Lemur Species Research Articles

The Sphenoidal Synchondroses: Implications for the Midfacial Growth of Anthropoid Primates

The basicranium of anthropoid primates is more flexed than in lemurs and lorises (strepsirrhines), which has implications for orientation of facial growth. Differential growth among cranial synchondroses is one suggested mechanism for variation in basicranial development. In this study, we measured length of bony elements of the cranial base using Amira software in a cross‐sectional age sample (late prenatal to juvenile), which included three monkey species and four species of lemurs and bushbabies (n = 59). In addition, we made preliminary measurements of the anteroposterior length of the spheno‐occipital synchondrosis (SOS), intrasphenoidal synchondrosis (ISS), and prespheno‐septal synchondrosis (PSept) using newborn samples. In order to assess differences in growth potential among sync hondroses, the diameter of the proliferating (PZ) or hypertrophic (HZ) zones were also measured. Our other work has indicated that measurements of ossified elements of the cranial base reveal disproportionately more growth of presphenoid (PS) relatively to basisphenoid (BS) in monkeys. But in strepsirrhines, these bones scale similarly to one another when plotted against increasing cranial or midfacial length. When expressed as a ratio of the length of the PZ or HZ to total anteroposterior diameter of the synchondrosis, growth is relatively similar in ISS and SOS among all species studied. However, in anthropoids the length of the PZ in PSept is notably (more than two‐fold) greater than in any other synchondrosis. In strepsirrhines, length of the PZ in PSept is relatively similar to the same zone of other synchondroses. This suggests that the rapid increase in length of the presphenoid in anthropoids is mostly occurring anteriorly, at the midfacial interface. These results, taken at face value, might suggest that anthropoids have a greater magnitude of growth in the septal cartilage compared to strepsirrhines. However, our previous work established that growth at PSept in more multidirectional (radial) than in most other mammals. Instead, our findings emphasize different patterns of sphenoid growth among primates, and offer a tissue‐level explanation for the relatively large PS segment in anthropoid primates. In addition, these findings indicate suggest that growth of the sphenoid is more highly integrated with PS than BS and more interdependent with facial growth in monkeys than in strepsirrhine primates.Support or Funding InformationNSF grant # BCS‐1830894, BCS‐1830919, BCS‐0959438

Forest edges affect ectoparasite infestation patterns of small mammalian hosts in fragmented forests in Madagascar

Habitat loss and fragmentation drive the worldwide depletion of biodiversity. Although it is known that anthropogenic disturbances severely affect host and ecosystem integrity, effects on parasites are largely understudied. This study aims to investigate if and how habitat fragmentation affects the composition of ectoparasite communities on small mammalian hosts in two networks of dry deciduous forest fragments in northwestern Madagascar. Forest sites differing in size, proportion of edge habitat and host density were studied in the Ankarafantsika National Park and in the Mariarano region. A total of 924 individuals of two mouse lemur species, Microcebus murinus (n = 200) and Microcebus ravelobensis (n = 426), and two rodent species, endemic Eliurus myoxinus (n = 114) and introduced Rattus rattus (n = 184), were captured to assess ectoparasite infestations. Ectoparasite prevalence and ectoparasite species richness were statistically related to nine ecological variables applying generalized linear mixed models. Hosts harbored ticks (Haemaphysalis microcebi), mites (Schoutedenichia microcebi, Listrophoroides spp., Laelaptidae gen. spp.) and sucking lice (Lemurpediculus spp., Polyplax sp., Hoplopleuridae gen. sp.). Parasite prevalence differed significantly between host species for all detected parasite taxa. Proximity to the forest edge led to a significant reduction in ectoparasites. Parasite-specific edge effects were observed up to a distance of 750 m from the forest edge. The obtained results imply that habitat fragmentation impacts ectoparasite communities, in particular by negatively affecting temporary parasite species. The results are best explained by an interplay of parasite life cycles, responses to changes in abiotic factors induced by edges and host-specific responses to habitat fragmentation. The negative responses of most studied ectoparasite taxa to forest edges and habitat fragmentation demonstrate their ecological vulnerability that may eventually threaten the integrity of ecosystems and potentially impact ectoparasite biodiversity worldwide.

