Mahafaly Special Reserve Research Articles

The effects of feeding frequency on jaw loading in two lemur species.

Studies on oral processing are often snapshots of behaviors that examine feeding through individual bouts. In this study, we expand on our previous work comparing bite/chew variables per feeding bout to summed daily biting, chewing, and food intake to interpret loading that could have potential morphological effects. We observed sympatric Lemur catta and Propithecus verreauxi over two field seasons in the dry forest of Bezà Mahafaly Special Reserve in southwestern Madagascar. Bite and chew rates determined from videos filmed during observations were multiplied with time spent feeding on specific foods during focal follows to calculate daily values for each feeding bout. Food mechanical properties (FMPs) were tested on dietary items with a portable tester. We contrasted daily bite/chew numbers and intake with FMPs, species, season, and food shape. Daily bite and chew numbers increased with maximum, but not average, food toughness. Daily intake decreased with average and maximum toughness. Season had a strong effect on daily bites and chews, but not on intake. Food shape influenced intake and total bite and chew numbers. The lemur species did not differ in our models. Maximum food toughness impacted feeding behaviors and intake, which is consistent with higher loads having a greater effect on morphology. In contrast to feeding per bout, cumulative biting and chewing did not differ between species; taking feeding frequency into consideration affects interpretation of jaw loading. Finally, biting, as much as chewing, may generate strains that impact morphology.

Potential evolutionary body size reduction in a Malagasy primate (Propithecus verreauxi) in response to human size‐selective hunting pressure

AbstractObjectivesThe Holocene arrival of humans on Madagascar precipitated major changes to the island's biodiversity. The now‐extinct, endemic “subfossil” megafauna of Madagascar were likely hunted by early human inhabitants. Perhaps in part due to preferential hunting of larger prey, no surviving endemic species on Madagascar is >10 kg. Moreover, some subfossil bones of extant lemurs are considerably larger than those of the modern members of their species, but subfossil versus modern locale differences for the comparisons conducted to date lead to uncertainty about whether these size differences reflect in situ change or pre‐existing ecogeographic variation. Here, we revisited this question with samples from nearby locales.Materials and MethodsWe used high‐resolution 3D scan data to conduct comparative morphological analyses of subfossil and modern skeletal remains of one of the larger extant lemurs, Verreaux's sifakas (Propithecus verreauxi) from subfossil and modern sites only ~10 km apart: Taolambiby (bones dated to 725–560—1075–955 cal. years before present) and Beza Mahafaly Special Reserve, respectively.ResultsThe mean aggregate score for all subfossil elements (n = 12; 0.089 ± 0.117) is significantly greater than that for the modern individuals (n = 31; 0.009 ± 0.045; t‐test; p = 0.039). We found that the average subfossil sifaka bone is ~9% larger than that of modern sifakas (permutation test p = 0.037).DiscussionWe cannot yet conclude whether this size difference reflects evolutionary change or an archaeological aggregation/taphonomic process. However, if this is a case of phyletic dwarfism in response to human size‐selective harvesting pressures then the estimated rate of change is greater than those previously calculated for other archaeological cases of this phenomenon.

Agonistic vocalization behaviour in the male ring-tailed lemur (Lemur catta).

Vocalizations are used by group-living animals as aggressive and submissive signals during agonistic interactions, and are also used to maintain dominance hierarchies in many species. For gregarious strepsirrhines with large vocal repertoires and differentiated dominance ranks like the ring-tailed lemur (Lemur catta), agonistic vocalization use is important to study to better understand their social adaptations.To determine whether ring-tailed lemur vocalizations such as the yip, cackle, twitter, chutter, and plosive bark were used as aggressive or submissive signals during agonism and uttered at different rates by males of differing dominance ranks and ages, 565 h of focal data were collected on 31 individual males aged ≥ 1 year from Beza Mahafaly Special Reserve, Madagascar. Yip, cackle, and twitter vocalizations were consistently used during agonistic submissive interactions with both males and females, chutter vocalizations were used during aggressive agonistic interactions with males and submissive agonistic interactions with males and females, and plosive bark vocalizations were used across behavioural contexts but not particularly during agonism. Males of all ages employed all vocalizations, and while low-ranking males uttered yip calls at higher rates, males of all dominance ranks uttered cackle, twitter, chutter, and plosive bark vocalizations. These results advance our knowledge of how male lemurs utilize agonistic vocalizations to maintain inter-individual relationships with males and females, and improve our overall understanding of the function of different agonistic vocalizations in wild lemurs.

