsic mortality (EM) a major factor in shaping longevity and ageing, yet most studies of functional ageing focus on species with low EM. This bias may cause overestimation of the influence of senescent declines in performance over condition-dependent mortality on demographic processes across taxa. To simultaneously investigate the roles of functional senescence (FS) and intrinsic, extrinsic and condition-dependent mortality in a species with a high predation risk in nature, we compared age trajectories of body mass (BM) in wild and captive grey mouse lemurs (Microcebus murinus) using longitudinal data (853 individuals followed through adulthood). We found evidence of non-random mortality in both settings. In captivity, the oldest animals showed senescence in their ability to regain lost BM, whereas no evidence of FS was found in the wild. Overall, captive animals lived longer, but a reversed sex bias in lifespan was observed between wild and captive populations. We suggest that even moderately condition-dependent EM may lead to negligible FS in the wild. While high EM may act to reduce the average lifespan, this evolutionary process may be counteracted by the increased fitness of the long-lived, high-quality individuals. PMID:25100693
Springer, Andrea; Kappeler, Peter M; Nunn, Charles L
Social networks provide an established tool to implement heterogeneous contact structures in epidemiological models. Dynamic temporal changes in contact structure and ranging behaviour of wildlife may impact disease dynamics. A consensus has yet to emerge, however, concerning the conditions in which network dynamics impact model outcomes, as compared to static approximations that average contact rates over longer time periods. Furthermore, as many pathogens can be transmitted both environmentally and via close contact, it is important to investigate the relative influence of both transmission routes in real-world populations. Here, we use empirically derived networks from a population of wild primates, Verreaux's sifakas (Propithecus verreauxi), and simulated networks to investigate pathogen spread in dynamic vs. static social networks. First, we constructed a susceptible-exposed-infected-recovered model of Cryptosporidium spread in wild Verreaux's sifakas. We incorporated social and environmental transmission routes and parameterized the model for two different climatic seasons. Second, we used simulated networks and greater variation in epidemiological parameters to investigate the conditions in which dynamic networks produce larger outbreak sizes than static networks. We found that average outbreak size of Cryptosporidium infections in sifakas was larger when the disease was introduced in the dry season than in the wet season, driven by an increase in home range overlap towards the end of the dry season. Regardless of season, dynamic networks always produced larger average outbreak sizes than static networks. Larger outbreaks in dynamic models based on simulated networks occurred especially when the probability of transmission and recovery were low. Variation in tie strength in the dynamic networks also had a major impact on outbreak size, while network modularity had a weaker influence than epidemiological parameters that determine transmission and recovery. Our study adds to emerging evidence that dynamic networks can change predictions of disease dynamics, especially if the disease shows low transmissibility and a long infectious period, and when environmental conditions lead to enhanced between-group contact after an infectious agent has been introduced. © 2016 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.
Mahajan, Neha; Barnes, Jennifer L.; Blanco, Marissa; Santos, Laurie R.
Both human infants and adult non-human primates share the capacity to track small numbers of objects across time and occlusion. The question now facing developmental and comparative psychologists is whether similar mechanisms give rise to this capacity across the two populations. Here, we explore whether non-human primates' object tracking…
This study presents a pilot survey of the avahis (pair-living, nocturnal prosimians) living in threatened littoral forest fragments of southeastern Madagascar. In the period of October-December 2004, I evaluated the density of adult and newborn avahis (carried by the mothers) by counting the individuals encountered during 58 night walks in seven fragments of Sainte Luce and Mandena forests, along one trail/fragment. Along each trail, I used random plots (5 m2) for a preliminary characterization of the vegetation. The density of the population was not correlated with fragment size and number of plant morphospecies, while it was correlated with large tree availability. Possibly due to a low energy diet based on leaves and to specialized and energetically expensive vertical leaping, the loss of large trees by selective logging seems to affect avahi populations more than other variables.
Mahajan, Neha; Barnes, Jennifer L.; Blanco, Marissa; Santos, Laurie R.
Both human infants and adult non-human primates share the capacity to track small numbers of objects across time and occlusion. The question now facing developmental and comparative psychologists is whether similar mechanisms give rise to this capacity across the two populations. Here, we explore whether non-human primates' object tracking…
Medlar, Alan; Aivelo, Tuomas; Löytynoja, Ari
Marker gene studies often use short amplicons spanning one or more hypervariable regions from an rRNA gene to interrogate the community structure of uncultured environmental samples. Target regions are chosen for their discriminatory power, but the limited phylogenetic signal of short high-throughput sequencing reads precludes accurate phylogenetic analysis. This is particularly unfortunate in the study of microscopic eukaryotes where horizontal gene flow is limited and the rRNA gene is expected to accurately reflect the species phylogeny. A promising alternative to full phylogenetic analysis is phylogenetic placement, where a reference phylogeny is inferred using the complete marker gene and iteratively extended with the short sequences from a metagenetic sample under study. Based on the phylogenetic placement approach we built Séance, a community analysis pipeline focused on the analysis of 18S marker gene data. Séance combines the alignment extension and phylogenetic placement capabilities of the Pagan multiple sequence alignment program with a suite of tools to preprocess, cluster and visualise datasets composed of many samples. We showcase Séance by analysing 454 data from a longitudinal study of intestinal parasite communities in wild rufous mouse lemurs (Microcebus rufus) as well as in simulation. We demonstrate both improved OTU picking at higher levels of sequence similarity for 454 data and show the accuracy of phylogenetic placement to be comparable to maximum likelihood methods for lower numbers of taxa. Séance is an open source community analysis pipeline that provides reference-based phylogenetic analysis for rRNA marker gene studies. Whilst in this article we focus on studying nematodes using the 18S marker gene, the concepts are generic and reference data for alternative marker genes can be easily created. Séance can be downloaded from http://wasabiapp.org/software/seance/ .
Toledano, A; Álvarez, M I; López-Rodríguez, A B; Toledano-Díaz, A; Fernández-Verdecia, C I
In the ageing process there are some species of non-human primates which can show some of the defining characteristics of the Alzheimer's disease (AD) of man, both in neuropathological changes and cognitive-behavioural symptoms. The study of these species is of prime importance to understand AD and develop therapies to combat this neurodegenerative disease. In this second part of the study, these AD features are discussed in the most important non-experimental AD models (Mouse Lemur -Microcebus murinus, Caribbean vervet -Chlorocebus aethiops, and the Rhesus and stump-tailed macaque -Macaca mulatta and M. arctoides) and experimental models (lesional, neurotoxic, pharmacological, immunological, etc.) non-human primates. In all these models cerebral amyloid neuropathology can occur in senility, although with different levels of incidence (100% in vervets;<30% in macaques). The differences between normal and pathological (Alzheimer's) senility in these species are difficult to establish due to the lack of cognitive-behavioural studies in the many groups analysed, as well as the controversy in the results of these studies when they were carried out. However, in some macaques, a correlation between a high degree of functional brain impairment and a large number of neuropathological changes ("possible AD") has been found. In some non-human primates, such as the macaque, the existence of a possible continuum between "normal" ageing process, "normal" ageing with no deep neuropathological and cognitive-behavioural changes, and "pathological ageing" (or "Alzheimer type ageing"), may be considered. In other cases, such as the Caribbean vervet, neuropathological changes are constant and quite marked, but its impact on cognition and behaviour does not seem to be very important. This does assume the possible existence in the human senile physiological regression of a stable phase without dementia even if neuropathological changes appeared. Copyright © 2011 Sociedad Española de
Springer, Andrea; Fichtel, Claudia; Calvignac-Spencer, Sébastien; Leendertz, Fabian H.; Kappeler, Peter M.
