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Sample records for ring-tailed lemurs lemur

  1. Cognition in ring-tailed lemurs.

    PubMed

    Kittler, Klara; Schnoell, Anna Viktoria; Fichtel, Claudia

    2015-01-01

    In order to better understand the evolution of cognitive abilities in primates, information on cognitive traits of the most basal living primates can provide important comparative baseline data. Compared to haplorhine primates, lemurs have relatively smaller brains and reduced abilities to solve problems in the technical and social domain. However, recent studies have suggested that some cognitive abilities of lemurs are qualitatively equal to those of haplorhines. Here, we review studies investigating cognitive abilities in the technical and social domain of ring-tailed lemur cognition. In the physical domain, ring-tailed lemurs exhibit similar qualitative cognitive skills as other lemurs but also haplorhine primates. In the social domain, ring-tailed lemurs appear to be more skilled in visual perspective taking than other lemurs. Compared to other lemurs, they also have highly elaborated communicative skills. Moreover, within-group coalitions have been observed in female ring-tailed lemurs during rare events of female evictions but not in other lemur species. However, in several other aspects of social cognition, such as reconciliation and social learning, ring-tailed lemurs' cognitive abilities are equal to those of other lemurs. Thus, additional systematic comparative studies in physical and social cognition are required for a more comprehensive understanding of the processes of cognitive evolution among primates. PMID:26022306

  2. Color vision in the ring-tailed lemur (Lemur catta).

    PubMed

    Blakeslee, B; Jacobs, G H

    1985-01-01

    Behavioral discrimination tests were used to examine spectral sensitivity and color vision in a pair of ring-tailed lemurs (Lemur catta). Sensitivity tests revealed the presence of a Purkinje shift and a photopic visual system. As measured at increment-threshold, the photopic spectral sensitivity function for the lemur has multiple peaks (at ca. 440-460, 540, and 620 nm). In color vision tests lemurs behave trichromatically in that (a) they show no evidence for a neutral point in the spectral range of 470-510 nm, and (b) they set a unique Rayleigh match (540 nm + 645 nm = 570 nm). Tests of wavelength and colorimetric purity discrimination reveal that although this prosimian has color vision, it is not an acute capacity--thresholds for these color discriminations were consistently much higher for lemurs than for normal human trichromats tested in the same situation. PMID:4084762

  3. Implicit sequence learning in ring-tailed lemurs (Lemur catta).

    PubMed

    Drucker, Caroline B; Baghdoyan, Talia; Brannon, Elizabeth M

    2016-01-01

    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. PMID:26615500

  4. Hepatic capillariasis in captive ring-tailed lemurs (Lemur catta).

    PubMed

    Zordan, Martin; Tirado, Marcela; López, Claudia

    2012-06-01

    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. PMID:22779256

  5. Solitary Osteochondroma in a Ring-Tailed Lemur (Lemur catta).

    PubMed

    Hope, Katharine L; Boedeker, Nancy C; Gordon, Sebastian S; Walsh, Timothy F

    2015-08-01

    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

  6. Solitary Osteochondroma in a Ring-Tailed Lemur (Lemur catta)

    PubMed Central

    Hope, Katharine L; Boedeker, Nancy C; Gordon, Sebastian S; Walsh, Timothy F

    2015-01-01

    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

  7. Numerical rule-learning in ring-tailed lemurs (lemur catta).

    PubMed

    Merritt, Dustin J; Maclean, Evan L; Crawford, Jeremy Chase; Brannon, Elizabeth M

    2011-01-01

    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

  8. Ring-tailed lemurs: a species re-imagined.

    PubMed

    Sauther, Michelle L; Gould, Lisa; Cuozzo, Frank P; O'Mara, M Teague

    2015-01-01

    For over 50 years, ring-tailed lemurs have been studied continuously in the wild. As one of the most long-studied primate species, the length and breadth of their study is comparable to research on Japanese macaques, baboons and chimpanzees. They are also one of the most broadly observed of all primates, with comprehensive research conducted on their behaviour, biology, ecology, genetics, palaeobiology and life history. However, over the last decade, a new generation of lemur scholars, working in conjunction with researchers who have spent decades studying this species, have greatly enhanced our knowledge of ring-tailed lemurs. In addition, research on this species has expanded beyond traditional gallery forest habitats to now include high altitude, spiny thicket, rocky outcrop and anthropogenically disturbed coastal forest populations. The focus of this special volume is to 're-imagine' the 'flagship species of Madagascar', bringing together three generations of lemur scholars. PMID:26022295

  9. Tamarind tree seed dispersal by ring-tailed lemurs.

    PubMed

    Mertl-Millhollen, Anne S; Blumenfeld-Jones, Kathryn; Raharison, Sahoby Marin; Tsaramanana, Donald Raymond; Rasamimanana, Hantanirina

    2011-10-01

    In Madagascar, the gallery forests of the south are among the most endangered. Tamarind trees (Tamarindus indica) dominate these riverine forests and are a keystone food resource for ring-tailed lemurs (Lemur catta). At Berenty Reserve, the presence of tamarind trees is declining, and there is little recruitment of young trees. Because mature tamarinds inhibit growth under their crowns, seeds must be dispersed away from adult trees if tree recruitment is to occur. Ring-tailed lemurs are likely seed dispersers; however, because they spend much of their feeding, siesta, and sleeping time in tamarinds, they may defecate a majority of the tamarind seeds under tamarind trees. To determine whether they disperse tamarind seeds away from overhanging tamarind tree crowns, we observed two troops for 10 days each, noted the locations of feeding and defecation, and collected seeds from feces and fruit for germination. We also collected additional data on tamarind seedling recruitment under natural conditions, in which seedling germination was abundant after extensive rain, including under the canopy. However, seedling survival to 1 year was lower when growing under mature tamarind tree crowns than when growing away from an overhanging crown. Despite low fruit abundance averaging two fruits/m(3) in tamarind crowns, lemurs fed on tamarind fruit for 32% of their feeding samples. Daily path lengths averaged 1,266 m, and lemurs deposited seeds throughout their ranges. Fifty-eight percent of the 417 recorded lemur defecations were on the ground away from overhanging tamarind tree crowns. Tamarind seeds collected from both fruit and feces germinated. Because lemurs deposited viable seeds on the ground away from overhanging mature tamarind tree crowns, we conclude that ring-tailed lemurs provide tamarind tree seed dispersal services. PMID:21629992

  10. Evaluation of modified techniques for immobilization of wild ring-tailed lemurs (Lemur catta).

    PubMed

    Larsen, R Scott; Sauther, Michelle L; Cuozzo, Frank P

    2011-12-01

    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. PMID:22204057

  11. Male-specific use of the purr in the ring-tailed lemur (Lemur catta).

    PubMed

    Bolt, Laura M

    2014-01-01

    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. PMID:25139722

  12. Surgical Correction of an Arteriovenous Fistula in a Ring-Tailed Lemur (Lemur catta)

    PubMed Central

    Boedeker, Nancy C; Guzzetta, Philip; Rosenthal, Steven L; Padilla, Luis R; Murray, Suzan; Newman, Kurt

    2014-01-01

    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

  13. Surgical correction of an arteriovenous fistula in a ring-tailed lemur (Lemur catta).

    PubMed

    Boedeker, Nancy C; Guzzetta, Philip; Rosenthal, Steven L; Padilla, Luis R; Murray, Suzan; Newman, Kurt

    2014-02-01

    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

  14. RADIOGRAPHIC AND ULTRASONOGRAPHIC ABDOMINAL ANATOMY IN CAPTIVE RING-TAILED LEMURS (LEMUR CATTA).

    PubMed

    Makungu, Modesta; du Plessis, Wencke M; Barrows, Michelle; Groenewald, Hermanus B; Koeppel, Katja N

    2016-06-01

    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

  15. Genetic Diversity of the Ring-Tailed Lemur (Lemur catta) in South-Central Madagascar.

    PubMed

    Clarke, Tara A; Gray, Olivia; Gould, Lisa; Burrell, Andrew S

    2015-01-01

    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. PMID:26022303

  16. Taenia crassiceps cysticercosis in a ring-tailed lemur (Lemur catta).

    PubMed

    Luzón, Mónica; de la Fuente-López, Concepción; Martínez-Nevado, Eva; Fernández-Morán, Jesús; Ponce-Gordo, Francisco

    2010-06-01

    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. PMID:20597227

  17. Squealing rate indicates dominance rank in the male ring-tailed lemur (Lemur catta).

    PubMed

    Bolt, Laura M

    2013-12-01

    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

  18. Well-differentiated hepatocellular carcinoma in a ring-tailed lemur (Lemur catta).

    PubMed

    Nemeth, N M; Blas-Machado, U; Cazzini, P; Oguni, J; Camus, M S; Dockery, K K; Butler, A M

    2013-02-01

    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. PMID:22819017

  19. Sex ratios provide evidence for monozygotic twinning in the ring-tailed lemur, Lemur catta.

    PubMed

    St Clair, John; Campbell-Palmer, Roisin; Lathe, Richard

    2014-02-01

    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. PMID:24384029

  20. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta)

    PubMed Central

    Ethan Pride, R

    2005-01-01

    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

  1. Field anesthesia of wild ring-tailed lemurs (Lemur catta) using tiletamine-zolazepam, medetomidine, and butorphanol.

    PubMed

    Larsen, R Scott; Moresco, Anneke; Sauther, Michelle L; Cuozzo, Frank P

    2011-03-01

    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

  2. Evaluating ring-tailed lemurs (Lemur catta) from southwestern Madagascar for a genetic population bottleneck.

    PubMed

    Parga, Joyce A; Sauther, Michelle L; Cuozzo, Frank P; Jacky, Ibrahim Antho Youssouf; Lawler, Richard R

    2012-01-01

    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. PMID:22052208

  3. Cuterebrid myiasis (Diptera: Oestridae) in captive ring-tailed lemurs (Lemur catta) at a South Carolina zoo.

    PubMed

    Tuten, Holly C; Miller, Heather C; Ellis, Angela E

    2011-09-01

    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. PMID:22950327

  4. Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear.

    PubMed

    Bray, Joel; Krupenye, Christopher; Hare, Brian

    2014-05-01

    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. PMID:24218121

  5. Localized toxoplasmosis in a ring-tailed lemur (Lemur catta) causing placentitis, stillbirths, and disseminated fetal infection.

    PubMed

    Juan-Sallés, Carles; Mainez, Mireia; Marco, Alberto; Sanchís, Ana M Malabia

    2011-09-01

    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. PMID:21908372

  6. Assessment of organochlorine pesticides and metals in ring-tailed lemurs (Lemur catta) at Beza Mahafaly Special Reserve, Madagascar.

    PubMed

    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

    2009-12-01

    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

  7. Nocturnal ranging by a diurnal primate: are ring-tailed lemurs (Lemur catta) cathemeral?

    PubMed

    Parga, Joyce A

    2011-07-01

    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. PMID:21717291

  8. Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Island.

    PubMed

    Parga, J A; Lessnau, R G

    2008-07-01

    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. PMID:18478578

  9. Bifidobacterium lemurum sp. nov., from faeces of the ring-tailed lemur (Lemur catta).

    PubMed

    Modesto, Monica; Michelini, Samanta; Stefanini, Ilaria; Sandri, Camillo; Spiezio, Caterina; Pisi, Annamaria; Filippini, Gianfranco; Biavati, Bruno; Mattarelli, Paola

    2015-06-01

    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). PMID:25736415

  10. Antipredator Vocalization Usage in the Male Ring-Tailed Lemur (Lemur catta).

    PubMed

    Bolt, Laura M; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho

    2015-01-01

    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. PMID:26022308

  11. Endocrine correlates of pregnancy in the ring-tailed lemur (Lemur catta): implications for the masculinization of daughters.

    PubMed

    Drea, Christine M

    2011-04-01

    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. PMID:20932838

  12. Comparison of the efficacy and cardiorespiratory effects of medetomidine-based anesthetic protocols in ring-tailed lemurs (Lemur catta).

    PubMed

    Williams, Cathy V; Glenn, Kelly M; Levine, Jay F; Horne, William A

    2003-06-01

    The relative efficacies and cardiorespiratory effects of three injectable anesthetic combinations containing medetomidine were evaluated in ring-tailed lemurs (Lemur catta). In addition, the direct effects of medetomidine on heart rate and blood pressure were evaluated in lemurs anesthetized with isoflurane. For injectable anesthesia, captive adult ring-tailed lemurs were anesthetized with medetomidine and ketamine (0.04-0.06 mg/kg, i.m. and 3 mg/kg, i.m., respectively), medetomidine, butorphanol, and ketamine (0.04 mg/kg, i.m., 0.4 mg/kg, i.m., and 3 mg/kg, i.m., respectively), or medetomidine, butorphanol, and midazolam (0.04 mg/kg, i.m., 0.4 mg/kg, i.m., and 0.3 mg/kg, i.m., respectively). For inhalation anesthesia, lemurs were mask-induced and maintained with isoflurane for 30 min before receiving medetomidine (0.04 mg/kg, i.m.). Sedation produced by medetomidine-ketamine was unpredictable and of short duration. Both medetomidine-butorphanol-ketamine (MBK) and medetomidine-butorphanol-midazolam (MBMz) provided adequate anesthesia for routine physical exams; however, the effects of MBMz lasted longer than those of MBK. Heart rates and respiratory rates were within clinically normal ranges for all groups, and lemurs remained normotensive throughout the study. Common side effects such as hypertension and bradycardia associated with the use of alpha2-adrenergic receptor agonist combinations in other species were not observed. Likewise, medetomidine administration had no effect on HR in lemurs receiving isoflurane. Lemurs in all groups were well ventilated and remained well oxygenated throughout the procedures, though arterial partial pressure of O2 was lowest in the MBMz group. All three injectable medetomidine combinations were effective in ring-tailed lemurs but only MBK and MBMz provided adequate depth and duration of anesthesia for use as sole regimes. For many clinical procedures in lemurs, MBMz offers advantages over MBK because of its longer duration of

  13. Seasonality, sociality, and reproduction: Long-term stressors of ring-tailed lemurs (Lemur catta).

    PubMed

    Starling, Anne P; Charpentier, Marie J E; Fitzpatrick, Courtney; Scordato, Elizabeth S; Drea, Christine M

    2010-01-01

    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. PMID:19804779

  14. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta).

    PubMed

    Cavigelli, S A; Pereira, M E

    2000-05-01

    The challenge hypothesis (J. C. Wingfield, R. E. Hegner, B. G. Ball, and A. M. Duffy, 1990, Am. Nat. 136, 829-846) proposes that in birds, reptiles, and fish, "the frequency or intensity of reproductive aggression as an effect of T[estosterone] is strongest in situations of social instability, such as during the formation of dominance relationships, the establishment of territorial boundaries, or challenges by a conspecific male for a territory or access to mates" (p. 833). To determine the extension of this hypothesis to mammalian species, we tested predictions of the hypothesis in a nonpaternal, seasonal breeding, prosimian primate (ring-tailed lemurs, Lemur catta). Semi-free-ranging males were studied during periods of social stability (premating period) and instability (mating period). The annual mating season consists of several days during which males fight for access to promiscuous group females as each individually becomes sexually receptive for 1 day. Male rates of aggression were compared to fecal testosterone levels within premating and mating periods. In the premating period male rate of aggression was not significantly correlated with testosterone level. By contrast, during the mating season testosterone and aggression levels were positively and significantly correlated. However, on days just preceding estrus, male rate of aggression was not significantly correlated with testosterone, but on days of estrus, when aggressive challenges peaked sharply, testosterone and aggression were highly positively correlated. These results suggest that the challenge hypothesis applies to mammals as well as to birds, reptiles, and fish. In addition, elevations in testosterone were tightly circumscribed around days of estrus, suggesting a compromise between costs and benefits of elevated testosterone levels. PMID:10868488

  15. Thoracic Limb Morphology of the Ring-tailed Lemur (Lemur catta) Evidenced by Gross Osteology and Radiography.

    PubMed

    Makungu, M; Groenewald, H B; du Plessis, W M; Barrows, M; Koeppel, K N

    2015-08-01

    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. PMID:25105809

  16. Seasonal feeding ecology of ring-tailed lemurs: a comparison of spiny and gallery forest habitats.

    PubMed

    LaFleur, Marni; Sauther, Michelle L

    2015-01-01

    Although Lemur catta persists in many habitat types in southern Madagascar, its ecology has been primarily studied within gallery forests. We compare plant food selection and properties for ring-tailed lemurs in the spiny and gallery forests over the synchronized lactation period (September to March) that includes both the dry and wet seasons. We found no significant habitat-specific differences in the type of plant part consumed per month (i.e. flower, fruit, leaf) or between the intake of soluble carbohydrates. However, the presence and use of Tamarindus indica plants appear to elevate protein and fiber intake in the gallery forest lemurs' diets. Protein is especially important for reproductive females who incur the added metabolic costs associated with lactation; however, fiber can disrupt protein digestion. Future work should continue to investigate how variations of protein and fiber affect ring-tailed lemur dietary choice and nutrient acquisition. PMID:26022298

  17. Occurrence of Encephalitozoon intestinalis in the Red ruffed lemur (Varecia rubra) and the Ring-tailed lemur (Lemur catta) housed in the Poznan Zoological Garden, Poland.