Plant Species Fed on by Wild Ring-Tailed Lemurs (Lemur catta) at Nine Sites

A key aspect of a primate’s ecology is its food source, the very nature of which is spatially and seasonally dependent and may be affected by anthropic pressures. One of the most endangered, yet best-studied, strepsirrhine primates is the ring-tailed lemur (Lemur catta), a species that has experienced significant human-induced habitat loss over many decades. To help understand feeding variability across time and space, I present a literature review of plant species (and parts) fed on by ring-tailed lemurs at nine sites in Madagascar: Ambatotsirongorongo, Andringitra Massif, Anja Reserve, Antserananomby, Berenty Reserve, Beza Mahafaly Special Reserve, Cap Sainte-Marie, Tsaranoro Valley Forest, and Tsimanampetsotsa National Park. I gathered literature using keyword searches on Google Scholar ( https://scholar.google.com/ ) and verified scientific names using the “Catalogue of the Plants of Madagascar” ( http://legacy.tropicos.org/Project/Madagascar ). From 24 studies, I identify 221 genera and 241 species of consumed plants, with 92 genera and 70 species consumed at two or more sites. Based on the available distribution data, 63% of species are endemic and 22% native. Sixty-seven plants are known only by Malagasy common names and excluded from analyses. When authors identify the plant tissue consumed, 52% of species in the diet are represented by a single tissue type, typically leaves (mature and immature) or fruit (ripe or unripe). This review highlights the importance of studying multiple populations when creating dietary summaries of species and should prove valuable to those exploring ecological trends and habitat use by ring-tailed lemurs.

Affiliative Contact Calls during Group Travel: Chirp and Wail Vocalization Use in the Male Ring-Tailed Lemur (Lemur catta)

Affiliative vocalizations occur across primate taxa and may be used to maintain spatial cohesion and/or to regulate social interactions in group-living species. For gregarious strepsirhines like the ring-tailed lemur (Lemur catta), with large vocal repertoires and several distinct affiliative vocalizations including the chirp and wail, it is important to understand behavioural usage of these vocalizations to gain insight into their social interactions. To determine whether chirp and wail vocalizations facilitate group cohesion, regulate interactions to achieve socially positive outcomes, and are correlated with differences in individual characteristics such as dominance rank and age, I collected 565 h of focal data on 31 males aged ≥1 year at Beza Mahafaly Special Reserve, Madagascar, from March to July 2010. I found that chirp and wail vocalizations occurred at the highest rates during group-wide travel compared to other behaviours. Although nearest neighbour distance did not influence calling rate, focal animals maintained the same distance or were located closer to nearest neighbours after calling. Both chirp and wail calls were heard in behavioural contexts without agonism rather than agonistic contexts. No relationship was found between male calling rate and dominance rank or age, although the chirp showed a non-significant tendency to be produced at higher rates by younger males. Overall, my results indicated that ring-tailed lemur males of all ages and dominance ranks used both chirp and wail vocalizations as contact calls during group-wide travel events, helping individuals maintain proximity to other group members during movement. Chirp and wail vocalizations may additionally help regulate the caller’s social interactions and promote increased tolerance from conspecifics. These findings add to our understanding of the breadth of communication behaviour in wild lemurs, thus furthering our knowledge of the social lives and cognitive abilities of strepsirhines. Through examining the complexity of vocalization use by a living lemur species with a communication system much like early social primates, we gain broad insight into the evolution of primate sociality.