Hemoparasites can cause serious morbidity in humans and animals and often involve wildlife reservoirs. Understanding patterns of hemoparasite infections in natural populations can therefore inform about emerging disease risks, especially in the light of climate change and human disruption of natural ecosystems. We investigated the effects of host age, sex, host group size and season on infection patterns of Plasmodium sp., Babesia sp. and filarial nematodes in a population of wild Malagasy primates, Verreaux's sifakas (Propithecus verreauxi), as well as the effects of these infections on hematological variables. We tested 45 blood samples from 36 individuals and identified two species of Plasmodium, one species of Babesia and two species of filarial nematodes. Plasmodium spp. and Babesia sp. infections showed opposite patterns of age-dependency, with babesiosis being prevalent among young animals, while older animals were infected with Plasmodium sp. In addition, Babesia sp. infection was a statistically significant negative predictor of Plasmodium sp. infection. These results suggest that Plasmodium and Babesia parasites may interact within the host, either through cross-immunity or via resource competition, so that Plasmodium infections can only establish after babesiosis has resolved. We found no effects of host sex, host group size and season on hemoparasite infections. Infections showed high prevalences and did not influence hematological variables. This preliminary evidence supports the impression that the hosts and parasites considered in this study appear to be well-adapted to each other, resulting in persistent infections with low pathogenic and probably low zoonotic potential. Our results illustrate the crucial role of biodiversity in host-parasite relationships, specifically how within-host pathogen diversity may regulate the abundance of parasites. PMID:26767166
To observe morphology of Auchenacantha galeopteri (A. galeopteri), Auchenacantha spinosa (A. spinosa) and Auchenacantha parva (A. parva) from Sukabumi and Ujung Kulon, Indonesia using scanning electron microscopy (SEM). Specimens for light microscopy examination were fixed with warm 70% alcohol, cleared and mounted in lactophenol for wet mounting. Drawings were made with the aid of a drawing tube attached to a Nikon compound microscope. Specimens for SEM examination were processed according to Bozzola. Measurements were given in micrometers (µm) as the average of findings, followed by the range in parentheses, unless otherwise stated. The measurements of Auchenacantha spp are same with those of previously described. The striations of male and female A. galeopteri are widen towards outside and wavy. The mouth of female with 6 lips, each of them is wider at base than distal end in A. galeopteri and rectangular in A. spinosa. Both species have dentiform protrusion from inner surface of lips, such structure absent in A. parva, but the lips with transverse festoon like pattern at anterior end of each lip. Using SEM, the lip and the striation pattern of three species of Auchenacantha can be clearly distinguished. Sukabumi and Ujung Kulon are new locality of A. galeopteri and A. spinosa, and A. parva is the new record in Indonesia.
The activity budgets and daily activity rhythms of Varecia rubra were examined over an annual cycle according to season and reproductive stage. Given the relatively high reproductive costs and patchy food resources of this species, I predicted that V. rubra would 1) travel less and feed more during seasonal resource scarcity in an attempt to maintain energy balance, and 2) show sex differences in activity budgets due to differing reproductive investment. Contrary to the first prediction, V. rubra does not increase feeding time during seasonal food scarcity; rather, females feed for a consistent amount of time in every season, whereas males feed most during the resource-rich, hot dry season. The results are consistent with other predictions: V. rubra travels less in the resource-scarce cold rainy season, and there are some pronounced sex differences, with females feeding more and resting less than males in every season and in every reproductive stage except gestation. However, there are also some provocative similarities between the sexes when activity budgets are examined by reproductive stage. During gestation, female and male activity budgets do not differ and appear geared toward energy accumulation: both sexes feed and rest extensively and travel least during this stage. During lactation, activity budgets are geared toward high energy expenditure: both sexes travel most and in equal measure, and rest least, although it remains the case that females feed more and rest less than males. These similarities between female and male activity budgets appear related to cooperative infant care. The high energetic costs of reproduction in V. rubra females may require that they allot more time to feeding year round, and that their overall activity budget be more directly responsive to seasonal climate change, seasonal food distribution, and reproductive schedules.
Calvey, Tanya; Patzke, Nina; Kaswera-Kyamakya, Consolate; Gilissen, Emmanuel; Bertelsen, Mads F; Pettigrew, John D; Manger, Paul R
The nuclear organization of the cholinergic, catecholaminergic, serotonergic and orexinergic systems in the brains of three species of strepsirrhine primates is presented. We aimed to investigate the nuclear complement of these neural systems in comparison to those of simian primates, megachiropterans and other mammalian species. The brains were coronally sectioned and immunohistochemically stained with antibodies against choline acetyltransferase, tyrosine hydroxylase, serotonin and orexin-A. The nuclei identified were identical among the strepsirrhine species investigated and identical to previous reports in simian primates. Moreover, a general similarity to other mammals was found, but specific differences in the nuclear complement highlighted potential phylogenetic interrelationships. The central feature of interest was the structure of the locus coeruleus complex in the primates, where a central compactly packed core (A6c) of tyrosine hydroxylase immunopositive neurons was surrounded by a shell of less densely packed (A6d) tyrosine hydroxylase immunopositive neurons. This combination of compact and diffuse divisions of the locus coeruleus complex is only found in primates and megachiropterans of all the mammalian species studied to date. This neural character, along with variances in a range of other neural characters, supports the phylogenetic grouping of primates with megachiropterans as a sister group.