    PubMed

    Słodkowicz-Kowalska, Anna; Majewska, Anna C; Trzesowska, Ewa; Skrzypczak, Łukasz

    2012-01-01

    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. PMID:23094336

  18. Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta).

    PubMed

    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

    2016-08-01

    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. PMID:27177345

  19. Hand preference on unimanual and bimanual tasks in strepsirrhines: The case of the ring-tailed lemur (Lemur catta).

    PubMed

    Regaiolli, Barbara; Spiezio, Caterina; Hopkins, William D

    2016-08-01

    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. PMID:27078687

  20. Osteology and radiographic anatomy of the pelvis and hind limb of healthy ring-tailed lemurs (Lemur catta).

    PubMed

    Makungu, M; Groenewald, H B; du Plessis, W M; Barrows, M; Koeppel, K N

    2014-06-01

    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. PMID:23651234

  1. Echinococcus multilocularis infection of a ring-tailed lemur (Lemur catta) and a nutria (Myocastor coypus) in a French zoo.

    PubMed

    Umhang, Gérald; Lahoreau, Jennifer; Nicolier, Alexandra; Boué, Franck

    2013-12-01

    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. PMID:23994606

  2. Coprophagy by wild ring-tailed lemurs (Lemur catta) in human-disturbed locations adjacent to the Beza Mahafaly Special Reserve, Madagascar.

    PubMed

    Fish, Krista D; Sauther, Michelle L; Loudon, James E; Cuozzo, Frank P

    2007-06-01

    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. PMID:17253614

  3. Ring-Tailed Lemur (Lemur catta) Health Parameters across Two Habitats with Varied Levels of Human Disturbance at the Bezà Mahafaly Special Reserve, Madagascar.

    PubMed

    Singleton, Cora L; Norris, Aimee M; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho

    2015-01-01

    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. PMID:26022301

  4. Mebendazole in the treatment of Hymenolepis nana infections in the captive ring-tailed lemur (Lemur catta), China.

    PubMed

    Li, Bo; Zhao, Bo; Yang, Guang-You; Wang, Qiang; Niu, Li-Li; Deng, Jia-Bo; Gu, Xiao-Bin; Wang, Shu-Xian

    2012-08-01

    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. PMID:22327317

  5. Behavioral responses to tooth loss in wild ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve, Madagascar.

    PubMed

    Millette, James B; Sauther, Michelle L; Cuozzo, Frank P

    2009-09-01

    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. PMID:19373842

  6. The gaits of primates: center of mass mechanics in walking, cantering and galloping ring-tailed lemurs, Lemur catta.

    PubMed

    O'Neill, Matthew C; Schmitt, Daniel

    2012-05-15

    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. PMID:22539740

  7. Variation in dental wear and tooth loss among known-aged, older ring-tailed lemurs (Lemur catta): a comparison between wild and captive individuals.

    PubMed

    Cuozzo, Frank P; Sauther, Michelle L; Gould, Lisa; Sussman, Robert W; Villers, Lynne M; Lent, Cheryl

    2010-11-01

    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. PMID:20872788

  8. Ecological risk aversion and juvenile ring-tailed lemur feeding and foraging.

    PubMed

    O'Mara, M Teague

    2015-01-01

    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. PMID:26022305

  9. Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ring-tailed lemurs in southwestern Madagascar.

    PubMed

    Sondgeroth, Kerry; Blitvich, Brad; Blair, Carol; Terwee, Julie; Junge, Randall; Sauther, Michelle; VandeWoude, Sue

    2007-01-01

    The ring-tailed lemur (Lemur catta) is an endangered species found in southwestern Madagascar, and understanding infectious disease susceptibility is an essential step towards the preservation of wild and captive lemur populations. Lemurs are primates that are widely dispersed throughout the island of Madagascar and may serve as hosts or reservoirs for zoonotic infections. The aim of this study was to determine the prevalence of antibodies to West Nile virus (WNV), simian immunodeficiency virus (SIV), and herpes simplex virus type 1 (HSV-1) in a population of free-ranging ring-tailed lemur from the Beza Mahafaly Special Reserve, Madagascar. Samples were collected from 50 animals during field capture studies in June and July 2004 and assayed for presence of viral antibodies during the 12 mo following collection. Forty-seven of the 50 lemurs sampled had antibodies against WNV detectable by epitope-blocking enzyme-linked immunosorbent assay (ELISA). In addition, 50 of 50 samples had titers against WNV ranging from 80 to > or = 1,280 using plaque reduction neutralization test (PRNT(90)). Ten lemurs had antibodies against lentiviral antigens as determined by Western blot analysis. None of the lemurs had antibodies against HSV-1 using ELISA. PMID:17347392

  10. Sources of tooth wear variation early in life among known-aged wild ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve, Madagascar.

    PubMed

    Cuozzo, Frank P; Head, Brian R; Sauther, Michelle L; Ungar, Peter S; O'Mara, M Teague

    2014-11-01

    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. PMID:24953664

  11. Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations.

    PubMed

    Villers, Lynne M; Jang, Spencer S; Lent, Cheryl L; Lewin-Koh, Sock-Cheng; Norosoarinaivo, Jeanne Aimée

    2008-02-01

    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. PMID:17854057

  12. Fatal infection with Taenia martis metacestodes in a ring-tailed lemur (Lemur catta) living in an Italian zoological garden.

    PubMed

    De Liberato, Claudio; Berrilli, Federica; Meoli, Roberta; Friedrich, Klaus G; Di Cerbo, Pilar; Cocumelli, Cristiano; Eleni, Claudia

    2014-10-01

    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. PMID:24928170

  13. Lifespan and Reproductive Senescence in a Free-Ranging Ring-Tailed Lemur (Lemur catta) Population at Berenty, Madagascar.

    PubMed

    Ichino, Shinichiro; Soma, Takayo; Miyamoto, Naomi; Chatani, Kaoru; Sato, Hiroki; Koyama, Naoki; Takahata, Yukio

    2015-01-01

    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. PMID:26022309

  14. Naturally occurring Ehrlichia chaffeensis infection in two prosimian primate species: ring-tailed lemurs (Lemur catta) and ruffed lemurs (Varecia variegata).

    PubMed

    Williams, Cathy V; Van Steenhouse, Jan L; Bradley, Julie M; Hancock, Susan I; Hegarty, Barbara C; Breitschwerdt, Edward B

    2002-12-01

    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

  15. Relaxed open mouth as a playful signal in wild ring-tailed lemurs.

    PubMed

    Palagi, Elisabetta; Norscia, Ivan; Spada, Giulia

    2014-11-01

    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. PMID:24810169

  16. Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs

    PubMed Central

    Greene, Lydia K.; Grogan, Kathleen E.; Smyth, Kendra N.; Adams, Christine A.; Klager, Skylar A.; Drea, Christine M.

    2016-01-01

    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

  17. Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs.

    PubMed

    Greene, Lydia K; Grogan, Kathleen E; Smyth, Kendra N; Adams, Christine A; Klager, Skylar A; Drea, Christine M

    2016-04-01

    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

  18. Analysis of dentition of a living wild population of ring-tailed lemurs (Lemur catta) from Beza Mahafaly, Madagascar.

    PubMed

    Sauther, M L; Cuozzo, F P; Sussman, R W

    2001-03-01

    Detailed descriptions of the dentition of many strepsirhine primate taxa are rare, despite their importance in understanding primate evolutionary biology. While several researchers have provided detailed morphological descriptions of ring-tailed lemur dentition (e.g., Schwartz and Tattersall [1985] Am. Mus. Nat. Hist. Anthropol. Pap. 60:1-100; Tattersall and Schwartz [1991] Am. Mus. Nat. Hist. Anthropol. Pap. 69:2-18), there are few studies (e.g., Eaglen [1986] Am. J. Phys. Anthropol. 71:185-201) that present quantitative data on the dentition of this species. Furthermore, prior analyses were based on museum specimens from various populations and locations. We present here quantitative and morphological data on the dentition of a population of wild Lemur catta from Beza Mahafaly Special Reserve, Madagascar. Measurements were made on dental casts (n = 39) taken from living members of this L. catta population. Our analysis indicates that no significant (P > 0.05) sexual dimorphism exists for the 30 dental measurements collected. These data support the generalizations (e.g., Plavcan and van Schaik [1994] Evol. Anthropol. 2:208-214; Kappeler [1996] J. Evol. Biol. 9:43-65) that little sexual dimorphism in dentition exists among Malagasy strepsirhines. In addition, the overall patterns of metric variation in this sample compare favorably with patterns seen among other primates, e.g., premolar measurements varying more than molars (e.g., Gingerich [1974] J. Paleontol. 48:895-903). However, there is a degree of intraspecific morphological variation indicated, with one of the morphological traits discussed in other studies as being species-specific for L. catta (absence of P(4) metaconids) observed to vary between specimens. Because the patterns of variation seen in this sample are from a known breeding population, the data presented here provide an important reference for interpreting and understanding the fossil record. PMID:11241187

  19. Patterns of Behaviour, Group Structure and Reproductive Status Predict Levels of Glucocorticoid Metabolites in Zoo-Housed Ring-Tailed Lemurs, Lemur catta.

    PubMed

    Smith, Tessa E; McCusker, Cara M; Stevens, Jeroen M G; Elwood, Robert W

    2015-01-01

    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. PMID:26824528

  20. Brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human head orientation as a cue to gaze direction in a food choice task.

    PubMed

    Botting, Jennifer L; Wiper, Mallory L; Anderson, James R

    2011-01-01

    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. PMID:22123170

  1. Gait-specific metabolic costs and preferred speeds in ring-tailed lemurs (Lemur catta), with implications for the scaling of locomotor costs.

    PubMed

    O'Neill, Matthew C

    2012-11-01

    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. PMID:22976581

  2. The impact of fallback foods on wild ring-tailed lemur biology: a comparison of intact and anthropogenically disturbed habitats.

    PubMed

    Sauther, Michelle L; Cuozzo, Frank P

    2009-12-01

    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. PMID:19890872

  3. Evidence that displacement activities facilitate behavioural transitions in ring-tailed lemurs.

    PubMed

    Buckley, Victoria; Semple, Stuart

    2012-07-01

    Displacement activities are behavioural patterns defined by their apparent irrelevance to an animal's ongoing actions. Despite being identified in diverse taxa, their function remains poorly understood. One hypothesis posits that displacement activities facilitate transitions between different behaviours by mediating changes in animals' motivational state. Under this hypothesis, it is predicted that displacement activities will occur more frequently around changes in behaviour than at other times, and also that rates of displacement activities will be higher before than after such behavioural transitions. We tested these two predictions in wild ring-tailed lemurs (Lemur catta). During focal observations, animals' behavioural state was continuously recorded, as were all occurrences of self-scratching, a common displacement activity in this species. Self-scratching rates were found to be significantly elevated both before and after behavioural transitions. Furthermore, self-scratching rates were significantly higher before behavioural transitions occurred than after. These results, therefore, provide support for the hypothesis that displacement activities facilitate behavioural transitions in L. catta. PMID:22561968

  4. Scent and the single male: ring-tailed lemurs produce honest signals.

    PubMed

    Asa, Cheryl S

    2008-07-01

    In mating systems that involve competing males and choosy females, males are expected to advertise their genetic quality to discriminating females. Most examples have focused on visual or acoustic signals, such as ornamentation or song; yet arguably, olfactory communication may be more important to the majority of vertebrates with the possible exception of birds. Fortunately, attention has begun to shift to the role of odours in mate choice, with most of that attention being directed at the major histocompatibility complex or more recently at the major urinary proteins. The study of male ring-tailed lemurs presented by Charpentier and colleagues in this issue adds a new dimension to investigations of the influence of genes on mate choice via odour production. By comparing genetic heterozygosity to the production of semiochemicals in the scrotal scent gland, they provide a link between genetic composition and scent-marking behaviour as a potential advertisement of male quality. PMID:18564085

  5. Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: a 15-year perspective.

    PubMed

    Gould, Lisa; Sussman, R W; Sauther, Michelle L

    2003-02-01

    Over 15 field seasons (1987-2001), we collected census and life-history data on a population of individually identified ring-tailed lemurs at the Beza Mahafaly Reserve, Madagascar. No significant difference was found in population size over the study period, though a marked decline in the population occurred following a 2-year drought. The population rebounded rapidly after the immediate postdrought period. There was nearly a complete replacement of individuals over the study period. Average group size is 11.5 animals, and adult male to female sex ratio is 0.92. Most females reproduce annually, and the average fecundity rate is 84.3%. The greatest variability in fecundity is found among old females. We suggest that ring-tailed lemur females follow an "income breeding" strategy, i.e., females use maximum resources during reproduction rather than relying on fat stores, as do "capital breeders." Infant mortality to 1 year of age in a nondrought year is 52%, higher than infant mortality in small to medium-sized anthropoids. The oldest known female was 18 years old in 2001. We suggest that 18-20 years may represent the maximum life-span for wild ring-tailed lemurs. Because males regularly emigrate from the population, we have no data regarding male life-span; however, there is some indication that males do not survive as long as females. Group fission has occurred three times: twice from one parent group living in the driest area of the reserve, with the most dispersed food resources. We suggest that the reproductive strategy that has evolved in this species, wherein females reproduce early in life and annually until old age, is a response to the unusual climate and environmental conditions under which Lemur catta has evolved. PMID:12541335

  6. Analyses of feeding lateralization in the small-eared bushbaby (Otolemur garnettii): a comparison with the ring-tailed lemur (Lemur catta).

    PubMed

    Milliken, G W; Stafford, D K; Dodson, D L; Pinger, C D; Ward, J P

    1991-09-01

    Feeding related lateralization was examined in a population of 23 small-eared bushbabies (Otolemur garnettii). The three measures used to determine lateralization were food reaching, holding, and manipulation. Sex and age differences were found, with adult females showing a strong right bias and adult males a left bias. Juvenile males were weakly lateralized and less consistent across measures than adult animals. The use of standard scores to assess lateralization allowed species comparisons to be made. The results of this study were compared with results from a previous study on lateralization in the ring-tailed lemur (Lemur catta). Species comparisons found sex differences to be a stronger factor in lateralization than species differences. PMID:1935006

  7. The impact of dental impairment on ring-tailed lemur food processing performance.

    PubMed

    Millette, James B; Sauther, Michelle L; Cuozzo, Frank P; Ness, Jenifer L

    2012-06-01

    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. PMID:22610899

  8. Comparison of the genetic variation of captive ring-tailed lemurs with a wild population in Madagascar.

    PubMed

    Pastorini, Jennifer; Sauther, Michelle L; Sussman, Robert W; Gould, Lisa; Cuozzo, Frank P; Fernando, Prithiviraj; Nievergelt, Caroline M; Mundy, Nicholas I

    2015-01-01

    Genetic variability among captive and wild ring-tailed lemurs (Lemur catta) was assessed using mitochondrial and nuclear DNA data. A 529 bp segment of mtDNA was sequenced and 9 microsatellite loci were genotyped for 286 ring-tailed lemurs. Samples were obtained from the well-studied L. catta population at the Bezà Mahafaly Special Reserve and from captive animals at six institutions worldwide. We found evidence of possible patrilineal contribution but the absence of matrilineal contribution from the Bezà area, and haplotypes not found in Bezà but present in Ambohimahavelona, Andringitra Massif, and other unknown locations, in the sampled captive population, indicating that the founders of the captive population originated from a wide geographic range. Total genetic variation and relatedness in captive L. catta in the six institutions were similar in extent to that of the wild population in Bezà. Based on the diverse origins of the captive population founders our results suggest the erosion of genetic diversity in the captive population. Sampled individuals from the same institution were more closely related to each other than members of a social group in the wild. Individuals housed at different institutions were less closely related than those of different social groups at Bezà, indicating lower genetic exchange between captive institutions than between social groups in a locality in the wild. Our findings underscore the usefulness of genotyping in determining the geographic origin of captive population founders, obtaining pedigree information if paternity is uncertain, and in maximizing preservation of extant genetic diversity in captivity. PMID:26032097

  9. Is wounding aggression in zoo-housed chimpanzees and ring-tailed lemurs related to zoo visitor numbers?

    PubMed

    Hosey, Geoff; Melfi, Vicky; Formella, Isabel; Ward, Samantha J; Tokarski, Marina; Brunger, Dave; Brice, Sara; Hill, Sonya P

    2016-05-01

    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. PMID:26928968

  10. Population ecology of the ring-tailed lemur, Lemur catta, and the white sifaka, Propithecus verreauxi verreauxi, at Berenty, Madagascar, 1981.

