Genetic population structure of endangered ring‐tailed lemurs (Lemur catta) from nine sites in southern Madagascar

Madagascar's ring‐tailed lemurs (Lemur catta) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring‐tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and F_ST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, H_O = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring‐tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate‐driven environmental instability, will therefore likely impede the long‐term viability of the species.     

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

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

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

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, especially those in regions with expanding agricultural and mining operations. Am. J. Primatol. 71:998–1010, 2009. © 2009 Wiley‐Liss, Inc.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.     

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

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. Am. J. Primatol. 72:1026–1037, 2010. © 2010 Wiley‐Liss, Inc.     

Characterization of new microsatellite loci for the ring‐tailed lemur (Lemur catta)

In this report we describe the development and characterization of six dinucleotide microsatellite loci for the ring‐tailed lemur (Lemur catta). The new markers were isolated from the genomic DNA of L. catta and all loci were found to be polymorphic when evaluated by genotyping a minimum of 34 individuals. Mendelian inheritance of each locus was verified using four families of captive ring‐tailed lemurs. The loci presented will facilitate the genetic survey of free‐ranging L. catta, enabling study of their social organization and mating patterns.     

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

The 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.     

Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata)

The zebra finch (Taeniopygia guttata) is a small Australian grassland songbird that has been domesticated over the past two centuries. Because it is easy to breed in captivity, it has become a widely used study organism, especially in behavioural research. Most work has been conducted on domesticated populations maintained at numerous laboratories in Europe and North America. However, little is known about the extent to which, during the process of domestication, captive populations have gone through bottlenecks in population size, leading to inbred and potentially genetically differentiated study populations. This is an important issue, because (i) behavioural studies on captive populations might suffer from artefacts arising from high levels of inbreeding or lack of genetic variation in such populations, and (ii) it may hamper the comparability of research findings. To address this issue, we genotyped 1000 zebra finches from 18 captive and two wild populations at 10 highly variable microsatellite loci. We found that all captive populations have lost some of the genetic variability present in the wild, but there is no evidence that they have gone through a severe bottleneck, as the average captive population still showed a mean of 11.7 alleles per locus, compared to a mean of 19.3 alleles/locus for wild zebra finches. We found significant differentiation between the captive populations (F(ST) = 0.062). Patterns of genetic similarity closely match geographical relationships, so the most pronounced differences occur between the three continents: Australia, North America, and Europe. By providing a tree of the genetic similarity of the different captive populations, we hope to contribute to a better understanding of variation in research findings obtained by different laboratories.     

Major histocompatibility complex variation and age‐specific endoparasite load in subadult European rabbits

Genes of the major histocompatibility complex (MHC) play a fundamental role in the vertebrate immune response and are amongst the most polymorphic genes in vertebrate genomes. It is generally agreed that the highly polymorphic nature of the MHC is maintained through host–parasite co‐evolution. Two nonexclusive mechanisms of selection are supposed to act on MHC genes: superiority of MHC heterozygous individuals (overdominance) and an advantage for rare MHC alleles. However, the precise mechanisms and their relative importance are still unknown. Here, we examined MHC dependent parasite load in European rabbits (Oryctolagus cuniculus) from a distinct population with low MHC diversity (three alleles, six genotypes). Using a multivariate approach, we tested for associations of individual MHC class II DRB constitution and the rabbits’ intestinal burden with nematodes and coccidia. Rabbits having a particular allele showed lower infestations with hepatic coccidia (E. stiedai). However, a comparison of all six genotypes in the population revealed that carriers of this allele only benefit when they are heterozygous, and furthermore, MHC heterozygosity in general did not affect individual parasite load. In conclusion, this study suggests an immunogenetic basis of European rabbit resistance to hepatic coccidiosis, which can strongly limit survival to maturity in this species. Our study gives a complex picture of MHC–parasite correlations, unveiling the limits of the classical hypotheses of how MHC polymorphism is maintained in natural systems.     

Troop fission in wild ring-tailed lemurs (Lemur catta) at Berenty, Madagascar

A detailed fission process in a wild ring-tailed lemur (Lemur catta) troop was observed at Berenty Reserve, Madagascar. The troop fission occurred as follows: 1) During the birth season in 2000, two adult females (mother and daughter) were evicted as a result of "targeted aggression" (i.e., intense and persistent aggressive behavior toward particular individuals). 2) Two adult and three immature females in the same kin group as the evicted females spontaneously immigrated into the new group. 3) A male immigrated into the new group 1.5 months later. 4) The new troop successfully established its own home range. This report exemplifies three characteristics of troop fission in ring-tailed lemurs. First, targeted aggression initiated the fission process. Second, the troop females divided along matrilineal lines. Finally, no male played a specific role in the fission process.     

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

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.     

Chemical composition of scent marks in the ringtailed lemur (Lemur catta): glandular differences, seasonal variation, and individual signatures

The apocrine and sebaceous scent glands of ringtailed lemurs (Lemur catta) appear to serve different social functions. In behavioral experiments, lemurs modulate their responses to scent marks based on the type of odorant, their own physiological state, the signaler's physiological state, and prior social experience. To examine variation in odorant chemistry relative to olfactory behavior, we used gas chromatography and mass spectrometry to analyze over 86 samples of glandular secretion collected over 2 years from 15 adult lemurs. Labial and scrotal secretions contained organic acids and esters, whereas male brachial secretions were composed almost entirely of squalene and cholesterol derivatives. Principal component and linear discriminant analyses revealed glandular, individual-specific, and seasonal variation in chemical profiles but no relationship to the signaler's social status. The chemical composition of the various secretions provides further clues about the function of the different glands: the higher molecular weight compounds in genital and brachial secretions may increase signal longevity and provide lasting information to conspecifics, consistent with a role in advertising resource ownership or reproductive state. Conversely, the lower molecular weight compounds of antebrachial secretions produce ephemeral signals used primarily in social dominance displays and require integration of multiple sensory modalities for effective signal transmission.