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.     

Mating system in mouse lemurs: theories and facts, using analysis of paternity

Among nocturnal Malagasy prosimians, the grey mouse lemur (Microcebus murinus) is considered a solitary species which has a promiscuous mating system. Indirect indicators, such as the lack of sexual dimorphism, the overlapping of male and female home ranges with each other, the synchronism of seasonal oestrus and the high relative testes size of males, support the presence of sperm competition. In captivity, an intense sexual precopulatory competition develops among males, leading to the emergence of a dominant male who fathers the majority of the litters. Although multiple mating did occur, the dominant male achieved the majority of the matings on the first day of oestrus. A 'mate-guarding' behaviour, exhibited by the dominant male, was observed in 11 groups out of 15, on only the first day of the vaginal opening and was significantly more often directed towards younger females. Females also played an important role in sexual competition among males, since their presence enhances the aggressive interactions between males. Difference in aggressive behaviours of females, in response to male sexual solicitations, suggests female mate choice. Compared with data from wild animals, it may be hypothesised that alternative mating strategies can be used by male grey mouse lemurs to enhance their reproductive success, depending on the availability and distribution of receptive females.     

Mating system of Microcebus murinus

Microcebus murinus, a small nocturnal lemur from Madagascar, has retained features of ancient primates. Based on these ancestral traits, its social organization has often been used as a model for early primate social systems. In captivity it breeds polygynously, i.e., one male mates with several females, while females usually copulate only with the dominant male. The present project tested whether or not sexual size dimorphism, spatial distribution, and relative testis size of M. murinus correspond with predictions of the sexual selection theory concerning polygynous mating systems. The study was combined with a mark‐recapture study and radio tracking of 12 animals in 1993 in a dry deciduous forest of western Madagascar at the end of the dry season. Large overlapping home ranges in males, lack of sexual size dimorphism, and relatively large testes suggest a multi‐male mating system, i.e., one that is promiscuous rather than polygynous. Am. J. Primatol. 48:127–133, 1999. © 1999 Wiley‐Liss, Inc.     

Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis)

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.     

Habitat Utilization of Three Sympatric Cheirogaleid Lemur Species in a Littoral Rain Forest of Southeastern Madagascar

I compared the habitat utilization in 3 sympatric species of Cheirogaleidae (Microcebus murinus [81 g], Cheirogaleus medius [183 g] and Cheirogaleus major [362 g]) in a littoral rain forest in southeastern Madagascar during 3 rainy seasons. Females of promiscuous Microcebus murinus had small home ranges and the males had large overlapping home ranges. Home ranges of family groups of monogamous Cheirogaleus medius and C. major overlapped extensively. Home ranges of all 3 species overlapped completely in the study area but home range sizes differed among species and correlate positively with body masses. Male Microcebus murinus slept in open vegetation (79%) and alone (71%), whereas female M. murinus and family group members of Cheirogaleus spp. preferred communal sleeping in tree holes. There are significant interspecific differences in the choice of sleeping sites: smaller lemurs chose smaller trees and used more sleeping sites than larger lemurs did. Species also differed significantly in the vertical dimension of forest utilization: Cheirogaleus major used the upper part of the trees, C. medius used the middle parts, and Microcebus murinus used the understory during nocturnal activities. The 3 species differed mainly in vertical habitat utilization and showed vertical stratification.     

Sperm Competition and Optimal Timing of Matings in Microcebus murinus

Female promiscuity is common in mammals and leads to sperm competition: the sperm of ≥2 males compete for ova. Scientists understand the possible role of optimal insemination periods for male reproductive success in many species as well as the impact of monopolization of receptive females. Information from experiments combined with detailed observations from the field that allow determining the relative impacts of the elements in the same species are rare. We studied sperm competition and the role of optimal insemination periods in gray mouse lemurs (Microcebus murinus), a small solitary nocturnal primate from Madagascar. We used controlled matings to identify the relative impact of both contest and scramble competition, which characterize their mating system, on paternity. Fifteen females mated with 3–6 males in quick succession. Our experiments revealed that the optimal insemination period is during early receptivity. Early but not first mating males are more likely to sire offspring. Comparison with our field data indicate that the timing of male monopolization efforts correspond with the optimal insemination period.     

Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?

In group-living Malagasy primates (Lemuriformes), certain demographic and morphological traits deviate both from theoretical expectations derived from sexual selection theory and from patterns in better-known anthropoid primates. Lemurs lack sexual dimorphism in body and canine size and live in relatively small multimale-multifemale groups with, on average, even adult sex ratios, despite a polygynous mating system. In addition, the majority of gregarious lemurs are cathemeral, that is, they are regularly active both day and night. The social system of cathemeral lemurs has been considered an adaptation to their activity pattern. If so, groups should consist of multiple pairs that aggregate during diurnal activity and range separately at night in response to predation and infanticide risk, respectively. Moreover, mating privileges should exist between pair partners. We tested this hypothesis with data collected on two groups of wild redfronted lemurs in western Madagascar during 1023 focal animal hours spanning 4 months including the mating season. In addition, data on spatial relations were collected on 12 nights. We found no differences in group cohesion between day and night and no behavioural evidence for multiple male-female pairs. Instead, one male in each group monopolized social interactions with all females. However, females copulated with all resident males, although most often with the central male. Thus, basic predictions of the cathemerality hypothesis are unsupported. Multiple matings and indications of oestrous synchrony can be viewed as female counterstrategies against infanticide, whereas reproductive strategies of redfronted lemur males remain obscure. Copyright 1999 The Association for the Study of Animal Behaviour.     

Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar

The mating system and social organization of the gray mouse lemur (Microcebus murinus) was investigated in two three-month field studies (covering a period before, during, and after the first mating season) in Ampijoroa, northwestern Madagascar. The spatial and temporal distribution of the sexes within a population was studied using mark/recapture techniques and radiotelemetry to assess possible contest or scramble competition between the males. Sociality was inferred from the occurrence and probability of nocturnal social encounters, the temporal stability of daily sleeping groups, and nocturnal ranging patterns of co-sleepers. Males and females were evenly distributed in the study area within a network of highly overlapping home ranges. No indications were found for the spatial monopolization of the females by certain dominant males. Males and females had spatial access to several potential mates; the mating system is therefore characterized as a multi-male/multi-female system. Male home range sizes increased during the first mating season, which was interpreted as an indicator for scramble competition between the males. Competitive mate searching, sperm competition, and temporary mate guarding as well as female mate choice are suggested as the most probable reproductive strategies. Over the course of the study the animals lived continually within the study area, and most females formed stable individualized sleeping associations. Females that slept together shared a higher percentage of their home range than did females that slept at different sites. It is suggested that this network of social relationships should be described as a dispersed but individualized neighborhood.     

Mutual mate choice in a female-dominant and sexually monomorphic primate

Sexual dimorphism is common in polygynous species, where intrasexual competition is often thought to drive the evolution of large male body size, and in turn, male behavioral dominance over females. In Madagascar, the entire lemur radiation, which embraces diverse mating systems, lacks sexual dimorphism and exhibits frequent female dominance over males. The evolution of such morphological and behavioral peculiarities, often referred to as "the lemur syndrome," has proven difficult to understand. Among other hypotheses, a potential role of intersexual selection has been repeatedly proposed but hardly ever tested. Here, we investigate whether female choice favors small and compliant males, and whether male choice favors large females in captive gray mouse lemurs (Microcebus murinus). Detailed analysis of a combination of behavioral observations and hormonal data available for both sexes shows that (1) females accept more matings from males with higher fighting abilities, (2) males adjust their investment in intrasexual competition to female fertility, and (3) both male and female strategies are weakly influenced by the body mass of potential partners, in directions contradicting our predictions. These results do not suggest a prominent role of intersexual selection in the evolution and maintenance of the lemur syndrome but rather point to alternative mechanisms relating to male-male competition, specifically highlighting an absence of relationship between male body mass and fighting ability. Finally, our findings add to the growing body of evidence suggesting flexible sex roles, by showing the expression of mutual mate choice in a female-dominant, sexually monomorphic and promiscuous primate.     