    PubMed

    Howarth, C J; Wilson, J M; Adamson, A P; Wilson, M E; Boase, M J

    1986-01-01

    The diurnal lemurs Propithecus verreauxi verreauxi and Lemur catta at Berenty in southern Madagascar, have been studied for the last 30 years. The August 1981 census indicates that the population size of L. catta remains stable at 150 adults but that P. v. verreauxi troops have become fragmented and scattered and the population is apparently increasing. Eight different vegetation types were classified within the reserve and their influence on the distribution of L. catta and P. v. verreauxi investigated. Behavioural data obtained shows the niche separation between these two, potentially competitive, sympatric lemurs. PMID:3557229

  11. Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations.

    PubMed

    LaFleur, Marni; Sauther, Michelle; Cuozzo, Frank; Yamashita, Nayuta; Jacky Youssouf, Ibrahim Antho; Bender, Richard

    2014-04-01

    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. PMID:24165866

  12. Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar.

    PubMed

    Gould, Lisa; Ziegler, Toni E; Wittwer, Daniel J

    2005-09-01

    Glucocorticoids, a group of adrenal hormones, are secreted in response to stress. In male primates, variables such as breeding seasonality, dominance hierarchy stability, and aggressive and affiliative interactions can affect glucocorticoid levels. In this study, we examined interindividual differences in mean fecal glucocorticoid (fGC) levels among males in three groups of wild ring-tailed lemurs to better understand the physiological costs of group living for males in a female-dominant species that exhibits strict reproductive seasonality. Fecal and behavioral data samples were collected during one mating and two postmating seasons (2001 and 2003). The mean fGC levels were examined in relation to reproductive season, male rank, number of resident males, intermale and female-male agonism, and affiliative behavior with females. The mean fGC levels were not significantly elevated during mating season compared to the postmating period. During the mating season, male dominance hierarchies broke down and rank effects could not be tested; however, there was no relationship between male rank and fGC levels in the postmating periods. In 2001, males that resided in the group with the fewest males exhibited lower fGC levels during the postmating period. They also affiliated more with females than did males in the other groups. During the mating season of 2003, males engaged in more affiliative behaviors with females compared to the postmating season, but female-male agonism did not differ by season. However, rates of intermale agonism were significantly higher during mating compared to postmating periods, but such heightened agonism did not translate to a higher stress response. Thus, neither male-male competition for mates nor heightened agonism between males during the breeding season affected male fGC levels. Fewer males residing in a group, however, did have some effect on male-female affiliation and male fGC levels outside of the mating period. Males that live in a

  13. Feeding behavior and nutrient intake in spiny forest-dwelling ring-tailed lemurs (Lemur catta) during early gestation and early to mid-lactation periods: compensating in a harsh environment.

    PubMed

    Gould, Lisa; Power, Michael L; Ellwanger, Nicholas; Rambeloarivony, Hajamanitra

    2011-07-01

    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. PMID:21541932

  14. Evaluation of male inter-troop transfer as a mating strategy among ring-tailed lemurs on St. Catherines Island, USA.

    PubMed

    Parga, Joyce A

    2010-01-01

    One commonly cited function of dispersal is to increase mating opportunities. In this study, I evaluated the hypothesis that male inter-troop transfer is used as a mating strategy in ring-tailed lemurs, Lemur catta, on St. Catherines Island (SCI), Ga., USA. I measured male mating success and inter-troop transfer behavior across 5 years in a population consisting of 4 lemur groups on SCI. Data strongly supported dispersal as a successful mating strategy of natal males, because these males did not mate within their natal groups, but always mated in their new groups of entry. For secondary male dispersal (transfers between 2 non-natal groups), data on 2 males collected in breeding seasons immediately prior to and following transfer show that their individual mating success measures increased following a transfer. Data revealed that among non-natal males, high-ranking males on SCI were more likely to transfer between groups than lower-ranking males, which is somewhat contrary to the more common trend among primates of lower-ranking males transferring more frequently. In sum, male primary dispersal appears to function as a mating strategy among male L. catta on SCI, with indications that secondary dispersal may also be successful at increasing male mating success. PMID:20720432

  15. Examining visual measures of coat and body condition in wild ring-tailed lemurs at the Bezà Mahafaly Special Reserve, Madagascar.

    PubMed

    Millette, James B; Sauther, Michelle L; Cuozzo, Frank P

    2015-01-01

    Coat and body mass status provide a potential noninvasive way to assess primate health status as well as the effects of seasonality, resource use and reproductive state. Coat and body condition were scored visually for 36 wild Lemur catta at the Bezà Mahafaly Special Reserve, Madagascar, from July 2012 to March 2013. Coat quality generally increased during the wet season when resource availability increased, in contrast to that observed during the resource-depleted dry season. Alopecia frequency increased from June to December and declined between January and March. Sex differences for coat condition were only observed in January, when males had superior coat scores. Body condition did not vary by month or sex except in February, when males were larger than females. Females that birthed infants were of lower body size than individuals who did not for November and from January to March. Our results indicate visual methods effectively detect variability in coat and body condition related to seasonality and reproductive status. Such methods present a noninvasive means for assessing the impact of seasonal resource availability, stresses of infant care and reproductive state on ring-tailed lemurs, and may be useful for assessing the impacts of these factors on general health status. PMID:26022300

  16. Social inhibitory control in five lemur species.

    PubMed

    Reddy, Rachna B; MacLean, Evan L; Sandel, Aaron A; Hare, Brian

    2015-07-01

    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. PMID:25822664

  17. Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta).

    PubMed

    Gould, L; Ziegler, T E

    2007-12-01

    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. PMID:17427976

  18. No evidence for contagious yawning in lemurs.

    PubMed

    Reddy, Rachna B; Krupenye, Christopher; MacLean, Evan L; Hare, Brian

    2016-09-01

    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. PMID:27075549

  19. Species-Specific Transmission of Novel Picornaviruses in Lemurs

    PubMed Central

    Lim, Efrem S.; Deem, Sharon L.; Porton, Ingrid J.; Cao, Song

    2015-01-01

    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

  20. Seroprevalence of Toxoplasma gondii, Sarcocystis neurona, and Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, GA, USA.

    PubMed

    Yabsley, Michael J; Jordan, Carly N; Mitchell, Sheila M; Norton, Terry M; Lindsay, David S

    2007-03-15

    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. PMID:17052854

  1. Evidence for social learning in wild lemurs (Lemur catta).

    PubMed

    Kendal, Rachel L; Custance, Deborah M; Kendal, Jeremy R; Vale, Gillian; Stoinski, Tara S; Rakotomalala, Nirina Lalaina; Rasamimanana, Hantanirina

    2010-08-01

    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. PMID:20628161

  2. The ecology of spatial memory in four lemur species.

    PubMed

    Rosati, Alexandra G; Rodriguez, Kerri; Hare, Brian

    2014-07-01

    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. PMID:24469310

  3. 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.

    PubMed

    LaFleur, M; Gould, L

    2009-01-01

    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. PMID:19776607

  4. Individual recognition through olfactory-auditory matching in lemurs.

    PubMed

    Kulahci, Ipek G; Drea, Christine M; Rubenstein, Daniel I; Ghazanfar, Asif A

    2014-06-01

    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

  5. Individual recognition through olfactory–auditory matching in lemurs

    PubMed Central

    Kulahci, Ipek G.; Drea, Christine M.; Rubenstein, Daniel I.; Ghazanfar, Asif A.

    2014-01-01

    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

  6. Preventing dental calculus formation in lemurs (Lemur catta, Eulemur fulvus collaris) and baboons (Papio cynocephalus).

    PubMed

    Willis, G P; Kapustin, N; Warrick, J M; Miller, L L; Stookey, G K; Hopkins, D T; Doan, E J; Ross, S R

    1999-09-01

    The prevention of calculus accumulation in exotic animals is a relatively unexplored topic. A 6-mo study in ring-tailed lemurs (Lemur catta) and collared lemurs (Eulemur fulvus collaris) and two studies in baboons (Papio cynocephalus) (7.5 wks and 6.5 mo) tested the benefits of a primate diet coated with 0.6% sodium hexametaphosphate (HMP) in controlling calculus in these species using a sequential crossover design. The control regimen was an identical, but non-HMP-coated, dry primate chow. At study initiation, the primates were given a thorough dental prophylaxis and provided with the control diet or experimental diet. At the conclusion of the test period, the animals were anesthetized and examined for clinical calculus independently by two examiners. The animals were then given another dental prophylaxis, provided the alternate ration, and the foregoing procedures were repeated. When the animals were provided the HMP-coated diet, significant reductions in calculus formation of 48-62% were observed in the lemurs and the baboons. No clinically significant changes were observed in body weights or in blood chemistry values as a result of ingestion of the HMP-coated regimen. PMID:10572860

  7. Can zoo records help answer behavioral research questions? The case of the left-handed lemurs (Lemur catta).

    PubMed

    Hosey, Geoff; Hill, Sonya P; Lherbier, Mary L

    2012-01-01

    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. PMID:21674604

  8. Ecology and conservation of the crowned lemur, Lemur coronatus, at Ankarana, n. Madagascar. With notes on Sanford's lemur, other sympatrics and subfossil lemurs.

    PubMed

    Wilson, J M; Stewart, P D; Ramangason, G S; Denning, A M; Hutchings, M S

    1989-01-01

    Forests of Ankarana limestone massif in northern Madagascar support one of the largest and least disturbed populations of Crowned Lemurs, Lemur coronatus. This paper reports a preliminary study of the ecology of this species in the Ankarana Special Reserve conducted at the end of the dry season in 1986, with additional information collected a year later. Crowned Lemurs occur in very high densities in the semi-deciduous canopy forest and this probably represents a dry season refuge for the species. They also use more open habitats, including sparsely vegetated limestone and degraded forest. Sanford's Lemur, Lemur fulvus sanfordi, also inhabits the Ankarana forests but is most abundant in degraded habitats. Crowned and Sanford's Lemurs had similar patterns of activity, which included nocturnal travelling and feeding bouts. Crowned Lemurs proved to be unusual among Lemur species in displaying low spatial troop cohesion and a lack of obvious troop hierarchy. Stronglyoides-like enteric helminths infested about one third of Crowned Lemurs but were apparently not causing disease. Crowned Lemurs fall prey to the Fosa, Cryptoprocta ferox, and the young possibly also to the largest raptors. A total of seven living lemur species (including the very rare Propithecus diadema perrieri and Daubentonia madagascariensis) were confirmed at Ankarana by the authors, and three further species have been reported by other observers. In addition to these ten extant lemurs, four subfossil species have been discovered: three of them (Hapalemur simus, Palaeopropithecus and Mesopropithecus) by the authors. The possibility that all 14 lemurs were once sympatric is discussed. For the present, the lemurs of Ankarana are protected from hunting by local taboo. Nevertheless they are under severe threat from habitat destruction, despite Ankarana's Special Reserve status. Given the very restricted distributions of Crowned and Sanford's Lemurs, both must be considered as threatened with extinction

  9. A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar.

    PubMed

    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

    2008-04-01

    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

  10. Captive Conditions of Pet Lemurs in Madagascar.

    PubMed

    Reuter, Kim E; Schaefer, Melissa S

    2016-01-01

    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. PMID:27092548

  11. Molecular and serologic evidence of tick-borne Ehrlichiae in three species of lemurs from St. Catherines Island, Georgia, USA.

    PubMed

    Yabsley, Michael J; Norton, Terry M; Powell, Malcolm R; Davidson, William R

    2004-12-01

    In recent years, several species of ehrlichiae have been recognized as tick-borne disease agents of veterinary and medical importance. Clinically normal free-ranging or previously free-ranging lemurs, including 46 ring-tailed lemurs (Lemur catta), six blue-eyed black lemurs (Eulemur macaco flavifrons), and four black and white ruffed lemurs (Varecia variegata variegata) from St. Catherines Island, Georgia, were tested for evidence of exposure to tick-borne ehrlichiae. All 52 adult lemurs were serologically tested for exposure to Ehrlichia chaffeensis and Anaplasma phagocytophilum. Polymerase chain reaction (PCR) assays for E. chaffeensis, A. phagocytophilum, Ehrlichia ewingii, and Ehrlichia canis were conducted on blood samples from all 56 lemurs. Blood from all lemurs was inoculated into DH82 cell cultures for E. chaffeensis isolation. Of the adult lemurs, 20 (38.5%) and 16 (30.8%) had antibodies reactive (> or =1:128) for E. chaffeensis and A. phagocytophilum, respectively. Two ring-tailed lemurs were PCR and culture positive for E. chaffeensis. Molecular characterization of the two E. chaffeensis isolates showed that both contained 5-repeat variants of the variable-length PCR target (VLPT) antigen gene and 3-repeat variants of the 120-kDa antigen gene. Sequencing of the VLPT genes revealed a novel amino acid repeat unit (type-9). One lemur infected with E. chaffeensis was slightly hypoproteinemic and had moderately elevated serum alanine aminotransferase (ALT) levels. These lemurs from St. Catherines Island have been exposed to or infected with tick-borne ehrlichiae, or both, but showed no clinical disease. PMID:15732591

  12. Interpreting food processing through dietary mechanical properties: a Lemur catta case study.

    PubMed

    Yamashita, Nayuta; Cuozzo, Frank P; Sauther, Michelle L

    2012-06-01

    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. PMID:22610896

  13. Androgen levels and female social dominance in Lemur catta.

    PubMed

    von Engelhardt, N; Kappeler, P M; Heistermann, M

    2000-08-01

    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

  14. Fatal echinococcosis in three lemurs in the United Kingdom--A case series.

    PubMed

    Denk, Daniela; Boufana, Belgees; Masters, Nicholas J; Stidworthy, Mark F

    2016-03-15

    Tapeworms of the genus Echinococcus reside in the small intestine of a number of carnivorous species, predominantly canids. In enzootic areas, hydatidosis caused by taeniid metacestodes can present a significant problem in accidental intermediate hosts, including humans. Whereas the United Kingdom is currently considered free of Echinococcus multilocularis, Echinococcus granulosus sensu stricto (s.s.) and Echinococcus equinus are endemic in the UK and have been reported in a variety of captive mammals. The presentation of echinoccocosis in non-human primates widely parallels disease in humans, and public health concerns are related to the four genera, E. granulosus, E. multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. In contrast, sporadic outbreaks and individual hydatid disease cases in non-human primates have been associated with several Echinococcus and Taenia species. Here we describe three fatal cases of cystic echinococcosis in two captive ring-tailed lemurs (Lemur catta) and one captive red-ruffed lemur (Varecia variegata rubra) and provide molecular tapeworm characterisation. To the best of the authors' knowledge, this includes the first report of Echinococcus ortleppi in a UK born ring-tailed lemur and provides the first in depth case reports of echinococcosis due to E. equinus in UK born ring-tailed and red ruffed lemurs with detailed clinical and pathological findings. The cestode life cycle and implications for zoo collections are discussed. PMID:26872922

  15. Scent marking as resource defense by female Lemur catta.

    PubMed

    Mertl-Millhollen, Anne S

    2006-06-01

    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. PMID

  16. Nutrition and behavior of lemurs.

    PubMed

    Junge, Randall E; Williams, Cathy V; Campbell, Jennifer

    2009-05-01

    Attention to nutritional and behavioral factors is important for appropriate care of lemurs in captivity. Although only a few species are commonly held in captivity, differences between them are important. Knowledge of feeding ecology and natural diet guide nutrition guidelines, as well as management and prevention of common nutrition-related disorders, including obesity, diabetes, and iron-storage disease. Behavioral characteristics that influence captive management are related to social organization, reproductive behavior, territoriality, and infant care. Housing animals in appropriate social groupings in adequately complex environments reduces abnormal behaviors, and addition of enrichment activities and operant conditioning encourages normal behaviors. PMID:19341960

  17. Blue eyes in lemurs and humans: same phenotype, different genetic mechanism.

    PubMed

    Bradley, Brenda J; Pedersen, Anja; Mundy, Nicholas I

    2009-06-01

    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. PMID:19278018

  18. Beyond the Gallery Forest: Contrasting Habitat and Diet in Lemur catta Troops at Bezà Mahafaly Special Reserve.

    PubMed

    Yamashita, Nayuta; Sauther, Michelle L; Cuozzo, Frank P; Youssouf Jacky, Ibrahim Antho

    2015-01-01

    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. PMID:26022299

  19. Behavioral thermoregulation in Lemur catta: The significance of sunning and huddling behaviors.

    PubMed

    Kelley, Elizabeth A; Jablonski, Nina G; Chaplin, George; Sussman, Robert W; Kamilar, Jason M

    2016-07-01

    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

  20. Lemur Biorhythms and Life History Evolution

    PubMed Central

    Hogg, Russell T.; Godfrey, Laurie R.; Schwartz, Gary T.; Dirks, Wendy; Bromage, Timothy G.