Mandibular symphyseal fusion in fossil primates: Insights from correlated patterns of jaw shape and masticatory function in living primates

Variation in primate masticatory form and function has been extensively researched through both morphological and experimental studies. As a result, symphyseal fusion in different primate clades has been linked to either the recruitment of vertically directed balancing-side muscle force, the timing and recruitment of transversely directed forces, or both. This study investigates the relationship between jaw muscle activity patterns and morphology in extant primates to make inferences about masticatory function in extinct primates, with implications for understanding the evolution of symphyseal fusion. Three-dimensional mandibular landmark data were collected for 31 extant primates and nine fossil anthropoids and subfossil lemur species. Published electromyography (EMG) data were available for nine of the extant primate species. Partial least squares analysis and phylogenetic partial least squares analysis were used to identify relationships between EMG and jaw shape data and evaluate variation in jaw morphology. Primates with partial and complete symphyseal fusion exhibit shape-function patterns associated with the wishboning motor pattern and loading regime, in contrast to shape-function patterns of primates with unfused jaws. All fossil primates examined (except Apidium) exhibit jaw morphologies suggestive of the wishboning motor pattern demonstrated in living anthropoids and indriids. Partial fusion in Catopithecus, similar to indriids and some subfossil lemurs, may be sufficient to resist, or transfer, some amounts of transversely directed balancing-side muscle force at the symphysis, representing a transition to greater reliance on transverse jaw movement during mastication. Furthermore, possible functional convergences in physiological patterns during chewing (i.e., Archaeolemur) are identified.

Lateralization in seven lemur species when presented with a novel cognitive task.

Asymmetrical behavior patterns are observed in many animal species, but the potential adaptive significance of lateralization and the evolutionary forces driving it remain unclear. Most laterality studies have focused on a single species, which makes interspecies comparisons difficult. The aim of this study was to examine differences in the strength and direction of lateralization in multiple lemur species when engaged in a standardized, novel cognitive task. We assessed laterality in seven lemur species at the Duke Lemur Center when using a novel puzzle-box. We recorded which hand opened the apparatus door and which hand picked up the food reward. We also recorded whether the mouth was used for either action instead of the hands. We then calculated handedness indices (HI), z-scores, and mouth-use rates. Overall, 62% of individuals were more lateralized than chance. However, within-genera, there were relatively equal numbers of individuals with a left- or right-hand bias, which resulted in ambipreference at the genus level. The hand a lemur used on its first success in the task predicted its overall HI value, and the strength of lateralization increased as the number of successes increased. Varecia had significantly higher mouth-use rates than all other genera. We found evidence of an individual learning trajectory in which the hand used on a lemur's first success was canalized as the preferred (and lateralized) hand, in support of the "cognitive simplicity" hypothesis. Individual variability in hand preference was high, which is consistent with previous research. Between-genera differences in mouth use appear to reflect species-specific feeding postures and differences in manual dexterity.

Do functional traits offset the effects of fragmentation? The case of large-bodied diurnal lemur species.

Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation, are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large-bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species' distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore-frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive folivores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape-level reforestation efforts.

Trends in forest fragment research in Madagascar: Documented responses by lemurs and other taxa

The rise in research investigating fragmentation and its impact on primates and other taxa reflects the growing presence of fragmented landscapes themselves. Although numerous studies report the negative effects of fragmentation on biodiversity, it is difficult to generalize responses to fragmentation for specific taxonomic groups, such as non-human primates, when studies have not employed a definitive concept of fragmentation or fragments themselves. Madagascar's high degree of fragmentation, wealth of endemic taxa, and extensive history of ecological research provide the opportunity to compare fragmentation studies across similar contexts. We conducted a literature search of peer-reviewed articles on fragmentation in Madagascar to characterize its trends. A total of 70 articles, 46 of which concentrated on lemurs, tested the impacts of fragmentation on Malagasy taxa, while additional sources conducted research in one or more fragments without testing its effects (n = 112 total, 79 on lemurs). Studies on lemurs most frequently tested fragmentation's impacts on genetics and biodiversity metrics (n = 16 and 15 studies, respectively), although health, modeling, behavioral, and cross-disciplinary techniques were also reported. Responses to fragmentation were reported for 49 lemur species, with most studies concentrated in eastern Madagascar (87%). Although there was variation in the metrics reported in studies testing the effects of fragmentation on Malagasy species, the most common measures were fragment area, isolation, or comparison to a control site. Landscape-scale approaches and examination of fragmentation per se were rarely employed. Characterizing trends of fragmentation research in Madagascar emphasizes the challenges of documenting fragmentation's effects while highlighting the benefits of research within fragmented landscapes, particularly when combined with consideration for how the matrix within human-modified landscapes may impact primate populations.

