The face is central to primate multicomponent signals

A wealth of experimental and observational evidence suggests that faces have become increasingly important in the communication system of primates over evolutionary time and that both the static and moveable aspects of faces convey considerable information. Therefore, whenever there is a visual component to any multicomponent signal the face is potentially relevant. However, the role of the face is not always considered in primate multicomponent communication research. We review the literature and make a case for greater focus on the face going forward. We propose that the face can be overlooked for two main reasons: first, due to methodological difficulty. Examination of multicomponent signals in primates is difficult, so scientists tend to examine a limited number of signals in combination. Detailed examination of the subtle and dynamic components of facial signals is particularly hard to achieve in studies of primates. Second, due to a common assumption that the face contains “emotional” content. A priori categorisation of facial behavior as “emotional” ignores the potentially communicative and predictive information present in the face that might contribute to signals. In short, we argue that the face is central to multicomponent signals (and also many multimodal signals) and suggest future directions for investigating this phenomenon.

The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura)

When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions, when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors, we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.

Third-party vocal intervention in the proboscis monkey (Nasalis larvatus)

Vocal intervention is a triadic social interaction, where a third party responds vocally to a conflict between group members, minimizing the costs of aggression in response to the intervention. Because there is little information on vocal third-party intervention in nonhuman mammals, we investigated whether adult male proboscis monkeys use the bray vocalization as a vocal third-party intervention signal to intervene in intragroup conflicts. First, we audio-recorded 1,811 vocalizations from 17 free-ranging proboscis monkey groups in the Lower Kinabatangan Wildlife Sanctuary, analyzing 378 vocal responses of the adult male to agonistic vocal exchanges (shrieks) of group members. Second, we video- and audio-recorded five habituated groups in the Labuk Bay Proboscis Monkey Sanctuary investigating the context of these vocalizations and the conflict dyads evoking vocal support. We found that adult males of one-male/multifemale groups mainly uttered bray vocalizations, whereas females, immatures, and infants uttered shrieks in intragroup conflicts or in response to other animal species. The adult male uttered significantly more often brays after agonistic shrieks than expected based on the overall occurrence of brays. Brays ended 65% of agonistic conflicts, which were accompanied by vocalizations of the conflict partners and occurred more often after conflicts between females than between offspring. This suggests that the bray functions as a vocal third-party intervention signal for intragroup conflict resolution. We suggest that living in the high canopies of the tropical rainforest might restrict direct access to conflict partners and prevent physical intervention, favoring the evolution of the bray as a third-party vocal intervention signal.

A 24-Year Record of Female Reproductive Dynamics in Two Sympatric Mouse Lemur Species in Northwestern Madagascar

Seasonal reproduction is widespread among primates but the degree of reproductive synchrony and plasticity can vary, even between closely related species. This study compares the dynamics of female reproductive seasonality in two mouse lemur species, Microcebus murinus and M. ravelobensis, in Ankarafantsika National Park, Madagascar, across 24 years. We collected 4321 records of female reproductive state from 1033 individual females (319 M. murinus, 714 M. ravelobensis). The analyses revealed disparate reproductive schedules: While female M. murinus showed high degrees of reproductive synchrony throughout all years, leading to the production of two successive litters, the seasonal onset of estrus (= reproductive activation) in female M. ravelobensis was more flexible than in M. murinus, starting 2-4 weeks earlier, varying by up to 4 weeks between years, and being less synchronized. M. ravelobensis females became reproductively active later in years with more rainfall, in particular rain in February, but the timing of reproductive activation was not related to differences in temperatures. The likelihood of early conception was significantly lower in M. ravelobensis than in M. murinus. This was partly due to delayed reproductive activation in young animals, and a lower likelihood of early conception for females with low body mass in M. ravelobensis. Our results suggest high, adaptive reproductive plasticity in M. ravelobensis that may enable individuals to respond flexibly to yearly environmental changes and expand the reproductive period under favorable conditions. These species differences in reproductive schedules may be the result of the divergent evolutionary histories of the two mouse lemur species in different parts of Madagascar.

After the smoke has cleared: Extended low fruit productivity following forest fires decreased gregariousness and social tolerance among wild female Bornean orangutans (Pongo pygmaeus wurmbii)

As climate change continues to fundamentally alter resource landscapes, the ability to flexibly respond to spatio-temporal changes in the distribution of preferred food sources is increasingly important for the overall health and fitness of animals living in seasonal, variable, and/or changing environments. Here, we investigate the effects of an uncharacteristically long period of fruit scarcity, following widespread thick haze caused by peat and forest fires in 2015, on the behaviour and sociality of female Bornean orangutans (Pongo pygmaeus wurmbii). We collected data from 2010 to 2018 at Tuanan, Central Kalimantan, Indonesia, and compared the activity, diet, and association patterns of adult females during low-fruit periods before the fires, i.e., regular, seasonal periods of low fruit availability (“pre-fire”), and after the fires, i.e., during the extended period of low fruit availability (“post-fire”). First, we found that, post-fire, female orangutans adopted a more extreme energy-saving activity pattern and diet — resting more, travelling less, and diet-switching to less-preferred foods — compared to pre-fire. Second, we found that the probabilities of association between females and their weaned immature offspring, and between related and unrelated adult females were lower, and the probability of agonism between unrelated females was higher, post-fire than pre-fire. This change in energetic strategy, and the general reduction in gregariousness and social tolerance, demonstrates how forest fires can have lasting consequences for orangutans. Fission–fusion species such as orangutans can mitigate the effects of changes in resource landscapes by altering their (sub)grouping patterns; however, this may have long-term indirect consequences on their fitness.