Population and social dynamics changes in ring-tailed lemur troops at Berenty,Madagascar between 1989 - 1999

In the present study, we recorded all births, immigrations, deaths, and emigrations for a population of ring-tailed lemurs at Berenty Reserve, Madagascar, between September 1989 and August 1999. In September 1989, three troops (C, B, and T) inhabited the study area of 14.2 ha. During the 10-year period, eight troop divisions, six evictions of females, and three troop takeovers of ranges by other troops occurred in and around the study area. Consequently, in August 1999, the number of troops in the same area increased to six (CX, C1, C2A, C2B, T1, and T2). The number of lemurs aged >1 year increased from 63 to 82, which resulted from 204 births, 58 immigrations, 125 deaths, and 118 emigrations. Of the 204 newborn lemurs during the study period, 103 died, 44 emigrated outside the study area, and 57 remained within the study area. The total number of lemurs that emigrated from natal troops was 69 (54 males and 15 females). Natal males left their troops around the age of 3. Non-natal males changed troops after a tenure varying from 1 to 7 years. Survival curves showed a fall in survival rates of both sexes to < 0.5 between the ages of 2 and 3. For females, the survival rate gradually decreased to < 0.2 at the age of 9. On the other hand, due to emigration, the survival rate of males could not be determined after the age of 5 yr. Since some males attained high-rank at the age of 6 – 10 yr, the prime age for male ring-tailed lemurs is thought to be around 7 – 10 yr. Ring-tailed lemurs are essentially female philopatric, because all cases of females leaving natal troops resulted from troop divisions or forced evictions. Such social changes may have resulted from competition among females. All cases of troop divisions or evictions occurred in larger troops consisting of ≥20 lemurs, and only a few females could rejoin their troops. When males joined such a female-group, a new troop was formed. Although promoted by an increase in population, frequent emigrations of females from original troops are the characteristics of ring-tailed lemurs at Berenty.     

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.     

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.     

Honest olfactory ornamentation in a female‐dominant primate

Sexual selection theory predicts that potential mates or competitors signal their quality to conspecifics. Whereas evidence of honest visual or vocal signals in males abounds, evidence of honest signalling via scent or by females is scarce. We previously showed that scent marks in male lemurs seasonally encode information about individual heterozygosity – a reliable predictor of immunocompetence and survivorship. As female lemurs dominate males, compete over resources, and produce sexually differentiated scent marks that likely evolved via direct selection, here we tested whether females also advertise genetic quality via olfactory cues. During the breeding season specifically, individual heterozygosity correlated negatively with the diversity of fatty acids (FAs) expressed in labial secretions and positively with the diversity of heavy FA esters. As odour–gene relationships predictive of health and survivorship emerged during a period critical to mate choice and female competition, we posit that genital scent marks function as honest olfactory ornaments in females.     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.     

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ² = 27.43, df = 3, p < 0.0001; 2001: χ² = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.     

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.     

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.     

Endocrine correlates of pregnancy in the ring-tailed lemur (Lemur catta): implications for the masculinization of daughters

Female ring-tailed lemurs (Lemur catta) are Malagasy primates that are size monomorphic with males, socially dominate males, and exhibit a long, pendulous clitoris, channeled by the urethra. These masculine traits evoke certain attributes of female spotted hyenas (Crocuta crocuta) and draw attention to the potential role of androgens in lemur sexual differentiation. Here, hormonal correlates of prenatal development were assessed to explore the possibility that maternal androgens may shape the masculine morphological and behavioral features of developing female lemurs. Maternal serum 17α-hydroxyprogesterone, dehydroepiandrosterone sulphate (DHEA-S), ?⁴ androstenedione (androst-4-ene-3,17,dione), testosterone, and 17β-estradiol were charted throughout the 19 pregnancies of 11 ring-tailed lemurs. As in spotted hyenas, lemur pregnancies were associated with an immediate increase in androgen concentrations (implicating early maternal derivation), followed by continued increases across stages of gestation. Pregnancies that produced singleton males, twin males, or mixed-sex twins were marked by greater androgen and estrogen concentrations than were pregnancies that produced singleton or twin females, especially in the third trimester, implicating the fetal testes in late-term steroid profiles. Concentrations of DHEA-S were mostly below detectable limits, suggesting a minor role for the adrenals in androgen biosynthesis. Androgen concentrations of pregnant lemurs bearing female fetuses, although less than those of pregnant hyenas, exceeded preconception and postpartum values and peaked in the third trimester. Although a maternal (and, on occasion, fraternal) source of androgen may exist for fetal lemurs, further research is required to confirm that these steroids would reach the developing female and contribute to her masculinization.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

豆野螟延迟交尾和多次交尾对生殖的影响

豆野螟Maruca vitrata(Fabricius)是一种严重的泛热带豆类蔬菜害虫。本文研究了豆野螟延迟交尾和多次交尾对其生殖的影响。延迟交尾实验结果表明:豆野螟雌雄同时延迟交尾,雌雄虫的寿命、产卵量均表现为先上升后下降的趋势,但是对卵的孵化率没有显著影响;雌虫延迟交尾,随着延迟时间的增加,雌虫的寿命、产卵量、卵的孵化率表现为下降的趋势,而雄虫的寿命延迟交尾第3天达到最大值;雄虫延迟交尾,随着延迟交尾时间的增加,雌雄虫的寿命、产卵量均表现为先上升后下降的趋势,卵的孵化率随着延迟逐渐下降。多次交尾实验结果表明,随着雄虫交尾次数的增加,成功交尾率逐渐降低,用于交尾的时间延长,雌虫和相应雄虫的寿命逐渐缩短,雌虫的产卵量下降,但对卵的孵化率影响不大;豆野螟雌虫一生只交尾一次,未见到雌虫2次交尾。     

