Information on basic reproductive parameters and life-history traits is crucial for the understanding of primate evolution, ecology, social behavior, and reproductive strategies. Here, we report 4 yr of data on reproductive and life-history traits for wild female Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, northeastern Thailand. During 2 consecutive reproductive seasons, we investigated reproductive behavior and sexual swelling size in 16 females and collected 1832 fecal samples. Using enzyme immunoassays, we measured fecal estrogen and progesterone metabolites to assess ovarian activity and timing of ovulation and to ascertain conceptions and pregnancies. Timing of reproduction was strictly seasonal (births: April–July, 86% in April–June, 4 yr, n = 29; conceptions: October–February, 65% in December–January, 2 yr, n = 17). Females showed no cyclic ovarian activity outside the mating season and conceived in their first or second cycle (mean: 1.2 cycles to conception, n = 13). Gestation length was on average 164.2 d (range: 158–170, n = 10), and females had their first infant at an age of 5 yr (n = 4). Interbirth intervals were bimodally distributed, with females giving birth on average every 13.9 or 23.2 mo. Shorter interbirth intervals were linked to early parturition within the birth season. Most females displayed subcaudal sexual swellings which, however, did not reliably indicate female reproductive status or fertility. Overall, our results fall within the range of findings reported for other macaque species. These results thus add to the growing body of information available for wild macaques, facilitating comparative studies for a better understanding of interspecific differences in social and reproductive patterns.
Summary1. Predation plays a fundamental role in evolutionary processes, driving changes in prey morphology, physiology and behaviour. With organisms being increasingly exposed to rapid environmental changes, there is growing interest in understanding individual phenotypic plasticity in response to changes in predation pressure. 2. Behavioural and physiological responses to predator exposure are of particular interest as differences in predation pressure are often reflected in correlated suites of behavioural and hormonal profiles across populations. Within populations, the association between endocrine profiles and behaviour is less understood and often lacking. 3. Adopting a reaction norm approach and a repeated measures design, we assessed withinpopulation effects of changes in perceived predation risk on endocrinology and behaviour in three-spined sticklebacks (Gasterosteus aculeatus). We repeatedly exposed subjects to a robotic model predator and assessed their behavioural response. The fish showed consistent behavioural profiles and were less active and shyer when predation risk was higher. 4. Using non-invasive waterborne hormone analysis, we assessed basal cortisol as well as the cortisol response to changes in predation risk. Individuals showed significantly higher cortisol levels following exposure to the model predator. Individual post-predator exposure cortisol was repeatable but unrelated to behavioural responses. Accounting for between versus withinsubject effects, we found that basal cortisol and shyness were positively related within individuals, that is individuals overall were shyer on days they had higher cortisol levels. We also tested if basal testosterone predicted risky behaviour and found no evidence for this hypothesis. 5. No individual differences in hormonal or behavioural responses to changes in predation risk were found, suggesting that individuals are not constrained by their personalities in their ability to cope with a potentially harmful threat. 6. Overall, we show that individuals of different personalities are equally 'flexible' in their response to changes in predation pressure. Our study offers novel insight into consistent individual differences and plasticity in hormones and behaviour as well as their interplay within populations. Future studies should assess the applicability of these findings to other changes in the environment, as well as the effects of social context on endocrine and behavioural reaction norms.
The earliest studies of collective animal behaviour were inspired by and conducted in the wild. Over the past decades much of the research in this field has shifted to the laboratory, combining high-resolution tracking of individuals with mathematical simulations or agent-based models. Today we are beginning to see a 're-wilding' of collective behaviour thanks to technological advances, providing researchers with the opportunity to quantify and model the heterogeneity that exists within the social groupings they study and within the environments in which these groups live. The perspective we present here aims to inspire and steer this research toward answering fundamental and outstanding behavioural and ecological questions, while also tackling pertinent conservation challenges.
