Tradition in Lemur catta Behavior at Berenty Reserve,Madagascar

Lemur catta Troop D at Berenty Reserve has been studied intermittently for 35 years. During 90 hours of continuous sampling in August 1998, I observed and mapped troop movement and scent marking. I compared these observations with data from June, 1975. The core of Troop D1's 1998 home range is the same as for Troop D in 1975. Sixty-two percent of Troop D1's time in 1998 was spent in the 1975 home range, and 52% of their scent marks were placed in that 1975 home range. The remainder of their time was spent in an extension of their home range, which is now an area of confrontation with an adjacent troop. They used the same sleeping trees in the 2 years, and all of the 1998 scent marks deposited in the 1975 home range were placed in the same locations marked in 1975. The similarities in their use of space in 1975 and 1998 were remarkable.     

Changes in behavior in free‐ranging Lemur catta following release in a natural habitat

The adjustment of captive‐reared and developmentally deprived ringtailed lemurs (Lemur catta) to supported release on St. Catherine's Island, Georgia, was studied over 7 years to examine if these animals developed behavior comparable to wild populations. Initial changes after release included decreased obesity and increased agility as well as foraging for appropriate novel plants. Ranging, daily behavior cycles, and vocalizations developed more slowly over 1–3 years, but eventually the behavior resembled that of wild groups. Group composition and social structure changed through conflict to resemble wild and captive troops in social organization, including the emergence of matrilineal dominance and male emigration. Since behavior eventually resembled that seen in the wild, some resilience of species‐typical wild behavior in captivity is supported. Am. J. Primatol. 47:15–28, 1999. © 1999 Wiley‐Liss, Inc.     

Beyond odor discrimination: demonstrating individual recognition by scent in Lemur catta

The current study demonstrates, for the first time, the occurrence of olfactory individual recognition in a nonhuman primate species. The empirical demonstration of recognition systems requires 1) a set of cues produced by the sender (expression component), 2) the perception of these cues by the receiver (perception component), and 3) a functional response by the receiver (action component). On the basis of this framework, we analyzed by gas chromatography 35 brachial secretions collected from 10 males of Lemur catta. Moreover, we performed habituation/discrimination tests to demonstrate the perception component, and we designed a specific bioassay, based on territorial competition, to highlight a functional response to individual odors. We demonstrated that recognition of conspecific odors goes beyond the perception of cues other than individuality (familiarity, kin, season, age, and rank) and that the receiver actually forms a mental representation of a specific individual by its scent.     

Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs

Because ring-tailed lemurs (Lemur catta) show handedness during feeding, I investigated whether they also show lateral preference in the limbs used by males during scent marking. During a bout of marking, a male alternates a variable number of shoulder rubs and arm marks. It is a complex social signal that has both olfactory and visual components and is frequently part of intrasexual agonistic interactions. I used all-occurrences behavior sampling, manually recorded all totally visible bouts, and required a minimum of 50 bouts per animal. The subjects included six wild and four group-living captive male lemurs. I considered limb usage to be lateralized for each individual lemur if the frequency of use of one side was significantly above chance as determined by binomial z-scores at P<.05. I measured consistency of lateral preference by calculating handedness index (HI) scores for each individual. Overall, I recorded 1,583 bouts of scent marking, and 66% of the bouts began with shoulder rubbing. Eight of the 10 males showed a significant, moderately strong lateral preference for the lead limb in the first shoulder rub performed in a bout, and for six of these eight the preferred lead limb for shoulder rubbing was the left one. Six of the 10 males showed a significant but weak lateral preference in the first arm mark, and five of these preferred the opposite limb to that used for the first shoulder rub. Although the preferences were not at the population level, eight of the 10 lemurs showed a lateral bias in the lead limb used for a component of this complex social signal.     

Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta)

Adaptive explanations for social grouping assume that thereare fitness consequences associated with group size, and individualsmaintain membership in groups of favorable size to maximizefitness. Here I examine fecal cortisol concentrations as a hormonalmeasure of stress to assess the relative well-being of Lemurcatta in groups of different size and in seasons of normal andlow tamarind fruit availability. I test the hypotheses thatthere is an optimal group size at which cortisol is lowest andthat optimal group size changes in food-scarce conditions. Icollected 799 fecal samples from 87 individuals in seven free-rangingL. catta groups at Berenty Reserve, Madagascar, over a 1-yearperiod (August 1999–July 2000) and determined fecal cortisolconcentrations using a radioimmunoassay. Expressing these asresiduals from monthly population means to control for temporalfluctuations in cortisol concentration, I calculated mean fecalcortisol levels for each animal in seasons of normal and lowtamarind fruit abundance and over the entire year. Overall,females exhibited lowest mean cortisol levels in groups of intermediatesize, suggesting that there are benefits to maintaining membershipin these groups. Females in groups that were atypically largeor small for their habitat type had higher mean cortisol levelsthan typical groups. Cortisol levels increased in food-scarceconditions for larger groups, suggesting that intergroup competitiveadvantages do not outweigh intragroup feeding competition atthis time. Group size may be optimized for long-term averageconditions, and short-term stresses may intermittently alterthe costs associated with group size.     

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

Most mammals have nose tips covered by glabrous skin, a labronasal area, or rhinarium. The surface of the rhinarium of Lemur catta has a dermatoglyphic pattern consisting of epidermal domes. Below the domes, epidermal pegs dip down into the dermis. In and below the tip of the epidermal peg, a complex sensory organ is found. It consists of an association of innervated Merkel cells, lamellate (Pacini‐like) bodies with a central nerve, and a ring of unmyelinated nerve endings in the epidermis. The Merkel cells are situated basally in the epidermis and the lamellated bodies just below the epidermis. The unmyelinated nerve endings related to the organ ascend in a circle straight through the epidermis ending below the corneal layer. From these nerve terminals, horizontal spikes enter the keratinocytes. The three components occur together forming an organ and are innervated from a common nerve plexus. The morphology of the complex sensory organ of the lemur shares most crucial components with Eimer's organs in moles, echidna, and platypus, while some structures are lacking, for example, the specific central pillar of keratinocytes, the cuticular cap, and a central unmyelinated fiber. The presence of the essentials of an Eimer's organ in many mammals suggests that a wider definition is motivated. J. Morphol. 276:649–656, 2015. © 2015 Wiley Periodicals, Inc.     

Correlates between locomotor anatomy and behavior in two sympatric of Lemur.

Sympatric populations of Lemur catta and Lemur fulvus show major differences in their occupation of canopy forest levels. Lemur catta is usually found in the lowest levels of the forest, and uses the ground for travel over 65% of the time. Lemur fulvus uses the upper levels of the canopy forest and is observed on the ground in less than 2% of all observations. Comparison of hindlimb musculoskeletal anatomy show statistically significant differences in the lengths of the long bones and the height of the talus. Differences also occur in ranges of tibio-talar and mid-talar joint mobility. The details of insertion of the biceps femoris muscle are distinct in the two species as is the relative mass of muscle associated with flexion of the pedal digits, and flexion of th tibio-talar joint. The metric and morphological differences in the hindlimb anatomy of Lemur catta and Lemur fulvus are consistent with differences in habitat and substrate utilization.     

Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli: a preliminary chemical examination

Although prosimians are greatly olfaction-oriented, little is known about the specifics of how they use scent to communicate. In this preliminary study we attempted to delineate intra- and interspecific differences among the anogenital gland secretions of two lemur species (Lemur catta and Propithecus verreauxi coquereli) using gas chromatography-mass spectrometry (GC-MS). The results indicate that the two species are discernible through scent. Furthermore, we were able to identify reproductive status using this technique. The anogenital secretions of the different sexes in L. catta, though perhaps not P. v. coquereli, are chemically distinguishable. Given this information, it appears that at least some lemur species can use scent marks to determine species, sex, and reproductive status.     

