Primate field research during a pandemic: Lessons learned from the SARS-CoV-2 outbreak.

The COVID-19 pandemic abruptly halted most primate field research in early 2020. While international travel bans and regional travel restrictions made continuing primate field research impossible early on in the pandemic, ethical concerns of transmitting the virus from researchers to primates and surrounding human communities informed decisions regarding the timing of resuming research. Between June and September 2020, we surveyed field primatologists regarding the impacts of the pandemic on their research. We received 90 completed surveys from respondents residing in 21 countries, though most were from the United States and Canada. These data provide a valuable window into the perspectives and actions taken by researchers during the early stages of the pandemic as events were still unfolding. Only 2.4% of projects reported continuing research as usual, 33.7% continued with some decrease in productivity, 42.2% reported postponing research projects, and 21.7% reported canceling projects or postponing research indefinitely. Respondents most severely impacted by the pandemic were those establishing new field sites and graduate students whose projects were postponed or canceled due to pandemic-related shutdowns. Fears about increased poaching, the inability to pay local assistants, frozen research funds, declining habituation, disruptions to data collection, and delays in student projects were among the top concerns of respondents. Nearly all the projects able to continue research in any capacity during the early months of the pandemic were run by or employed primate habitat country primatologists. This finding is a major lesson learned from the pandemic; without habitat country scientists, primate research is not sustainable.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

Modelling collective decision-making: Insights into collective anti-predator behaviors from an agent-based approach.

Collective decision-making is a widespread phenomenon across organisms. Studying how animal societies make group decisions to the mutual benefit of group members, while avoiding exploitation by cheaters, can provide unique insights into the underlying cognitive mechanisms. As a step toward dissecting the proximate mechanisms that underpin collective decision-making across animals, we developed an agent-based model of antipredatory alarm signaling and mobbing during predator-prey encounters. Such collective behaviors occur in response to physical threats in many distantly related species with vastly different cognitive abilities, making it a broadly important model behavior. We systematically assessed under which quantitative contexts potential prey benefit from three basic strategies: predator detection, signaling about the predator (e.g., alarm calling), and retreating from vs. approaching the predator. Collective signaling increased survival rates over individual predator detection in several scenarios. Signaling sometimes led to fewer prey detecting the predator but this effect disappeared when prey animals that had seen the predator both signaled and approached it, as in mobbing. Critically, our results highlight that collective decision-making in response to a threat can emerge from simple rules without needing a central leader or needing to be under conscious control.

Female-committed infanticide followed by juvenile-enacted cannibalism in wild white-faced capuchins.

On 5 February 2021, we observed the first instance of female-committed infanticide followed by cannibalism in a long-studied (> 35 years) population of wild white-faced capuchins (Cebus imitator) in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. The events leading up to and including the infanticide and cannibalism were observed and documented ad libitum, with segments digitally recorded, and a post-mortem necropsy performed. Here we detail our observations and evaluate the events within the framework of leading adaptive explanations. The infanticide may have been proximately motivated by resource competition or group instability. The circumstances of the observed infanticide provided support for the resource competition, adoption avoidance, and social status hypotheses of infanticide, but not for the exploitation hypothesis, as neither the perpetrator nor her kin consumed the deceased infant. The subsequent cannibalism was performed by juveniles who observed the infanticide and may have been stimulated by social facilitation and their prior experience of meat consumption as omnivores. To our knowledge, cannibalism has been documented only once before in C. imitator, in an adjacent study group, with the two cases sharing key similarities in the context of occurrence and manner of consumption. These observations add to our growing knowledge of the evolutionary significance of infanticide and its importance as a reproductive strategy in nonhuman primates.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Major histocompatibility complex class II DR and DQ evolution and variation in wild capuchin monkey species (Cebinae).

The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure.

Costs of male infanticide for female capuchins: When does an adaptive male reproductive strategy become costly for females and detrimental to population viability?

