Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus)

The aim of this study was to examine effects of seasonal and social factors on male androgen excretion in a seasonally breeding primate living in multimale-multifemale groups. By combining detailed behavioural observations (>2,500 h) on 3 groups of redfronted lemurs living in Kirindy Forest/Madagascar with non-invasive hormone analysis of >800 faecal samples collected concomitantly from the same animals, we tested predictions on: (1) the effect of social status on immunoreactive testosterone (iT) excretion; (2) seasonal variation of iT across reproductive periods; and (3) the relationship between aggression and iT excretion. The study lasted 14 months, covering two mating and one birth season. The results revealed that males fall into two distinct social classes, with one dominant male and several subordinate males in each group. In contrast to our prediction, the behavioural differences between these two classes were not reflected by differences in androgen levels, making physiological suppression of testicular function an unlikely mechanism of male reproductive competition. As expected for a seasonally breeding animal, iT values were elevated during the mating season. Androgen levels tracked the increase in the rate of reproductive aggression during the mating season as predicted by the challenge hypothesis. An increase in aggression due to spontaneous social instability outside the mating season, however, was not linked to a parallel rise of iT. Furthermore, the highest iT levels were obtained during the birth season, which may be part of a male strategy to remain aggressive during this period of high infanticide risk. These findings suggest that redfronted lemurs do not respond with increases in androgens to short-term challenges and that high androgen levels instead correlate with longer-lasting and predictable situations, such as the mating and birth seasons.     

Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system

Many mammals warn conspecifics with alarm calls about detected predators. These alarm calls are either functionally referential, urgency based, or they can have multiple functions, including predator deterrence. The taxonomic distribution of these alarm call systems is uneven, with primates providing the best-known examples for a functionally referential system and rodents most examples of an urgency-based system. Reports of different alarm call systems in lemurid primates prompted us to examine the anti-predator behavior of two additional lemur species. In an experimental field study we exposed adult redfronted lemurs (Eulemur fulvus rufus) and white sifakas (Propithecus verreauxi verreauxi) to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own alarm calls given in response to the presentation of these predators. We scored the subjects' immediate behavioral responses, including alarm calls, from video recordings made during the first minute following a playback. We found that both species gave specific alarm calls only in response to raptor playbacks and the corresponding alarm calls, whereas calls given in response to carnivores and the corresponding alarm calls were also observed in other situations characterized by high arousal. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two predator classes, suggesting that the corresponding vocalizations were categorized correctly. These two lemur species, which represent different families, have therefore independently evolved a mixed alarm call system, characterized by functionally referential calls for diurnal raptors, but not for carnivores. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00265-001-0436-0 Electronic Publication     

Sex in the dark: determinants and consequences of mixed male mating tactics in<Emphasis Type="Italic"> Microcebus murinus</Emphasis>, a small solitary nocturnal primate

In mammals with solitary females, the potential for males to monopolize matings is relatively low, and scramble competition polygyny is presumed to be the predominant mating system. However, combinations of male traits and mating tactics within this type of polygyny have been described. The main aim of our study was to identify the relative importance of, and interactions among, potential determinants of contrasting male reproductive tactics, and to determine their consequences for male reproductive success in a small solitary nocturnal Malagasy primate, the gray mouse lemur (Microcebus murinus). We studied their mating behavior over three consecutive annual mating seasons. In addition, we determined the genetic relationships among more than 300 study animals to quantify the reproductive success of individual males. We found that, with a given relatively low overall monopolization potential, successful male mouse lemurs roamed extensively in search of mates, had superior finding ability and mated as early as possible. However, contest competition was important too, as temporary monopolization was also possible. Males exhibited different mating tactics, and heavier males had a higher reproductive success, although most litters had mixed paternities. Switching between tactics depended on short-term local variation in monopolization potential determined by a pronounced dynamic in fertilization probability, number of alternative mating opportunities, and the operational sex ratio. This study also revealed that the dynamics of these determinants, as well as the mutual interactions between them, necessitate a detailed knowledge of the mating behavior of a species to infer the impact of determinants of alternative mating tactics.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by S. AlbertsThis revised version was published online in August 2004 with corrections to Figure 2.     

Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer

Sperm competition will be the inevitable consequence of polyandrous mating behavior if two or more males inseminate a single female. It has been demonstrated for a wide variety of animals that males adapt to this situation behaviorally, physiologically and morphologically, e.g. by evolving relatively large testes size to produce more sperm. All pair-living primates investigated so far were found to have relatively small testes, suggesting a monandrous mating system. We investigated the relationship between extra-pair paternity (EPP) rate as a measure of sperm competition intensity and relative testes size in a pair-living primate, the fork-marked lemur (Phaner furcifer). Paternity exclusion analyses for seven offspring using six polymorphic DNA-microsatellite markers suggested a high EPP rate. Female nocturnal travel distances were longer during the mating season, suggesting that females take an active role in achieving extra-pair copulations (EPCs). Surprisingly, fork-marked lemur testes size was relatively small compared to 23 other lemuroid primates, a result that is in contrast to predictions of sperm competition theory. Neither possible behavioral and morphological adaptations to an alternative paternity guard (i.e. mate guarding), nor sampling biases, phylogenetic constraints, and population density effects explain the absence of large testes in a species with high EPP, a phenomenon also known from birds with moderate to low EPP rates. We conclude that more data are needed on the frequency of EPCs, the timing of in-pair and extra-pair copulations, as well as the role of female choice, to explain why males of some species apparently do not adapt to sperm competition.Communicated by S. Alberts     

Microgeographic heterogeneity in spatial distribution and mtDNA variability of gray mouse lemurs (<Emphasis Type="Italic">Microcebus murinus</Emphasis>, Primates: Cheirogaleidae)

The objective of our study was to investigate the spatial distribution and genetic structure of a solitary primate at the microgeographical scale of adjacent local populations. We obtained spatial data and tissue samples for mtDNA analysis from 205 gray mouse lemurs (Microcebus murinus) captured along transects and within 3 grid systems within a 12.3 km² area in Kirindy Forest, western Madagascar. Our capture data revealed that, even though the forest was continuous, gray mouse lemurs were not evenly distributed, and that daily and maximum dispersal distances were significantly greater in males. The frequency distribution of 22 mtDNA D-loop haplotypes was highly skewed. Nine haplotypes were unique to males, indicating male-mediated gene flow from surrounding areas. The geographic distribution of haplotypes revealed that males were also more dispersed than females. Females with the same haplotype showed a tendency towards spatial aggregation, and the correlation between genetic and geographic distances was higher in females. In several areas of the forest, however, spatially clustered females were not of the same haplotype, and females were not always found in clusters. Hence, in contrast to suggestions from previous studies, matrilineal clustering is not the only way females are socially organized. In addition, our study revealed heterogeneity and patterns in population structure that were not evident at smaller spatial scales, some of which may be relevant for designing conservation strategies.Communicated by C. Nunn     

Primate Socioecology: New Insights from Males

Primate males have only recently returned to the center stage of socioecological research. This review surveys new studies that examine variation in the behavior of adult males and their role in social evolution. It is shown that group size, composition, and social behavior are determined not only by resource distribution, predation risk, and other ecological factors, but that life history traits and social factors, especially those related to sexual coercion, can have equally profound consequences for social systems. This general point is illustrated by examining male behavior at three levels: the evolution of permanent associations between males and females, the causes and consequences of variation in the number of males between group-living species, and the determinants of social relationships within and between the sexes. Direct and indirect evidence reviewed in connection with all three questions indicates that the risk of infanticide has been a pervasive force in primate social evolution. Several areas are identified for future research on male life histories that should contribute to a better understanding of male reproductive strategies and corresponding female counter-strategies.     

Females go where the food is: does the socio-ecological model explain variation in social organisation of solitary foragers?

The socio-ecological model (SEM) links ecological factors with characteristics of social systems and allows predictions about the relationships between resource distribution, type of competition and social organisation. It has been mainly applied to group-living species but ought to explain variation in social organisation of solitary species as well. The aim of this study was to test basic predictions of the SEM in two solitary primates, which differ in two characteristics of female association patterns: (1) spatial ranging and (2) sleeping associations. Beginning in August 2002, we regularly (re-)captured and marked individuals of sympatric populations of Madame Berthe's and grey mouse lemurs (Microcebus berthae, Microcebus murinus) in Kirindy Forest (Madagascar). We recorded data on spatial patterns, feeding and social behaviour by means of direct observation of radio-collared females. The major food sources of M. berthae occurred in small dispersed patches leading to strong within-group scramble competition and over-dispersed females with a low potential for female associations. In contrast, M. murinus additionally used patchily distributed, high-quality (large) resources facilitating within-group contest competition. The combined influence of less strong within-group scramble and contest as well as between-group contest over non-food resources allowed females of this species to cluster in space. Additionally, we experimentally manipulated the spatial distribution of food sources and found that females adjusted their spatial patterns to food resource distribution. Thus, our results support basic predictions of the SEM and demonstrated that it can also explain variation in social organisation of solitary foragers.     

Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus)

The aim of this study was to investigate reproductive strategies and their consequences in gray mouse lemurs (Microcebus murinus), small solitary nocturnal primates endemic to Madagascar. Previous reports of sexual dimorphism in favor of males and females, respectively, a high potential for sperm competition and pheromonal suppression of mating activity among captive males, led us to investigate mechanisms of intrasexual competition in a wild population. Based on 3 years of mark-recapture data, we demonstrate that sexual dimorphism in this species fluctuated annually as a result of independent changes in male and female body mass. Male body mass increased significantly prior to the short annual mating season. Because their testes increased by 100% in the same period and because their canines are not larger than those of females, we suggest that large male size may be advantageous in searching for estrous females and in enabling them to sustain periods of short-term torpor. In contrast to reports from captive colonies, we found no evidence for two morphologically distinct classes of males. Finally, we also show that most adult males are active throughout the cool dry season that precedes the mating season, whereas most adult females hibernate for several months. This is in contrast to other solitary hibernating mammals, where males typically emerge 1–2 weeks before females. Thus, this first extended field study of M.␣murinus clarified previous conflicting reports on sexual dimorphism and male reproductive strategies in this primitive primate by showing that their apparent deviation from predictions of sexual selection theory is brought about by specific environmental conditions which result in sex-specific life history tactics not previously described for mammals. A general conclusion is that sexual selection can operate more strongly on males without resulting in sexual dimorphism because of independent selection on the same traits in females. Received: 6 July 1997 / Accepted after revision: 28 March 1998     

Delayed juvenile dispersal and monogamy, but no cooperative breeding in white-breasted mesites (Mesitornis variegata)

Although cooperative breeding is known from only about 9 % of bird species, it has received substantial attention because individuals foregoing their own reproduction to help others represent a long-standing evolutionary puzzle. We studied group formation, breeding system, spatial distribution and several life-history traits of white-breasted mesites (Mesitornis variegata). Based on field observations across 3 years, we found that white-breasted mesites live in year-round stable pairs, and that groups are formed by juvenile philopatry. As other family-living birds, M. variegata exhibit a slow pace-of-life, characterized by high annual adult survival, low productivity, long chick dependence and extended parental care. However, although reproduction is monogamous and juveniles showed interest in their parents’ nests, we found no evidence of cooperative breeding. We suggest that slow life-histories, extended parental care and year-round territoriality predispose juvenile mesites to delay dispersal. However, adult intolerance toward older juveniles may prevent them from adopting a cooperative lifestyle. Comparisons with other species of mesite indicate that monogamy and delayed juvenile dispersal are necessary, but not sufficient for the evolution of cooperative breeding in this family of birds, and that particular ecological and social conditions have facilitated the transition from pair-living to a type of group that may represent a stepping stone in the evolution of cooperative breeding in mesites and other birds.     

Polyandrous mating in treetops: how male competition and female choice interact to determine an unusual carnivore mating system

The diversity of mammalian mating systems is primarily shaped by sex-specific reproductive strategies. In the present study, we explored determinants and consequences of a unique mating system exhibited by fossas (Cryptoprocta ferox), the largest Malagasy carnivore, where females mate polyandrously on traditional mating trees, and males exhibit intrasexual size dimorphism. Males face both contest and scramble competition, and inter-sexual size dimorphism can be pronounced, but its magnitude depends on the male morph. Using a continuous behavioral observation of six estrous females over 4 years, we investigated correlates of male contest competition and female choice based on 316 copulations. Furthermore, we assessed correlates of male scramble competition based on testes size and movement data obtained from GPS tracking. We found that females dominated males regardless of their smaller size and that females actively solicited copulations. Heavy males had highest mating success during the female’s peak mating activity, but were discriminated against afterwards. Female choice and male–male competition thus converged to generate a mating advantage for heavier males. Our results suggest that females actively seek polyandrous matings, presumably for indirect genetic benefits. Since body mass is the major determinant of male mating success and is at the same time dependent on the degree of sociality and associated hunting mode of the respective male morph, a male’s feeding ecology is likely to influence its reproductive tactic. A combination of benefits from female polyandry and the consequences of different subsistence strategies may thus ultimately explain this unusual mating system.