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

A survey to identify the major intestinal species of aerobic bacteria, protozoa and helminths was conducted on captive and wild populations of ring-tailed lemurs (Lemur catta). Samples were collected from 50 captive lemurs at 11 zoological institutions in the United States. In Madagascar, 98 aerobic bacteria samples and 99 parasite samples were collected from eight sites chosen to cover a variety of populations across the species range. Identical collection, preservation and lab techniques were used for captive and wild populations. The predominant types of aerobic bacteria flora were identified via five separate tests. The tests for parasites conducted included flotation, sedimentation and FA/GC. Twenty-seven bacteria unique to either the captive or wild populations were cultured with eight of these being statistically significantly different. Fourteen bacteria common to both populations were cultured, of which six differed significantly. Entamoeba coli was the only parasite common to both the captive and wild populations. Giardia spp., Isospora spp., strongyles-type ova, Entamoeba spp. and Entamoeba polecki were found only in captive samples. Cryptosporidium, Balantidium coli, pinworm-type ova, and two fluke-like ova were seen only in wild samples. In addition, samples were compared for both bacteria and parasites from three unique field sites in Madagascar. In this three-site comparison, six types of bacteria were statistically significantly different. No significant differences regarding parasites were seen. Significant differences were found between the captive and wild populations, whereas fewer differences were found between sites within Madagascar. Although we isolated Campylobacter and Giardia, all animals appeared clinically healthy.     

A scoring system for coat and tail condition in ringtailed lemurs,Lemur catta

Coat condition can be influenced by a wide variety of disorders and thus provides a useful tool for noninvasive health and welfare assessments in wild and captive animals. Using Lemur catta as an exemplar, we offer a 6‐step scoring system for coat and tail condition, ranging from perfectly fluffy to half or more of body and tail being hairless. The categories are described in detail and illustrated with sample pictures from a wild population in Berenty Reserve, Madagascar. Furthermore, we elaborate on intermediate conditions and discoloration of fur. Coat condition scoring allows the comparison between years, seasons, and the effect of toxin, disease or stress. Although this system was developed for wild L. catta, we believe it can also be of value for other species. We recommend scoring coat condition in healthy wild mammal populations to give a baseline on yearly and seasonal variations vs. deteriorating health conditions or pathology. Am. J. Primatol. 71:183–190, 2009. © 2009 Wiley‐Liss, Inc.     

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

Strong resource seasonality in Madagascar has led to the evolution of female feeding priority and weaning synchrony in most lemur species. For these taxa, pregnancy/early lactation periods coincide with low food availability, and weaning of infants is timed with increased resources at the onset of the rainy season. Reproductive females experience high metabolic requirements, which they must accommodate, particularly when food resources are scarce. Female ring-tailed lemurs (Lemur catta) residing in spiny forest habitat must deal with resource scarcity, high temperatures (～36-40°C) and little shade in early to mid-lactation periods. Considered "income breeders," these females must use resources obtained from the environment instead of relying on fat stores; thus, we expected they would differ from same-sized males in time spent on feeding and in the intake of food and nutrients. We investigated these variables in two groups (N = 11 and 12) of Lemur catta residing in spiny forest habitat during early gestation and early to mid-lactation periods. Focal animal data and food plant samples were collected, and plants were analyzed for protein, kcal, and fiber. We found no sex differences for any feeding or nutrient intake variable for the top five food species consumed. Females in early gestation spent more time feeding compared with early/mid-lactation. Physiological compensation for spiny forest-dwelling females may be tied to greater time spent resting compared with gallery forest conspecifics, consuming foods high in protein, calories, and water, reduced home range defense in a sparsely populated habitat, and for Lemur catta females in general, production of relatively dilute milk compared with many strepsirrhines.     

Male aggression during mating: evidence for sexual coercion in a female dominant primate?