Okon, Avi; Kennedy, Brett; Garrett, Michael; Magnone, Lee
The figure shows the LEMUR IIb, which is a modified version of the LEMUR II the second generation of the Limbed Excursion Mechanical Utility Robot (LEMUR). Except as described below, the LEMUR IIb hardware is mostly the same as that of the LEMUR II. The IIb and II versions differ in their kinematic configurations and characteristics associated with their kinematic configurations. The differences are such that relative to the LEMUR II, the LEMUR IIb is simpler and is better suited to climbing on inclined surfaces. The first-generation LEMUR, now denoted the LEMUR I, was described in Six-Legged Experimental Robot (NPO-20897), NASA Tech Briefs, Vol. 25, No. 12 (December 2001), page 58. The LEMUR II was described in Second-Generation Six-Limbed Experimental Robot (NPO-35140) NASA Tech Briefs, Vol. 28, No. 11 (November 2004), page 55. To recapitulate: the LEMUR I and LEMUR II were six-legged or sixlimbed robots for demonstrating robotic capabilities for assembly, maintenance, and inspection. They were designed to be capable of walking autonomously along a truss structure toward a mechanical assembly at a prescribed location. They were equipped with stereoscopic video cameras and image-data-processing circuitry for navigation and mechanical operations. They were also equipped with wireless modems, through which they could be commanded remotely. Upon arrival at a mechanical assembly, the LEMUR I would perform simple mechanical operations by use of one or both of its front legs (or in the case of the LEMUR II, any of its limbs could be used to perform mechanical operations). Either LEMUR could also transmit images to a host computer. The differences between the LEMUR IIb and the LEMUR II are the following: Whereas the LEMUR II had six limbs, the LEMUR IIb has four limbs. This change has reduced both the complexity and mass of the legs and of the overall robot. Whereas each limb of the LEMUR II had four degrees of freedom (DOFs), each limb of the LEMUR IIb has three DOFs
... (Nanger dama) Ring-tailed lemur (Lemur catta) Panamanian golden frog (Atelopus zeteki) Applicant: Santa... activities conducted by the applicant over a 5-year period. Applicant: Britt Rice, College Station, TX; PRT...
...-horned gazelle (Gazella leptoceros) Indian rhinoceros (Rhinoceros unicornis) Eld's deer (Cervus eldii... and white ruffed lemur (Varecia variegata) Red ruffed lemur (Varecia rubra) Cottontop tamarin... nasomaculatus) Red lechwe (Kobus leche) Applicant: Larry Johnson, Boerne, TX; PRT-89186A The applicant...
queries, is IDF(t) = log „ # docs. in corpus + 1 0.5 + # docs. t appears in « . (6) This rather ad hoc scoring formula is implemented in the Lemur ...problems with passage R-precision as an evaluation metric. Fernando was instrumental in extending the Lemur toolkit to make all of these experiments...and C. Zhai. The lemur toolkit for language modeling and information retrieval. http://www.cs.cmu.edu/∼ lemur /, 2003.  C. Buckley and E. M
... Wild Mammals and Birds to the United States Specifications for Sloths, Bats, and Flying Lemurs... located on the upper one-half of the primary enclosure. (b) No more than one sloth, bat, or flying lemur..., bats, or flying lemurs shall be large enough to ensure that each animal has sufficient space to move...
... Wild Mammals and Birds to the United States Specifications for Sloths, Bats, and Flying Lemurs... located on the upper one-half of the primary enclosure. (b) No more than one sloth, bat, or flying lemur..., bats, or flying lemurs shall be large enough to ensure that each animal has sufficient space to move...
... Wild Mammals and Birds to the United States Specifications for Sloths, Bats, and Flying Lemurs... located on the upper one-half of the primary enclosure. (b) No more than one sloth, bat, or flying lemur..., bats, or flying lemurs shall be large enough to ensure that each animal has sufficient space to move...
... Wild Mammals and Birds to the United States Specifications for Sloths, Bats, and Flying Lemurs... located on the upper one-half of the primary enclosure. (b) No more than one sloth, bat, or flying lemur..., bats, or flying lemurs shall be large enough to ensure that each animal has sufficient space to...
Lemur Project developers to index ClueWeb09. We built 30 separate indexes across 10 machines. Each machine was a modern (2-2.3 GHz CPU) 4 core machine... Lemur . Lemur Toolkit for Language Modeling and IR, 2003. http://www.lemurproject.org/.  D. Metzler and W. B. Croft. A markov random field model for
2004. Indri was originally meant to be a small modification to the Lemur Project code. There were enough scalability is- sues with the original Lemur ...code that we built almost an entirely new system. The Indri system is now distributed as a component of the new, larger Lemur toolkit1. It is open
Ramanankirahina, Rindrahatsarana; Joly, Marine; Scheumann, Marina; Zimmermann, Elke
How social groups govern their distribution in time and space is a central question in socioecology. The aim of this study is to explore the role of acoustic signaling for spacing and cohesiveness in a nocturnal, cohesive, pair-living strepsirrhine. The study was conducted in northwestern Madagascar. Six pairs of Avahi occidentalis were radio-collared and home range usage, vocalizations and call-associated behavior recorded using GPS-based focal animal sampling. Home range size was analyzed using ArcView GIS 3.3. Calls were characterized by a multiparametric sound analysis. Three frequently used, acoustically distinct call types were identified: the avahee call, the whistle call, and the growling call, the latter is a soft; the two others are loud calls. Call types are given by both sexes and convey individually-specific signatures. Call types are used primarily in the locomotion context in the non-core-area of home ranges. The least common avahee call is responded by the avahee call from farther away. The more common whistle call, given when partners become visually isolated, and the growling call emitted at close distances, were answered by the whistle and the growling call. Results suggest a spacing function for the avahee call and group coordination functions for the other call types. Our study provides first empirical evidence for a nocturnal, cohesive pair-living strepsirrhine that vocal signaling represents an important mechanism for spacing, group coordination and decision making. Findings contribute to a better understanding of the evolutionary roots of primate vocal communication. © 2015 Wiley Periodicals, Inc.
Clausing, J.A.; Hagstrom, R.T.; Lusk, E.L.; Overbeek, R.A.
A set of macro libraries has been developed that allows programmers to write portable Pascal code for multiprocessors. This document presents, in tutorial form, the macros used to implement three common synchronization patterns: self-scheduling FOR-loops, barrier synchronization, and the askfor monitor.