Long-term changes in dominance ranks among ring-tailed lemurs at Berenty Reserve, Madagascar

A study was conducted between 1989 and 2001 to monitor changes in the dominance ranks among adult ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Adult females were observed to be dominant over adult males. Their rank fluctuated greatly. However, in some troops, female rank orders were fairly stable over a period of several years. In general, male ranks were more unstable than female ranks. Most young females aged 3 years occupied the lowest ranks among adult females. However, several were also observed to have attained relatively higher ranks, placing them right beneath their high-ranking mothers; this suggested the existence of dependent ranks. Mothers were dominant over their daughters. Similarly, older sisters were usually dominant over younger sisters. The mean duration of alpha status for females was 1.95 years, although considerable variation was observed in the duration of the alpha status (1–5 or more years). Most young males aged 3 years initially occupied the lowest ranks in their natal troops, and then they migrated to non-natal troops around the age of 4 years. They ascended in rank between the ages of 4 and 6 years, although there was considerable variation in the acquirement of high rank. The mean duration of alpha status for males was 2.2 years. Larger males were observed to occupy higher ranks. Occasionally, both males and females showed intense aggression (i.e., targeting aggression) towards others.     

The relative importance of different direct benefits in the mate choices of a field cricket

Discussions about the evolution of female mating preferences have often suggested that females should express multiple strong preferences when different male traits are correlated with different mating benefits, yet few studies have directly tested this hypothesis by comparing the strength of female preferences for male traits known to be correlated with different benefits. In the variable field cricket, Gryllus lineaticeps, females receive fecundity and fertility benefits from mating with males with higher chirp rates and life-span benefits from mating with males with longer chirp durations. Although females prefer higher chirp rates and longer chirp durations when the other trait is held constant, it is possible that they give priority to one of these song traits when both vary. In this study, we examined the relative importance of chirp rate and chirp duration in female mate choice using single-stimulus presentations of songs that varied in both chirp rate and chirp duration. Females expressed both directional and stabilizing preferences based on chirp rate, responding most strongly to a chirp rate approximately one standard deviation above the population mean. Females did not express preferences based on chirp duration, and did not express correlational preferences. These results suggest that females may give priority to the reproductive benefits provided by males that produce higher chirp rates.     

Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

Androgen levels and female social dominance in Lemur catta

Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are influenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and conflict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming effects for a complete understanding of this phenomenon.     

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.     

Social System of <Emphasis Type="Italic">Microcebus berthae</Emphasis>, the World’s Smallest Primate

Our goal was to provide a first characterization of the social system of pygmy mouse lemurs (Microcebus berthae), the worlds smallest primate species. During a 4-mo field study of 12 females and 27 males, we combined capture-recapture and morphometric data with detailed behavioral observations of individually marked subjects and genetic paternity analyses of a population in Kirindy Forest, western Madagascar. We describe the social organization of Microcebus berthae as a solitary forager living in an individualized neighborhood system characterized by extensive intra- and intersexual home range overlap of adult individuals within a male-biased population. Male and female pygmy mouse lemurs inhabited home ranges (males: 4.9 ha; females: 2.5 ha) that are more than twice as large as those of sympatric Microcebus murinus. On average, pygmy mouse lemurs of both sexes spent about half of the days sleeping alone. Preliminary analysis of genetic population structure suggests female philopatry and male dispersal. Sleeping associations of variable composition that consisted not preferentially of close relatives and proximity during part of the nightly activity contributed together with regular social interactions to the maintenance of a social network. The spatial distribution pattern of adult males and females, the absence of sexual size dimorphism, relatively large male testicular volume and moderate female estrous synchrony suggest a promiscuous mating system with a high potential for scramble competition. In general, there are many similarities between the social system of Microcebus berthae and those of other Microcebus spp. However, striking differences with sympatric gray mouse lemurs (Microcebus murinus) in female home range size, dispersion and sleeping behavior indicate the existence of species-specific socioecological adaptations in closely related species occupying very similar ecological niches.     

Total Energy Expenditure and Body Composition in Two Free-Living Sympatric Lemurs

Background

Evolutionary theories that account for the unusual socio-ecological traits and life history features of group-living prosimians, compared with other primates, predict behavioral and physiological mechanisms to conserve energy. Low energy output and possible fattening mechanisms are expected, as either an adaptive response to drastic seasonal fluctuations of food supplies in Madagascar, or persisting traits from previously nocturnal hypometabolic ancestors. Free ranging ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur sp.) of southern Madagascar have different socio-ecological characteristics which allow a test of these theories: Both gregarious primates have a phytophagous diet but different circadian activity rhythms, degree of arboreality, social systems, and slightly different body size.

Methodology and Results

Daily total energy expenditure and body composition were measured in the field with the doubly labeled water procedure. High body fat content was observed at the end of the rainy season, which supports the notion that individuals need to attain a sufficient physical condition prior to the long dry season. However, ring-tailed lemurs exhibited lower water flux rates and energy expenditure than brown lemurs after controlling for body mass differences. The difference was interpreted to reflect higher efficiency for coping with seasonally low quality foods and water scarcity. Daily energy expenditure of both species was much less than the field metabolic rates predicted by various scaling relationships found across mammals.

Discussion

We argue that low energy output in these species is mainly accounted for by low basal metabolic rate and reflects adaptation to harsh, unpredictable environments. The absence of observed sex differences in body weight, fat content, and daily energy expenditure converge with earlier investigations of physical activity levels in ring-tailed lemurs to suggest the absence of a relationship between energy constraints and the evolution of female dominance over males among lemurs. Nevertheless, additional seasonal data are required to provide a definitive conclusion.