    2015-01-01

    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

  1. Lemur Biorhythms and Life History Evolution.

    PubMed

    Hogg, Russell T; Godfrey, Laurie R; Schwartz, Gary T; Dirks, Wendy; Bromage, Timothy G

    2015-01-01

    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

  2. Relatedness communicated in lemur scent

    NASA Astrophysics Data System (ADS)

    Morelli, Toni Lyn; Hayes, R. Andrew; Nahrung, Helen F.; Goodwin, Thomas E.; Harelimana, Innocent H.; MacDonald, Laura J.; Wright, Patricia C.

    2013-08-01

    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.

  3. Scratching around mating: factors affecting anxiety in wild Lemur catta.

    PubMed

    Sclafani, Valentina; Norscia, Ivan; Antonacci, Daniela; Palagi, Elisabetta

    2012-07-01

    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. PMID:22278710

  4. A molecular approach to comparative phylogeography of extant Malagasy lemurs

    PubMed Central

    Pastorini, Jennifer; Thalmann, Urs; Martin, Robert D.

    2003-01-01

    The lemurs of Madagascar provide an excellent model for exploring evolutionary diversification. This study investigates genetic divergence among most extant lemur taxa in relation to potential geographical boundaries to gene flow. For this purpose, ≈2,400 bp of mitochondrial DNA (part of the COIII gene; ND3, ND4L, and ND4 genes; and five tRNAs) were sequenced in a total of 131 lemurs from 5 families, 12 genera, 25 species, and 18 subspecies to reconstruct phylogenetic relationships among them. The comprehensive range of taxa makes this a particularly suitable molecular data set to examine lemur evolution. Those data clearly reveal that the Betsiboka River acts as an isolating barrier between populations of lemurs in north-western Madagascar. The Tsiribihina River similarly serves as a barrier to gene flow between northern and southern populations of lemurs in central western Madagascar, whereas the Mahavavy River does not seem to lead to genetic isolation of lemur populations. Several discrepancies among molecular data, current taxonomy, and geographic distribution along the western coast emerged. Examination of geographical distribution of the taxa concerned in comparison with distribution boundaries of other lemur taxa in that region yielded explanations for these inconsistencies. Eulemur fulvus and Eulemur mongoz are the only lemur taxa that also occur outside Madagascar, on the Comoro Islands. Genetic data show no significant differentiation between Malagasy and Comorian populations of these species, supporting the interpretation that both were introduced only recently to the Comoro Islands. PMID:12719521

  5. Analysis of chromosome conservation in Lemur catta studied by chromosome paints and BAC/PAC probes.

    PubMed

    Cardone, Maria Francesca; Ventura, Mario; Tempesta, Sergio; Rocchi, Mariano; Archidiacono, Nicoletta

    2002-12-01

    A panel of human chromosome painting probes and bacterial and P1 artificial chromosome (BAC/PAC) clones were used in fluorescence in situ hybridization (FISH) experiments to investigate the chromosome conservation of the ring-tailed lemur (Lemur catta, LCA) with respect to human. Whole chromosome paints specific for human chromosomes 7, 9, 11, 13, 14, 17, 18, 20, 21, and X were found to identify a single chromosome or an uninterrupted chromosomal region in LCA. A large set of partial chromosome paints and BAC/PAC probes were then used to refine the characterization of the rearrangements differentiating the two karyotypes. The results were also used to reconstruct the ancestral Lemuridae karyotype. Lemur catta, indeed, can be used as an outgroup, allowing symplesiomorphic (ancestral) rearrangements to be distinguished from apomorphic (derived) rearrangements in lemurs. Some LCA chromosomes are difficult to distinguish morphologically. The 'anchorage' of most LCA chromosomes to specific probes will contribute to the standardization of the karyotype of this species. PMID:12474064

  6. Coevolution of Cyanogenic Bamboos and Bamboo Lemurs on Madagascar

    PubMed Central

    Ballhorn, Daniel J.; Rakotoarivelo, Fanny Patrika; Kautz, Stefanie

    2016-01-01

    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

  7. Coevolution of Cyanogenic Bamboos and Bamboo Lemurs on Madagascar.

    PubMed

    Ballhorn, Daniel J; Rakotoarivelo, Fanny Patrika; Kautz, Stefanie

    2016-01-01

    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

  8. Olfactory demarcation of territorial but not home range boundaries by Lemur catta.

    PubMed

    Mertl-Millhollen, A S

    1988-01-01

    Over 350 h of observations were collected using focal animal sampling of scent-marking behavior by 2 troops of ring-tailed lemurs (Lemur catta) in the field in Madagascar. Although they did not mark any branch species preferentially, they did have preferred marking sites. Significantly more scent marks were deposited in the area of home range overlap between troops than in the area of exclusive use. However, few marks were deposited at the periphery of the area of overlap. Instead, the majority of the marks were in a narrow band within the area of overlap that coincided with the positions of intertroop confrontations. Female genital marks and male arm marks, as well as the accompanying male shoulder rubs thus appear to demarcate territorial borders. PMID:3240911

  9. Sight or Scent: Lemur Sensory Reliance in Detecting Food Quality Varies with Feeding Ecology

    PubMed Central

    Rushmore, Julie; Leonhardt, Sara D.; Drea, Christine M.

    2012-01-01

    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

  10. Sight or scent: lemur sensory reliance in detecting food quality varies with feeding ecology.

    PubMed

    Rushmore, Julie; Leonhardt, Sara D; Drea, Christine M

    2012-01-01

    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

  11. Pathogenic Enterobacteria in Lemurs Associated With Anthropogenic Disturbance

    PubMed Central

    BUBLITZ, DEANNA C.; WRIGHT, PATRICIA C.; RASAMBAINARIVO, FIDISOA T.; ARRIGO-NELSON, SUMMER J.; BODAGER, JONATHAN R.; GILLESPIE, THOMAS R.

    2015-01-01

    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

  12. Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance.

    PubMed

    Bublitz, DeAnna C; Wright, Patricia C; Rasambainarivo, Fidisoa T; Arrigo-Nelson, Summer J; Bodager, Jonathan R; Gillespie, Thomas R

    2015-03-01

    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

  13. The vomeronasal organ of Lemur catta.

    PubMed

    Smith, Timothy D; Muchlinski, Magdalena N; Bhatnagar, Kunwar P; Durham, Emily L; Bonar, Christopher J; Burrows, Anne M

    2015-02-01

    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. PMID:25220179

  14. Systemic effects of Leucaena leucocephala ingestion on ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar.

    PubMed

    Crawford, Graham; Puschner, Birgit; Affolter, Verena; Stalis, Ilse; Davidson, Autumn; Baker, Tomas; Tahara, John; Jolly, Alison; Ostapak, Susan

    2015-06-01

    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

  15. Human eccrine hamartoma of the forearm-antebrachial organ of the ringtailed lemur (Lemur catta). A possible phylogenetic relationship?

    PubMed

    Kopera, D; Soyer, H P; Kerl, H

    1994-06-01

    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. PMID:7943634

  16. Unusual sleeping site selection by southern bamboo lemurs.

    PubMed

    Eppley, Timothy M; Donati, Giuseppe; Ganzhorn, Jörg U

    2016-04-01

    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

  17. Interspecific semantic alarm call recognition in the solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis.

    PubMed

    Seiler, Melanie; Schwitzer, Christoph; Gamba, Marco; Holderied, Marc W

    2013-01-01

    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

  18. Olfactory signals and the MHC: a review and a case study in Lemur catta.

    PubMed

    Knapp, Leslie A; Robson, Julie; Waterhouse, John S

    2006-06-01

    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. PMID:16715507

  19. Female rule in lemurs is ancestral and hormonally mediated.

    PubMed

    Petty, Joseph M A; Drea, Christine M

    2015-01-01

    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

  20. Female rule in lemurs is ancestral and hormonally mediated

    PubMed Central

    Petty, Joseph M. A.; Drea, Christine M.

    2015-01-01

    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

  1. Smelling wrong: hormonal contraception in lemurs alters critical female odour cues.

    PubMed

    Crawford, Jeremy Chase; Boulet, Marylène; Drea, Christine M

    2011-01-01

    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

  2. Diurnality and cone photopigment polymorphism in strepsirrhines: examination of linkage in Lemur catta.

    PubMed

    Jacobs, Gerald H; Deegan, Jess F

    2003-09-01

    Trichromatic color vision is routine among catarrhine primates, but occurs only as a variant form of color vision in some individuals in most platyrrhine genera. This arises from a fundamental difference in the organization of X-chromosome cone opsin genes in these two lineages: catarrhines have two opsin genes specifying middle- and long-wavelength-sensitive cone pigments, while platyrrhines have only a single gene. Some female platyrrhine monkeys achieve trichromacy because of a species polymorphism that allows the possibility of different opsin gene alleles on the two X-chromosomes. Recently, a similar opsin gene polymorphism was detected in some diurnal strepsirrhines, while at the same time appearing to be absent in any nocturnal genera. The aim of this study was to assess whether cone pigment polymorphism is inevitably linked to diurnality in strepsirrhines. Cone photopigments were measured in a species usually classified as diurnal, the ring-tailed lemur (Lemur catta), using electroretinogram flicker photometry, a noninvasive electrophysiological procedure. Each of 12 animals studied was found to have the same middle-wavelength cone pigment, with peak sensitivity at about 547 nm. In conjunction with earlier results, this implies that cone pigment polymorphism is unlikely to exist in this species and that, accordingly, such variation is not a consistently predictable feature of vision in diurnal strepsirrhines. PMID:12923905

  3. An Alu-Based Phylogeny of Lemurs (Infraorder: Lemuriformes)

    PubMed Central

    McLain, Adam T.; Meyer, Thomas J.; Faulk, Christopher; Herke, Scott W.; Oldenburg, J. Michael; Bourgeois, Matthew G.; Abshire, Camille F.

    2012-01-01

    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

  4. An alu-based phylogeny of lemurs (infraorder: Lemuriformes).

    PubMed

    McLain, Adam T; Meyer, Thomas J; Faulk, Christopher; Herke, Scott W; Oldenburg, J Michael; Bourgeois, Matthew G; Abshire, Camille F; Roos, Christian; Batzer, Mark A

    2012-01-01

    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

  5. LEMUR: Large European Module for Solar Ultraviolet Research

    NASA Technical Reports Server (NTRS)

    Teriaca, Luca; Vincenzo, Andretta; Auchere, Frederic; 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.; Martinez-Pillet, Valentin; Parenti, Susanna; Patsourakos, Spiros; Peter, Hardi; Poletto, Luca; Rutten, Robert J.; Schuhle, 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

    2012-01-01

    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

  6. Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur, Lepilemur sahamalazensis

    PubMed Central

    Seiler, Melanie; Schwitzer, Christoph; Gamba, Marco; Holderied, Marc W.

    2013-01-01

    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

  7. (Un-)expected nocturnal activity in "Diurnal" Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation.

    PubMed

    Donati, Giuseppe; Santini, Luca; Razafindramanana, Josia; Boitani, Luigi; Borgognini-Tarli, Silvana

    2013-01-01

    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. PMID:23180596

  8. Delimiting Species without Nuclear Monophyly in Madagascar's Mouse Lemurs

    PubMed Central

    Weisrock, David W.; Rasoloarison, Rodin M.; Fiorentino, Isabella; Ralison, José M.; Goodman, Steven M.; Kappeler, Peter M.; Yoder, Anne D.

    2010-01-01

    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

  9. Evidence of early butchery of giant lemurs in Madagascar.

    PubMed

    Perez, Ventura R; Godfrey, Laurie R; Nowak-Kemp, Malgosia; Burney, David A; Ratsimbazafy, Jonah; Vasey, Natalia

    2005-12-01

    We report here definitive evidence of butchery, most probably associated with hunting, of giant extinct lemurs by early human settlers in Madagascar. Specimens of Palaeopropithecus ingens and Pachylemur insignis from two sites in southwestern Madagascar, Taolambiby and Tsirave, show classic signs of butchering. We compared these to the bones (also from Taolambiby) of butchered Propithecus verreauxi, a lemur still living in the region. The characteristics of the tool-induced extinct-lemur bone alterations (sharp cuts and chop marks near joints, oblique cuts along the shafts, spiral fractures, and percussion striae) suggest skinning, disarticulation, and filleting. Conclusive evidence of megafaunal modification by humans in Madagascar was limited previously to a few hippo and elephant bird bones and one extinct aye-aye tooth. New evidence comes not from archaeological sites, but from specimens collected in the early 1900s, without stratigraphic records, at "subfossil" sites (i.e., sites renowned for their late Pleistocene or Holocene fossils, often lacking human artifacts). Whereas these are hardly the most ideal samples for analysis of this kind, careful scrutiny of the characteristics of the cut marks has allowed us to document butchery beyond any reasonable doubt. One bone with definitive cut marks has been dated to the very earliest part of the human period in Madagascar. Continued, careful research on the bones in subfossil collections is warranted. PMID:16225904

  10. DNA from extinct giant lemurs links archaeolemurids to extant indriids

    PubMed Central

    2008-01-01

    Background Although today 15% of living primates are endemic to Madagascar, their diversity was even greater in the recent past since dozens of extinct species have been recovered from Holocene excavation sites. Among them were the so-called "giant lemurs" some of which weighed up to 160 kg. Although extensively studied, the phylogenetic relationships between extinct and extant lemurs are still difficult to decipher, mainly due to morphological specializations that reflect ecology more than phylogeny, resulting in rampant homoplasy. Results Ancient DNA recovered from subfossils recently supported a sister relationship between giant "sloth" lemurs and extant indriids and helped to revise the phylogenetic position of Megaladapis edwardsi among lemuriformes, but several taxa – such as the Archaeolemuridae – still await analysis. We therefore used ancient DNA technology to address the phylogenetic status of the two archaeolemurid genera (Archaeolemur and Hadropithecus). Despite poor DNA preservation conditions in subtropical environments, we managed to recover 94- to 539-bp sequences for two mitochondrial genes among 5 subfossil samples. Conclusion This new sequence information provides evidence for the proximity of Archaeolemur and Hadropithecus to extant indriids, in agreement with earlier assessments of their taxonomic status (Primates, Indrioidea) and in contrast to recent suggestions of a closer relationship to the Lemuridae made on the basis of analyses of dental developmental and postcranial characters. These data provide new insights into the evolution of the locomotor apparatus among lemurids and indriids. PMID:18442367

  11. Optional strategies for reduced metabolism in gray mouse lemurs

    NASA Astrophysics Data System (ADS)

    Schmid, J.; Ganzhorn, J. U.

    2009-06-01

    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.