sentences are likely to be relevant. These top relevant sentences are re-indexed using Lemur .1 No stopping or stemming is used at this stage. Our two...collection language model and a sentence language model in Lemur : collLM(i) (the collection language model for sentence i) is a maximum likelihood model...of these sentences does quite well, because about 80% of them are novel. 1 Lemur is a
model. For the experiment, we used batch query service offered by lemur project website . Clue- Web12-Full dataset is our test corpus. Waterloo spam...Prior score SDM : Sequential dependence model Regarding SNUMedinfo13, we used Pagerank Prior  scores offered by lemur project website. 3...information retrieval. 2005, ACM: Salvador, Brazil. p. 472-479. 2. The Lemur Project. [cited 2014 Oct 28]; Available from: http
expansion. 3.1.3 Pseudo-relevance Feedback Based Retrieval Lemur  was used to carry the pseudo-relevance feedback based retrieval. There are seven...retrieval models in Lemur and Indri model was finally selected to retrieval. 3.2 OPINIONATIVE DOCUMENT RANKING The topic relevant documents have...dalianu.blog.final.pdf Wikipedia, http://en.wikipedia.org/wiki/Wikipedia The lemur Toolkit: http://www.lemurproject.org/  http
experimental variable was the algorithm for suggesting related articles. We considered two: • Using language modeling retrieval, implemented with Lemur [16...similarity algorithm in PubMed, accessed through the PubMed eUtils API.5 Quite explicitly, our goal was not to compare Lemur with PubMed, but rather to...for the simulation (utility). The top graph shows the greedy browsing strategy and the bottom graph the breadth-like browsing strategy, both with Lemur
finding. In the topic retrieval task, we applied Lemur IR toolkit and used various techniques for query expansion. In the opinion finding and...context, and extract content from the blog web pages. Second, we apply the Lemur Information Retrieval toolkit to retrieve 1000 relevant documents...process, we built index using the Lemur Information Retrieval Toolkit1 based on the preprocessed corpus. For each of the topic queries, the retrieval
containing ClueWeb09 collection using Lemur Toolkit 4.10. We used no stemming and stop-word removal on the collection level. However, we applied a very...approach implemented in Lemur with Dirichlet smoothing (µ = 1500). In order to have some flexibility in development and also for the sake of better...consider them as the only entities allowed (actu- ally, using #scoreif directive of the Lemur query language). Since we still could not be sure that all
constructing retrieval model and allocating homepages for entities. We also used some external resources, such as Stanford NER Tool, Indri1 & Lemur ...obtained less than 1,000 documents. This information was stored for the latter needs. In order to indexing by Indri or Lemur , we parsed the...priority to entities extracted manually PRIS3 Entity-Centered Model by Indri PRIS4 Entity-Centered Model by Lemur (BM25) Because the evaluation
contains about 50 million English pages for the entity track, was used. For indexing, the Lemur tool kit in Red Hat Enterprise Linux platform and for...the entity related finding Base Run with Simple Query For indexing the Clueweb09 the Lemur Tool Kit version 10 was installed, since the...ClueWeb09 collection, which was indexed using the Lemur were also retrieved. In addition, the queries were defined according to the output required
... cultures from various primate species including, bonobos (Pan paniscus), chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), orangutans (Pongo spp.), gibbons (Hylobatidae), lemurs (Lemuridae), spider...
... Wild Mammals and Birds to the United States Specifications for Sloths, Bats, and Flying Lemurs... located on the upper one-half of the primary enclosure. (b) No more than one sloth, bat, or flying lemur... together may be shipped in the same primary enclosure. (c) A primary enclosure used to transport...
relevance modeling (method 2)  as implemented in Lemur .1 This relevance model was built using the top 75 terms from the top 50 documents. Ciirtbas uses...forms, namely cluster-by-size CF, cluster-by- distribution CF, and passage CF. 1http://www-2.cs.cmu.edu/ lemur / 2 Figure 1: A snapshot of the top-term
UMLS Metathesaurus. Queries and documents are now represented as a list of SNOMED CT concept ids. 3. Documents are indexed using the Indri Lemur ...Informatics 40, 3 (2007), 288–299.  Zhai, C. Notes on the Lemur TDIDF model. Tech. rep., School of Computer Science, Carnegie Mellon University
Rahm, Nadia; Yap, Melvyn; Snoeck, Joke; Zoete, Vincent; Muñoz, Miguel; Radespiel, Ute; Zimmermann, Elke; Michielin, Olivier; Stoye, Jonathan P.; Ciuffi, Angela; Telenti, Amalio
Lentiviruses, the genus of retrovirus that includes HIV-1, rarely endogenize. Some lemurs uniquely possess an endogenous lentivirus called PSIV (“prosimian immunodeficiency virus”). Thus, lemurs provide the opportunity to study the activity of host defense factors, such as TRIM5α, in the setting of germ line invasion. We characterized the activities of TRIM5α proteins from two distant lemurs against exogenous retroviruses and a chimeric PSIV. TRIM5α from gray mouse lemur, which carries PSIV in its genome, exhibited the narrowest restriction activity. One allelic variant of gray mouse lemur TRIM5α restricted only N-tropic murine leukemia virus (N-MLV), while a second variant restricted N-MLV and, uniquely, B-tropic MLV (B-MLV); both variants poorly blocked PSIV. In contrast, TRIM5α from ring-tailed lemur, which does not contain PSIV in its genome, revealed one of the broadest antiviral activities reported to date against lentiviruses, including PSIV. Investigation into the antiviral specificity of ring-tailed lemur TRIM5α demonstrated a major contribution of a 32-amino-acid expansion in variable region 2 (v2) of the B30.2/SPRY domain to the breadth of restriction. Data on lemur TRIM5α and the prediction of ancestral simian sequences hint at an evolutionary scenario where antiretroviral specificity is prominently defined by the lineage-specific expansion of the variable loops of B30.2/SPRY. PMID:21345948
ranking. (Wang et al., 2009) UALR CB We used Lemur tool kit version 4.10 to index the WARC format documents which were given on Red Hat Enterprise Linux...Technology employs Lemur toolkit to index and retrieve dataset stemmed by Krovetz stemmer and stopped using a standard list of 421 common terms; devised
Methodology We indexed the GOV2 collection and the ClueWeb09 (category B) collection using the Indri Search Engine from the Lemur Toolkit . The...predictions. References  The lemur toolkit. http://www.lemurproject.org.  Letor 4.0. http://research.microsoft.com/en-us/um/beijing/projects/letor/. [3
We used several standard Lemur built in systems (tfidf bm25, tfidf log, kl abs, kl dir, inquery, cos, okapi) and combined their output (metasearch...the Lemur implementations: a vector-space cosine similarity run (000cos), a language modeling run (000klabs), an Okapi formula run (000okapi), a BM25
this strategy. • In LiaIIcAuto run, a small set of documents was extracted and concatenated using Lemur and the query title field. • In LiaIcAuto run...address oc- curring in the corpus. These summaries were indexed using Lemur and addresses were ranked based on indri #combine operator applied to titles
Technology, China Used Lemur . IBM Haifa This year, the experiments of IBM Haifa were focused on the scoring function of Lucene, an Apache open-source...several standard Lemur built in systems (tfidf bm25, tfidf log, kl abs,kl dir,inquery,cos, okapi) and combined their output (metasearch) using the
Lehman, Shawn M
The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis
Backues, K A; Hill, M; Palmenberg, A C; Miller, C; Soike, K F; Aguilar, R
Encephalomyocarditis virus (EMCV), has caused the deaths of many species of animals in zoological parks and research institutions. The Audubon Park Zoo, (New Orleans, Louisiana, USA) attempted vaccination of several species with a killed EMCV vaccine with mixed results. This paper reports an attempt at vaccination against EMCV using a genetically engineered, live attenuated Mengo virus (vMC0) at the Audubon Park Zoo and Miami Metro Zoo, (Miami, Florida, USA) from December 1996 to June 1997. Several species of animals were vaccinated with vMC0, which is serologically indistinguishable from the field strain of EMCV. Serum samples were taken at the time of vaccination and again 21 days later, then submitted for serum neutralization titers against EMCV. The vaccinate species included red capped mangebey (Cercocebus torquatus), colobus (Colobus guereza), angolan colobus (Colobus angolensis), ruffed lemur (Lemur variegatus ruber and Lemur variegatus variegatus), back lemur (Lemur macaco), ring-tailed lemur (Lemur catta), siamang (Hylobates syndactylus), diana guenon (Cercopithicus diana), spider monkey (Ateles geoffroyi), common marmoset (Callithrix jacchus), talapoin monkey (Cercopithecus talapoin), Brazilian tapir (Tapirus terrestris), Baird's tapir (Tapirus bairdii), Malayan tapir (Tapirus indicus), dromedary camel (Camelus dromedarius), bactrian camel (Camelus bactrianus), gerenuk (Litocranius walleri), guanaco (Lama glama guanicoe), black duiker (Cephalophus niger), Vietnamese potbellied pig (Sus scrofa), babirusa (Babyrousa babyrussa), collard peccary (Tayass tajacu), and African crested porcupine (Hystrix africaeaustralis). The vaccine response was variable, with high virus neutralizing antibody titer responses in some primate species and mixed to poor responses for other species. No ill effects were seen with vaccination.
