Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty,Madagascar

The mating behavior of ring-tailed lemurs at Berenty, Madagascar, was observed in April 1982. Although Troop A included five adult females, only two were observed to mate. The mating period covered two consecutive days, April 24 and 25. Each female was receptive for about 4 hr. Data from 47 copulations, of which 38 were with ejaculation, suggest that to be the first mating partner is of importance for male ring-tailed lemurs. Previously it has been suggested that male dominance is of little significance in determining mating partners. In this investigation it was observed that the second most dominant male MK was always the first mating partner. Only after several ejaculations and resultant fatigue did he lose possession of the female to lower ranking males, and the first ranking male was not seen to copulate with either female at any time. These results suggest that a male's mating success is partly, but not completely correlated with his dominance rank, and that other factors, including his length of residence in the group and female choice, also determine patterns of mating.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar

Glucocorticoids, a group of adrenal hormones, are secreted in response to stress. In male primates, variables such as breeding seasonality, dominance hierarchy stability, and aggressive and affiliative interactions can affect glucocorticoid levels. In this study, we examined interindividual differences in mean fecal glucocorticoid (fGC) levels among males in three groups of wild ring-tailed lemurs to better understand the physiological costs of group living for males in a female-dominant species that exhibits strict reproductive seasonality. Fecal and behavioral data samples were collected during one mating and two postmating seasons (2001 and 2003). The mean fGC levels were examined in relation to reproductive season, male rank, number of resident males, intermale and female-male agonism, and affiliative behavior with females. The mean fGC levels were not significantly elevated during mating season compared to the postmating period. During the mating season, male dominance hierarchies broke down and rank effects could not be tested; however, there was no relationship between male rank and fGC levels in the postmating periods. In 2001, males that resided in the group with the fewest males exhibited lower fGC levels during the postmating period. They also affiliated more with females than did males in the other groups. During the mating season of 2003, males engaged in more affiliative behaviors with females compared to the postmating season, but female-male agonism did not differ by season. However, rates of intermale agonism were significantly higher during mating compared to postmating periods, but such heightened agonism did not translate to a higher stress response. Thus, neither male-male competition for mates nor heightened agonism between males during the breeding season affected male fGC levels. Fewer males residing in a group, however, did have some effect on male-female affiliation and male fGC levels outside of the mating period. Males that live in a group with only a few (two or three) males may experience less physiological stress than those that live in groups with more males.     

Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve,Madagascar

In 1987, a long-term study of the demography of Lemur catta was begun in southern Madagascar. Eighty-five ringtailed lemurs were captured, marked, and released. Adult age classes were estimated using patterns of dental attrition. Including young, 155 individuals from nine groups were identified and monitored over 18 months. The study population of the reserve remained stable, with a growth rate of 0.98. Group sizes ranged from nine to 22 individuals (mean 14). Home ranges were larger (32 ha) and population densities lower (135/km²) than those for previously studied populations, and there was a relationship between habitat quality (e.g., no. of large trees) and these factors. At the beginning of the study, there were more adult males than females, but the sex ratio reached 1.00 by the last census. Females first gave birth at 3 years of age, and 80% or more of the females gave birth in 2 consecutive years. Fifty-two percent of the infants died in the first year and, given preliminary findings, only 40% of those born reach adulthood. Age-specific fertility patterns were similar to those reported for anthropoid primates. Forty-seven percent of the adult males migrated or were missing within a year. This included 78% of the 3–4 year olds and 38% of older age classes. No females were observed to migrate. One group split during the study. Demographic patterns are discussed and related to patterns in other populations of ringtailed lemurs as well as in anthropoids.     

Intra-troop affiliative relationships of females with newborn infants in wild ring-tailed lemurs (Lemur catta)

To determine how the birth and development of infants influence their mothers' social relationships with other adult troop members, we observed two free-ranging troops of ring-tailed lemurs (Lemur catta) at the Berenty Reserve, Madagascar. The number of acts of affiliative contact that the mothers received from other adult troop members during the first and second months of infant life were significantly higher than those before they gave birth, and the values during the third month were as low as that before giving birth. Two mothers received acts of affiliative contact less frequently after their infants died, compared with the values while the infants were alive. On the other hand, more than 95% of all acts of licking of infants by adult troop members other than their mothers occurred when the infants were in contact with their mothers. These findings suggest that infants per se and mothers per se were not attractive, but rather the mother-infant pair was attractive to other troop members. Acts of infant-licking were observed in almost all mother-mother pairs and mother-non-mother adult female pairs, and in two thirds of mother-adult male pairs. Moreover, the frequency of infant-licking was not affected by female parity, female and male dominance rank, or infant sex. Therefore, acts of infant-licking, which are widespread among troop members, may function to make or maintain stable social relationships.     

