Eulemur Mongoz Research Articles

Infant survival is significantly impacted by dam- and management-related factors in zoo-managed Eulemur populations.

Due to their potential impact on population growth, many studies have investigated factors affecting infant survival in mammal populations under human care. Here we used more than 30 years of Association of Zoos and Aquariums (AZA) studbook data and contraception data from the AZA Reproductive Management Center, along with logistic regression models, to investigate which factors affect infant survival in four Eulemur species managed as Species Survival Plans® in AZA. Across species, infant survival to 1 month ranged from 65% to 78%. Previous experience producing surviving offspring was positively correlated to infant survival in collared (Eulemur collaris), crowned (Eulemur coronatus), and mongoose (Eulemur mongoz) lemurs. Both dam age and previous use of contraception were negatively correlated to infant survival for collared lemurs, though our results suggest the latter may be confounded with other factors. Blue-eyed black lemurs (Eulemur flavifrons) were affected by birth location, suggesting differences in husbandry that may affect infant survival. These results can be used to assist in reproductive planning or to anticipate the likelihood of breeding success. Population managers may also be able to focus their reproductive planning on younger dams or those with previous experience to predict successful births. Future studies should seek to determine what aspects of previous dam success are most important to infant survival, investigate sire-related factors, and examine factors related to cause of death in infants that may lead to differential survival. Our hope is to present a framework that may be useful for investigating infant survival in other mammal species' breeding programs.

Habitat Suitability and Population Size Estimates for the Mongoose Lemurs (Eulemur mongoz) of Madagascar and the Comoro Islands, and Implications for Their Conservation

Habitat Suitability and Population Size Estimates for the Mongoose Lemurs (Eulemur mongoz) of Madagascar and the Comoro Islands, and Implications for Their Conservation

The Evolution of Cognitive Control in Lemurs

Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel’s sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species’ natural history to understand the origins of complex cognition.

Eulemur mongoz

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A comparison of intestinal parasite infections and activity budgets in three free-ranging vs. enclosure-housed lemur species (Lemur catta, Varecia rubra, and Eulemur mongoz).

This study examines how range size affects intestinal parasite infections, and how such infections affect activity budgets in captive lemurs. There were no differences in parasite richness or intensity attributable to habitat type. However, there was a strong suggestion that parasite loads reduce activity levels.

Headfirst descent behaviors in a comparative sample of strepsirrhine primates.

The ability to safely ascend and descend is critical to the success of arboreal animals. Nonprimate mammals typically descend supports headfirst aided by their claws, but primates must rely on grasping, and use a variety of behaviors to move down within an arboreal environment, including headfirst and tailfirst descending. This study assesses hypothesized body mass limits on vertical headfirst descent and identifies approximate support orientations and diameters at which headfirst descent is ceased in a sample of nine strepsirrhines species ranging in mass from 0.06 to 4.5 kg. Species under 1 kg, arboreal quadrupeds Cheirogaleus medius and Microcebus murinus, and slow climber Nycticebus pygmaeus, always descended supports headfirst regardless of orientation and diameter as long as a grasp could be established. Arboreal quadrupedal species above 1 kg, Daubetonia madagascariensis, Eulemur coronatus, Eulemur mongoz, Lemur catta, and Varecia variegata differed in the orientation at which they ceased using headfirst descent and the types of alternative descending behaviors they employed. Lemur catta, a highly terrestrial species, started to employ tailfirst descents at 45° and completely stopped using headfirst descent on steeper and thicker supports. Other arboreal quadrupeds, D. madagascariensis, E. coronatus, E. mongoz, and V. variegata, began using tailfirst descent at 60°. The vertical clinging and leaping species Propithecus coquereli rarely engaged in above branch quadrupedalism, and individuals were observed using tailfirst descents on supports as shallow as 15°. This study shows the ways in which mass and anatomy may constrain use of headfirst descent through arboreal environments, and the alternate strategies strepsirrhine primates employ to descend.