  12. Blood transcriptomes reveal novel parasitic zoonoses circulating in Madagascar's lemurs.

    PubMed

    Larsen, Peter A; Hayes, Corinne E; Williams, Cathy V; Junge, Randall E; Razafindramanana, Josia; Mass, Vanessa; Rakotondrainibe, Hajanirina; Yoder, Anne D

    2016-01-01

    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

  13. GASTROINTESTINAL PARASITES OF CAPTIVE AND FREE-LIVING LEMURS AND DOMESTIC CARNIVORES IN EASTERN MADAGASCAR.

    PubMed

    Alexander, Amy B; Poirotte, Clémence; Porton, Ingrid J; Freeman, Karen L M; Rasambainarivo, Fidisoa; Olson, Kimberly G; Iambana, Bernard; Deem, Sharon L

    2016-03-01

    Fecal samples from captive and free-living lemurs at Ivoloina Zoological Park (IZP) and domestic carnivores from six villages surrounding IZP were evaluated between July and August 2012. Free-living lemurs from Betampona Natural Reserve (BNR), a relatively pristine rainforest fragment 40 km away, were also evaluated in November 2013. All 33 dogs sampled (100%) and 16 of 22 cats sampled (72.7%) were parasitized, predominantly with nematodes (strongyles, ascarids, and spirurids) as well as cestodes and protozoans. Similar types of parasites were identified in the lemur populations. Identification of spirurid nematodes and protozoans in the lemur fecal samples were of concern due to previously documented morbidity and mortality in lemurs from these parasitic agents. Twelve of 13 free-living (93%) and 31 of 49 captive (63%) lemurs sampled at IZP had a higher parasite prevalence than lemurs at BNR, with 13 of 24 (54%) being parasitized. The lemurs in BNR are likely at risk of increased exposure to these parasites and, therefore, increased morbidity and mortality, as humans and their domestic animals are encroaching on this natural area. PMID:27010275

  14. Discovery of an island population of dwarf lemurs (Cheirogaleidae: Cheirogaleus) on Nosy Hara, far northern Madagascar.

    PubMed

    Gardner, Charlie J; Jasper, Louise D

    2015-10-01

    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. PMID:26243504

  15. Comparative and population mitogenomic analyses of Madagascar's extinct, giant 'subfossil' lemurs.

    PubMed

    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

    2015-02-01

    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. PMID:25523037

  16. Jumping Stand Apparatus Reveals Rapidly Specific Age-Related Cognitive Impairments in Mouse Lemur Primates

    PubMed Central

    Picq, Jean-Luc; Villain, Nicolas; Gary, Charlotte; Pifferi, Fabien; Dhenain, Marc

    2015-01-01

    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

  17. Transitive inference in two lemur species (Eulemur macaco and Eulemur fulvus).

    PubMed

    Tromp, D; Meunier, H; Roeder, J J

    2015-03-01

    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. PMID:25328141

  18. Jumping Stand Apparatus Reveals Rapidly Specific Age-Related Cognitive Impairments in Mouse Lemur Primates.

    PubMed

    Picq, Jean-Luc; Villain, Nicolas; Gary, Charlotte; Pifferi, Fabien; Dhenain, Marc

    2015-01-01

    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

  19. The influence of growth patterns on sexual size monomorphism in lemurs.

    PubMed

    Tennenhouse, E M

    2015-09-01

    The lack of sexual size dimorphism among lemurs is puzzling given the high degree of polygyny in this clade. It has been proposed that the unique ecological conditions of Madagascar favour rapid completion of growth, limiting the opportunities for bimaturism and sexual size dimorphism in lemurs. Using recently compiled large data sets on many species across the lemur clade, I examined the prevalence of sexual size monomorphism of body mass among lemurs and tested the hypothesis that limited growth durations constrain sexual size dimorphism. I used segmented regression analyses to accurately model growth in each species. The majority of species analysed exhibited a period of rapid growth followed by a distinct period of slow growth prior to attainment of adult body mass. Whereas the first period of growth was constrained by the need to attain the majority of adult body mass prior to the onset of the infant's first dry season, the subsequent period of slow growth was unconstrained and sufficiently long to promote sexual bimaturism. Sex differences in the duration and rate of growth during this second growth phase appeared to account for the sexual size dimorphism exhibited by three lemur species. Therefore, constraints on growth processes do not limit sexual size dimorphism in lemurs, and other explanations for the prevalence of sexual size monomorphism in this clade should be examined. The importance of considering ontogeny in future investigations of sexual size monomorphism in lemurs is highlighted. PMID:26134876

  20. Analog number representations in mongoose lemurs (Eulemur mongoz): evidence from a search task.

    PubMed

    Lewis, Kerrie P; Jaffe, Sarah; Brannon, Elizabeth M

    2005-10-01

    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. PMID:15660208

  1. A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang.

    PubMed

    Ramsier, Marissa A; Dominy, Nathaniel J

    2010-03-01

    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

  2. Innovation and behavioral flexibility in wild redfronted lemurs (Eulemur rufifrons).

    PubMed

    Huebner, Franziska; Fichtel, Claudia

    2015-05-01

    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. PMID:25673157

  3. The asymmetric scent: ringtailed lemurs ( Lemur catta) have distinct chemical signatures in left and right brachial glands

    NASA Astrophysics Data System (ADS)

    Dapporto, Leonardo

    2008-10-01

    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.

  4. Better Few than Hungry: Flexible Feeding Ecology of Collared Lemurs Eulemur collaris in Littoral Forest Fragments

    PubMed Central

    Donati, Giuseppe; Kesch, Kristina; Ndremifidy, Kelard; Schmidt, Stacey L.; Ramanamanjato, Jean-Baptiste; Borgognini-Tarli, Silvana M.; Ganzhorn, Joerg U.

    2011-01-01

    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

  5. Hybridization of mouse lemurs: different patterns under different ecological conditions

    PubMed Central

    2011-01-01

    Background Several mechanistic models aim to explain the diversification of the multitude of endemic species on Madagascar. The island's biogeographic history probably offered numerous opportunities for secondary contact and subsequent hybridization. Existing diversification models do not consider a possible role of these processes. One key question for a better understanding of their potential importance is how they are influenced by different environmental settings. Here, we characterized a contact zone between two species of mouse lemurs, Microcebus griseorufus and M. murinus, in dry spiny bush and mesic gallery forest that border each other sharply without intermediate habitats between them. We performed population genetic analyses based on mtDNA sequences and nine nuclear microsatellites and compared the results to a known hybrid zone of the same species in a nearby wide gradient from dry spiny bush over transitional forest to humid littoral forest. Results In the spiny-gallery system, Microcebus griseorufus is restricted to the spiny bush; Microcebus murinus occurs in gallery forest and locally invades the dryer habitat of its congener. We found evidence for bidirectional introgressive hybridization, which is closely linked to increased spatial overlap within the spiny bush. Within 159 individuals, we observed 18 hybrids with mitochondrial haplotypes of both species. Analyses of simulated microsatellite data indicate that we identified hybrids with great accuracy and that we probably underestimated their true number. We discuss short-term climatic fluctuations as potential trigger for the dynamic of invasion and subsequent hybridization. In the gradient hybrid zone in turn, long-term aridification could have favored unidirectional nuclear introgression from Microcebus griseorufus into M. murinus in transitional forest. Conclusions Madagascar's southeastern transitional zone harbors two very different hybrid zones of mouse lemurs in different environmental

  6. Mechanical food properties and dental topography differentiate three populations of Lemur catta in southwest Madagascar.

    PubMed

    Yamashita, Nayuta; Cuozzo, Frank P; Sauther, Michelle L; Fitzgerald, Emily; Riemenschneider, Andrea; Ungar, Peter S

    2016-09-01

    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

  7. Dental use wear in extinct lemurs: evidence of diet and niche differentiation.

    PubMed

    Godfrey, Laurie R; Semprebon, Gina M; Jungers, William L; Sutherland, Michael R; Simons, Elwyn L; Solounias, Nikos

    2004-09-01

    A new technique for molar use-wear analysis is applied to samples of all 16 species of extinct lemurs with known dentitions, as well as to a large comparative sample of extant primates. This technique, which relies on the light refractive properties of wear pits and scratches as seen under a standard stereoscopic microscope, has shown itself to be effective in distinguishing the diets of ungulates and extant primates. We draw dietary inferences for each of the 16 extinct lemur species in our database. There is a strong phylogenetic signal, with the Palaeopropithecidae showing use-wear signatures similar to those of the Indriidae; extinct lemurids (Pachylemur spp.) showing striking similarities to extant lemurids (except Hapalemur spp.); and Megaladapis showing similarities to Lepilemur spp. Only the Archaeolemuridae have dietary signatures unlike those of any extant lemurs, with the partial exception of Daubentonia. We conclude that the Archaeolemuridae were hard-object feeders; the Palaeopropithecidae were seed predators, consuming a mixed diet of foliage and fruit to varying degrees; Pachylemur was a fruit-dominated mixed feeder, but not a seed predator; and all Megaladapis were leaf browsers. There is no molar use wear evidence that any of the extinct lemurs relied on terrestrial foods (C4 grasses, tubers, rhizomes). This has possible implications for the role of the disappearance of wooded habitats in the extinction of lemurs. PMID:15337413

  8. Interstitial cell tumor in a black-and-white ruffed lemur (Varecia variegatus variegatus).

    PubMed

    Neiffer, D L; Klein, E C

    2001-06-01

    A 14.5-yr-old, male black-and-white ruffed lemur (Varecia variegatus variegatus) presented for acute enlargement of the left testicle and hemiscrotum. Physical examination also revealed poor pelage quality with short guard hairs, sparse undercoat, and areas of alopecia. Increased aggression was also reported. A unilateral, open orchiectomy was performed, with the left testicle, epidydymis, associated vaginal tunic, and attached spermatic cord removed. Microscopic evaluation was consistent with an interstitial cell tumor, with many morphologic features similar to this neoplasm in people. No overt histopathologic criteria of malignancy were present. Following orchiectomy, gradual improvement in pelage quality was noted and was considered almost normal by 5 mo postoperative. In contrast with the aggressive preoperative behavior, the lemur was extremely submissive for 3 mo following the surgery. Gradual return to normal behavior and social status occurred over the next 2 mo. Multiple follow-up examinations and radiographs revealed no evidence of metastasis, and biopsy of the remaining testicle 4 mo later revealed no evidence of neoplasia. Serial measurements of testosterone and estradiol revealed levels within the range of those for other ruffed lemurs, as were repeated measurements taken of the remaining testicle. At 19 mo postoperative, the lemur had a coat quality considered nearly normal and maintained its historical social position in the lemur group without abnormal aggressive behavior. PMID:12790432

  9. First direct evidence of hibernation in an eastern dwarf lemur species ( Cheirogaleus crossleyi) from the high-altitude forest of Tsinjoarivo, central-eastern Madagascar

    NASA Astrophysics Data System (ADS)

    Blanco, Marina B.; Rahalinarivo, Vololonirina

    2010-10-01

    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.

  10. Does nonnutritive tree gouging in a rainforest-dwelling lemur convey resource ownership as does loud calling in a dry forest-dwelling lemur?

    PubMed

    Rasoloharijaona, Solofonirina; Randrianambinina, Blanchard; Joly-Radko, Marine

    2010-12-01

    Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high-density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00-10:00 p.m.) and the early morning (02:00-05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree-gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non-nutritive tree gouging is used as a scent-marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms. PMID:20623502

  11. Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar’s lemurs

    PubMed Central

    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.

    2008-01-01

    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

  12. Phylogeny and Divergence Times of Lemurs Inferred with Recent and Ancient Fossils in the Tree.

    PubMed

    Herrera, James P; Dávalos, Liliana M

    2016-09-01

    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. PMID:27113475

  13. Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: implications for seasonal thermoregulation.

    PubMed

    Sato, Hiroki

    2012-07-01

    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

  14. Effects of Substrate Size and Orientation on Quadrupedal Gait Kinematics in Mouse Lemurs (Microcebus murinus).

    PubMed

    Shapiro, Liza J; Kemp, Addison D; Young, Jesse W

    2016-06-01

    As the smallest living primate, the mouse lemur is a suitable model for reconstructing the locomotor mechanisms by which primate ancestors might have responded to the challenges of an arboreal environment. In this study, we tested the effects of substrate diameter and orientation on quadrupedal gait kinematics in mouse lemurs (Microcebus murinus). Mouse lemurs highly preferred asymmetrical to symmetrical gaits as they moved across a flat board and poles of three diameters (2.5, 1.0, and 0.5 cm), set at horizontal, 30° inclined, and 30° declined orientations. During symmetrical gaits, mouse lemurs used diagonal sequence walking and ambling gaits on the same substrates and at the same duty factors for which some similarly sized nonprimate mammals use lateral sequence gaits, suggesting that reliance on diagonal sequence walking in primates may not be explicitly a response to body size relative to substrate diameter. When using asymmetrical gaits, kinematic adjustments to small diameter and/or nonhorizontal substrates included a preference for transverse gallops over other gaits, the avoidance of whole-body suspensions, increases in limb contact duration, and increases in the time interval between the landing of trailing and leading limbs. All of these adjustments are consistent with increasing locomotor stability by dampening center of mass movements and reducing the forces imparted to the substrate. Like mouse lemurs, small-bodied ancestral primates likely used symmetrical gaits occasionally, but more frequently used asymmetrical gaits that were adjusted in response to challenging substrates. Therefore, asymmetrical gait dynamics should be incorporated into hypotheses addressing early primate locomotor evolution. PMID:27222465

  15. LEMUR: Large European module for solar Ultraviolet Research. European contribution to JAXA's Solar-C mission

    NASA Astrophysics Data System (ADS)

    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

    2012-10-01

    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

  16. Evolutionary history inferred from the de novo assembly of a nonmodel organism, the blue-eyed black lemur

    PubMed Central

    Meyer, Wynn K; Venkat, Aarti; Kermany, Amir R; van de Geijn, Bryce; Zhang, Sidi; Przeworski, Molly

    2015-01-01

    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

  17. Phylogenetic and functional affinities of Babakotia (primates), a fossil lemur from northern Madagascar.

    PubMed Central

    Jungers, W L; Godfrey, L R; Simons, E L; Chatrath, P S; Rakotosamimanana, B

    1991-01-01

    Recent paleontological expeditions to the Ankarana range of northern Madagascar have recovered the partial remains of four individuals of a newly recognized extinct lemur, Babakotia radofilai. Craniodental and postcranial material serve to identify Babakotia as a member of the palaeopropithecids (also including the extinct genera Palaeopropithecus, Archaeoindris, and Mesopropithecus). Living indrids form the sister group to this fossil clade. The postcranial anatomy indicates that Babakotia was a medium-sized (approximately 15 kg) indroid whose inferred positional behaviors were primarily slow climbing and hanging. Although it is probable that a leaping component typified the ancestral positional repertoire of all Malagasy lemurs, the mosaic nature of the locomotor skeleton of Babakotia further suggests that vertical climbing and hang-feeding rather than ricochetal leaping were primitive for indrids and palaeopropithecids and that the dramatic saltatory adaptations of the living indrids postdate the divergence of these two lineages. Images PMID:1924371

  18. Shifting ranges and conservation challenges for lemurs in the face of climate change

    PubMed Central

    Brown, Jason L; Yoder, Anne D

    2015-01-01

    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

  19. Telomere regulation during ageing and tumorigenesis of the grey mouse lemur.

    PubMed

    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

    2015-06-01

    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. PMID:25882681

  20. Cytokine and Antioxidant Regulation in the Intestine of the Gray Mouse Lemur (Microcebus murinus) During Torpor

    PubMed Central

    Tessier, Shannon N.; Katzenback, Barbara A.; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.

    2015-01-01

    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

  1. Cytokine and Antioxidant Regulation in the Intestine of the Gray Mouse Lemur (Microcebus murinus) During Torpor.

    PubMed

    Tessier, Shannon N; Katzenback, Barbara A; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B

    2015-04-01

    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

  2. AMS 14C Dates for Extinct Lemurs from Caves in the Ankarana Massif, Northern Madagascar

    NASA Astrophysics Data System (ADS)

    Simons, Elwyn L.; Burney, David A.; Chatrath, Prithijit S.; Godfrey, Laurie R.; Jungers, William L.; Rakotosamimanana, Berthe

    1995-03-01

    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.

