Male-female affiliative relationships in naturally occurring ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

Affiliative behavior between adult male and female ringtailed lemurs was examined as part of a project concerning male affiliation with conspecifics of all age/sex classes. Males in three social groups were studied over a 12 month period. Male-female preferred partnerships existed, and were variable according to reproductive season. Dominance rank, age, or tenure of the male did not appear to affect either the number of partnerships or frequency of affiliative behaviors that males had with females. However, males residing in groups with fewer males exhibited both higher frequencies of affiliative interactions with females and were nearest neighbors to females more often than males living in a group containing more males. Females were found to be responsible for proximity maintenance of male-female dyads in the majority of cases. Neither reproductive season nor seasonal availability of food resources strongly affected the frequency of affiliative interactions between males and females, it is proposed that an important aspect of successful group membership for male ringtailed lemurs relates to the development of social relationships with adult females. Males can benefit from such relationships in terms of greater centrality to the spatial core of the group, which can result in enhanced predator protection, greater opportunities for social contact, and potentially greater access to estrous females. © 1996 Wiley-Liss, Inc.     

Lactation and care for unrelated infants in forest-living ringtailed Lemurs

An adult female ringtailed lemur (Lemur catta) known not to have been pregnant showed spontaneous lactation in response to twin infants born to an unrelated female. The females had met only 7 months earlier, when they and two other unrelated adult females were released from separate locations in a forest enclosure to form a new social group. Three months after release, an adult male from an adjacent enclosure gained access to the new group for 1 day, the day of one female's estrus. No males had access to the females throughout the remainder of the breeding season. Within 2 weeks of the birth of the twins, one of the other adult females began carrying the infants frequently, typically one at a time. All three females were checked for lactation when the infants were two months old. Both their mother and the unrelated adult who had been carrying the infants were producing milk. The third adult female, who never carried either infant, had no milk. The third adult female, who never carried either infant, had no milk. This female, however, like the two maternal females, frequently attacked unfamiliar immigrating adult males when the males approached the infants. Potential implications of these observations concerning the social organization of ringtailed lemurs are discussed.     

Male life history and intergroup mobility among ringtailed lemurs (Lemur catta)

Lemur catta shares a male-biased dispersal pattern with most primate species and the majority of mammals. Individuals in a free-ranging population of ringtailed lemurs were captured, marked, released, and monitored for a 40-month period. Sixty-four percent of the males (43 of 67) migrated or were missing within this period and all nine censused groups were affected by migration. Males migrate from their natal group and then may migrate again after reaching full adult body weight. Full-sized adult males migrate at a rate of 0.28 per year or once every 3.5 years and may change groups a number of times during their life. Migrations occurred within a 6-month period, ending just after the mating season. However, there is no direct connection between mating success and male migration. Females mate with transferring males, with group males, and with visitors from adjacent groups. The age-related pattern of male migration and the occurrence of extragroup mating inLemur catta is similar to that described for several species of macaques.     

Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis)

Knowledge of the social organization of lemurs is still limited for most species. Where there is sufficient information, it has been shown that lemur social organization differs in essential points from that of other primates. In the field study reported here, demographic structure and life-history processes were investigated in order to characterize the social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data were obtained through captures and observations. Alaotran gentle lemurs were found in small groups of up to nine individuals. Although most groups contained just one breeding female, a substantial proportion of groups (35%) had two breeding females. Therefore, Alaotran gentle lemurs cannot be classed as being organized in monogamous family groups. An extended birth season was found, and groups with two breeding females had significantly higher breeding output per adult than groups with a single adult female. Limited data suggest that females emigrate from their natal group while still subadult, whereas males can stay in the natal group until they are fully grown and disperse as adults. Variability in group composition, significantly higher reproductive output per adult in groups with two breeding females, and delayed dispersal of males suggest that Alaotran gentle lemurs pursue a resource-defense mating strategy, rather than a female-defense mating strategy. The suggestion that extant social lemurs may have evolved from a monogamous system, could explain the differences between lemur social systems and those of other primates.     