Behavioural traits that co-vary across contexts or situations often reflect fundamental trade-offs which individuals experience in different contexts (e.g. fitness trade-offs between exploration and predation risk). Since males tend to experience greater variance in reproductive success than females, there may be considerable fitness benefits associated with “bolder” behavioural types, but only recently have researchers begun to consider sex-specific and life-history strategies associated with these. Here we test the hypothesis that male three-spined sticklebacks (Gasterosteus aculeatus) show high risk but potentially high return behaviours compared to females. According to this hypothesis we predicted that male fish would show greater exploration of their environment in a foraging context, and be caught sooner by an experimenter than females. We found that the time fish spent out of cover exploring their environment was correlated over two days, and males spent significantly more time out of cover than females. Also, the order in which fish were net-caught from their holding aquarium by an experimenter prior to experiments was negatively correlated with the time spent out of cover during tests, and males tended to be caught sooner than females. Moreover, we found a positive correlation between the catch number prior to our experiments and nine months after, pointing towards consistent, long-term individual differences in behaviour.
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.
Cortisol coregulation, which is the up- or down-regulation of partners’ physiological stress responses, has been described for individuals with strong attachment bonds, e.g. parents and their children, and romantic relationship partners. Research into moderating effects on cortisol coregulation suggests stronger covariation among distressed partners. Whether cortisol coregulation is unique to humans or can also be found in other species that share universal features of the vertebrate stress response remains unexplored. Using a repeated measures approach and non-invasive waterborne hormone analysis, we test the hypothesis that dyads of three-spined stickleback fish (Gasterosteus aculeatus) coregulate their cortisol levels in shared environments. Dyadic cortisol levels were unrelated when cohabiting (home tank), but significantly covaried when sharing a more stressful (as indicated by higher cortisol levels) environment (open field). Time-lag analysis further revealed that open field cortisol levels were predicted by partner’s cortisol levels prior to the shared experience. To our knowledge, this study provides the first evidence for coregulatory processes on cortisol responses in a non-human animal that lacks strong bonds and social attachment relationships, suggesting a shared evolutionary origin of cortisol coregulation in vertebrates. From an adaptive perspective, cortisol coregulation may serve to reduce risk in challenging, potentially threatening situations.
Extended female sexuality in species living in multimale-multifemale groups appears to enhance benefits from multiple males. Mating with many males, however, requires a low female monopolizability, which is affected by the spatiotemporal distribution of receptive females. Ovarian cycle synchrony potentially promotes overlapping receptivity if fertile and receptive periods are tightly linked. In primates, however, mating is often decoupled from hormonal control, hence reducing the need for synchronizing ovarian events. Here, we test the alternative hypothesis that females behaviorally coordinate their receptivity while simultaneously investigating ovarian cycle synchrony in wild, seasonal Assamese macaques (Macaca assamensis), a promiscuous species with extremely extended female sexuality. Using fecal hormone analysis to assess ovarian activity we show that fertile phases are randomly distributed, and that dyadic spatial proximity does not affect their distribution. We present evidence for mating synchrony, i.e., the occurrence of the females' receptivity was significantly associated with the proportion of other females mating on a given day. Our results suggest social facilitation of mating synchrony, which explains (i) the high number of simultaneously receptive females, and (ii) the low male mating skew in this species. Active mating synchronization may serve to enhance the benefits of extended female sexuality, and may proximately explain its patterning and maintenance.
Ocean acidification (OA)—caused by rising concentrations of carbon dioxide (CO2)—is thought to be a major threat to marine ecosystems and has been shown to induce behavioural alterations in fish. Here we show behavioural resilience to near-future OA in a commercially important and migratory marine finfish, the Sea bass (Dicentrarchus labrax). Sea bass were raised from eggs at 19°C in ambient or near-future OA (1000 µatm pCO2) conditions and n = 270 fish were observed 59–68 days post-hatch using automated tracking from video. Fish reared under ambient conditions, OA conditions, and fish reared in ambient conditions but tested in OA water showed statistically similar movement patterns, and reacted to their environment and interacted with each other in comparable ways. Thus our findings indicate behavioural resilience to near-future OA in juvenile sea bass. Moreover, simulated agent-based models indicate that our analysis methods are sensitive to subtle changes in fish behaviour. It is now important to determine whether the absences of any differences persist under more ecologically relevant circumstances and in contexts which have a more direct bearing on individual fitness.
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