  3. Modeling the origins of mammalian sociality: moderate evidence for matrilineal signatures in mouse lemur vocalizations

    PubMed Central

    2014-01-01

    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

  4. Comparing apples and oranges-the influence of food mechanical properties on ingestive bite sizes in lemurs.

    PubMed

    Hartstone-Rose, Adam; Parkinson, Jennifer A; Criste, Taylor; Perry, Jonathan M G

    2015-07-01

    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. PMID:25727399

  5. Eco-evo-devo of the lemur syndrome: did adaptive behavioral plasticity get canalized in a large primate radiation?

    PubMed Central

    2015-01-01

    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

  6. Torpor and energetic consequences in free-ranging grey mouse lemurs ( Microcebus murinus): a comparison of dry and wet forests

    NASA Astrophysics Data System (ADS)

    Schmid, J.; Speakman, J. R.

    2009-05-01

    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.

  7. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests.

    PubMed

    Schmid, J; Speakman, J R

    2009-05-01

    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. PMID:19229507

  8. Modulation of Gene Expression in Key Survival Pathways During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus.

    PubMed

    Biggar, Kyle K; Wu, Cheng-Wei; Tessier, Shannon N; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B

    2015-04-01

    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

  9. Evolutionary history inferred from the de novo assembly of a nonmodel organism, the blue-eyed black lemur.

    PubMed

    Meyer, Wynn K; Venkat, Aarti; Kermany, Amir R; van de Geijn, Bryce; Zhang, Sidi; Przeworski, Molly

    2015-09-01

    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

  10. Modulation of Gene Expression in Key Survival Pathways During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus

    PubMed Central

    Biggar, Kyle K.; Wu, Cheng-Wei; Tessier, Shannon N.; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.

    2015-01-01

    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

  11. Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs.

    PubMed

    Hohenbrink, Philipp; Radespiel, Ute; Mundy, Nicholas I

    2012-12-01

    Chemosensory genes are frequently the target of positive selection and are often present in large gene families, but little is known about heterogeneity of selection in these cases and its relation to function. Here, we use the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs (Microcebus spp.) as a model system to study patterns of selection of chemosensory genes at several different levels. Mouse lemurs are small nocturnal strepsirrhine primates and have a large (~200 loci) repertoire of V1R loci that are likely important for intraspecific pheromonal communication and interspecific interactions, for example, recognition of predator cues. We investigated signals and patterns of positive selection among the 105 identified full length V1R loci in the gray mouse lemur and within 7 V1R loci amplified across multiple mouse lemur species. Phylogenetic reconstructions of published sequences revealed at least nine monophyletic clusters of V1Rs in gray mouse lemurs that have diversified since the split between lemurs and lorisoid primates. A large majority of clusters evolved under significant positive selection. Similar results were found in V1Rs of closely related greater galagos. Comparison with function of related V1R clusters in mice suggested a potential relationship between receptor function and strength of selection. Interestingly, most codons identified as being under positive selection are located in the extracellular domains of the receptors and hence likely indicate the position of residues involved in ligand binding. Positive selection was also detected within five V1R loci (=71% of analyzed loci) sequenced from 6 to 10 mouse lemur species, indicating ongoing selection within the genus, which may be related to sexual selection and, potentially, speciation processes. Variation in strength of positive selection on V1Rs showed no simple relationship to cluster size. The diversity of V1R loci in mouse lemurs reflects their adaptive evolution and is most

  12. Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past

    PubMed Central

    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.

    2016-01-01

    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

  13. Species concepts, diversity, and evolution in primates: lessons to be learned from mouse lemurs.

    PubMed

    Zimmermann, Elke; Radespiel, Ute

    2014-01-01

    Humans primarily rely on vision when categorizing the world. If you just look at the same-sized but strikingly differently colored Neotropical poison-dart frogs such as strawberry frogs (Fig. ), you would be convinced that they must belong to different species. However, this is an excellent example of a polymorphic species, meaning that although these frogs look quite different, mating decisions are made based on their conspicuous and species-specific advertisements calls, which are not primarily linked to specific color pattern. The situation is quite different among nocturnal primates living in dense forest environments, such as the tiny nocturnal Malagasy mouse lemurs. In this case, even geographically isolated, well-accepted species look superficially quite similar and are therefore often termed cryptic species (Fig. ). Some morphs are a bit larger than others or show minor phenotypic differences, but morph-specific differences are difficult to detect in living subjects. This phenomenon explains why, until the end of the last century, species diversity in mouse lemurs was assumed to be low, with only two morphologically distinct species. Over the last two decades, several international working groups, including our own, undertook a massive island-wide sampling effort, including DNA sequencing and phylogenetic analyses of mouse lemurs. These revealed a 10-fold higher species diversity, with 21 currently described species. Are these new species, mostly defined based on the phylogenetic species concept (sensu Cracraft), or independent evolutionary lineages or, perhaps, only artifacts of taxonomic inflation? What is a species? How can we identify primate species? How and why do species emerge during evolution? PMID:24591134

  14. Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past.

    PubMed

    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

    2016-07-19

    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

  15. Complete mitochondrial genome of the gray mouse lemur, Microcebus murinus (Primates, Cheirogaleidae).

    PubMed

    Lecompte, Emilie; Crouau-Roy, Brigitte; Aujard, Fabienne; Holota, Hélène; Murienne, Jérôme

    2016-09-01

    We report the high-coverage complete mitochondrial genome sequence of the gray mouse lemur Microcebus murinus. The sequencing has been performed on an Illumina Hiseq 2500 platform, with a genome skimming strategy. The total length of this mitogenome is 16 963 bp, containing 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and 1 non-coding region (D-loop region). The genome organization, nucleotide composition and codon usage are similar to those reported from other primate's mitochondrial genomes. The complete mitochondrial genome sequence reported here will be useful for comparative genomics studies in primates. PMID:27158869

  16. Biomedical evaluation of free-ranging red ruffed lemurs (Varecia rubra) within the Masoala National Park, Madagascar.

    PubMed

    Dutton, Christopher J; Junge, Randall E; Louis, Edward E

    2008-03-01

    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. PMID:18432099

  17. Regulation of Torpor in the Gray Mouse Lemur: Transcriptional and Translational Controls and Role of AMPK Signaling.

    PubMed

    Zhang, Jing; Tessier, Shannon N; Biggar, Kyle K; Wu, Cheng-Wei; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B

    2015-04-01

    The gray mouse lemur (Microcebus murinus) is one of few primate species that is able to enter daily torpor or prolonged hibernation in response to environmental stresses. With an emerging significance to human health research, lemurs present an optimal model for exploring molecular adaptations that regulate primate hypometabolism. A fundamental challenge is how to effectively regulate energy expensive cellular processes (e.g., transcription and translation) during transitions to/from torpor without disrupting cellular homeostasis. One such regulatory mechanism is reversible posttranslational modification of selected protein targets that offers fine cellular control without the energetic burden. This study investigates the role of phosphorylation and/or acetylation in regulating key factors involved in energy homeostasis (AMP-activated protein kinase, or AMPK, signaling pathway), mRNA translation (eukaryotic initiation factor 2α or eIF2α, eukaryotic initiation factor 4E or eIF4E, and initiation factor 4E binding protein or 4EBP), and gene transcription (histone H3) in six tissues of torpid and aroused gray mouse lemurs. Our results indicated selective tissue-specific changes of these regulatory proteins. The relative level of Thr172-phosphorylated AMPKα was significantly elevated in the heart but reduced in brown adipose tissue during daily torpor, as compared to the aroused lemurs, implicating the regulation of AMPK activity during daily torpor in these tissues. Interestingly, the levels of the phosphorylated eIFs were largely unaltered between aroused and torpid animals. Phosphorylation and acetylation of histone H3 were examined as a marker for transcriptional regulation. Compared to the aroused lemurs, level of Ser10-phosphorylated histone H3 decreased significantly in white adipose tissue during torpor, suggesting global suppression of gene transcription. However, a significant increase in acetyl-histone H3 in the heart of torpid lemurs indicated a possible

  18. Regulation of Torpor in the Gray Mouse Lemur: Transcriptional and Translational Controls and Role of AMPK Signaling

    PubMed Central

    Zhang, Jing; Tessier, Shannon N.; Biggar, Kyle K.; Wu, Cheng-Wei; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.

    2015-01-01

    The gray mouse lemur (Microcebus murinus) is one of few primate species that is able to enter daily torpor or prolonged hibernation in response to environmental stresses. With an emerging significance to human health research, lemurs present an optimal model for exploring molecular adaptations that regulate primate hypometabolism. A fundamental challenge is how to effectively regulate energy expensive cellular processes (e.g., transcription and translation) during transitions to/from torpor without disrupting cellular homeostasis. One such regulatory mechanism is reversible posttranslational modification of selected protein targets that offers fine cellular control without the energetic burden. This study investigates the role of phosphorylation and/or acetylation in regulating key factors involved in energy homeostasis (AMP-activated protein kinase, or AMPK, signaling pathway), mRNA translation (eukaryotic initiation factor 2α or eIF2α, eukaryotic initiation factor 4E or eIF4E, and initiation factor 4E binding protein or 4EBP), and gene transcription (histone H3) in six tissues of torpid and aroused gray mouse lemurs. Our results indicated selective tissue-specific changes of these regulatory proteins. The relative level of Thr172-phosphorylated AMPKα was significantly elevated in the heart but reduced in brown adipose tissue during daily torpor, as compared to the aroused lemurs, implicating the regulation of AMPK activity during daily torpor in these tissues. Interestingly, the levels of the phosphorylated eIFs were largely unaltered between aroused and torpid animals. Phosphorylation and acetylation of histone H3 were examined as a marker for transcriptional regulation. Compared to the aroused lemurs, level of Ser10-phosphorylated histone H3 decreased significantly in white adipose tissue during torpor, suggesting global suppression of gene transcription. However, a significant increase in acetyl-histone H3 in the heart of torpid lemurs indicated a possible

  19. A complex sensory organ in the nose skin of the prosimian primate Lemur catta.

    PubMed

    Elofsson, Rolf; Tuminaite, Inga; Kröger, Ronald H H

    2015-06-01

    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. PMID:25645577

  20. Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates

    PubMed Central

    Karanth, K. Praveen; Delefosse, Thomas; Rakotosamimanana, Berthe; Parsons, Thomas J.; Yoder, Anne D.

    2005-01-01

    The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded amplifiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close relationship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur. Thus, the classification of the latter in the family Megaladapidae is misleading. By correlating the geographic location of subfossil specimens with relative amplification success, we reconfirm the global trend of increased success rates of ancient DNA recovery from nontropical localities. PMID:15784742

  1. Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates.

    PubMed

    Karanth, K Praveen; Delefosse, Thomas; Rakotosamimanana, Berthe; Parsons, Thomas J; Yoder, Anne D

    2005-04-01

    The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded amplifiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close relationship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur. Thus, the classification of the latter in the family Megaladapidae is misleading. By correlating the geographic location of subfossil specimens with relative amplification success, we reconfirm the global trend of increased success rates of ancient DNA recovery from nontropical localities. PMID:15784742

  2. Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge

    NASA Astrophysics Data System (ADS)

    Kobbe, Susanne; Dausmann, Kathrin H.

    2009-10-01

    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.

  3. A novel feeding behaviour in wild redfronted lemurs (Eulemur rufifrons): depletion of spider nests.

    PubMed

    Schnoell, Anna Viktoria; Fichtel, Claudia

    2013-10-01

    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. PMID:23661028

  4. Testing yawning hypotheses in wild populations of two strepsirrhine species: Propithecus verreauxi and Lemur catta.

    PubMed

    Zannella, Alessandra; Norscia, Ivan; Stanyon, Roscoe; Palagi, Elisabetta

    2015-11-01

    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. PMID:26317594

  5. Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences.

    PubMed

    Pastorini, J; Forstner, M R; Martin, R D

    2000-09-01

    The brown lemurs (Eulemur fulvus) include seven subspecies, whose evolutionary relationships remain contentious. In particular, it is unclear whether the Malagasy and Comorian E. f. fulvus populations are differentiated at the subspecific level (E. f. mayottensis). Furthermore, it has been suggested that E. f. collaris and E. f. albocollaris are separate species. Analyses of approximately 2400 bp of mitochondrial DNA sequence data from part of the COIII gene, together with complete genes for ND3, ND4L, and ND4 and 5 tRNAs, resolved 34 E. fulvus specimens into six clades: ((albocollaris, collaris) (rufus (rufus (fulvus/mayottensis (albifrons/fulvus/sanfordi))))). Based on the information available and our analyses we conclude that E. f. albocollaris and E. f. collaris do not represent species distinct from E. fulvus and that Comorian brown lemurs do not deserve subspecific rank. No genetic differentiation was detected between E. f. albifrons and E. f. sanfordi; on the other hand, there are obviously two separate lineages of E. f. rufus. PMID:10991794

  6. Coordination of Group Movements in Wild Red-fronted Lemurs (Eulemur rufifrons): Processes and Influence of Ecological and Reproductive Seasonality.

    PubMed

    Pyritz, Lennart W; Kappeler, Peter M; Fichtel, Claudia

    2011-12-01

    Group-living species have to coordinate collective actions to maintain cohesion. In primates, spatial movements represent a meaningful model to study group coordination processes across different socio-ecological contexts. We studied 4 groups of red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar, between 2008 and 2010 across different ecological and reproductive seasons. We collected data on ranging patterns using GPS collars and observational data on different predefined parameters of group movements, including initiation, leadership, followership, overtaking events, termination, and travel distances. Cohesion of these relatively small, egalitarian lemur groups was high year-round, but daily path length and home range size varied considerably between ecological seasons, presumably due to long-distance migrations of some groups at the beginning of the rainy season. Individuals of different age and sex classes successfully initiated group movements. However, stable female leadership prevailed year-round, irrespective of ecological and reproductive season, which might be due to higher or more specific energetic requirements of reproduction. In contrast to lemur species with a more despotic social structure, female red-fronted lemurs did not recruit more followers than males. Adult leaders recruited more followers than subadult ones. Further, recruitment success was higher during the peak of the dry season, when predation risk appeared to be higher. Distances of single group movements did not depend on the initiator's sex and age or on ecological seasons. Our results provide new insights into seasonal variability of coordination processes and the role of social dominance in lemur group movements, thereby contributing to a comparative perspective from a primate radiation that evolved group living independently of anthropoids. PMID:22207771

  7. The influence of visitor interaction on the behavior of captive crowned lemurs (Eulemur coronatus) and implications for welfare.

    PubMed

    Jones, H; McGregor, P K; Farmer, H L A; Baker, K R

    2016-05-01

    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. PMID:27142724

  8. Behavioral study in the gray mouse lemur (Microcebus murinus) using compounds considered sweet by humans.

    PubMed

    Schilling, Alain; Danilova, Vicktoria; Hellekant, Goran

    2004-01-01

    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. PMID:14752812

  9. Colour and odour drive fruit selection and seed dispersal by mouse lemurs

    PubMed Central

    Valenta, Kim; Burke, Ryan J.; Styler, Sarah A.; Jackson, Derek A.; Melin, Amanda D.; Lehman, Shawn M.

    2013-01-01

    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

  10. Brown skin disease: A syndrome of dysecdysis in Puerto Rican crested toads (Peltophryne lemur).

    PubMed

    Crawshaw, Graham; Pienkowski, Maria; Lentini, Andrew; Dutton, Christopher; Delnatte, Pauline; Russell, Deanna; Berkvens, Charlene; Barker, Ian; Smith, Dale

    2014-01-01

    The endangered Puerto Rican crested toad (Peltophryne [Bufo] lemur) has been held and bred in zoos for release into protected areas in Puerto Rico since 1982. In 2004, several cases of a novel syndrome of skin changes in toads were noticed at the Toronto Zoo. A total of 21 toads were found to have similar lesions and the condition has been seen in several other groups of toads in subsequent years. Affected toads show an uncharacteristic sheen of dark-brown leathery skin, followed by recurring dysecdysis, reduced appetite, weight loss, and death from secondary causes. Histologically the condition is characterized by epithelial hyperplasia and hyperkeratosis, ulceration, and the presence of superficial mats of bacterial and fungal agents. No etiology has been identified and to date toads have not permanently responded to treatment with various pharmaceutical and nutritional therapies. PMID:25234808

  11. Molar microwear of subfossil lemurs: improving the resolution of dietary inferences.

    PubMed

    Rafferty, K L; Teaford, M F; Jungers, W L

    2002-11-01

    In this study we use molar microwear analyses to examine the trophic distinctions among various taxa of Malagasy subfossil lemurs. High resolution casts of the teeth of Megaladapis, Archaeolemur, Palaeopropithecus, Babakotia, and Hadropithecus were examined under a scanning electron microscope. Megaladapis was undoubtedly a browsing folivore, but there are significant differences between species of this genus. However, dietary specialists appear to be the exception; for example, Palaeopropithecus and Babakotia probably supplemented their leaf-eating with substantial amounts of seed-predation, much like modern indrids. Hadropithecus was decidedly not like the modern gelada baboon, but probably did feed on hard objects. Evidence from microwear and coprolites suggests that Archaeolemur probably had an eclectic diet that differed regionally and perhaps seasonally. Substantial trophic diversity within Madgascar's primate community was diminished by the late Quaternary extinctions of the large-bodied species (>9 kg). PMID:12457853

  12. Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata).