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.     

High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta)

Glucocorticoid levels are commonly used as measures of stress in wild animal populations, but their relevance to individual fitness in a wild population has not been demonstrated. In this study I followed 93 ring-tailed lemurs (Lemur catta) at Berenty Reserve in Madagascar, collecting 1089 faecal samples from individually recognized animals, and recording their survival over a 2 year period. I evaluated faecal glucocorticoid levels as predictors of individual survival to the end of the study. Animals with high glucocorticoid levels had a significantly higher mortality rate. This result suggests that glucocorticoid measures can be useful predictors of individual survival probabilities in wild populations. The 'stress landscape' indicated by glucocorticoid patterns may approximate the fitness landscape to which animals adapt.     

Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar

In the present study, we describe a change in the dominance rank of the top-ranking female in a wild troop of ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. After the top-ranking female fell to the bottom-ranking position, she was able to outrank a low-ranking female with the support of her adult daughter or an unrelated high-ranking female. These results indicate that, as in cercopithecine monkeys such as macaques and baboons, close proximity and alliances influence dominance relations among adult females in a wild troop of ring-tailed lemurs.     

Grooming and touching behaviour in captive ring-tailed lemurs (Lemur catta L.)

The distribution of grooming and touching behaviours was recorded in a group of captive ring-tailed lemurs. Grooming was found to be performed chiefly by older, higher ranking animals; touching (i.e., “reach out and touch” behaviour) was directed primarily by younger, low ranking animals to older, high ranking individuals. It is suggested that such touching is a submissive gesture in this species.     

Antipredator behavior in troops of free-rangingLemur catta at Beza Mahafaly special reserve,Madagascar

Observations of antipredator behavior in two troops of free-rangingLemur catta were made during a 13-month study ofL., catta feeding ecology. Both responses to and frequency of encounters with other species were recorded. Ringtailed lemur antipredator calls differentiated between terrestrial and avian predators. L. catta responded to the Madagascar harrier hawk (Polyboroides radiatus) and the Madagascar buzzard (Buteo brachypterus) in a specific manner that differed from their reaction to the other bird of prey in the reserve, the Black kite (Milvus migrants) and to potential mammalian and reptilian predators. Encounters with avian predators peaked during the birth season and when infants were being weaned. These periods coincide with previously observed nesting periods for the Harrier hawk and the buzzard, and with times when their offspring are fledged. Both were periods whenL. catta infants might have been especially vulnerable to prédation.     

Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta)

The challenge hypothesis (J. C. Wingfield, R. E. Hegner, B. G. Ball, and A. M. Duffy, 1990, Am. Nat. 136, 829-846) proposes that in birds, reptiles, and fish, "the frequency or intensity of reproductive aggression as an effect of T[estosterone] is strongest in situations of social instability, such as during the formation of dominance relationships, the establishment of territorial boundaries, or challenges by a conspecific male for a territory or access to mates" (p. 833). To determine the extension of this hypothesis to mammalian species, we tested predictions of the hypothesis in a nonpaternal, seasonal breeding, prosimian primate (ring-tailed lemurs, Lemur catta). Semi-free-ranging males were studied during periods of social stability (premating period) and instability (mating period). The annual mating season consists of several days during which males fight for access to promiscuous group females as each individually becomes sexually receptive for 1 day. Male rates of aggression were compared to fecal testosterone levels within premating and mating periods. In the premating period male rate of aggression was not significantly correlated with testosterone level. By contrast, during the mating season testosterone and aggression levels were positively and significantly correlated. However, on days just preceding estrus, male rate of aggression was not significantly correlated with testosterone, but on days of estrus, when aggressive challenges peaked sharply, testosterone and aggression were highly positively correlated. These results suggest that the challenge hypothesis applies to mammals as well as to birds, reptiles, and fish. In addition, elevations in testosterone were tightly circumscribed around days of estrus, suggesting a compromise between costs and benefits of elevated testosterone levels.     