OBJECTIVES: Infanticide in white-faced capuchins (Cebus capucinus imitator) typically occurs in association with alpha male replacements (AMRs). Although infanticide is likely adaptive for males, it imposes costs on females that are difficult to quantify without long-term demographic data. Here we investigate effects of AMRs and infanticide on female reproductive success and how these costs affect capuchin groups. We investigate (1) effects of AMR frequency on the production of surviving infants; (2) energetic and (3) temporal "opportunity costs" of infant loss; and (4) how AMR frequency impacts capuchin group sizes. MATERIALS AND METHODS: We censused six groups (7-33 years/group, 74 adult females). We modeled surviving infant production in relation to AMR. We estimated a female's energy requirements for lost infants and the temporal cost relative to the median reproductive window. We simulated how varying AMR rates would affect future capuchin group sizes. RESULTS: Females exposed to more frequent AMR tended to produce fewer surviving offspring. We estimate the average lost infant requires approximately 33% additional energy intake for its mother and represents 10% of the average reproductive opportunity window available to females. Simulated populations remain viable at the observed rate of AMR occurrence but decrease in size at even slightly higher rates. DISCUSSION: While infanticide is adaptive for males, for females it affects lifetime reproductive success and imposes energetic and opportunity costs. Although capuchin populations have evolved with AMRs and infanticide, small increases in AMR frequency may lead to population decline/extinction. Infanticide likely plays a large role in population maintenance for capuchins.

Infant cannibalism in wild white-faced capuchin monkeys.

Cannibalism has been observed in a variety of animal taxa; however, it is relatively uncommon in primates. Thus, we rely heavily on case reports of this behavior to advance our understanding of the contexts under which it occurs. Here, we report the first observation of cannibalism in a group of wild white-faced capuchin monkeys (Cebus imitator). The subject was a dead infant, estimated to be 10 days old, and the probable victim of infanticide. Consumption of the corpse was initiated by a 2-year-old male (second cousin of the infant), though it was eventually taken over and monopolized by the group's alpha female (grandaunt of the infant). Although most group members expressed interest in the corpse (sniffing, touching, and threatening it), no others made an attempt to consume it. Given that this is the only observation of cannibalism recorded in over 37 years of study on this population, we consider it to be a rare behavior in this species. This detailed record contributes new data, which, when combined with other reports within and across species and contexts, enables the evaluation of adaptive explanations of cannibalism.

Cooperative rescue of a juvenile capuchin (Cebus imitator) from a Boa constrictor.

The threat of predation by snakes is considered to have played a significant role in the evolution of primate sensory systems and behavior. However, we know relatively little about individual and group responses given the rarity of observed predation events. Here we report an observed (filmed) predation attempt by an adult Boa constrictor (~ 2 m) on a juvenile white-faced capuchin (Cebus imitator) in the Sector Santa Rosa of the Área de Conservación Guanacaste, Costa Rica. The snake caught the juvenile monkey on the ground during a terrestrial play session. When the victim screamed, the alpha male, alpha female, and another adult female ran to the scene, physically attacked the snake (with bites and hits), and pulled the victim to safety. Most group members participated in the vocal mobbing of the snake both during and after the attack. Based on the outcomes of this predation attempt and published reports of other B. constrictor attacks on primates, the coordinated efforts of ≥ 2 group members is needed for a successful rescue. This observation adds to our growing knowledge of cooperative group behavior and its importance in predator defense.

Differential impact of severe drought on infant mortality in two sympatric neotropical primates.

Extreme climate events can have important consequences for the dynamics of natural populations, and severe droughts are predicted to become more common and intense due to climate change. We analysed infant mortality in relation to drought in two primate species (white-faced capuchins, Cebus capucinus imitator, and Geoffroy's spider monkeys, Ateles geoffroyi) in a tropical dry forest in northwestern Costa Rica. Our survival analyses combine several rare and valuable long-term datasets, including long-term primate life-history, landscape-scale fruit abundance, food-tree mortality, and climate conditions. Infant capuchins showed a threshold mortality response to drought, with exceptionally high mortality during a period of intense drought, but not during periods of moderate water shortage. By contrast, spider monkey females stopped reproducing during severe drought, and the mortality of infant spider monkeys peaked later during a period of low fruit abundance and high food-tree mortality linked to the drought. These divergent patterns implicate differing physiology, behaviour or associated factors in shaping species-specific drought responses. Our findings link predictions about the Earth's changing climate to environmental influences on primate mortality risk and thereby improve our understanding of how the increasing severity and frequency of droughts will affect the dynamics and conservation of wild primates.