Taxonomic identification of Madagascar’s free-ranging “forest cats”

Madagascar does not have native wild felid species; however, distinct populations of free-ranging “forest cats” of unknown species are known throughout the island, including at Ankarafantsika National Park, Beza Mahafaly Special Reserve, Makira Natural Park and the Masoala peninsula. Malagasy “forest cats” are commonly considered invasive lemur predators and competitors with endemic carnivores as well as a nuisance exotic species that kill poultry. These cats may be descendants of African wildcats, European wildcats and/or domestic cats; however, no research on their genetic origin has been published. To determine their taxonomic status, genetic data from short tandem repeat markers was assessed for three wild-caught “forest cats” from the Beza Mahafaly Special Reserve (BMSR) and 27 “forest cats” from Ankarafantsika National Park. Bayesian analyses comparing the Malagasy “forest cats” to approximately 1900 domestic and wildcat sub-species suggest the Malagasy cats are descendents of domestic cats from the Arabian Sea region, including the islands of Lamu and Pate, Dubai, Kuwait and Oman. Additional genetic influences may descend from India and Pakistan. Combined with cultural and historical information, these data suggest that these felid populations are likely descendents from cats that immigrated to the island on trade ships, particularly along early Arab trade routes.

AGE-RELATED CHANGES IN HEMATOLOGY AND BLOOD BIOCHEMISTRY VALUES IN ENDANGERED, WILD RING-TAILED LEMURS ( LEMUR CATTA) AT THE BEZÀ MAHAFALY SPECIAL RESERVE, MADAGASCAR.

The health of 44 wild ring-tailed lemurs ( Lemur catta) at the Bezà Mahafaly Special Reserve was assessed across three age classes: <5 yr (young), 5-9 yr (adult), and ≥10 yr (old). Hematology and biochemistry tests were performed manually (leukocyte count and differential, packed cell volume, total protein) and using a point-of-care analyzer (hematocrit, hemoglobin, glucose, blood urea nitrogen, creatinine, sodium, potassium, chloride, ionized calcium, total carbon dioxide, anion gap), respectively. Urine specific gravity was measured via refractometry. Age- and sex-related differences were detected. Old lemurs had significantly lower lymphocyte count than adult and young lemurs, leading to markedly lower total leukocyte count and higher neutrophil-to-lymphocyte ratio. Decreased lymphocyte count with advanced age is consistent with immunosenescence. Young lemurs had significantly higher total protein, monocyte count, and potassium than adult and old lemurs but significantly lower ionized calcium than adult lemurs. Males had significantly higher leukocyte, neutrophil, and monocyte counts; lower percentage basophils; and higher blood urea nitrogen than females. Females had markedly higher glucose than males. Young females had the highest monocyte count and total protein, which were significantly lower in the adult and old age classes. Basophil count was stable in females across age but dropped precipitously in males in the adult and old age classes. Within adult and old age classes, males had significantly higher blood urea nitrogen and lower basophils than females. Glucose was significantly higher after α2 agonist administration. Identifying age-related hematologic and biochemical changes in apparently healthy wild ring-tailed lemurs will aid in clinical diagnosis and treatment of lemurs in human care, which is especially relevant for management of geriatric animals in zoo populations. Equally important, a better understanding of the ability of aging lemurs to tolerate environmental stressors will inform the capacity for this species to cope with ongoing and future habitat alteration.

Mycobacterium leprae genomes from naturally infected nonhuman primates.

Leprosy is caused by the bacterial pathogens Mycobacterium leprae and Mycobacterium lepromatosis. Apart from humans, animals such as nine-banded armadillos in the Americas and red squirrels in the British Isles are naturally infected with M. leprae. Natural leprosy has also been reported in certain nonhuman primates, but it is not known whether these occurrences are due to incidental infections by human M. leprae strains or by M. leprae strains specific to nonhuman primates. In this study, complete M. leprae genomes from three naturally infected nonhuman primates (a chimpanzee from Sierra Leone, a sooty mangabey from West Africa, and a cynomolgus macaque from The Philippines) were sequenced. Phylogenetic analyses showed that the cynomolgus macaque M. leprae strain is most closely related to a human M. leprae strain from New Caledonia, whereas the chimpanzee and sooty mangabey M. leprae strains belong to a human M. leprae lineage commonly found in West Africa. Additionally, samples from ring-tailed lemurs from the Bezà Mahafaly Special Reserve, Madagascar, and chimpanzees from Ngogo, Kibale National Park, Uganda, were screened using quantitative PCR assays, to assess the prevalence of M. leprae in wild nonhuman primates. However, these samples did not show evidence of M. leprae infection. Overall, this study adds genomic data for nonhuman primate M. leprae strains to the existing M. leprae literature and finds that this pathogen can be transmitted from humans to nonhuman primates as well as between nonhuman primate species. While the prevalence of natural leprosy in nonhuman primates is likely low, nevertheless, future studies should continue to explore the prevalence of leprosy-causing pathogens in the wild.