Anatomical reorganization within the hand and forelimb of Perodicticus potto

Historical behavioral accounts note extraordinarily high grip strength in Perodicticus potto. Anatomical analysis of the potto’s hand and forelimb reveal several specializations that may facilitate this enhanced gripping ability, including a specialized vascular bundle (the retia mirabilia) within the wrist, a hyper‐abducted pollex, and a highly reduced second digit. The myological correlates of grip strength (i.e., the contractile potential of the hand and wrist musculature) of P. potto, however, have yet to be quantitatively evaluated. The current study contrasts the myology of the hand and forearm muscles within P. potto to a series of closely‐related strepsirrhines (Nycticebus coucang, Otolemur crassicaudatus, Hapalemur griseus, and Eulemur mongoz), as well as comparing the forearm musculature to a broader (n= 41) primate sample. Despite reports of the potto’s high grip strength, our findings demonstrate relatively below‐average force capacity (relatively low physiological cross‐sectional area) within the digital flexors of this species, which suggests that the gripping ability of this species may be less extraordinary than previously hypothesized. In addition to this observation, we report a number of unusual myological features within the potto, including the largest brachioradialis (an elbow flexor) of any taxon within our sample. Even more surprisingly, we identified an independent extensor indicis within P. potto, despite the vestigial nature of the second digit, and the absence of this muscle within ~25% of other taxa within our sample ‐ all of which possessed a more substantial second digit than the potto. These data underscore the curious nature of the potto’s antebrachial musculature, but suggest that adaptations within the potto’s forelimb may be more related to maximizing endurance grip potential than towards increasing myological force.Support or Funding InformationNational Science Foundation (IOS‐15‐57125 and BCS‐14‐40599)

Phylogenetic comparison on cognition: Advances in evolutionary psychology

More and more biological evidence has been yielded in support of physical evolution of species. In contrast, psychological evolution has been, so far, studied primarily with theoretical exploration. There are two theoretical approaches to the evolution on cognitive ability. The first, Common Ancestor, states that all species, including humans, have a common ancestor, from whom particular cognitive abilities in all existing species are inherited. The second, Evolutionary Convergence holds that different species possess similar cognitive abilities. The controversy between the two theories lies in the explanation of similar cognitive abilities in different species, one focusing on theoretical deduction and the other on parsimony in interpretation. However, both agree that basic cognitive abilities can be a starting point for studying the evolution on cognitive abilities. The top-down and the bottom-up approaches are usually used to study the cognitive abilities of different species. The top-down approach focuses on the cross-species levels of presence of a certain cognitive ability, and explores its level of presence among different species in relation to that in human beings. For the bottom-up approach, researchers generally analyze and study basic cognitive abilities, or the basic components of complex cognitive abilities, and systematically study the degree of difference between species in these basic cognitive abilities, which are universally present across species. The top-down approach can provide a precondition for defining the species boundaries of certain cognitive abilities, or which species have such abilities, while the bottom-up approach employs systematic methods to study the basic components of relevant cognitive abilities through cross-species experiments. The elaboration above suggests that we can understand the emergence and development of certain cognitive abilities, and the relationship between human’s advanced and basic cognitive abilities from the perspective of phylogenesis. Phylogenetic comparative methods are an important kind of bottom-up method. For a basic cognitive ability, the method of phylogenetic comparison is used to conduct cross-species experiments, so that the data obtained can be compared systematically. The results are of great significance for answering theoretical questions regarding cognitive evolution. For example, Amici and colleagues examined the ability of social inhibitory control in six primates (chimpanzees, bonobos, orangutans, gorillas, capuchin monkeys, and spider monkeys), and found that the level of fission-fusion dynamics could partially predict this ability. MacLean and colleagues studied the inhibitory control of 567 individuals from 36 species (birds and mammals), and showed that inhibitory control was positively correlated with absolute brain volume. Dietary breadth also predicted inhibitory control in the primate species studied. Jones and colleagues tested numerical cognition in three lemurs ( Lemur catta , Eulemur mongoz , and Eulemur Macaco flavifrons ), rhesus monkeys ( Macaca mulatta ), and human adults. They did not find any difference in nature among the four non-human groups in this ability. Specifically, the internal representation by all four non-humans was as predicted by the approximate number system and fit the linear representation model of the system. Cognitive differences among the five groups mainly lied in their numerical acuity, with humans having the lowest Weber fractions and the highest sensitivity. Chen improved their methods, tested humans in five age groups and golden snub-nosed monkeys ( Rhinopithecus roxellana ), and obtained findings consistent with those of the previous study. With the rise of cross-species systematic comparison, the latest trend of in-depth exploration into cognitive ability, research on phylogenesis on cognitive ability has entered a quantitative stage. Quantitative research on the relationship between evolutionary adaptive pressure and cognitive ability will help reveal patterns in the emergence and development on cognitive abilities in different species and even human beings.