Measuring social tolerance: An experimental approach in two lemurid primates

Social tolerance crucially affects the life of group‐living animals as it can influence, among other things, their competitive regimes, access to food, learning behavior, and recruitment. However, social tolerance tests were mainly conducted in semi‐free or captive populations, and we know little about the behavioral mechanisms and consequences of social tolerance under natural conditions. We therefore developed a co‐feeding experiment to measure social tolerance in groups of wild and captive animals across two primate species. Specifically, we recorded the social tolerance level of redfronted lemurs (Eulemur rufifrons, four wild, one captive group) and ringtailed lemurs (Lemur catta, three wild, three captive groups) by presenting a clumped food resource in an experimental arena, and recorded patterns of resource use during the experiment. Because redfronted lemurs exhibit lower levels of decided conflicts than ringtailed lemurs, we predicted that they would be socially more tolerant. The probability for an individual to feed in the arena was higher in redfronted lemurs than in ringtailed lemurs. In addition, in both species, the probability for an individual to feed in the arena was higher in the captive populations than in their wild counterparts, suggesting that proximate factors, such as a relaxation of feeding competition in captivity, may adapt species‐specific levels of social tolerance to local levels of food availability. Hence, the number of individuals co‐feeding on a valuable food resource appears to be a useful proxy of social tolerance that could be measured with this experimental setup in other wild and captive species as well.     

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.     

藏酋猴社群雌体的性行为模式

猕猴属中大部分种类的繁殖类型可划分为季节性繁殖和非季节性繁殖两大类型。但是藏酋猴全年均有交配行为发生, 而产仔仅在1～8月间, 其类型属特殊的非季节性交配-季节性产仔繁殖类型。藏酋猴雌性在妊娠后选择的交配对象主要是高序位的雄性, 但非妊娠雌性则主要选择低序位雄性。妊娠后的雌性交配频率低于非妊娠雌性, 同时它们与成年雄性间理毛行为的发生频率亦低, 反之受到成年雄性攻击的频率却高。     

Sex and seasonal differences in aggression and steroid secretion in Lemur catta: are socially dominant females hormonally 'masculinized'?

Female social dominance characterizes many strepsirrhine primates endemic to Madagascar, but currently there is no comprehensive explanation for how or why female lemurs routinely dominate males. Reconstructing the evolutionary pressures that may have shaped female dominance depends on better understanding the mechanism of inheritance, variation in trait expression, and correlating variables. Indeed, relative to males, many female lemurs also display delayed puberty, size monomorphism, and 'masculinized' external genitalia. As in the spotted hyena (Crocuta crocuta), a species characterized by extreme masculinization of the female, this array of traits focuses attention on the role of androgens in female development. Consequently, I examined endocrine profiles and social interaction in the ringtailed lemur (Lemur catta) to search for a potential source of circulating androgen in adult females and an endocrine correlate of female dominance or its proxy, aggression. I measured serum androstenedione (A(4)), testosterone (T), and estradiol (E(2)) in reproductively intact, adult lemurs (10 females; 12 males) over four annual cycles. Whereas T concentrations in males far exceeded those in females, A(4) concentrations were only slightly greater in males than in females. In both sexes, A(4) and T were positively correlated, implicating the Delta(4)-biosynthetic pathway. Moreover, seasonal changes in reproductive function in both sexes coincided with seasonal changes in behavior, with A(4) and T in males versus A(4) and E(2) in females increasing during periods marked by heightened aggression. Therefore, A(4) and/or E(2) may be potentially important steroidal sources in female lemurs that could modulate aggression and underlie a suite of masculinized features.     