provided by the Lemur package  to generate the initial retrieval list. Stop word removal is not used. The porter stemmer  is used. The setting of...using the initial retrieval list generated by Lemur and re-ranked by our model 1 for feedback sets B-E. Set P@10 P@30 MAP R-precision A .3977...SIGIR ‘05, pp. 472-479. 7. Ogilvie, P. and Callan, J. (2002.) Experiments using the Lemur toolkit. In Proceedings of the 2001 Text REtrieval
Blanco, Marina B; Dausmann, Kathrin H; Ranaivoarisoa, Jean F; Yoder, Anne D
Hibernation in mammals is a remarkable state of heterothermy wherein metabolic rates are reduced, core body temperatures reach ambient levels, and key physiological functions are suspended. Typically, hibernation is observed in cold-adapted mammals, though it has also been documented in tropical species and even primates, such as the dwarf lemurs of Madagascar. Western fat-tailed dwarf lemurs are known to hibernate for seven months per year inside tree holes. Here, we report for the first time the observation that eastern dwarf lemurs also hibernate, though in self-made underground hibernacula. Hence, we show evidence that a clawless primate is able to bury itself below ground. Our findings that dwarf lemurs can hibernate underground in tropical forests draw unforeseen parallels to mammalian temperate hibernation. We expect that this work will illuminate fundamental information about the influence of temperature, resource limitation and use of insulated hibernacula on the evolution of hibernation.
... samples from captive-bred non-human primates from the following species: lowland gorilla (Gorilla gorilla gorilla), white- cheeked gibbon (Hylobates leucogenys), Siamang (Hylobates syndactylus), ring-tailed lemur...
... barasingha (Rucervus duvaucelii), Eld's deer (Rucervus eldii), scimitar-horned oryx (Oryx dammah), Arabian oryx (Oryx leucoryx), addax (Addax nasomaculatus), dama gazelle (Nanger dama), and red lechwe (Kobus... variegata) Red ruffed lemur (Varecia rubra) Mandrill (Mandrillus sphinx) Japanese macaque (Macaca...
part of the Lemur toolkit. Galago supports indexing of large scale data in a distributed cluster environment with a MapReduce -like framework called...english wikipedia concepts. In Con- ference on Language Resources and Evaluation.
Blanco, Marina B.; Dausmann, Kathrin H.; Ranaivoarisoa, Jean F.; Yoder, Anne D.
Hibernation in mammals is a remarkable state of heterothermy wherein metabolic rates are reduced, core body temperatures reach ambient levels, and key physiological functions are suspended. Typically, hibernation is observed in cold-adapted mammals, though it has also been documented in tropical species and even primates, such as the dwarf lemurs of Madagascar. Western fat-tailed dwarf lemurs are known to hibernate for seven months per year inside tree holes. Here, we report for the first time the observation that eastern dwarf lemurs also hibernate, though in self-made underground hibernacula. Hence, we show evidence that a clawless primate is able to bury itself below ground. Our findings that dwarf lemurs can hibernate underground in tropical forests draw unforeseen parallels to mammalian temperate hibernation. We expect that this work will illuminate fundamental information about the influence of temperature, resource limitation and use of insulated hibernacula on the evolution of hibernation. PMID:23636180
1− β)αf + βαd where if αd < αf , β = 1; otherwise β = 0. 5. EXPERIMENT RESULTS 5.1 Data Preprocessing We employ the Lemur toolkit (version 4.5) and... Lemur toolkit, we adopt the KL-Divergence retrieval model with mixture model feedback to do relevance feed- back experiments (related parameters are
Crowley, B. E.; Godfrey, L. R.; Guilderson, T. P.; Zermeno, P.; Koch, P. L.; Dominy, N. J.
The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced community-wide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.
Kennedy, Brett; Okon, Avi; Aghazarian, Hrand; Robinson, Matthew; Garrett, Michael; Magnone, Lee
The figure shows the LEMUR II - the second generation of the Limbed Excursion Mechanical Utility Robot (LEMUR), which was described in "Six-Legged Experimental Robot" (NPO-20897), NASA Tech Briefs, Vol. 25, No. 12 (December 2001), page 58. The LEMUR II incorporates a number of improvements, including new features, that extend its capabilities beyond those of its predecessor, which is now denoted the LEMUR I. To recapitulate: the LEMUR I was a six-limbed robot for demonstrating robotic capabilities for assembly, maintenance, and inspection. The LEMUR I was designed to be capable of walking autonomously along a truss structure toward a mechanical assembly at a prescribed location and to perform other operations. The LEMUR I was equipped with stereoscopic video cameras and image-data-processing circuitry for navigation and mechanical operations. It was also equipped with a wireless modem, through which it could be commanded remotely. Upon arrival at a mechanical assembly, the LEMUR I would perform simple mechanical operations with one or both of its front limbs. It could also transmit images to a host computer. Each of the six limbs of the LEMUR I was operated independently. Each of the four rear limbs had three degrees of freedom (DOFs), while each of the front two limbs had four DOFs. The front two limbs were designed to hold, operate, and/or be integrated with tools. The LEMUR I included an onboard computer equipped with an assortment of digital control circuits, digital input/output circuits, analog-to-digital converters for input, and digital-to-analog (D/A) converters for output. Feedback from optical encoders in the limb actuators was utilized for closed-loop microcomputer control of the positions and velocities of the actuators. The LEMUR II incorporates the following improvements over the LEMUR I: a) The drive trains for the joints of the LEMUR II are more sophisticated, providing greater torque and accuracy. b) The six limbs are arranged symmetrically about
A fatal Encephalomyocarditis virus (EMCV) infection epidemic involving fifteen primates occurred between October 2006 and February 2007 at the Natura Viva Zoo. This large open-field zoo park located near Lake Garda in Northern Italy hosts one thousand animals belonging to one hundred and fifty different species, including various lemur species. This lemur collection is the most relevant and rich in Italy. A second outbreak between September and November 2008 involved three lemurs. In all cases, the clinical signs were sudden deaths generally without any evident symptoms or only with mild unspecific clinical signs. Gross pathologic changes were characterized by myocarditis (diffuse or focal pallor of the myocardium), pulmonary congestion, emphysema, oedema and thoracic fluid. The EMCV was isolated and recognized as the causative agent of both outbreaks. The first outbreak in particular was associated with a rodent plague, confirming that rats are an important risk factor for the occurrence of the EMCV infection. PMID:20298561