Effect of Group Size and Individual Characteristics on Intergroup Encounters in Primates

Intergroup encounters are common in nonhuman primates and can vary from affiliative to aggressive. We extracted data from the literature to test five different hypotheses: 1) where there are group size differences between opposing groups, whether the larger group is more likely to win an intergroup encounter than the smaller group; 2) whether the likelihood of a group engaging in aggressive intergroup encounters increases with group size; and 3–5) whether dominant, older individuals, and/or males are more likely to participate aggressively in intergroup encounters than subordinate, younger individuals and/or females. Our data set comprised 52 studies on 31 primate species (3 lemur species, 5 New World monkeys, 19 Old World monkeys, and 4 apes). We found that the larger group is more likely to win an encounter against a smaller group than vice versa. We found no significant relationship between group size and propensity to be aggressive during intergroup encounters. We found weak/no support for the effect of age, dominance rank, and sex on the frequency of aggression displayed toward outgroup individuals during intergroup encounters. Species- and population-specific differences in inter- and intragroup competition and in the degree of the unequal distribution of resources across group members may explain why age, dominance rank, and sex are not strong predictors of aggression during intergroup encounters.

Supplemental Material for Do Lemurs Know When They Could Be Wrong? An Investigation of Information Seeking in Three Species of Lemur (Lemur catta, Eulemur rubriventer, and Varecia variegata)

Supplemental Material for Do Lemurs Know When They Could Be Wrong? An Investigation of Information Seeking in Three Species of Lemur (Lemur catta, Eulemur rubriventer, and Varecia variegata)

Occupancy Modeling Reveals Interspecific Variation in Habitat Use and Negative Effects of Dogs on Lemur Populations

Effective, targeted management and conservation plans for wildlife populations require reliable population sampling and estimation. Unfortunately, robust, comprehensive primate population estimates are often lacking, particularly for rare, elusive species. Historically, population estimates of primates have relied on labor-intensive line-transect sampling and distance estimation techniques. We used occupancy sampling to estimate the probability of occupancy and detection of seven lemur species in Ranomafana National Park, Madagascar, and explore relationships between occupancy and detection and landscape, habitat, and co-occurring species variables. We detected and provide estimates of occupancy and/or detection for seven lemur species in a World Heritage Site: Ranomafana National Park, Madagascar. We found habitat type was an important variable explaining occupancy patterns for detection of golden bamboo lemur (Hapalemur aureus), as well as red bellied lemur (Eulemur rubriventer) and black-and-white ruffed lemur (Varecia variegata). The presence of free-ranging dogs (Canis familiaris) was an important factor in several competing models for red-bellied lemurs and eastern lesser bamboo lemurs (Hapalemur griseus), highlighting the threat posed by this exotic predator to primates. While some estimates had error values overlapping zero, reflecting the rarity and low detection of these species, these results indicate the importance of protecting multiple forest types to maintain lemur biodiversity and the underappreciated conservation threat of invasive species in Madagascar.

First experimental evidence for olfactory species discrimination in two nocturnal primate species (Microcebus lehilahytsara and M. murinus)

Olfactory communication is highly important for nocturnal mammals, especially for solitary foragers, but knowledge is still limited for nocturnal primates. Mouse lemurs (Microcebus spp.) are nocturnal solitary foragers with a dispersed lifestyle and frequently use chemo-sensory signalling behaviour for governing social interactions. Different mouse lemur species can co-occur in a given forest but it is unknown whether olfaction is involved in species recognition. We first screened 24 captive mouse lemurs (9 M. murinus, 15 M. lehilahytsara) for their olfactory learning potential in an experimental arena and then tested the species discrimination ability with urine odour in an operant conditioning paradigm in four individuals. The majority of the screened animals (75%) did not pass the screening criteria within a 2-week test period. However, all four final test animals, two M. murinus and two M. lehilahytsara, were successfully trained in a 5-step-conditioning process to reliably discriminate conspecific from heterospecific urine odour (requiring an overall median of 293 trials). Findings complement previous studies on the role of acoustic signalling and suggest that olfaction may be an important additional mechanism for species discrimination.