DiceCT Analysis of the Extreme Gouging Adaptations Within the Masticatory Apparatus of the Aye-Aye (Daubentonia madagascariensis).

Relative to all other primates, the aye-aye (Daubentonia madagascariensis) exists at the extremes of both morphology and behavior. Its specialized anatomy-which includes hypselodont incisors and highly derived manual digits-reflects a dietary niche, unique among primates, which combines tap-foraging with gouging to locate and extract wood-boring larvae. Here, we explore the impact of this extreme dietary ecology upon the masticatory musculature of this taxon with reference to a second, similarly sized but highly generalist lemuriform-the mongoose lemur (Eulemur mongoz). Using non-destructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography techniques, we reconstruct the three-dimensional volumes of eight masticatory muscles, and, for the first time in strepsirrhines, isolate and visualize their constituent muscle fascicles in situ and in three dimensions. Using these data, we report muscle volumes, forces, and fascicle lengths from each muscle portion, as well as their orientation relative to two standardized anatomical planes. Our findings demonstrate the overbuilt nature of the aye-aye's masticatory apparatus, in which each muscle possesses an absolutely and relatively larger muscle volume and PCSA than its counterpart in the mongoose lemur. Likewise, for several adductor muscles, aye-ayes also possess relatively greater fascicle lengths. Finally, we note several unusual features within the lateral pterygoid of the aye-aye-the muscle most responsible for jaw protrusion-that relate to force maximization and reorientation. As this jaw motion is critical to gouging, we interpret these differences to reflect highly specific specializations that facilitate the aye-aye's extreme subsistence strategy. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:282-294, 2020. © 2019 American Association for Anatomy.

The cost of deep sleep: Environmental influences on sleep regulation are greater for diurnal lemurs.

Primates spend almost half their lives asleep, yet we know little about how evolution has shaped variation in the duration or intensity of sleep (i.e., sleep regulation) across primate species. Our objective was to test hypotheses related to how sleeping site security influences sleep intensity in different lemur species. We used actigraphy and infrared videography to generate sleep measures in 100 individuals (males = 51, females = 49) of seven lemur species (genera: Eulemur, Lemur, Propithecus, and Varecia) at the Duke Lemur Center in Durham, NC. We also generated experimental data using sleep deprivation for 16 individuals. This experiment used a pair-wise design for two sets of paired lemurs from each genus, where the experimental pair experienced a sleep deprivation protocol while the control experienced normal sleeping conditions. We calculated a sleep depth composite metric from weighted z scores of three sleep intensity variables. We found that, relative to cathemeral lemurs, diurnal Propithecus was characterized by the deepest sleep and exhibited the most disruptions to normal sleep-wake regulation when sleep deprived. In contrast, Eulemur mongoz was characterized by significantly lighter sleep than Propithecus, and E. mongoz showed the fewest disruptions to normal sleep-wake regulation when sleep deprived. Security of the sleeping site led to greater sleep depth, with access to outdoor housing linked to lighter sleep in all lemurs that were studied. We propose that sleeping site security was an essential component of sleep regulation throughout primate evolution. This work suggests that sleeping site security may have been an important factor associated with the evolution of sleep in early and later hominins.

Lemur species-specific metapopulation responses to habitat loss and fragmentation.