    PubMed

    Stoinski, T S; Drayton, L A; Price, E E

    2011-06-23

    Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates. PMID:21227976

  13. SUMMER AND WINTER VITAMIN D3 LEVELS IN FOUR LEMUR SPECIES HOUSED AT A BRITISH ZOO, WITH REFERENCE TO UVB LEVELS.

    PubMed

    Killick, Rowena; Saunders, Richard; Redrobe, Sharon P

    2015-09-01

    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. PMID:26352953

  14. Determinants of Pair-Living in Red-Tailed Sportive Lemurs (Lepilemur ruficaudatus)

    PubMed Central

    Hilgartner, Roland; Fichtel, Claudia; Kappeler, Peter M; Zinner, Dietmar

    2012-01-01

    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

  15. A Genome Sequence Resource for the Aye-Aye (Daubentonia madagascariensis), a Nocturnal Lemur from Madagascar

    PubMed Central

    Perry, George H.; Reeves, Darryl; Melsted, Páll; Ratan, Aakrosh; Miller, Webb; Michelini, Katelyn; Louis, Edward E.; Pritchard, Jonathan K.; Mason, Christopher E.; Gilad, Yoav

    2012-01-01

    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

  16. A genome sequence resource for the aye-aye (Daubentonia madagascariensis), a nocturnal lemur from Madagascar.

    PubMed

    Perry, George H; Reeves, Darryl; Melsted, Páll; Ratan, Aakrosh; Miller, Webb; Michelini, Katelyn; Louis, Edward E; Pritchard, Jonathan K; Mason, Christopher E; Gilad, Yoav

    2012-01-01

    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

  17. Hearing and age-related changes in the gray mouse lemur.

    PubMed

    Schopf, Christian; Zimmermann, Elke; Tünsmeyer, Julia; Kästner, Sabine B R; Hubka, Peter; Kral, Andrej

    2014-12-01

    In order to examine auditory thresholds and hearing sensitivity during aging in the gray mouse lemur (Microcebus murinus), suggested to represent a model for early primate evolution and Alzheimer research, we applied brainstem-evoked response audiometry (BERA), traditionally used for screening hearing sensitivity in human babies. To assess the effect of age, we determined auditory thresholds in two age groups of adult mouse lemurs (young adults, 1-5 years; old adults, ≥7 years) using clicks and tone pips. Auditory thresholds indicated frequency sensitivity from 800 Hz to almost 50 kHz, covering the species tonal communication range with fundamentals from about 8 to 40 kHz. The frequency of best hearing at 7.9 kHz was slightly lower than that and coincided with the dominant frequencies of communication signals of a predator. Aging shifted auditory thresholds in the range between 2 and 50.4 kHz significantly by 12-27 dB. This mild presbyacusis, expressed in a drop of amplitudes of BERA signals, but not discernible in latencies of responses, suggests a metabolic age-related decrease potentially combined with an accompanying degeneration of the cochlear nerve. Our findings on hearing range of this species support the hypothesis that predation was a driving factor for the evolution of hearing in small ancestral primates. Likewise, results provide the empirical basis for future approaches trying to differentiate peripheral from central factors when studying Alzheimer's disease-like pathologies in the aging brain. PMID:25112886

  18. Regional, seasonal and interspecific variation in 15N and 13C in sympatric mouse lemurs

    NASA Astrophysics Data System (ADS)

    Rakotondranary, S. Jacques; Struck, Ulrich; Knoblauch, Christian; Ganzhorn, Jörg U.

    2011-11-01

    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.

  19. Root sepsis associated with insect-dwelling Sebaldella termitidis in a lesser dwarf lemur (Cheirogaleus medius).

    PubMed

    Eisenberg, Tobias; Glaeser, Stefanie P; Kämpfer, Peter; Schauerte, Nicole; Geiger, Christina

    2015-12-01

    Sebaldella termitidis is a rare fastidious microorganism of the Leptotrichiaceae family. A variety of closely related species are associated with severe and even life-threatening disease in humans and animals, such as Streptobacillus moniliformis, the etiological organism of rat-bite fever as well as members of Leptotrichia spp. and Sneathia sanguinegens, which have been reported from cases of septicaemia. In contrast, since its description some 50 years ago, S. ermitidis has so far never been reported as a vertebrate pathogen, nor has it been found aside from its natural termite host. A lesser dwarf lemur was presented with unilateral facial inflammation originating from rotten maxillary teeth and septic root abscess. Surgical intervention and root extraction significantly improved the clinical cause in that a pus-filled cavity underneath the right eye could be drained, sampled and flushed. Bacteria displaying substantial characteristics of S. termitidis were cultured from the sampled pus. Morphological features observed included strictly anaerobic regular Gram-negative rods. Significant shared biochemical properties included negative reactions for cytochrome oxidase, catalase, urease, nitrate reduction and indole production. Furthermore, 16S rRNA gene sequencing revealed 99.9 % sequence homology to the S. termitidis type strain NCTC 11300(T), from which it, nevertheless, differed with respect to rep and rep- and RAPD-PCR profiles. An affiliation of the lemur isolate described in this study with the type strain of S. termitidis as well as a clear discrimination from other members of the Leptotrichiaceae could also be confirmed by matrix-assisted laser desorption/ionization time-of flight mass spectrometry and Fourier transform-infrared spectroscopy. This is the first evidence for clinical disease caused by S. termitidis in a vertebrate species indicating a broader host spectrum of this rarely encountered microorganism. PMID:26377576

  20. The socio-matrix reloaded: from hierarchy to dominance profile in wild lemurs

    PubMed Central

    Norscia, Ivan

    2015-01-01

    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

  1. New developments in the behavioral ecology and conservation of ruffed lemurs (Varecia).

    PubMed

    Vasey, Natalie

    2005-05-01

    The papers in this issue were presented at a symposium during the 25th Annual Meeting of the American Society of Primatologists held in Oklahoma City, Oklahoma, in June 2002. This symposium brought together many of the scientists who have contributed to our knowledge of ruffed lemur ecology, behavior, and conservation in the past decade. One objective was to share and compare key findings about ruffed lemurs (Varecia) resulting from long-term field studies at various sites in Madagascar. A second objective was to cross-fertilize work being done in the wild with that being done in captivity, with the aim of advancing a common conservation mission for this critically endangered genus. Varecia is a prime candidate for synthetic assessments such as these because it has now been studied in both the northern and southern reaches of its geographic range, and has also been the focus of a captive-to-wild reinforcement project. The papers in this issue contribute to 1) the establishment of reference ranges for a suite of physiological parameters in healthy wild Varecia populations; 2) environmental enrichment aimed at preserving species-typical behaviors in captivity; 3) an understanding of how forest structure, floristic composition, and fruiting phenology in areas with differing disturbance histories correlate with the natural occurrence and abundance of Varecia; 4) primary knowledge concerning dominance relations between the sexes and group leadership in wild Varecia; and 5) primary knowledge concerning how wild Varecia, with their unusual reproductive pattern and heavy reliance on fruit, modulate their activity budgets seasonally and in tandem with reproductive stages. PMID:15898070

  2. Necrotizing Meningoencephalitis in a Captive Black and White Ruffed Lemur (Varecia variegata variegata) Caused by Acanthamoeba T4 Genotype.

    PubMed

    Gaide, N; Pelandakis, M; Robveille, C; Albaric, O; Jouvion, G; Souchon, M; Risler, A; Abadie, J

    2015-11-01

    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. PMID:26297109

  3. Resource seasonality and reproduction predict fission-fusion dynamics in black-and-white ruffed lemurs (Varecia variegata).

    PubMed

    Baden, Andrea L; Webster, Timothy H; Kamilar, Jason M

    2016-02-01

    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. PMID:26606154

  4. Characterization of blood biochemical markers during aging in the Grey Mouse Lemur (Microcebus murinus): impact of gender and season

    PubMed Central

    2012-01-01

    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

  5. The Use of an Invasive Species Habitat by a Small Folivorous Primate: Implications for Lemur Conservation in Madagascar.

    PubMed

    Eppley, Timothy M; Donati, Giuseppe; Ramanamanjato, Jean-Baptiste; Randriatafika, Faly; Andriamandimbiarisoa, Laza N; Rabehevitra, David; Ravelomanantsoa, Robertin; Ganzhorn, Jörg U

    2015-01-01

    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

  6. Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse.

    PubMed

    Donati, G; Lunardini, A; Kappeler, P M; Borgognini Tarli, S M

    2001-02-01

    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. PMID:11170168

  7. The Use of an Invasive Species Habitat by a Small Folivorous Primate: Implications for Lemur Conservation in Madagascar

    PubMed Central

    Eppley, Timothy M.; Donati, Giuseppe; Ramanamanjato, Jean-Baptiste; Randriatafika, Faly; Andriamandimbiarisoa, Laza N.; Rabehevitra, David; Ravelomanantsoa, Robertin; Ganzhorn, Jörg U.

    2015-01-01

    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

  8. Touchscreen-Based Cognitive Tasks Reveal Age-Related Impairment in a Primate Aging Model, the Grey Mouse Lemur (Microcebus murinus)

    PubMed Central

    2014-01-01

    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. PMID:25299046

  9. Discovery of Sympatric Dwarf Lemur Species in the High-Altitude Rain Forest of Tsinjoarivo, Eastern Madagascar: Implications for Biogeography and Conservation

    PubMed Central

    Blanco, Marina B.; Godfrey, Laurie R.; Rakotondratsima, Mamihasimbola; Rahalinarivo, Vololonirina; Samonds, Karen E.; Raharison, Jean-Luc; Irwin, Mitchell T.

    2009-01-01

    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

  10. The hidden matrilineal structure of a solitary lemur: implications for primate social evolution.

    PubMed Central

    Kappeler, Peter M; Wimmer, Barbara; Zinner, Dietmar; Tautz, Diethard

    2002-01-01

    Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious. PMID:12350262

  11. Lemur Tyrosine Kinase 2, a novel target in prostate cancer therapy.

    PubMed

    Shah, Kalpit; Bradbury, Neil A

    2015-06-10

    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

  12. Eulemur, me lemur: the evolution of scent-signal complexity in a primate clade.

    PubMed

    delBarco-Trillo, Javier; Sacha, Caitlin R; Dubay, George R; Drea, Christine M

    2012-07-01

    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. PMID:22641829

  13. Deficits of psychomotor and mnesic functions across aging in mouse lemur primates

    PubMed Central

    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

    2015-01-01

    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

  14. Need for speed: Sexual maturation precedes social maturation in gray mouse lemurs.

    PubMed

    Hohenbrink, Sarah; Zimmermann, Elke; Radespiel, Ute

    2015-10-01

    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. PMID:26119105

  15. True lemurs…true species - species delimitation using multiple data sources in the brown lemur complex

    PubMed Central

    2013-01-01

    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

  16. Daily rhythms of core temperature and locomotor activity indicate different adaptive strategies to cold exposure in adult and aged mouse lemurs acclimated to a summer-like photoperiod.

    PubMed

    Terrien, Jeremy; Zizzari, Philippe; Epelbaum, Jacques; Perret, Martine; Aujard, Fabienne

    2009-07-01

    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

  17. Functional promiscuity in a mammalian chemosensory system: extensive expression of vomeronasal receptors in the main olfactory epithelium of mouse lemurs.

    PubMed

    Hohenbrink, Philipp; Dempewolf, Silke; Zimmermann, Elke; Mundy, Nicholas I; Radespiel, Ute

    2014-01-01

    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

  18. Sleep deprivation impairs spatial retrieval but not spatial learning in the non-human primate grey mouse lemur.

    PubMed

    Rahman, Anisur; Languille, Solène; Lamberty, Yves; Babiloni, Claudio; Perret, Martine; Bordet, Regis; Blin, Olivier J; Jacob, Tom; Auffret, Alexandra; Schenker, Esther; Richardson, Jill; Pifferi, Fabien; Aujard, Fabienne

    2013-01-01

    A bulk of studies in rodents and humans suggest that sleep facilitates different phases of learning and memory process, while sleep deprivation (SD) impairs these processes. Here we tested the hypothesis that SD could alter spatial learning and memory processing in a non-human primate, the grey mouse lemur (Microcebus murinus), which is an interesting model of aging and Alzheimer's disease (AD). Two sets of experiments were performed. In a first set of experiments, we investigated the effects of SD on spatial learning and memory retrieval after one day of training in a circular platform task. Eleven male mouse lemurs aged between 2 to 3 years were tested in three different conditions: without SD as a baseline reference, 8 h of SD before the training and 8 h of SD before the testing. The SD was confirmed by electroencephalographic recordings. Results showed no effect of SD on learning when SD was applied before the training. When the SD was applied before the testing, it induced an increase of the amount of errors and of the latency prior to reach the target. In a second set of experiments, we tested the effect of 8 h of SD on spatial memory retrieval after 3 days of training. Twenty male mouse lemurs aged between 2 to 3 years were tested in this set of experiments. In this condition, the SD did not affect memory retrieval. This is the first study that documents the disruptive effects of the SD on spatial memory retrieval in this primate which may serve as a new validated challenge to investigate the effects of new compounds along physiological and pathological aging. PMID:23717620

  19. Shades of gray mouse lemurs: Ontogeny of female dominance and dominance-related behaviors in a nocturnal primate.

    PubMed

    Hohenbrink, Sarah; Koberstein-Schwarz, Maren; Zimmermann, Elke; Radespiel, Ute

    2015-11-01

    The ontogeny and establishment of dominance relationships in young individuals have been investigated in various group-living, diurnal primates but respective information is almost entirely lacking for nocturnal, non-gregarious species. As in many other mammals male primates often represent the dominant sex, but the opposite phenomenon (female dominance) is particularly frequent in lemurs, although almost nothing is known about its development. Therefore, we investigated the development of intersexual dominance in parallel to age-related changes in other relevant behaviors in the gray mouse lemur, a solitary forager with female dominance. In particular, the temporal trajectories of social play, marking behavior, social tolerance, and agonistic behaviors were characterized in captive dyads of three different age categories (ACs), among juveniles (ACI: 4-5 months, N = 6), adolescents (ACII: 8-9 months, N = 8) and young adults (ACIII: 12-13 months, N = 8). Data were collected during a series of three encounter experiments between one male and one female per dyad and age category (total observation time: 49.5 hr). Play behavior was observed in all age classes, although the number of playing dyads decreased with increasing age. A significant age-dependent increase in marking behavior was found in females, especially in substrate rubbing and urine washing, but not in males. Although conflict rates did not differ significantly between ACs, females started to win more conflicts from ACII onwards, and social tolerance decreased partly with increasing age. Clear dominance relationships were not observed in ACI and first indications of dominant females were found in ACII with an increasing number in ACIII. This study provides first information about the ontogeny of female dominance in a nocturnal primate and shows that this behavior develops relatively late during ontogeny. In conclusion, this study provides evidence for significant changes in the social lives

  20. Species discovery and validation in a cryptic radiation of endangered primates: coalescent-based species delimitation in Madagascar's mouse lemurs.