The acquisition process of a novel behavior pattern in a group of ring-tailed lemurs (Lemur catta)

The process of acquisition and propagation of a novel behavior pattern in a group of 18Lemur catta was examined. Six of eight animals that acquired the new habit were infants or juveniles. Adult males did not take up the new behavior pattern. Effects of rank and kinship on the aquisition process were not obvious.     

Drinking from tails: Social learning of a novel behaviour in a group of ring-tailed lemurs (Lemur catta)

Several examples have been documented of novel behaviours which have apparently arisen spontaneously in primate groups and then spread through the group by learning. Here we describe the first recorded instance of such an acquired behaviour in a prosimian. The behaviour, consisting of immersing the tail in water and then drinking from the wet tail, was observed in a group of semi free-ranging ring-tailed lemurs (Lemur catta). Seventeen of 28 animals showed the behaviour, including adult males. Several animals which did not show the behaviour were observed watching and sometimes sharing the wet tail of animals who did. Several incomplete sequences, notably of non-stimulus directed elements, were also seen in non-performers. It is likely that stimulus enhancement is the mechanism of spread of this behaviour through the group, although the presence of the incomplete sequences suggests that imitation is also a possibility.     

Diets of Two Lemur Species in Different Microhabitats in Beza Mahafaly Special Reserve,Madagascar

Studies of primate diets usually focus on differences that distinguish species or populations. However, variation in diet can occur at a more local level of groups within a population, especially in a non-homogeneous habitat. I compared dietary variation in food composition and toughness across groups of 2 lemur species in Beza Mahafaly special reserve, Madagascar. Beza Mahafaly contains an 80-ha reserve (Parcel 1) that, while small, hosts a dense population of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas). Microhabitats in the eastern vs. western sides of the parcel are structurally and floristically distinct. Sifakas in this parcel have small, discrete home ranges and are morphological folivores. For these reasons, I expected that the 6 groups studied would eat a different menu of food plants but with similar toughness values. Ring-tailed lemurs have comparatively large, overlapping home ranges, and I expected that the 5 study groups would eat similar foods. Despite living in different microhabitats across the parcel, sifakas exhibit high dietary uniformity both in dietary plant species composition and the toughness of the foods. Food selection in sifakas operates on two distinct levels. Sifaka groups share many key food species that appear independent of local abundances, but the ranking of the foods within each group appears related to availability. Ring-tailed lemur groups are more heterogeneous in the composition of their diets relative to sifakas, though the time spent feeding on individual foods reveals a marked preference for the fruits of Tamarindus indica by all groups. Food toughness is consistent across the parcel with the exception of the most western group. Ring-tailed lemurs are highly specific feeders, but indiscriminate nibblers. Sifakas are targeted, balanced feeders. There does not appear to be a consistent microhabitat effect operating across species. Differences within sifaka and ring-tailed lemur populations in food composition and toughness, however, correspond to an east-west microhabitat gradient. Measures of dietary flexibility must take into account not only the plant species consumed and the different parts eaten but also their associated food properties and proportion of time spent feeding on them.     

Disseminated toxoplasmosis in a captive ring-tailed lemur (Lemur catta)

A 3-yr-old secundiparous female ring-tailed lemur presented to the Auburn University Small Animal Clinic with signs of dyspnea, lethargy, and anorexia. The animal died before she could be examined, and a full necropsy was immediately performed. Provisional necropsy findings included moderate pneumonia and hepatopathy. Acute interstitial pneumonia and focal hepatocellular necrosis were confirmed histologically. Lung impression smears, histopathology, electron microscopy, immunohistochemistry, and tissue culture isolation resulted in a diagnosis of acute disseminated Toxoplasma gondii infection, which was confirmed by polymerase chain reaction. The isolate of T. gondii was avirulent for mice and was named AU Tgl and genetically is type II. The source of the infection remains unclear, but speculation suggests contaminated fruit or blackbirds (Passeriformes: Icteridae) acting as transport hosts for oocysts from nondomestic felids and feral cats on the property.     