The effect of extreme weather events on hair cortisol and body weight in a wild ring-tailed lemur population (Lemur catta) in southwestern Madagascar.

Madagascar is known for its hypervariable climate with periodic droughts and cyclones, but little is known of the impact of such events on lemur physiology. We examined the effects of sequential weather periods, drought, normal, cyclone and post-cyclone, on hair cortisol concentrations (HCC) and body weight in wild ring-tailed lemurs, Lemur catta (n = 185), at the Bezà Mahafaly Special Reserve in southwestern Madagascar. Data were modeled and analyzed by sex, age, and troop. Given the ecological consequences of extreme climatic perturbations, we hypothesized that drought and cyclone would significantly impact lemur HCC. Among adults, drought was associated with higher HCC than other periods and the lowest HCC was associated with the post-cyclone period. Adult females had greater variation in HCC during drought and males had greater variation during cyclone and Post-cyclone periods, suggesting sexes were differentially affected in terms of how individuals responded to extreme weather events. Low HCC in the post-cyclone period followed a 12-month period of reduced availability of primary and fallback food resources. Based on the known extreme and chronic nutritional stress during this time, our results indicate hypocortisolism in the animals included in our analysis. Higher HCC in sub-adults during the cyclone also suggests that immature lemurs may experience extreme weather events differently than adults. Body weight, used as a gauge for environmental stress, was lowest during the post-cyclone for sub-adults, young adults, and adults. Body weight did not differ by sex among adults across any of the weather events. Overall, ring-tailed lemur's HCC appear to be more immediately impacted by drought, or stressors associated with that specific weather event, and influenced by the long-term impact of cyclones on resource availability evidenced by data from the post-cyclone period.

Genetic wealth, population health: Major histocompatibility complex variation in captive and wild ring-tailed lemurs (Lemur catta).

Across species, diversity at the major histocompatibility complex (MHC) is critical to individual disease resistance and, hence, to population health; however, MHC diversity can be reduced in small, fragmented, or isolated populations. Given the need for comparative studies of functional genetic diversity, we investigated whether MHC diversity differs between populations which are open, that is experiencing gene flow, versus populations which are closed, that is isolated from other populations. Using the endangered ring‐tailed lemur (Lemur catta) as a model, we compared two populations under long‐term study: a relatively “open,” wild population (n = 180) derived from Bezà Mahafaly Special Reserve, Madagascar (2003–2013) and a “closed,” captive population (n = 121) derived from the Duke Lemur Center (DLC, 1980–2013) and from the Indianapolis and Cincinnati Zoos (2012). For all animals, we assessed MHC‐DRB diversity and, across populations, we compared the number of unique MHC‐DRB alleles and their distributions. Wild individuals possessed more MHC‐DRB alleles than did captive individuals, and overall, the wild population had more unique MHC‐DRB alleles that were more evenly distributed than did the captive population. Despite management efforts to maintain or increase genetic diversity in the DLC population, MHC diversity remained static from 1980 to 2010. Since 2010, however, captive‐breeding efforts resulted in the MHC diversity of offspring increasing to a level commensurate with that found in wild individuals. Therefore, loss of genetic diversity in lemurs, owing to small founder populations or reduced gene flow, can be mitigated by managed breeding efforts. Quantifying MHC diversity within individuals and between populations is the necessary first step to identifying potential improvements to captive management and conservation plans.

Contact calling behaviour in the male ring‐tailed lemur (Lemur catta)