Contest versus scramble competition for mates: The composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in North-west Madagascar

The modes of intrasexual competition interacting in many dispersed societies of nocturnal solitary foragers are still poorly understood. In this study we investigate the spatial structure within a free-living population of gray mouse lemurs (Microcebus murinus) in order to test for the first time the predictions from two contrasting models of male intrasexual competition on the population level. The contest competition model predicts an uneven distribution of the sexes in a population nucleus with a female biased sex ratio in the center and a male biased sex ratio in the periphery. In contrast the scramble competition model predicts males and females being distributed evenly throughout their habitat with a constant sex ratio. Nine capture/recapture periods within three consecutive mating seasons revealed a continuous male biased sex ratio in the adult population with even trapping rates for the sexes. The male biased sex ratio could either be explained with postnatal female biased mortality or with a male biased natal sex ratio. This male biased sex ratio was apparent in all parts of the study site, indicating that the population was not subdivided into a female biased core and a male biased periphery. Furthermore, the majority of adult males have been captured at the same site as or in vicinity to females. Consequently, a large proportion of males had spatial access to females during the mating season. No signs of monopolization of females by certain dominant males could be detected. These data support the predictions from the scramble competition model and the concept of a promiscuous mating system for this species.     

The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate

Male excess mortality is widespread among mammals and frequently interpreted as a cost of sexually selected traits that enhance male reproductive success. Sex differences in the propensity to engage in risky behaviours are often invoked to explain the sex gap in survival. Here, we aim to isolate and quantify the survival consequences of two potentially risky male behavioural strategies in a small sexually monomorphic primate, the grey mouse lemur Microcebus murinus: (i) most females hibernate during a large part of the austral winter, whereas most males remain active and (ii) during the brief annual mating season males roam widely in search of receptive females. Using a 10-year capture-mark-recapture dataset from a population of M. murinus in Kirindy Forest, western Madagascar, we statistically modelled sex-specific seasonal survival probabilities. Surprisingly, we did not find any evidence for direct survival benefits of hibernation-winter survival did not differ between males and females. By contrast, during the breeding season males survived less well than females (sex gap: 16%). Consistent with the 'risky male behaviour' hypothesis, the period for lowered male survival was restricted to the short mating season. Thus, sex differences in survival in a promiscuous mammal can be substantial even in the absence of sexual dimorphism.     

Comparison of Reproductive Characteristics and Changes in Body Weight Between Captive Populations of Rufous and Gray Mouse Lemurs

The nocturnal Malagasy mouse lemurs are among the smallest primates worldwide. Several sibling species are known. Of these, the rufous and the gray mouse lemur differ with respect to morphology, genetics, and communication. They might also differ in seasonal reproduction and body weight changes. We investigated and compared reproductive activities and changes in monthly body weight in males and females of successfully breeding colonies of both species under the same photoperiodic conditions. Females of both species showed estrous cycles only during the long-day period. Rufous mouse lemur females seemed to have a shorter gestation than their sibling species (57 vs. 62 days). The number of estrous cycles (2.25 vs. 2.5/season) and their lengths (59 vs. 52 days) were similar. Litter size (2) seemed to be similar. Latency of estrous occurrence after photoperiodic stimulation was longer in Microcebus rufus than in its sibling species (71.6 and 42.3 days). The same was true for the onset of the growth of the testes. The rate of growth and size of the testes were similar, and precede the estrous onset in both species. The reproductive activity was shorter in both sexes of the rufous than of the gray mouse lemurs. In both species, body weight showed similar seasonal changes. Males lost more weight during the breeding season than females did. In rufous mouse lemurs, body weight was similar in both sexes during the nonbreeding season. In gray mouse lemurs, sexes differed throughout the year.     

Sleeping and Ranging Behavior of the Sambirano Mouse Lemur, <Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>