Anthropogenic pressures drive population genetic structuring across a Critically Endangered lemur species range

In recent decades Madagascar has experienced significant habitat loss and modification, with minimal understanding of how human land use practices have impacted the evolution of its flora and fauna. In light of ongoing and intensifying anthropogenic pressures, we seek new insight into mechanisms driving genetic variability on this island, using a Critically Endangered lemur species, the black-and-white ruffed lemur (Varecia variegata), as a test case. Here, we examine the relative influence of natural and anthropogenic landscape features that we predict will impose barriers to dispersal and promote genetic structuring across the species range. Using circuit theory, we model functional connectivity among 18 sampling localities using population-based genetic distance (FST). We optimized resistance surfaces using genetic algorithms and assessed their performance using maximum-likelihood population-effects mixed models. The best supported resistance model was a composite surface that included two anthropogenic features, habitat cover and distance to villages, suggesting that rapid land cover modification by humans has driven change in the genetic structure of wild lemurs. Primary conservation priority should be placed on mitigating further forest loss and connecting regions identified as having low dispersal potential to prevent further loss of genetic diversity and promote the survival of other moist forest specialists.

Elevation gradients of lemur abundance emphasise the importance of Madagascar’s lowland rainforest for the conservation of endemic taxa

Abstract Elevation gradients correlate with changes in several environmental conditions and are known to be related to animal abundance. Animals in regions with a naturally limited extent of lowland rainforest are expected to have evolved adaptations to intermediate elevations that provided a stable environment during their evolution. Since the lowland rainforest of Madagascar has a limited extent and suffers from increasing anthropogenic pressure, it is essential to understand how well species tolerate intermediate and high elevations. In this study, we aim to quantify the relationship between lemur abundance and elevation in the eastern rainforest of Madagascar. We correlated abundance data on 26 lemur species (10 genera), including 492 records from 26 studies, with elevation. We analysed the consistency of correlations across species with a meta‐analytical approach. We controlled for species’ body mass, elevational range and median elevation. We then ran generalised linear mixed models to determine whether lemur abundance was related to elevation, body mass, plant productivity and anthropogenic disturbance. Overall, the abundance of lemur species in Malagasy rainforests was negatively correlated with elevation, and species occupying broader elevational ranges showed stronger correlations. Body mass was not related to species’ tolerance of high elevations. Even though several lemur species are able to occupy the entire elevation gradient, the few remaining patches of lowland rainforests host lemur species at greater abundances than other sites. Abundance across species was negatively related to body mass, elevation and seasonality in plant productivity and positively related to plant productivity. Despite the ecological flexibility of many lemur species, the remnant patches of lowland rainforests host the highest levels of lemur abundance and are key to lemur conservation. It is crucial to preserve this priority habitat both for biodiversity conservation and for our understanding of lemur adaptations.

Food Insecurity and the Unsustainable Hunting of Wildlife in a UNESCO World Heritage Site

Madagascar faces dual challenges in biodiversity conservation and public health. In order to identify strategies to reduce the unsustainable hunting of threatened species while maintaining or improving child nutrition, we quantified interactions among ecosystem indicators (lemur density and habitat biodiversity indices), health indicators (stunting, underweight, wasting, and anemia), nutrition, food security, and wildlife hunting through interviews of 1750 people in 387 households and surveys of 28 wildlife transects with 156 habitat plots at 15 sites on Madagascar’s Masoala Peninsula, a UNESCO World Heritage Site. The surveyed population ate 6,726 forest animals (mammals and birds), or a mean of 3.27 kg of wild meat per person (4.48 kg per adult equivalent) during the prior year. Local Malagasy were highly food insecure (78% of households) and malnourished (for children under five, as many as 67% were stunted, 60% were underweight, 25% were wasted, and 40% were anemic). In some communities, nearly 75% of animal-sourced calories, 76% of protein, and 74% of iron came from forest animals- demonstrating a strong dependence on wild foods. Few micronutrient-rich alternatives to wild meats were available in adequate supply and many were highly volatile; for example, 79% of chickens died from Newcastle disease in the prior year. The survivorship of lemurs (94% of lemur species are threatened with extinction) depends on providing food security to a malnourished human population who commonly hunts wildlife for food. Currently, wildlife provides a critical source of micronutrients, yet the hunting of threatened species is an untenable solution to poor diet and food insecurity. Given the established connection between wild foods and human nutrition, reductions in forests and wildlife populations will also threaten the local food supply. In order to reduce the unsustainable hunting of threatened species while improving household food security and child health, we suggest testing the effects of increasing the affordability, accessibility, and stability of micro-nutrient rich animal-sourced foods in communities where forests contribute the most to food security.