Determining what factors affect species occurrence is vital to the study of primate biogeography. We investigated the metapopulation dynamics of a lemur community consisting of eight species (Avahi occidentalis, Propithecus coquereli, Microcebus murinus, Microcebus ravelobensis, Lepilemur edwardsi, Cheirogaleus medius, Eulemur mongoz, and Eulemur fulvus) within fragmented tropical dry deciduous forest habitat in Ankarafantsika National Park, Madagascar. We measured fragment size and isolation of 42 fragments of forest ranging in size from 0.23 to 117.7 ha adjacent to continuous forest. Between June and November 2011, we conducted 1218 surveys and observed six of eight lemur species (M. murinus, M. ravelobensis, C. medius, E. fulvus, P. coquereli, and L. edwardsi) in the 42 fragments. We applied among patch incidence function models (IFMs) with various measures of dispersal and a mainland-island IFM to lemur species occurrence, with the aim of answering the following questions: 1) Do lemur species in dry deciduous forest fragments form metapopulations? 2) What are the separate effects of area (extinction risk) and connectivity/isolation (colonization potential) within a lemur metapopulation? 3) Within simulated metapopulations over time, how do area and connectivity/isolation affect occurrence? and 4) What are the conservation implications of our findings? We found that M. murinus formed either a mainland-island or an among patch metapopulation, M. ravelobensis formed a mainland-island metapopulation, C. medius and E. fulvus formed among patch metapopulations, and neither P. coquereli or L. edwardsi formed a metapopulation. Metapopulation dynamics and simulations suggest that area was a more consistent positive factor determining lemur species occurrence than fragment isolation and is crucial to the maintenance of lemur populations within this fragmented landscape. Using a metapopulation approach to lemur biogeography is critical for understanding how lemur species respond to forest loss and fragmentation.

Effects of human disturbance on the mongoose lemur Eulemur mongoz in Comoros: implications and potential for the conservation of a Critically Endangered species

AbstractThe decline of the mongoose lemur Eulemur mongoz has resulted in a change of its conservation status from Vulnerable to Critically Endangered. Assessing the current threats to the species and the attitudes of the people coexisting with it is fundamental to understanding whether and how human impacts may affect populations. A questionnaire-based analysis was used to study the impact of agriculture and other subsistence activities, and local educational initiatives, on lemur abundance, group size and composition in the Comoros. On the islands of Mohéli and Anjouan we recorded 214 lemurs in 63 groups, the size and composition of which depended both on environmental parameters and the magnitude and type of anthropogenic pressure. There was no evidence of an impact of anthropogenic disturbance on abundance. In contrast, group size and composition were sensitive to human impacts. The most important threats were conflicts related to crop raiding, as well as illegal capture and hunting. The promotion of educational activities reduced the negative impact of hunting and illegal activities. These results highlight a need for urgent conservation measures to protect the species.

The vocal communication of the mongoose lemur (Eulemur mongoz): phonation mechanisms, acoustic features and quantitative analysis

We recorded vocalisations of wild Eulemur mongoz groups in Madagascar and the Comoros Islands, as well as from habituated captive groups housed in European and Madagascan zoos. Each vocalisation was quantitatively described by means of an acoustic analysis procedure implemented in Praat, and vocal types were distinguished both by ear and by the visual screening of spectrograms. Vocal signals were then associated with the context in which they were produced, to explore whether they occur only in specific behavioural contexts or are uttered in a range of situations. We found that mongoose lemurs possess highly context-specific aerial alarm calls and territorial calls, while the ‘croui-croui’ is usually emitted to communicate between individuals regrouping at sunset. The other calls we recorded, such as those including low-pitched pulse trains sometimes followed by harmonic elements, were not tightly associated with a particular context. Mongoose lemur utterances included calls produced with closed mouths and the involvement of nasal resonance, or with constant degrees of mouth opening or mandible ‘articulation’ during phonation. We observed 15 vocal types, nine of which were entered into a multivariate model that classified vocal types with a high degree of reliability. The second and third formants played an important role in discriminating among types of calls.

Social inhibitory control in five lemur species.

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.