Primates require secure sleeping sites for periods of rest, but despite their importance, the characteristics of desired sleeping sites are poorly known. Here we investigated the sleeping ecology of a radio-collared population of the Sambirano mouse lemur, Microcebus sambiranensis, during the nonreproductive season in the Anabohazo forest, northwestern Madagascar. We also investigated their ranging behavior and examined the spatial distribution of sleeping sites within the home ranges of the collared individuals. We took measurements of the sleeping tree’s physical characteristics and recorded the number of collared individuals using each sleeping site. We found that M. sambiranensis generally use foliage sleeping sites more frequently than tree holes and individuals slept more frequently in densely foliated trees than in sparsely foliated trees, often alone. We observed no significant differences in home range size or nightly travel distance between males and females; however, home ranges were smaller than those described for other mouse lemur species. Finally, we found that M. sambiranensis sleep peripherally and forage centrally within their home ranges, a behavior not previously described for mouse lemurs. Our results indicate profound differences in the social organization between M. sambiranensis and other mouse lemur species described in the literature, suggesting species-specificity in mouse lemur ecology. Understanding the sleeping ecology and ranging behavior of mouse lemurs is of great importance to their conservation, as these data facilitate the planning of long-term reforestation, habitat management, and population assessment.     

Indications for female mate choice in grey-cheeked mangabeys <Emphasis Type="Italic">Lophocebus albigena johnstoni</Emphasis> in Kibale National Park,Uganda

Female sexual strategies affect male strategies and can play an important role in shaping mating systems. We investigated female sexual behaviour within five groups of grey-cheeked mangabeys in Kibale National Park, Uganda, and tested the hypothesis that females exhibit mate choice using as indications the prevalence of (1) females soliciting matings by presenting to males and (2) females refusing to mate with approaching males. In addition, we describe how these behaviours as well as grooming and copulation calls are distributed over high-ranking, low-ranking and migrating males and discuss these patterns with regard to trade-offs that could play a roll in female mate choice in multi-male groups. Females were promiscuous and initiated almost half of the matings, with both resident and migrating males. More than half of male mating approaches were refused by peak females. Female mate choice in this species may depend on individual female preferences, oestrus phase and male tactic.     

Spatio-Temporal Factors Shaping Diurnal Space Use by Pygmy Rabbits

Abstract: Factors influencing patterns of space use by pygmy rabbits (Brachylagus idahoensis) are poorly understood. We studied diurnal space use by adult pygmy rabbits during multiple breeding and nonbreeding seasons at 3 sites in the Lemhi Valley, Idaho, USA, during 2004–2005. Pygmy rabbits used larger areas than predicted by allometric models and documented by some previous investigations. Sex and season strongly influenced space use by rabbits. Males used larger home ranges and core areas, more burrow systems, and more widely dispersed burrow systems than did female rabbits. We also documented significant differences among study sites in many movement parameters, which suggested that local resource distribution also might influence how pygmy rabbits use space. Our results indicated that pygmy rabbits use large areas and exhibit seasonal, sex, and site-specific variation in patterns of movement and space use. Therefore, larger areas of habitat may be needed to conserve pygmy rabbits to accommodate seasonal, regional, and potentially annual variation in resource availability and to maintain linkages among populations.     

Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar

I aimed to determine when and under which seasonal environmental conditions gray mouse lemurs (Microcebus murinus), a small nocturnal primate species endemic to Madagascar, utilize daily torpor. Using temperature-sensitive radio collars, I measured skin temperature (T _sk ) of free-ranging mouse lemurs under natural conditions. My results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a ) during the dry season, but not during the rainy season. Mouse lemurs that remained normothermic had significantly lower body masses (mean: 59.7 g) than individuals that used torpor (mean: 80.2 g). Skin temperatures dropped to 20.9°C and the mean torpor bout duration is 10.3 h. The use of torpor on a given night varied among individuals, whereas the propensity for torpor did not differ significantly between males and females. I found no evidence that T _a can be used to predict whether mouse lemurs will remain normothermic or enter torpor. It appears that the most reliable indicator for the occurrence of torpor in free-ranging Microcebus murinus is time of the year, i.e., photoperiod.     

Preliminary observations on sexual behavior and the mating system in free-ranging lesser galagos. (Galago moholi)

Sexual and associated patterns of behavior of lesser galagos (Galago moholi) were recorded during an 18-month study conducted at the Nylsvley Nature Reserve in South Africa. Animals were trapped and fitted with radio transmitter belts in order to monitor nocturnal activities during twice-yearly mating seasons. Most copulations occurred during the last week in May, while a subsidiary (post-partum) mating season occurred in late September-early October. Females came into estrus sequentially during the May season. Adult males exhibited increase in body weight and testes volume during the mating season, changes which were most pronounced among the larger males (> 226 g). Larger males also had the greatest mating success, initiating 88% of observed copulations. Sixty-seven percent of matings involved more than one male copulating with the same female during her estrus, which lasted 1-3 days. Mounts were prolonged (range 2-53 min, mean 9.0 min) and males copulated repeatedly (2-5 times) with the same partner during a single night. These observations of sexual behavior and of large relative testes size in free-ranging lesser galagos are consistent with the occurrence of a dispersed mating system involving sperm competition in this nocturnal prosimian species.     