Lemurs in Cacao: Presence and Abundance within the Shade Plantations of Northern Madagascar

The recognition that much biodiversity exists outside protected areas is driving research to understand how animals survive in anthropogenic landscapes. In Madagascar, cacao (Theobroma cacao) is grown under a mix of native and exotic shade trees, and this study sought to understand whether lemurs were present in these agroecosystems. Between November 2016 and March 2017, discussions with farmers, nocturnal reconnaissance surveys and camera traps were used to confirm the presence of lemurs in the Cokafa and Mangabe plantations near Ambanja, north-west Madagascar. Four species of lemur were encountered in nocturnal surveys: Mirza zaza, Phaner parienti, Microcebussp. and Cheirogaleussp. with encounter rates of 1.2, 0.4, 0.4 and 0.3 individuals/km, respectively. The presence of Lepilemur dorsalis was confirmed by camera trap. This is the first time lemurs have been studied in cacao plantations, and understanding how these threatened animals use anthropogenic landscapes is vital for their conservation.

Selecting and Testing Environmental Enrichment in Lemurs.

Environmental enrichment has become a standard tool for improving the welfare of animals in zoos. Two critical steps in the manipulation of environmental enrichment are (1) selection of objects/procedures and (2) evaluation of their effects. In this study, we examined the selection and evaluation of feeding enrichment for four species of lemur. Experiment 1 used a paired-choice preference assessment to divide eight food items into high- and low-preferred categories. Experiment 2 separately assessed the effects of high- versus low-preferred items (placed in bamboo dispensers) on the behavior of two of the species in the preference assessment. Both high- and low-preferred items increased general activity and overall enclosure use, with high-preferred items having a greater effect than low-preferred items on most measures. The results suggest that preference assessments can serve as useful tools in selecting potential enrichment and that enrichment testing is important in evaluating the significance of these preferences.

Extensive variability in the gut microbiome of a highly-specialized and critically endangered lemur species across sites.

Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black-and-white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on-going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full-day focal animal behavioral follows and collected fecal samples opportunistically across a three-month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea. While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, thereby underscoring the importance of monitoring endangered species at the population-level.

Eulerian videography technology improves classification of sleep architecture in primates.

Sleep is a critically important dimension of primate behavior, ecology, and evolution, yet primate sleep is under-studied because current methods of analyzing sleep are expensive, invasive, and time-consuming. In contrast to electroencephalography (EEG) and actigraphy, videography is a cost-effective and non-invasive method to study sleep architecture in animals. With video data, however, it is challenging to score subtle changes that occur in different sleep states, and technology has lagged behind innovations in EEG and actigraphy. Here, we applied Eulerian videography to magnify pixels relevant to scoring sleep from video, and then compared these results to analyses based on actigraphy and standard infrared videography. We studied four species of lemurs (Eulemur coronatus, Lemur catta, Propithecus coquereli, Varecia rubra) for 12-h periods per night, resulting in 6480 1-min epochs for analysis. Cramer'sV correlation between actigraphy-classified sleep and infrared videography-classified sleep revealed consistent results in eight of the nine 12-h videos scored. A sample of the infrared videography was then processed by Eulerian videography for movement magnification and re-coded. A second Cramer'sV correlation analysis, between two independent scorers coding the same Eulerian-processed video, found that interobserver agreement among Eulerian videography increased sleep vs. awake, NREM, and REM classifications by 7.1%, 46.7%, and 34.3%, respectively. Furthermore, Eulerian videography was more strongly correlated with actigraphy data when compared to results from standard infrared videography. The increase in agreement between the two scorers indicates that Eulerian videography has the potential to improve the identification of sleep states in lemurs and other primates, and thus to expand our understanding of sleep architecture without the need for EEG.