Coat condition of ringtailed lemurs,Lemur catta at Berenty Reserve,Madagascar: I. differences by age,sex, density and tourism, 1996–2006

An index of coat condition can be a non‐invasive tool for tracking health and stress at population level. Coat condition in ringtailed lemurs, Lemur catta, was recorded during September–November birth seasons of 1996, 1997, 1999, and 2001–2006 at Berenty Reserve, Madagascar. Condition was scored on a scale from 0: full, fluffy coat with guard hairs present, to 5: half or more of body hairless. Adult males did not differ overall from adult females. Coats were worse in adults than in 2‐year‐old subadults; 1‐year‐old juveniles were intermediate. Mothers and adult males lost coat condition as the season progressed: non‐mother females maintained condition. Years 1999–2002 scored better coats than either 1996–1997 or 2003–2006. Lemurs in high population density areas had worse coats than in natural forest, but tourist presence had less effect than density. Monitoring coat condition in an apparently healthy population reveals differences between population segments, and in a forest fragment with limited immigration or emigration it can track progressive changes, correcting impressions of progressive improvement or degradation over time. Above all it gives a baseline for response to climate changes or eventual pathology. Am. J. Primatol. 71:191–198, 2009. © 2008 Wiley‐Liss, Inc.     

Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides

The hormonal mediation of dispersal in female mammals is poorly understood, in part because of the difficulties of detecting the onset of ovarian cycling and puberty in dispersing individuals. We used noninvasive methods of faecal steroid assays to determine the timing of dispersal relative to puberty and ovarian cycling in wild female muriqui monkeys, a species in which males are philopatric and nearly all females transfer from their natal groups. Natal females had a mean+/-SE age of 73.4+/-7.2 months (N=18) at the time of their transfers. Intergroup transfers occurred when one or more sexually active adult females were present, but did not show any seasonal patterns. Faecal progesterone and oestradiol profiles from nine natal females prior to transfer and four non-natal females that transferred into our study group demonstrate unequivocally that dispersal occurs prior to puberty in this species. All females showed baseline oestradiol levels and low progesterone levels compared with cycling adult females. Immigrants were first observed to copulate at 11.2+/-2.2 months of age (N=4), prior to the onset of normal ovarian cycles, and gave birth to their first offspring at 33.8+/-7.3 months (N=4) after transferring. Mean cortisol levels did not differ between natal emigrants or recent immigrants, and were within the range of those of adult males during the nonbreeding season in 10 of the 11 prepubertal females sampled. These results indicate that female dispersal is not triggered by activational hormones associated with puberty or escape from reproductive suppression in this species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Patterns of wounding in stumptail macaques (macaca arctoides)

A three-year study of the patterns of wounding in a group of stumptail macaques (Macaca arctoides) was conducted at the Yerkes Regional Primate Research Center Field Station. Wounds were classified as punctures, lacerations or abrasions. Data were analyzed to determine if patterns of wounding vary by age/sex class, body part or wound type. Results indicate that adult males receive significantly more total wounds than expected, based on their total time spent in the group. Adult males also receive more serious wounds than other age/sex classes. Low-ranking animals are wounded more often than high-ranking individuals. Moreover, the location of wounds within each age/sex class is non-random. Adult males receive a disproportionate number of wounds on the forequarters, but adult and immature females are wounded disproportionately on the hindquarters. Finally, age/sex classes differ in the number of wounds on individual body parts. Adult males receive more wounds on the head, arms and hands than other age/sex classes, but adult and immature females receive more wounds on the feet than other age/sex classes. These results demonstrate that wounding patterns are clearly non-random and depend on a variety of factors such as age, sex and dominance rank.     

Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus

We examined predictions on the proportion of dispersing natal males and females, dispersal distances, the age at dispersal and the potential for inbreeding over a 6-year period in a free-living population of grey mouse lemurs. We used monthly mark-recapture procedures to determine individual locations and interindividual distances. The analysis of seven polymorphic microsatellite markers for 213 (130 males, 83 females) individuals allowed us to estimate relatedness coefficients and kinship relationships. Closely related males ranged further from each other than closely related females and natal males were found further from their potential mothers than were females. Natal males were more likely to disperse from their birth sites than females, although male dispersal was not universal. Male breeding dispersal was detected in half of the long-term observations. Males therefore seem to be the predominant vectors for gene flow between populations and social units. Females usually stayed within one to two home range diameters of their potential mother, facilitating the evolution of cooperative behaviour by kin selection among females. Most dispersal took place before the mating season, indicating an age of less than 7 months for natal dispersal. The analysis of spatiotemporal coexistence revealed the potential for inbreeding in only 3.8% of the potential mother-son dyads, but in 21.9% of the potential father-daughter dyads and in 41.7% of other closely related male-female dyads. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Reproductive parameters of female Japanese macaques: Thirty years data from the arashiyama troops,Japan

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mother's age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A female's rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.     