Maas, M C
This study describes the molar enamel microstructure of seven lemurid primates: Hapalemur griseus, Varecia variegata, Lemur catta, Lemur macaco, Lemur fulvus rufus, Lemur fulvus fulvus, and Lemur fulvus albifrons. Contrary to earlier accounts, which reported little or no prism decussation in lemurid enamel, both Lemur and Varecia molars contain a prominent inner layer of decussating prisms (Hunter-Schreger bands), in addition to an outer radial prism layer, and a thin, nonprismatic enamel surface layer. In contrast, Hapalemur enamel consists entirely of radial and, near the surface, nonprismatic enamel. In addition, for all species, prism packing patterns differ according to depth from the tooth surface, and for all species but Varecia (which also has the thinnest enamel of any lemurid), average prism area increases from the enamel-dentine junction to the surface; this may be a developmental solution to the problem of accommodating a larger outer surface area with enamel deposited from a fixed number of cells. Finally, contradicting some previous reports, Pattern 1 prisms predominate only in the most superficial prismatic enamel. In the deeper enamel, prism cross-sections include both closed (Pattern 1) and arc-shaped (Pattern 2 or, most commonly, Pattern 3). This sequence of depth-related pattern change is repeated in all taxa. It should also be emphasized that all taxa can exhibit all three prism patterns in their mature enamel. The high degree of quantitative and qualitative variation in prism size, shape, and packing suggests that these features should be used cautiously in phylogenetic studies. Hapalemur is distinguished from the other lemurids by unique, medially constricted or rectangular prism cross-sections at an intermediate depth and the absence of prism decussation, but, without further assessment of character polarity, these differences do not clarify lemurid phylogenetic relations. Some characters of enamel microstructure may represent synapomorphies
Donati, Giuseppe; Borgognini-Tarli, Silvana M
The role environmental factors play in influencing circadian rhythms in natural habitats is still poorly described in primates, especially for those taxa with an activity cycle extended over the 24-hour cycle. In this paper, we elucidate the importance of abiotic factors in entraining the activity of cathemeral primates, focussing on results from a long-term study of Eulemur fulvus collaris (collared brown lemur) in south-eastern Malagasy littoral forest. Two groups of lemurs were followed for 60 whole-day and 59 whole-night observation periods over 14 months. Diurnal and nocturnal observations were equally distributed among moon phases and seasons. Temperature and humidity were recorded hourly by automatic data loggers. The littoral forest has a climatic environment where rainfall and humidity are uncorrelated with temperature and photoperiod. Diurnal and nocturnal activity varied seasonally, with the former increasing significantly with extended day length and the latter increasing significantly with shortened day length. Dusk seemed to act as a primary zeitgeber for these lemurs, coordinating the onset of evening activity throughout the entire year. Lunar phase and the nocturnal luminosity index correlated positively with the duration of nocturnal activity and negatively with the length of diurnal activity. Temperature was positively associated with diurnal activity but did not seem to influence lemur rhythms at night. Finally, lemur nocturnal activity significantly decreased when levels of humidity and rainfall were high. Cathemeral biorhythm is triggered by zeitgebers and influenced by masking factors. The activity of collared brown lemurs appears to be seasonally influenced by photoperiod and directly modulated by nocturnal ambient luminosity. These results are discussed by comparing data from other cathemeral species living in various climatic situations.
McKenney, Erin A.; Rodrigo, Allen; Yoder, Anne D.
Host fitness is impacted by trillions of bacteria in the gastrointestinal tract that facilitate development and are inextricably tied to life history. During development, microbial colonization primes the gut metabolism and physiology, thereby setting the stage for adult nutrition and health. However, the ecological rules governing microbial succession are poorly understood. In this study, we examined the relationship between host lineage, captive diet, and life stage and gut microbiota characteristics in three primate species (infraorder, Lemuriformes). Fecal samples were collected from captive lemur mothers and their infants, from birth to weaning. Microbial DNA was extracted and the v4 region of 16S rDNA was sequenced on the Illumina platform using protocols from the Earth Microbiome Project. Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli. Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut. Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies. PMID:25970595
Federman, Sarah; Dornburg, Alex; Daly, Douglas C.; Downie, Alexander; Perry, George H.; Yoder, Anne D.; Sargis, Eric J.; Richard, Alison F.; Donoghue, Michael J.; Baden, Andrea L.
Madagascar’s lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar’s lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses. PMID:27071108
This book is written for children 5 through 10. Part of a series designed to develop their curiosity, fascinate them and educate them, this volume introduces the primate family, their physiology, and habits. Topics described include: (1) kinds of monkeys, including lemur, chimpanzee, gorilla, squirrel monkey, and marmoset; (2) behaviors when…
... 50 Wildlife and Fisheries 1 2014-10-01 2014-10-01 false Primary enclosures. 14.142 Section 14.142 Wildlife and Fisheries UNITED STATES FISH AND WILDLIFE SERVICE, DEPARTMENT OF THE INTERIOR TAKING... outside the enclosure. Specifications for Sloths, Bats, and Flying Lemurs (Cynocephalidae)...
... 50 Wildlife and Fisheries 1 2011-10-01 2011-10-01 false Primary enclosures. 14.142 Section 14.142 Wildlife and Fisheries UNITED STATES FISH AND WILDLIFE SERVICE, DEPARTMENT OF THE INTERIOR TAKING... outside the enclosure. Specifications for Sloths, Bats, and Flying Lemurs (Cynocephalidae)...
... 50 Wildlife and Fisheries 1 2012-10-01 2012-10-01 false Primary enclosures. 14.142 Section 14.142 Wildlife and Fisheries UNITED STATES FISH AND WILDLIFE SERVICE, DEPARTMENT OF THE INTERIOR TAKING... outside the enclosure. Specifications for Sloths, Bats, and Flying Lemurs (Cynocephalidae)...
... 50 Wildlife and Fisheries 1 2013-10-01 2013-10-01 false Primary enclosures. 14.142 Section 14.142 Wildlife and Fisheries UNITED STATES FISH AND WILDLIFE SERVICE, DEPARTMENT OF THE INTERIOR TAKING... outside the enclosure. Specifications for Sloths, Bats, and Flying Lemurs (Cynocephalidae)...