In this article we document male sexual coercion of a Lemur catta female on St. Catherines Island (SCI), USA. Data presented in this paper were collected on one free-ranging L. catta group during October-November 2002 using all-occurrences sampling for agonism and reproductive behavior. We observed a male forcefully attempting to mate with a year-old estrous female. Despite the fact that we observed this female to present to the male during her estrus, throughout the episode the male employed the use of force, and achieved penile intromission on at least one occasion while the female struggled and resisted. We interpret his behavior as sexual coercion. As measured by sexual presents, the female appeared to more strongly prefer two other males as mates, yet each of these males gained fewer mounts and less cumulative time spent in mounts than the coercive male. The coercive male was one of two group males with the lowest observed mating success, suggesting that coercion might be a strategy used by males who are not highly sexually preferred. Females undergo early sexual maturation at this site owing to provisioning, and can therefore enter estrus before fully attaining dominance over males. As such, these data suggest that one consequence of provisioning a wild L. catta population (or of maintaining L. catta in captivity) may be that young females can be the targets of sexual coercion if they reach sexual maturity before fully achieving social dominance over males. In conclusion, male sexual coercion can occur in L. catta despite the female dominance characteristic of this species, and can constrain the mating behavior of females.     

Intraspecific variation in hair delta(13)C and delta(15)N values of ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology

Stable carbon and nitrogen isotope compositions were analyzed from hair samples of 30 sympatric ring-tailed lemurs (Lemur catta) inhabiting the Beza Mahafaly Special Reserve, Madagascar. All lemurs were known individuals involved in a longitudinal study, which allowed us to explore the degree to which group membership, sex, health status, and migration influenced their stable isotope compositions. The differences in delta(13)C and delta(15)N values between groups were small (<1.5 per thousand) but highly significant. In fact, each group was tightly clustered, and discriminant function analysis of the stable isotope data assigned individuals to the group in which they were originally collared with over 90% accuracy. In general, the differences between groups reflected the degree to which they utilized forested versus open habitats. As open habitats at Beza Mahafaly often correspond to areas of anthropogenic disturbance, these data suggest that isotopic data can be useful for addressing questions of lemur conservation. There were few sex differences, but significant differences did occur between individuals of normal and suboptimal health, with those in poor health (especially those in the worst condition) being enriched in (15)N and to a lesser degree (13)C compared with healthy individuals. Moreover, lemurs that had emigrated between 2003 and 2004 had different delta(13)C and delta(15)N compositions than their original groups.     

Social behavior of the emperor tamarin in captivity: Components of agonistic display and the agonistic network

Agonistic behavior was studied longitudinally for 16 months in an intact family groups of captive emperor tamarins (Saguinus imperator subgrisescens) using methods from quantitative ethology and social network analysis. A motivational analysis of the components of agonistic display revealed the relative strength of each component along a continuum from strongly dominant to strongly subordinate. Tabulations of exchanges of strongly dominant and strongly subordinate components in interactions among the tamarins revealed an agonistic network (“dominance hierarchy”) that approached, but did not quite reach, the ideal state of a transitive order (“linear dominance hierarchy”). The frequency with which individual tamarins long called and scent marked was not closely correlated with their position (“dominance rank”) in the agonistic network. Instead, individuals undergoing change in status long called and scent marked frequently, irrespective of their rank.     

Face to face with the woolly spider monkey. Review of faces in the forest: The Endangered Muriqui Monkeys of Brazil,by Karen B. Strier. New York,Oxford University Press,Inc., 1992, 138 pp, $49.50

During an intertroop encounter, an infanticide was observed in a population of ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. The killer was a male that had not been previously observed to mate with any females in the infant's troop. This observation, combined with other observations of infanticidal behavior by males at Berenty Reserve and the Duke University Primate Center, is consistent with the hypothesis that infanticide is a reproductive tactic for some male ringtailed lemurs. © 1994 Wiley-Liss, Inc.