Intermale affiliative behavior in ringtailed lemurs (Lemur catta) at the Beza-Mahafaly reserve, Madagascar

Intermale affiliative behavior was studied in three groups of naturally occurring ringtailed lemurs over a one-year period. The adult males in the sample exhibited affiliative behavior with all other males in their social groups; but affiliative behavior between some male-male dyads occurred markedly more often than between others. These dyads are called “preferred partnerships.” The formation of preferred partnerships did not appear to be influenced by male dominance rank or age-class. Furthermore, these partnerships were of a short-term nature, and none persisted throughout the entire study period. The following factors may explain the absence of rank or age effects, and the brevity of preferred partnerships: (1) frequent fluctuation in the male dominance hierarchy in each study group; (2) the fact that higher-ranking males may not offer specific benefits to lower-ranking males; and (3) the fact that male dispersal affected the male membership of each group over the 12-month study period. The focal males engaged in significantly more affiliative behavior during the lactation period compared with the other reproductive seasons. Migration partners may offer each other predator protection during the transfer process, and although males that transfer together do not engage in alliance or coalition behavior towards resident males, males transferring in pairs or threesomes are in a better position to spot and defend themselves against attack by resident males. Migration partners also provide social contact for each other while in the process of immigration.     

Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta

The study of physiological stress and its context in free-ranging animals provides a means for understanding the challenges found in the natural habitat. Patterns of physiological stress in free-ranging animals have yet to be well characterized. Methodological difficulties in measuring physiological responses in the natural habitat have limited this area of research. In this research, physiological stress in free-ranging ring-tailed lemurs, Lemur catta, was estimated using a steroid-extraction method to measure cortisol levels from female faeces. Ten females were observed across two social groups in southwestern Madagascar during a 5-month period including portions of the annual wet and dry seasons. I used behavioural measures to estimate predation threat, food accessibility and individual dominance status, to determine whether these variables predict faecal cortisol levels. Faecal cortisol levels were relatively high during two distinct periods: one period coincided with late gestation and the other period corresponded with the end of the dry season, when high-intensity antipredatory behaviour and estimates of feeding effort were elevated. In addition, faecal cortisol measures were significantly correlated with dominance indices: high-index individuals had high cortisol values, and low-index individuals had low cortisol values. These results suggest that faecal cortisol measures can be used to assess seasonal and individual differences in adrenal activity in this lemurid primate, and that this measure could provide a means for quantifying physiological stress in free-ranging animals. Copyright 1999 The Association for the Study of Animal Behaviour.     

Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history

The ring-tailed lemurs at Beza Mahafaly Special Reserve, Madagascar, exhibit a high frequency of severe wear and antemortem tooth loss. As part of a long-term study, we collected dental data on 83 living adult ring-tailed lemurs during 2003 and 2004. Among these individuals, 192 teeth were scored as absent. The most frequently missing tooth position is M1 (24%). As M1 is the first tooth to erupt, its high frequency of absence (primarily a result of wear) is not remarkable. However, the remaining pattern of tooth loss does not correlate with the sequence of eruption. We suggest that this pattern is a function of 1) feeding ecology, as hard, tough tamarind fruit is a key fallback food of ring-tailed lemurs living in gallery forests; 2) food processing, as tamarind fruit is primarily processed in the P3-M1 region of the mouth; and 3) tooth structure, as ring-tailed lemurs possess thin dental enamel. The incongruity between thin enamel and use of a hard, tough fallback food suggests that ring-tailed lemurs living in riverine gallery forests may rely on resources not used in the past. When comparing dental health in the same individuals (n=50) between 2003 and 2004, we found that individual tooth loss can show a rapid increase over the span of one year, increasing by as much as 20%. Despite this rapid loss, individuals are able to survive, sometimes benefiting from unintentional assistance from conspecifics, from which partially processed tamarind fruit is obtained. Although less frequent in this population, these longitudinal data also illustrate that ring-tailed lemurs lose teeth due to damage and disease, similar to other nonhuman primates. The relationship between tooth loss, feeding ecology, dental structure, and individual life history in this population has implications for interpreting behavior based on tooth loss in the hominid fossil record.