Range overlap and spatiotemporal relationships of frugivorous lemurs at Kianjavato, Madagascar

Interspecific competition can strongly influence patterns of space use in animal communities, particularly between closely related species, and may be exacerbated in marginal habitat. This may be important in Madagascar, as lemurs face diminishing resources due to deforestation. We examined the range overlap and spatiotemporal relationships of three species of frugivorous lemur in the fragmented forests of Kianjavato, Madagascar. We conducted simultaneous location and behaviour sampling of black-and-white ruffed lemurs, Varecia variegata , red-fronted lemurs, Eulemur rufifrons , and red-bellied lemurs, Eulemur rubriventer , at two sites over a period of 11 months. We used Doncaster's index of dynamic interaction to investigate the relative amount of time species spent within 30 m and 100 m of each other, compared to the time expected based on random use of location points. All three species showed low core range overlap compared to home range overlap, and while core overlap was higher between interspecific groups than intraspecific groups, the difference was not substantial. Conversely, no spatiotemporal avoidance was observed, and red-fronted lemurs showed positive association (indicating possible attraction) with both red-bellied and ruffed lemurs. These positive spatiotemporal associations may be related to shared resource use in small forests, or predation avoidance strategies. At present, these species may rely more on spatial segregation and niche separation than spatiotemporal avoidance to minimize interspecific competition. • Frugivorous lemurs spatially avoid heterospecifics via low core range overlap. • Spatiotemporally, red-fronted lemurs associate positively with probable competitors. • Positive associations may result from shared limited resources or predators. • Spatial avoidance and niche differentiation may offset spatiotemporal overlap costs.

Differences in infection patterns of vector-borne blood-stage parasites of sympatric Malagasy primate species (Microcebus murinus, M. ravelobensis).

The dynamic relationship of vector-borne parasites, arthropod vectors and their hosts is prone to change under the influence of climate change, global integration, shifting demographics and deforestation. It is therefore essential to better understand parasitism in wildlife populations, including parasites transmitted by blood-feeding vectors, and explore host range and heterogeneity of parasitic infections. We investigated Giemsa stained blood smears of two sympatric Malagasy primate species (Microcebus murinus: 184 samples from 69 individuals and M. ravelobensis: 264 samples from 91 individuals) for blood-stage parasites and tested for a potential influence of host species, sex, body mass and sampling month on blood-stage parasite prevalence and infection intensity. No protozoan parasites were detected in either host species. A host-specific difference was observed in filarial nematode infections, with higher risk of infection in M. murinus (prevalence 30.43%), than in M. ravelobensis (prevalence 6.59%), which may be explained by differences in host behavior and/or immune competence, linked to the period of host-parasite coevolution. Neither sex nor sampling month influenced infection prevalence or intensity significantly. We did not observe a negative effect of microfilarial infections on host fitness when taking body mass as a proxy. Our results support the hypothesis of a long-term evolutionary adaptation of hosts and parasites, leading to persistent infection with low morbidity. Morphological and molecular analyses indicate the finding of a new species, “Lemurfilaria lemuris”. Genetic analysis furthermore showed >99% sequence identity with microfilariae described from a sympatric, larger-bodied lemur species of a different genus, suggesting low host-specificity of the detected filariae and pathogen transmission across genus boundaries. Findings contribute to a more comprehensive picture of vector-borne diseases of Malagasy lemurs.

Sources of variation in social tolerance in mouse lemurs (Microcebus spp.)

BackgroundSocial tolerance strongly influences the patterns of affiliation and aggression in animal societies. However, not much is known about the variation of social tolerance in species living in dispersed social systems that combine solitary foraging activities with the need of coordinating social interactions with conspecifics on a regular basis. This study aims to investigate the sources of variation in social tolerance within a Malagasy primate radiation with dispersed social systems, the mouse lemurs (Microcebus spp.). Six mouse lemur species were selected as model species that belong to three different taxonomic clades, live in two types of forest environments (dry and humid), and differed in this study with respect to their reproductive activity. Six male–female and six male–male dyads of each species were tested temporarily in a standardized social encounter paradigm in Madagascar to collect data on joint use of space, non-agonistic body contacts, aggression rates, the number of conflicts and the establishment of intra- and intersexual dominance.ResultsMale–female dyads of the six species differed significantly in the frequency of affiliative and agonistic behaviors. In contrast, the variations between male–male dyads could not be explained by one parameter only, but clade membership, forest type, reproductive state as well as species were all suggested to be partially influential. Only one species (Microcebus mamiratra) showed signals of unambiguous female dominance in all male–female dyads, whereas the others had no or only a few dyads with female dominance.ConclusionsVariations in social tolerance and its consequences are most likely influenced by two factors, ecology (via forest type) and physiology (via reproductive activity), and only to a lesser extent by clade membership. The study suggests that mouse lemur females have higher aggression rates and more agonistic conflicts with males when females in the population are reproducing, at least in resource-rich humid forests. The study confirms a high degree of social plasticity between species in these small solitary foragers that supports their taxonomic distinctiveness and requires further scientific attention.