This book is written for children 5 through 10. Part of a series designed to develop their curiosity, fascinate them and educate them, this volume introduces the primate family, their physiology, and habits. Topics described include: (1) kinds of monkeys, including lemur, chimpanzee, gorilla, squirrel monkey, and marmoset; (2) behaviors when…
Federman, Sarah; Dornburg, Alex; Daly, Douglas C; Downie, Alexander; Perry, George H; Yoder, Anne D; Sargis, Eric J; Richard, Alison F; Donoghue, Michael J; Baden, Andrea L
Madagascar's lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar's lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.
Maclean, Evan L; Merritt, Dustin J; Brannon, Elizabeth M
Transitive Inference is a form of deductive reasoning that has been suggested as one cognitive mechanism by which animals could learn the many relationships within their group's dominance hierarchy. This process thus bears relevance to the social intelligence hypothesis which posits evolutionary links between various forms of social and nonsocial cognition. Recent evidence corroborates the link between social complexity and transitive inference and indicates that highly social animals may show superior transitive reasoning even in nonsocial contexts. We examined the relationship between social complexity and transitive inference in two species of prosimians, a group of primates that diverged from the common ancestor of monkeys, apes, and humans over 50 million years ago. In Experiment 1, highly social ring-tailed lemurs, Lemur catta, outperformed the less social mongoose lemurs, Eulemur mongoz, in tests of transitive inference and showed more robust representations of the underlying ordinal relationships between the stimuli. In Experiment 2, after training under a correction procedure that emphasized the underlying linear dimension of the series, both species showed similar transitive inference. This finding suggests that the two lemur species differ not in their fundamental ability to make transitive inferences, but rather in their predisposition to mentally organize information along a common underlying dimension. Together, these results support the hypothesis that social complexity is an important selective pressure for the evolution of cognitive abilities relevant to transitive reasoning.
Balestri, Michela; Barresi, Marta; Campera, Marco; Serra, Valentina; Ramanamanjato, Jean Baptiste; Heistermann, Michael; Donati, Giuseppe
The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species. PMID:25229944
Balestri, Michela; Barresi, Marta; Campera, Marco; Serra, Valentina; Ramanamanjato, Jean Baptiste; Heistermann, Michael; Donati, Giuseppe
The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.
Shepherd, Stephen V.; Platt, Michael L.
Behavioral and neurophysiological studies strongly suggest that visual orienting reflects the integration of sensory, motor, and motivational variables with behavioral goals. Relatively little is known, however, regarding the goals that govern visual orienting of animals in their natural environments. Field observations suggest that most nonhuman primates orient to features of their natural environments whose salience is dictated by the visual demands of foraging, locomotion and social interaction. This hypothesis is difficult to test quantitatively, however, in part because accurate gaze-tracking technology has not been employed in field studies. We here report the implementation of a new, telemetric, infrared-video gaze-tracker (ISCAN) to measure visual orienting in freely-moving, socially-housed prosimian primates (Lemur catta). Two male lemurs tolerated the system at approximately ¼ body weight, permitting successful measurements of gaze behavior during spontaneous locomotion through both terrestrial and arboreal landscapes, and in both social and asocial environments. PMID:16431130
Slodkowicz-Kowalska, Anna; Graczyk, Thaddeus K; Tamang, Leena; Girouard, Autumn S; Majewska, Anna C
Human microsporidiosis, a serious disease of immunocompetent and immunosuppressed people, can be due to zoonotic transmission of microsporidian spores. A survey utilizing chromotrope 2R stain and fluorescent in situ hybridization techniques for testing feces from 193 captive mammals demonstrated that 3 animals (1.6%) shed Encephalitozoon bieneusi spores. These include two critically endangered species (i.e., black lemurs, Eulemur macaco flavifrons; and Visayan warty pig, Sus cebifrons negrinus) and a threatened species (mongoose lemur, Eulemur mongoz). The concentration of spores varied from 2.7 x 10(5) to 5.7 x 10(5)/g of feces, and all infections were asymptomatic. The study demonstrates that E. bieneusi spores can originate from captive animals, which is of particular epidemiologic importance because the close containment of zoological gardens can facilitate pathogen spread to other animals and also to people such as zoo personnel and visitors.
Hostetler, J R; Cannon, M S; Belt, W D
Crystalloids of what appear to be smooth reticulum have been observed in the zona fasciculata and zona reticularis in both the stressed and nonstressed adrenal gland of the Siamese tree shrew (Tupaia glis). No crystalloids are observed in the zona glomerulosa. Similar crystalloids have been described in other steroid-secreting organs, including the antebrachial organ of the lemur (Lemur catta), the parotoid gland of Bufo alvarius and in sebaceous gland cells of the Galagos and Macaques. Moreover, the crystalloids in the present investigation resemble the paracrystalline arrays of smooth reticulum present in the adrenal cortex of the fetal guinea pig. The crystalloids show much variation in degree of organization, sometimes appearing as wavy tubules parallel with one another or as fused tubules having a "donut" configuration. In addition, the crystalloids are nearly identical to configurations which have been described in mitochondrial cristae of the protozoan, Pelomyxa carolinensis.
configurable suite of natural language processing ( NLP ) compo- nents, to compute a relevance score for each article and topic. We describe our ensemble...approach, the strategies and tools we use to create labeled data to support this approach, the components in our IR / NLP pipeline, and our results on...Indri/Lemur5 – and includes several text processing and natural lan- guage processing ( NLP ) modules, such as negation tagging, age grouping, and
Balko, E.A.; Underwood, H.B.