A Preliminary Assessment of Sifaka (Propithecus) Distribution, Chromatic Variation and Conservation in Western Central Madagascar

To help inform conservation efforts for the Endangered crowned sifaka Propithecus coronatus, in 2010, we attempted to better define the known distribution of sifakas in western central Madagascar through field surveys of 17 sites we considered likely to fall in or close to the historic range of P. coronatus. We observed P. coronatus at seven sites, in the Boeny, Betsiboka and Bongolava regions. At three sites at the intersection of the regions of Bongolava, Melaky and Menabe we observed populations containing sifaka of P. deckenii appearance mixed with melanistic individuals. We observed P. verreauxi at the two most southerly sites, in the Amoron'i Mania Region, and P. coquereli at one north-easterly site in the Betsiboka Region, a southern extension of 90 km to the known range of the species. At the four remaining sites, sifaka appeared to be either absent or extinct. We observed two other lemur species, Eulemur mongoz in the Boeny Region, and E. rufus in the Betsiboka Region, the latter observation being a small extension to the species' known range. We noted variation in pelage coloration amongst the P. coronatus individuals we observed, mainly regarding the extent and tone of the rufous wash on the back, arms and legs, but also in the color of the head, and the presence or absence of dark patches on the nape or at the root of the tail. The melanistic forms of P. deckenii varied greatly, some being very dark brown on large areas of the head, back, arms and legs, and appearing unlike any typical sifaka species, others exhibiting an intermediate coloration fairly similar to P. coronatus. We therefore suggest that P. coronatus should not be considered to represent an extreme melanistic form of P. deckenii, and that most previous reports of possible sympatry between the two taxa might alternatively be explained by a melanistic tendency in P. deckenii, possibly arising from occasional gene flow from P. coronatus. Our results show that P. coronatus may now be considered widely distributed through western central Madagascar, but most forests in this area are small and fragmented, and sifaka populations are highly endangered. We therefore recommend the implementation of immediate conservation interventions to ensure the maintenance of the full range of chromatic and genetic diversity of P. coronatus.

Social Behavior and Dominance of the Crowned Sifaka(Propithecus coronatus)in Northwestern Madagascar

We carried out a study of the social behavior and dominance hierarchy in three groups of crowned sifaka (Propithecus coronatus) in the Antrema Forest Station in north-west Madagascar. Data were collected from April to June 2009 and October to November 2009 using all-occurrence sampling. During 273 hours of observation, the majority of social behaviors observed were grooming interactions (39%), followed by agonistic behavior (25%), play (19%), scent-marking (9%), call-localization (5%) and approach (3%). A social hierarchy was maintained in the groups of P. coronatus, with females dominating the males. Although dif- ferent groups of P. coronatus defended their territories against other neighboring groups of the same species, the most frequently observed outcome of intergroup encounters was tolerance. In addition, we detected no significant change of sifaka behavior during interspecific encounters with rufous brown lemur ( Eulemur rufus) or with mongoose lemur (Eulemur mongoz), suggesting these two species live in total sympatry with P. coronatus.

The ecology of spatial memory in four lemur species

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.

Wichtige veterinärmedizinische Aspekte der Lemurenhaltung im Tierpark Berlin

The author describes diseases in lemurs, which occurred in the last ten years at Tierpark Berlin. After a short introduction of the importance of lemur husbandry and breeding in zoological gardens a review of the following diseases is given: periarticular hyperostosis in black lemurs, acute alkaloid intoxication in black lemurs, amoebiasis in ruffed lemurs and obesity in mongoose lemurs. Clinical symptoms, diagnosis, therapy and post mortem findings are explained in detail.

Daily activity and light exposure levels for five species of lemurs at the duke lemur center

Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24-hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light-dark exposure and activity-rest patterns in free-ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter-D pendant that contained light and accelerometer sensors. Our results reveal common as well as species-specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre-sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid-day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species-specific photic niches and behaviors. The eventual application of the Daysimeter-D in the wild may help to better understand the adaptive evolution of ancestral primates.

Lemurs and macaques show similar numerical sensitivity

We investigated the precision of the approximate number system (ANS) in three lemur species (Lemur catta, Eulemur mongoz, and Eulemur macaco flavifrons), one Old World monkey species (Macaca mulatta) and humans (Homo sapiens). In Experiment 1, four individuals of each nonhuman primate species were trained to select the numerically larger of two visual arrays on a touchscreen. We estimated numerical acuity by modeling Weber fractions (w) and found quantitatively equivalent performance among all four nonhuman primate species. In Experiment 2, we tested adult humans in a similar procedure, and they outperformed the four nonhuman species but showed qualitatively similar performance. These results indicate that the ANS is conserved over the primate order.