Sperm storage in a seasonally reproducing African vespertilionid, the banana bat (Pipistrellus nanus) from Malawi

Spermatogenesis in the banana bat ( Pipistrellus nanus ) from southern Malawi began in the hot, wet season (February to April) and spermatozoa were released to the cauda epididymides at the beginning of the cool, dry season (May). Mating occurred between mid-June and early July, in the middle of the cool, dry season. After mating, spermatozoa were stored by the female until ovulation in August and by the male until at least September. The period of female sperm storage effectively lengthened the reproductive cycle so that early spermatogenesis occurred during the second half of one hot, wet season and births at the beginning of the following hot, wet season. During the period of sperm storage, males and females roosted together and group membership was labile, suggesting that the mating system may be promiscuous (both males and females mating with more than one partner) and that sperm competition may occur. The similarity between the chronology of reproduction in Malawi, Kenya, and South Africa leads us to propose that sperm storage occurs at all three localities.     

Male and Female Activity Patterns in Microcebus murinus During the Dry Season at Kirindy Forest, Western Madagascar

I investigated sexual differences in activity levels, and their adaptive significance in gray mouse lemurs, Microcebus murinus, during the dry season. I studied them between April and September, 1999, at Kirindy Forest, a dry deciduous forest in western Madagascar. Six males and 6 females were radiocollared and followed using focal individual sampling. The males remained active throughout the dry season, whereas the females hibernated for up to 3 mo. Males exhibited a gradual decrease in activity from May to June and some of them remained inactive for periods of a few days to 1 wk. Males were more active in July. Though there were changes in the duration of time spent sleeping, there was no significant change in male body mass throughout the period. Males appear to prefer to rest in nests that are close to or coincident with those preferred by females, and multiple males may simultaneously share nests with multiple hibernating females. Males occupying nests that are close to or coincident with nests preferred by females tend to switch nests less frequently than others do. Researchers have suggested that high levels of activity prepare males for the mating season, which occurs at the end of the dry season. Presumably, by maintaining an active lifestyle throughout the dry season, certain males may position themselves to monopolize the best tree holes during the mating season. The reproductive advantages gained by this behavior may overshadow the costs of remaining active during the dry season when resources are scarce, temperatures are low, and predator pressure is high. Measurements on captured males confirm a weak (nonsignificant) positive correlation between body mass and activity levels. There is no indication that the heavier, more active males were better able to monopolize the best tree holes.     

The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups

We examined genetic consequences of basic predictions of life history and sexual selection theory in a wild population of redfronted lemurs. Because group living in lemurs evolved independently from other primates, and because polygynous lemurs deviate in several sexually selected traits from theoretical predictions, data on genetic correlates of their social and mating systems can make important contributions to studies of convergence in social evolution, but such data are not available from wild populations. We extracted DNA from tissue samples obtained from 59 animals living in Kirindy forest, Madagascar, and examined individual variability at several microsatellite loci and the mitochondrial D-loop. We found that closely related females of a single matriline formed the core of the four main study groups. Virtually all haplotypes of adult males differed from those of coresident females, and many male haplotypes were represented by only one or two individuals. Paternity analyses for infants from groups with detailed behavioural data revealed that a disproportionate share of infants were sired by the central, dominant male of a group, despite promiscuous mating. Extragroup paternities were not detected. The skew in male reproductive success cannot be reconciled with the lack of sexual dimorphism and the even adult sex ratios. We therefore conclude that these group-living lemurs converge with many other primates in sex-specific life history trajectories, including female philopatry and male dispersal, but that the observed skew in male reproductive success makes the apparent lack of adaptation to intrasexual selection in certain behavioural, demographic and morphological traits even more puzzling. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.