We present a summary of a long-term field study that examined the effects of forest disturbance on the availability of palatable fruit and its utilization by V. variegata. Forest structure and tree species composition were measured in three adjacent study areas, with different histories of disturbance, in Ranomafana National Park (RNP), Madagascar. V. variegata abundance was monitored by frequent encounters with resident groups and periodic censuses conducted along trails. Finally, the abundance of mature fruit in species used by V. variegata was scored monthly at representative trees at several locations. V. variegata abundance was most consistent in the least anthropogenically disturbed site, while no established lemur groups were observed in the heavily logged site for over a decade post-harvest. Lemur abundance was variable in the selectively logged site. The presence of select food trees, particularly specimens with voluminous crowns capable of producing abundant fruit crops, appears to be key to the establishment and expansion of V variegata groups. Our analysis of year-long fruit utilization revealed a high degree of preference for several species of trees. Two species exhibited mature fruit in a low percentage of stems but were available for a protracted period of time, while two additional species showed high intraspecific fruiting synchrony and were available for a shorter period of time. These contrasting phenologies, rather than the individual tree species, may be most important to V. variegata due to their coincident timing of fruit maturation with key lemur life-history events. Any disturbance-natural or anthropogenic-that disrupts the phenology cycles of food trees has the potential to impact lemur abundance and dispersion. Intense disturbances, such as heavy logging or severe cyclones, have long-lasting impacts on fruit production, while selective logging or moderate cyclonic windthrow cause more transient impacts. V. variegata is adapted to deal
Hamrick, M W
A comparative study of carpal joint structure and function in six Malagasy lemuriforms was undertaken to test predicted morphoclines in carpal joint morphology between pronograde and orthograde arboreal primates. Patterns of movement at the wrist during locomotion were observed and described for the lemuriform species Lemur fulvus and Propithecus verreauxi. Lemur fulvus, which assumes a pronograde posture during locomotion, extends and pronates the wrist during the support phase of quadrupedal walking and running stride cycles. Furthermore, the forearm of this species exhibits some transverse movement across the proximal wrist joint during the support phase. In contrast, the indriid Propithecus maintains the hand and wrist in a flexed and partially supinated position during vertical clinging and suspensory postures. Habitual quadrupedal and vertical postures in Malagasy primates are in turn related to very different patterns of carpal joint morphology and articular mechanics. Those lemurs which are predominantly pronograde share a series of structural features related to stabilizing the antebrachiocarpal joint during extension and mediolateral deviation and the midcarpal joint during pronation: an intraarticular labrum is present on the inner portion of the radiocarpal ligament, the radiocarpal articular surface is quite flat dorsoventrally, the capitate-trapezoid embrasure is expanded dorsally, and development of the radial and ulnar styloids is more pronounced. The wrists of Propithecus, Avahi, and Lepi-lemur (vertical clingers) differ from those of quadrupedal lemuriforms in possessing a suite of morphological features related to stabilizing the wrist during antebrachiocarpal flexion and midcarpal supination: the radiocarpal articular surface is deeply curved and tilted anteriorly, the dorsal radiocarpal ligament is very broad, thick, and fibrous, the hamate's triquetral facet is directed proximodistally, and the capitate-trapezoid embrasure is dorsally
presented in the proceedings of the Twenty-Third Text REtrieval Conference (TREC 2014) held in Gaithersburg, Maryland, November 19-21, 2014. The...and B corpora were created may be found on the Lemur project website2. We strongly encouraged participants to use the full Category A data set if...some information on the topic, which may be minimal; the relevant information must be on that page, not just promising-looking anchor text pointing
Jacobs, Rachel L.; Bradley, Brenda J.
Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; NX chromosomes = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to
Muldoon, Kathleen M.; Goodman, Steven M.
The geographic distribution of species is the typical metric for identifying priority areas for conservation. Since most biodiversity remains poorly studied, a subset of charismatic species, such as primates, often stand as surrogates for total biodiversity. A central question is therefore, how effectively do primates predict the pooled species richness of other mammalian taxa? We used lemurs as indicator species to predict total non-primate mammal community richness in the forest ecosystems of Madagascar. We combine environmental and species occurrence data to ascertain the extent to which primate diversity can predict (1) non-primate mammal α-diversity (species richness), (2) non-primate complementarity, and (3) non-primate β-diversity (species turnover). Our results indicate that primates are effective predictors of non-primate mammal community diversity in the forest ecosystems of Madagascar after controlling for habitat. When individual orders of mammals are considered, lemurs effectively predict the species richness of carnivorans and rodents (but not afrosoricids), complementarity of rodents (but not carnivorans or afrosoricids), and all individual components of β-diversity. We conclude that lemurs effectively predict total non-primate community richness. However, surrogate species alone cannot achieve complete representation of biodiversity. PMID:26334525
Bromley, Keith M.; Hacia, Joseph G.; Bromage, Timothy G.; Snead, Malcolm L.; Moradian-Oldak, Janet; Paine, Michael L.
Strepsirrhines are members of a primate suborder that has a distinctive set of features associated with the development of the dentition. Amelogenin (AMEL), the better known of the enamel matrix proteins, forms 90% of the secreted organic matrix during amelogenesis. Although AMEL has been sequenced in numerous mammalian lineages, the only reported strepsirrhine AMEL sequences are those of the ring-tailed lemur and galago, which contain a set of additional proline-rich tandem repeats absent in all other primates species analyzed to date, but present in some non-primate mammals. Here, we first determined that these repeats are present in AMEL from three additional lemur species and thus are likely to be widespread throughout this group. To evaluate the functional relevance of these repeats in strepsirrhines, we engineered a mutated murine amelogenin sequence containing a similar proline-rich sequence to that of Lemur catta. In the monomeric form, the MQP insertions had no influence on the secondary structure or refolding properties, whereas in the assembled form, the insertions increased the hydrodynamic radii. We speculate that increased AMEL nanosphere size may influence enamel formation in strepsirrhine primates. PMID:21437261
Meyer, Wynn K; Zhang, Sidi; Hayakawa, Sachiko; Imai, Hiroo; Przeworski, Molly
How many distinct molecular paths lead to the same phenotype? One approach to this question has been to examine the genetic basis of convergent traits, which likely evolved repeatedly under a shared selective pressure. We investigated the convergent phenotype of blue iris pigmentation, which has arisen independently in four primate lineages: humans, blue-eyed black lemurs, Japanese macaques, and spider monkeys. Characterizing the phenotype across these species, we found that the variation within the blue-eyed subsets of each species occupies strongly overlapping regions of CIE L*a*b* color space. Yet whereas Japanese macaques and humans display continuous variation, the phenotypes of blue-eyed black lemurs and their sister species (whose irises are brown) occupy more clustered subspaces. Variation in an enhancer of OCA2 is primarily responsible for the phenotypic difference between humans with blue and brown irises. In the orthologous region, we found no variant that distinguishes the two lemur species or associates with quantitative phenotypic variation in Japanese macaques. Given the high similarity between the blue iris phenotypes in these species and that in humans, this finding implies that evolution has used different molecular paths to reach the same end. Am J Phys Anthropol 151:398–407, 2013.© 2013 Wiley Periodicals, Inc. PMID:23640739
Sjöqvist, Lars; Allard, Lars; Pettersson, Magnus; Börjesson, Per; Lindskog, Nils; Bodin, Johan; Widén, Anders; Persson, Hâkan; Fredriksson, Jan; Edström, Sten
Magnifying optical assemblies used for weapon guidance or rifle scopes may possess a threat for a combat vehicle and its personnel. Detection and localisation of optical threats is consequently of interest in military applications. Typically a laser system is used in optics detection, or optical augmentation, to interrogate a scene of interest to localise retroreflected laser radiation. One interesting approach for implementing optics detection on a combat vehicle is to use a continuous scanning scheme. In addition, optics detection can be combined with laser countermeasures, or a laser dazzling function, to efficiently counter an optical threat. An optics detection laser sensor demonstrator has been implemented on a combat vehicle. The sensor consists of a stabilised gimbal and was integrated together with a LEMUR remote electro-optical sight. A narrow laser slit is continuously scanned around the horizon to detect and locate optical threats. Detected threats are presented for the operator within the LEMUR presentation system, and by cueing a countermeasure laser installed in the LEMUR sensor housing threats can be defeated. Results obtained during a field demonstration of the optics detection sensor and the countermeasure laser will be presented. In addition, results obtained using a dual-channel optics detection system designed for false alarm reduction are also discussed.
Crawford, Jeremy Chase; Drea, Christine M.