AbstractThe ring‐tailed lemur (Lemur catta) is a group‐living strepsirhine primate endemic to Madagascar that has a complex vocal repertoire including affiliative moan and hmm calls. Past research has suggested that both vocalisations may be contact calls, and we assessed their usage in addition to examining the effect of individual differences and social factors on male calling behaviour. We tested three hypotheses: the group cohesion, preferred companion and individual differences hypotheses. From March to July 2010, 565 h of focal animal data were collected on 31 males aged ≥1 year at the Beza Mahafaly Special Reserve, Madagascar. Focal males were observed for 30 min, with vocalisations, allogrooming and agonistic interactions noted using one‐zero sampling, and general behaviour, nearest neighbour identity and distance noted using instantaneous point sampling, all at 2.5 min intervals. We found support for the group cohesion hypothesis for both vocalisations, and support for the preferred companion and individual differences hypotheses for the hmm but not the moan vocalisation. Moan and hmm calls maintained the distance between a male and his nearest neighbour, and were made at higher rates during behaviours which may lead to separation from conspecifics, such as travel and vigilance. Males made hmm calls at higher rates when they were low‐ranking, and/or when the nearest neighbour of a male or a preferred companion of either sex. Low‐ranking males may hmm call to maintain proximity to specific individuals within social groups who will show them increased tolerance, with the hmm signalling peaceful intent. Ring‐tailed lemurs are one of the best living models of gregarious primate ancestors, and gaining a better knowledge of the function and range of usage of their contact calls informs our understanding of the evolution of primate cognition.

A simple, economical protocol for DNA extraction and amplification where there is no lab

Genetic analyses are well suited to address many research questions in the study of wild populations, yet species of interest often have distributions that are geographically distant from molecular laboratories, necessitating potentially lengthy transport of biological specimens. Performing basic genetic analyses on site would avoid the project delays and risks of sample quality decline associated with transport, as well as allow original specimens to remain in the country of origin. Further, diagnostic genetic assays performed in the field could provide real-time information allowing for more nimble adjustments to research plans and use of resources. To this end, we developed protocols for reliably performing front-end genetics bench work in the field, without the requirements of electricity or permanent shelter. We validated these protocols on buccal swabs collected during routine capturing of sifaka lemurs (Propithecus verreauxi) at Beza Mahafaly Special Reserve in Southwest Madagascar and faecal samples collected from captive sifakas (P. coquereli) at the Duke Lemur Center. Our basic protocol pipeline involves a chelating resin based DNA extraction followed by whole genome amplification or polymerase chain reaction using reagents stored at ambient temperature and portable, compact equipment powered by a lightweight solar panel. We achieved a high success rate (>80%) in downstream procedures, demonstrating the promise of such protocols for performing basic genetic analyses in a broad range of field situations.

Paternity in wild ring-tailed lemurs (Lemur catta): Implications for male mating strategies.

1In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.

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

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.

Seasonal variation in the abundance and distribution of ticks that parasitize Microcebus griseorufus at the Bezà Mahafaly Special Reserve, Madagascar

At Bezà Mahafaly Special Reserve (BMSR), Madagascar, mouse lemurs (Microcebus griseorufus) are parasitized by multiple species of haemaphysaline ticks. At present we know little about the role ticks play in wild lemur populations and how they can alter interspecies relationships within communities or impact host fitness. In order to better understand these dynamics at BMSR, we examined parasite-host interactions as well as the ecology of mouse lemurs and their infesting ticks, Haemaphysalis lemuris and H. sp. cf. simplex. We show that season, host sex, and habitat influence the relative abundance of ticks on mouse lemurs. Specifically, infestations occur only during the dry season (May–October), are higher in males, and are higher at the study site with the most ground cover and with greater density of large-bodied hosts. Microcebus likely experience decreased susceptibility to tick infestations during the wet season because at that time they rarely if ever descend to the ground. Similarly, male mouse lemurs have higher infestation rates than females because of the greater time they spend traveling and foraging on the ground. During the dry season, Microcebus likely serve as hosts for the tenrec tick, H. sp. cf. simplex, when tenrecs hibernate. In turn, during the wet season when mouse lemurs rarely descend to the ground, other small mammals at the reserve may serve as maintenance hosts for populations of immature ticks. The synchronous development of larvae and nymphs could present high risk for vector-borne disease in Microcebus. This study also provides a preliminary description of the ecology and life cycle of the most common lemur tick, H. lemuris.

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

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 populations can develop different dental wear patterns resulting from a mix of intrinsic factors (thin enamel) and local conditions (food properties, frequency of consumption).

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

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.

Examining Visual Measures of Coat and Body Condition in Wild Ring-Tailed Lemurs at the Bezà Mahafaly Special Reserve, Madagascar

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.

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

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.

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

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.