Victims of Infanticide and Conspecific Bite Wounding in a Female-Dominant Primate: A Long-Term Study

The aggression animals receive from conspecifics varies between individuals across their lifetime. As poignantly evidenced by infanticide, for example, aggression can have dramatic fitness consequences. Nevertheless, we understand little about the sources of variation in received aggression, particularly in females. Using a female-dominant species renowned for aggressivity in both sexes, we tested for potential social, demographic, and genetic patterns in the frequency with which animals were wounded by conspecifics. Our study included 243 captive, ring-tailed lemurs (Lemur catta), followed from infancy to adulthood over a 35-year time span. We extracted injury, social, and life-history information from colony records and calculated neutral heterozygosity for a subset of animals, as an estimate of genetic diversity. Focusing on victims rather than aggressors, we used General Linear Models to explain bite-wound patterns at different life stages. In infancy, maternal age best predicted wounds received, as infants born to young mothers were the most frequent infanticide victims. In adulthood, sex best predicted wounds received, as males were three times more likely than females to be seriously injured. No relation emerged between wounds received and the other variables studied. Beyond the generally expected costs of adult male intrasexual aggression, we suggest possible additive costs associated with female-dominant societies – those suffered by young mothers engaged in aggressive disputes and those suffered by adult males aggressively targeted by both sexes. We propose that infanticide in lemurs may be a costly by-product of aggressively mediated, female social dominance. Accordingly, the benefits of female behavioral ‘masculinization’ accrued to females through priority of access to resources, may be partially offset by early costs in reproductive success. Understanding the factors that influence lifetime patterns of conspecific wounding is critical to evaluating the fitness costs associated with social living; however, these costs may vary substantially between societies.     

General Gregariousness and Specific Social Preferences among Wild Chimpanzees

Wild chimpanzees form temporary parties that vary in size and composition. Previous studies have revealed considerable intraspecific variation in party compositions. We examined patterns of association among age, sex, and reproductive classes of chimpanzees at Ngogo in the Kibale National Park, Uganda. We employed a class-based association index and a randomization procedure to control for confounding factors and to test for differences between classes. Results indicate that males associated with other males significantly more than expected if all classes behaved equivalently, while females generally associated with individuals of the same sex less than expected. To interpret these patterns we used two additional indices that separate associations into two components: general gregariousness and preference for particular classes of associates. Males and estrous females were more gregarious than other classes, while anestrous females were less so. After controlling for general gregariousness, adult males as a class showed no specific preference for associating with each other. Anestrous females preferred each other as party members, and estrous females avoided each other. These results are consistent with previous findings that adult males are more gregarious than females. They diverge from the standard picture of chimpanzee society, however, by suggesting a mutual affinity among anestrous females, but not among adult males as a class.     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality

Body mass is a key determinant of fitness components in many organisms, and adult mass varies considerably among individuals within populations. These variations have several causes, involve temporal and spatial factors, and are not yet well understood. We use long-term data from 20 roe deer cohorts (1977-96) in a 2600 ha study area (Chizé, western France) with two habitats contrasting in quality (rich oak forest in the North versus poor beech forest in the South) to analyse the effects of both cohort and habitat quality on adult mass (i.e. median body mass between 4 and 10 years of age) of roe deer (Capreolus capreolus). Cohort strongly influenced the adult body mass of roe deer in both sexes: males born in 1994 were 5.2 kg heavier when aged between 4 and 10 years old than males born in 1986, while females born in 1995 were 4.7 kg heavier between 4 and 10 years old than females born in 1982. For a given cohort, adult males were, on average, 0.9 kg heavier in the rich oak forest than in the poor beech forest. A similar trend occurred for adult females (0.5 kg heavier in the oak forest). The effects of cohort and habitat were additive and accounted for ca. 40% of the variation observed in the adult mass of roe deer at Chizé (males: 41.2%; females: 40.2%). Population density during the spring of the birth accounted for about 35% of cohort variation, whereas rainfall in May-June had no effect. Such delayed effects of density at birth on adult body mass probably affect population dynamics, and might constitute a mechanism by which delayed density-dependence occurs in ungulate populations.     

Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve,Madagascar: a 15-year perspective

Over 15 field seasons (1987-2001), we collected census and life-history data on a population of individually identified ring-tailed lemurs at the Beza Mahafaly Reserve, Madagascar. No significant difference was found in population size over the study period, though a marked decline in the population occurred following a 2-year drought. The population rebounded rapidly after the immediate postdrought period. There was nearly a complete replacement of individuals over the study period. Average group size is 11.5 animals, and adult male to female sex ratio is 0.92. Most females reproduce annually, and the average fecundity rate is 84.3%. The greatest variability in fecundity is found among old females. We suggest that ring-tailed lemur females follow an "income breeding" strategy, i.e., females use maximum resources during reproduction rather than relying on fat stores, as do "capital breeders." Infant mortality to 1 year of age in a nondrought year is 52%, higher than infant mortality in small to medium-sized anthropoids. The oldest known female was 18 years old in 2001. We suggest that 18-20 years may represent the maximum life-span for wild ring-tailed lemurs. Because males regularly emigrate from the population, we have no data regarding male life-span; however, there is some indication that males do not survive as long as females. Group fission has occurred three times: twice from one parent group living in the driest area of the reserve, with the most dispersed food resources. We suggest that the reproductive strategy that has evolved in this species, wherein females reproduce early in life and annually until old age, is a response to the unusual climate and environmental conditions under which Lemur catta has evolved.     

Hibernating patterns of free-ranging Columbian ground squirrels

Summary The patterns of torpor and euthermy during hibernation was documented for 28 free-ranging Columbian ground squirrels (Spermophilus columbianus) fitted with temperature-sensitive radio transmitter collars. Adult males began hibernation earlier, were euthermic for a greater proportion of the hibernating season and emerged earlier than other age and sex classes. The patterns of hibernation of adult females did not differ significantly from those of juveniles. Emergence from the hibernaculum was preceded by a long (3–12 d) euthermic interval in adult males but not in adult females or juveniles. Changes in soil temperature did not appear to initiate emergence. The greater time spent euthermic by adult males is interpreted as a significantly greater energy cost of hibernation for adult males than for other age and sex classes. The benefits offsetting these costs may be increased reproductive potential in spring and avoidance of predation in late summer.     

Natural Disasters and Primate Populations: The Effects of a 2-Year Drought on a Naturally Occurring Population of Ring-Tailed Lemurs (Lemur catta) in Southwestern Madagascar

We examine demographic patterns from a long-term study (1987–1996) of the population of ring-tailed lemurs in the Beza-Mahafaly Special Reserve, in southwestern Madagascar. In particular, we focus on the effects that a severe drought in 1991 and 1992 had on the population. The population of adult animals peaked in 1991 but decreased rapidly during the subsequent drought and immediate postdrought years. In the 1992 birth season (and second year of the drought) infant mortality reached 80%, and 20.8% of all adult females in the reserve died. The following year, adult female mortality reached a high of 29.9%. Juvenile mortality in 3 intensively studied groups was 57% during the second year of the drought. We compare these data with infant, juvenile, and adult female mortality in non-drought years. We are not able to calculate adult male mortality, as they often emigrate from the reserve to the adjacent forest; however, in the same 3 intensively studied groups, 89% of the males disappeared during the 2 immediate postdrought years. By 1996, the population had begun to recover after the decline that correlated with the drought conditions. Annual reproduction, high birth rates (.80–.86 annually), early sexual maturity, and dietary adaptability may be contributing factors to the recovery. Effects of and recovery from this type of natural disaster in the Beza Mahafaly ring-tailed lemur population parallel responses of some species of macaques and baboons with respect to the adaptability of edge species.