    PubMed

    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

    2016-05-01

    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. PMID:26946180

  1. Functional promiscuity in a mammalian chemosensory system: extensive expression of vomeronasal receptors in the main olfactory epithelium of mouse lemurs

    PubMed Central

    Hohenbrink, Philipp; Dempewolf, Silke; Zimmermann, Elke; Mundy, Nicholas I.; Radespiel, Ute

    2014-01-01

    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

  2. Effects of Resveratrol on Daily Rhythms of Locomotor Activity and Body Temperature in Young and Aged Grey Mouse Lemurs

    PubMed Central

    Dal-Pan, Alexandre; Languille, Solène; Aujard, Fabienne

    2013-01-01

    In several species, resveratrol, a polyphenolic compound, activates sirtuin proteins implicated in the regulation of energy balance and biological clock processes. To demonstrate the effect of resveratrol on clock function in an aged primate, young and aged mouse lemurs (Microcebus murinus) were studied over a 4-week dietary supplementation with resveratrol. Spontaneous locomotor activity and daily variations in body temperature were continuously recorded. Reduction in locomotor activity onset and changes in body temperature rhythm in resveratrol-supplemented aged animals suggest an improved synchronisation on the light-dark cycle. Resveratrol could be a good candidate to restore the circadian rhythms in the elderly. PMID:23983895

  3. Assessment of Polycyclic Aromatic Hydrocarbon Contamination of Breeding Pools Utilized by the Puerto Rican Crested Toad, Peltophryne lemur

    PubMed Central

    Gjeltema, Jenessa; Stoskopf, Michael; Shea, Damian; De Voe, Ryan

    2012-01-01

    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

  4. The Season for Peace: Reconciliation in a Despotic Species (Lemur catta).

    PubMed

    Palagi, Elisabetta; Norscia, Ivan

    2015-01-01

    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

  5. The Season for Peace: Reconciliation in a Despotic Species (Lemur catta)

    PubMed Central

    Palagi, Elisabetta; Norscia, Ivan

    2015-01-01

    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

  6. The ranging behavior of Lemur catta in the region of Cap Sainte-Marie, Madagascar.

    PubMed

    Kelley, Elizabeth A

    2013-01-01

    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. PMID:23180618

  7. 76 FR 61733 - Endangered Species; Receipt of Applications for Permit

    Federal Register 2010, 2011, 2012, 2013, 2014

    2011-10-05

    ... generic tiger), Hylobatidae, Tapiridae, Gruidae, Crocodylidae. Species: Ring-tailed lemur (Lemur catta), Black and white ruffed lemur (Varecia variegata), Parma wallaby (Macropus parma), Somali wild ass...

  8. 76 FR 66954 - Endangered Species; Receipt of Applications for Permit

    Federal Register 2010, 2011, 2012, 2013, 2014

    2011-10-28

    ...). radiated tortoise (Astrochelys radiata). Red-crowned crane (Grus japonica). ring-tailed lemur (Lemur catta). black lemur (Eulemur macaco). brown lemur (Eulemur fulvus). black and white ruffed lemur (Varecia... tortoise (Chelonoids nigra). radiated tortoise (Astrochelys radiate). ring-tailed lemur (Lemur...

  9. Life history profiles for 27 strepsirrhine primate taxa generated using captive data from the Duke Lemur Center

    PubMed Central

    Zehr, Sarah M; Roach, Richard G; Haring, David; Taylor, Julie; Cameron, Freda H; Yoder, Anne D

    2014-01-01

    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

  10. Patterns of Dental Macrowear in Subfossil Lemur catta from Ankilitelo Cave, Madagascar: Indications of Ecology and Habitat Use over Time.

    PubMed

    Cuozzo, Frank P; Sauther, Michelle L

    2015-01-01

    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. PMID:26022310

  11. Nocturnal light environments influence color vision and signatures of selection on the OPN1SW opsin gene in nocturnal lemurs.

    PubMed

    Veilleux, Carrie C; Louis, Edward E; Bolnick, Deborah A

    2013-06-01

    Although loss of short-wavelength-sensitive (SWS) cones and dichromatic color vision in mammals has traditionally been linked to a nocturnal lifestyle, recent studies have identified variation in selective pressure for the maintenance of the OPN1SW opsin gene (and thus, potentially dichromacy) among nocturnal mammalian lineages. These studies hypothesize that purifying selection to retain SWS cones may be associated with a selective advantage for nocturnal color vision under certain ecological conditions. In this study, we explore the effect of nocturnal light environment on OPN1SW opsin gene evolution in a diverse sample of nocturnal lemurs (106 individuals, 19 species, and 5 genera). Using both phylogenetic and population genetic approaches, we test whether species from closed canopy rainforests, which are impoverished in short-wavelength light, have experienced relaxed selection compared with species from open canopy forests. We identify clear signatures of differential selection on OPN1SW by habitat type. Our results suggest that open canopy species generally experience strong purifying selection to maintain SWS cones. In contrast, closed canopy species experience weaker purifying selection or a relaxation of selection on OPN1SW. We also found evidence of nonfunctional OPN1SW genes in all Phaner species and in Cheirogaleus medius, implying at least three independent losses of SWS cones in cheirogaleids. Our results suggest that the evolution of color vision in nocturnal lemurs has been influenced by nocturnal light environment. PMID:23519316

  12. LEMUR (Large European Module for solar Ultraviolet Research): a VUV imaging spectrograph for the JAXA Solar-C Mission

    NASA Astrophysics Data System (ADS)

    Korendyke, Clarence M.; Teriaca, Luca; Doschek, George A.; Harra, Louise K.; Schühle, Udo H.; Shimizu, Toshifumi

    2011-10-01

    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.

  13. Induction of Antioxidant and Heat Shock Protein Responses During Torpor in the Gray Mouse Lemur, Microcebus murinus.

    PubMed

    Wu, Cheng-Wei; Biggar, Kyle K; Zhang, Jing; Tessier, Shannon N; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B

    2015-04-01

    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

  14. Induction of Antioxidant and Heat Shock Protein Responses During Torpor in the Gray Mouse Lemur, Microcebus murinus

    PubMed Central

    Wu, Cheng-Wei; Biggar, Kyle K.; Zhang, Jing; Tessier, Shannon N.; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.

    2015-01-01

    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

  15. On-Going Frontal Alpha Rhythms Are Dominant in Passive State and Desynchronize in Active State in Adult Gray Mouse Lemurs

    PubMed Central

    Rahman, Anisur; Lamberty, Yves; Bordet, Regis; Richardson, Jill C.; Forloni, Gianluigi; Drinkenburg, Wilhelmus; Lopez, Susanna; Aujard, Fabienne; Babiloni, Claudio; Pifferi, Fabien

    2015-01-01

    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

  16. On-Going Frontal Alpha Rhythms Are Dominant in Passive State and Desynchronize in Active State in Adult Gray Mouse Lemurs.

    PubMed

    Infarinato, Francesco; Rahman, Anisur; Del Percio, Claudio; Lamberty, Yves; Bordet, Regis; Richardson, Jill C; Forloni, Gianluigi; Drinkenburg, Wilhelmus; Lopez, Susanna; Aujard, Fabienne; Babiloni, Claudio; Pifferi, Fabien

    2015-01-01

    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

  17. MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener.

    PubMed

    Pechouskova, Eva; Dammhahn, Melanie; Brameier, Markus; Fichtel, Claudia; Kappeler, Peter M; Huchard, Elise

    2015-04-01

    The polymorphism of immunogenes of the major histocompatibility complex (MHC) is thought to influence the functional plasticity of immune responses and, consequently, the fitness of populations facing heterogeneous pathogenic pressures. Here, we evaluated MHC variation (allelic richness and divergence) and patterns of selection acting on the two highly polymorphic MHC class II loci (DRB and DQB) in the endangered primate Madame Berthe's mouse lemur (Microcebus berthae). Using 454 pyrosequencing, we examined MHC variation in a total of 100 individuals sampled over 9 years in Kirindy Forest, Western Madagascar, and compared our findings with data obtained previously for its sympatric congener, the grey mouse lemur (Microcebus murinus). These species exhibit a contrasting ecology and demography that were expected to affect MHC variation and molecular signatures of selection. We found a lower allelic richness concordant with its low population density, but a similar level of allelic divergence and signals of historical selection in the rare feeding specialist M. berthae compared to the widespread generalist M. murinus. These findings suggest that demographic factors may exert a stronger influence than pathogen-driven selection on current levels of allelic richness in M. berthae. Despite a high sequence similarity between the two congeners, contrasting selection patterns detected at DQB suggest its potential functional divergence. This study represents a first step toward unravelling factors influencing the adaptive divergence of MHC genes between closely related but ecologically differentiated sympatric lemurs and opens new questions regarding potential functional discrepancy that would explain contrasting selection patterns detected at DQB. PMID:25687337

  18. Biomedical evaluation of two sympatric lemur species (Propithecus verreauxi deckeni and Eulemur fulvus rufus) in Tsiombokibo Classified Forest, Madagascar.

    PubMed

    Junge, Randall E; Louis, Edward E

    2005-12-01

    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. PMID:17312713

  19. Dietary palmitate and linoleate oxidations, oxidative stress, and DNA damage differ according to season in mouse lemurs exposed to a chronic food deprivation.

    PubMed

    Giroud, Sylvain; Perret, Martine; Gilbert, Caroline; Zahariev, Alexandre; Goudable, Joëlle; Le Maho, Yvon; Oudart, Hugues; Momken, Iman; Aujard, Fabienne; Blanc, Stéphane

    2009-10-01

    This study investigated the extent to which the increase in torpor expression in the grey mouse lemur, due to graded food restriction, is modulated by a trade-off between a whole body sparing of polyunsaturated dietary fatty acids and the related oxidative stress generated during daily torpor. We measured changes in torpor frequency, total energy expenditure (TEE), linoleate (polyunsaturated fatty acid) and palmitate (saturated fatty acid) oxidation, hexanoyl-lysine (HEL; the product of linoleate peroxidation), and 8-hydroxydeoxyguanosine (8OHdG; a marker of DNA damage). Animals under summer-acclimated long days (LD) or winter-acclimated short days (SD) were exposed to a 40% (LD40 and SD40) and 80% (LD80 and SD80) 35-day calorie restriction (CR). During CR, all groups reduced their body mass, but LD80 animals reached survival-threatened levels at day 22 and were then excluded from the CR trial. Only SD mouse lemurs increased their torpor frequency with CR and displayed a decrease in their TEE adjusted for fat-free mass. After CR, SD40 mouse lemurs shifted the dietary fatty acid oxidation toward palmitate and spared linoleate. Such a shift was not observed in LD animals and during severe CR, during which oxidation of both dietary fatty acids was increased. Concomitantly, HEL increased in both LD40 and SD80 groups, whereas DNA damage was only seen in SD80 food-restricted animals. HEL correlated positively with linoleate oxidation confirming in vivo the substrate/product relationship demonstrated in vitro, and negatively with TEE adjusted for fat-free mass, suggesting higher oxidative stress associated with increased torpor expression. This suggests a seasonal-dependant, cost-benefit trade-off between maximizing torpor propensity and minimizing oxidative stress that is associated with a shift toward sparing of dietary polyunsaturated fatty acids that is dependent upon the expression of a winter phenotype. PMID:19625694

  20. ESTIMATED COMPOSITION OF DIETS FED TO CAPTIVE BLACK-AND-WHITE RUFFED LEMURS (VARECIA VARIEGATA) AT 33 U.S. ZOOLOGICAL INSTITUTIONS.

    PubMed

    Donadeo, Brett C; Kerr, Katherine R; Morris, Cheryl L; Swanson, Kelly S

    2016-03-01

    Data on captive diets for black-and-white ruffed lemurs (Varecia variegata) are limited. Information on food items used, inclusion amounts, and the chemical composition of diets is needed to improve the management of nutrition-related health problems seen in captive lemurs (e.g., obesity) that have not been reported in their wild counterparts. To determine the ingredient and nutrient composition of diets for captive V. variegata, U.S. zoological institutions were surveyed. Chemical composition of reported diets was estimated using Nutritionist Pro™ (Axxya Systems, Stafford, Texas 77477, USA), and these values were compared numerically to wild lemur diets from the literature. Institutions included from six to greater than 30 different ingredients in their diets, including fruits (0.0-84.1%), vegetables (7.5-70.0%), greens (1.0-28.5%), and commercially available feeds (1.5-68.6%). Nutrient concentrations of captive diets ranged as follows: dry matter (DM), 14.5-67.6%; organic matter, 93.1-97.2% DM basis (DMB); crude protein, 7.9-23.9% DMB; fat, 2.0-6.5% DMB; total dietary fiber, 10.1-28.1% DMB; and N-free extract, 38.9-74.4% DMB. Captive diets had lower fat and total dietary fiber and higher protein and N-free extract compared to wild fruit items from Madagascar. Reducing the amount of fruit in captive diets for V. variegata would be expected to decrease digestible carbohydrate content and increase fiber content of these diets, which has implications for the prevalence of obesity in captive animals. PMID:27010276

  1. The Grey Mouse Lemur Uses Season-Dependent Fat or Protein Sparing Strategies to Face Chronic Food Restriction

    PubMed Central

    Giroud, Sylvain; Perret, Martine; Stein, Peter; Goudable, Joëlle; Aujard, Fabienne; Gilbert, Caroline; Robin, Jean Patrice; Le Maho, Yvon; Zahariev, Alexandre

    2010-01-01

    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. PMID:20098678

  2. Primate Torpor: Regulation of Stress-activated Protein Kinases During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus.

    PubMed

    Biggar, Kyle K; Wu, Cheng-Wei; Tessier, Shannon N; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B

    2015-04-01

    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

  3. Primate Torpor: Regulation of Stress-activated Protein Kinases During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus

    PubMed Central

    Biggar, Kyle K.; Wu, Cheng-Wei; Tessier, Shannon N.; Zhang, Jing; Pifferi, Fabien; Perret, Martine; Storey, Kenneth B.

    2015-01-01

    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

  4. Baylisascaris procyonis larva migrans in two white-headed lemurs (Eulemur albifrons) in Spain and response to treatment derived from a human pediatric protocol.

    PubMed

    Jimenez Martinez, Maria-Angeles; Valderrabano Cano, Esther; Rois, Jose L

    2015-06-15

    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. PMID:25936436

  5. Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar

    PubMed Central

    2013-01-01

    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

  6. Long-chain n-3 PUFAs from fish oil enhance resting state brain glucose utilization and reduce anxiety in an adult nonhuman primate, the grey mouse lemur.

    PubMed

    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

    2015-08-01

    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. 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

  7. Long-chain n-3 PUFAs from fish oil enhance resting state brain glucose utilization and reduce anxiety in an adult nonhuman primate, the grey mouse lemur

    PubMed Central

    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

    2015-01-01

    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

  8. Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel's sifaka and mongoose lemur.

    PubMed

    Taufik, Epi; Fukuda, Kenji; Senda, Akitsugu; Saito, Tadao; Williams, Cathy; Tilden, Chris; Eisert, Regina; Oftedal, Olav; Urashima, Tadasu

    2012-04-01

    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. PMID:22311613

  9. 76 FR 54480 - Endangered Species; Receipt of Applications for Permit

    Federal Register 2010, 2011, 2012, 2013, 2014

    2011-09-01

    ... gorilla), white- cheeked gibbon (Hylobates leucogenys), Siamang (Hylobates syndactylus), ring-tailed lemur (Lemur catta), bonobo (Pan paniscus), chimpanzee (Pan troglodytes), and Sumatran orangutan...

  10. Anatomy is important, but need not be destiny: novel uses of the thumb in aye-ayes compared to other lemurs.

    PubMed

    Pellis, Sergio M; Pellis, Vivien C

    2012-06-01

    Aye-ayes (Daubentonia madagascerensis) have highly specialized hands with long digits, especially the thin middle one (D3), which is used for extracting food, such as beetle larvae, under bark. Due to the elongation of their fingers, including the thumb, it is presumed that aye-ayes have a rather limited capacity for delicate manipulation of objects. However, studies have reported independent movement of digits D3 and D4, and one report noted a seemingly independent thumb (D1) movement in holding food. Sixteen captive adult aye-ayes were videotaped feeding on a diverse range of foods so as to document how the thumb is used during food holding. To determine if the patterns observed were unique to aye-ayes, 24 individuals from 9 other species of lemurs were also videotaped. Two patterns of thumb use idiosyncratic to aye-ayes and one other lemur, the sifaka (Propithecus verreauxi), were identified: (1) when holding a food item in one hand, the thumb was used to secure the food, with the other digits playing a secondary role; (2) when holding a food item with both hands, the thumbs once again took a predominant role in securing the food. In the majority of these cases, whether held by one or two thumbs, the thumbs curled around the item, but some descriptive evidence is provided that suggests that aye-ayes exaggerate the role of the thumbs by shifting the hold to the outer edge. The novel uses of the thumbs in aye-ayes demonstrate that brain mechanisms can sometimes override the behavioral (or motor) limitations imposed by the morphology of the body. PMID:21924295