Group versus population level demographics: An analysis of comparability using long term data on wild white-faced capuchin monkeys (Cebus capucinus imitator).

Primates have long been used as indicator species for assessing overall ecosystem health. However, area-wide census methods are time consuming, costly, and not always feasible under many field conditions. Therefore, it is important to establish whether monitoring a subset of a population accurately reflects demographic changes occurring in the population at large. Over the past 35 years, we have conducted 15 area-wide censuses in Sector Santa Rosa, Costa Rica. These efforts have revealed important trends in population growth patterns of capuchin monkeys following the protection and subsequent regeneration of native forests. During this same period, we have also intensively studied a subset of the capuchin groups. Comparing these two datasets, we investigate whether the population structures of the closely monitored groups are reliable indicators of area-wide demographic patterns. We compare the overall group size and the individual age/sex class compositions of study groups and nonstudy groups (i.e., those contacted during area-wide censuses only). Our study groups contained more individuals overall with a larger proportion of infants, and there were indications that the proportion of adult and subadult males was lower. These differences can be ascribed either to sampling errors or real differences attributable to human presence and/or better habitat quality for the study groups. No other sex/age classes differed, and major demographic changes were simultaneously evident in both study and nonstudy groups. This study suggests that the Santa Rosa capuchin population is similarly impacted by large-scale ecological patterns observable within our study groups.

Infant mortality in white-faced capuchins: The impact of alpha male replacements.

Infanticide is common in the context of alpha male replacements (AMR), particularly in groups where alpha males experience high reproductive skew and the infants are unlikely to be related to a new alpha male. We examined the relationship between the rate of infant mortality, infant age, and the occurrence and type of AMR in white-faced capuchin monkeys (Cebus capucinus imitator) of the Santa Rosa population in Sector Santa Rosa, Área de Conservación Guanacaste. Specifically, we investigated how the source of the new alpha male (coresident or extragroup) and relative aggression level during AMRs influenced infant mortality in this species. Between 1986 and 2015, we recorded 221 births in five study groups. Infants present at the time of an AMR, or born within 5.5 months following an AMR (i.e., conceived prior to AMR), experienced significantly higher mortality than those born during periods of group stability. Infant age was a significant predictor of infant survival, with the probability of surviving increasing by 0.4% for each additional day older an infant was at the time of the AMR. Infant mortality rates did not differ between AMRs by coresident males and extragroup males, possibly because the degree of relatedness between infants and new alphas did not significantly differ between coresident and extragroup AMRs. Infant mortality rates did not differ significantly between aggressive AMRs and more peaceful AMRs. Our results are consistent with predictions derived from the sexual selection hypothesis (SSH) of infanticide and suggest that future studies examine the role of testosterone as an underlying proximate mechanism for the aggression leading to this behavior. We argue that the sexual selection and generalized aggression hypotheses (GAH) of infanticide are best considered as different levels of analysis rather than competing hypotheses.

Alpha male replacements in nonhuman primates: Variability in processes, outcomes, and terminology.

Alpha male replacements occur in all primates displaying a dominance hierarchy but the process can be extremely variable. Here, we review the primate literature to document differences in patterns of alpha male replacements, showing that group composition and dispersal patterns account for a large proportion of this variability. We also examine the consequences of alpha male replacements in terms of sexual selection theory, infanticide, and group compositions. Though alpha male replacements are often called takeovers in the literature, this term masks much of the variation that is present in these processes. We argue for more concise terminology and provide a list of terms that we suggest more accurately define these events. Finally, we introduce the papers in this special issue on alpha male replacements in the American Journal of Primatology and discuss areas where data are still lacking.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate.

Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator).

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug-of-war) or by how easily females can be monopolized (priority-of-access). These models have rarely been investigated in species with exceptionally long male tenures, such as white-faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white-faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well-established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.

Paternal kin recognition and infant care in white-faced capuchins (Cebus capucinus).

Evidence for paternal kin recognition and paternally biased behaviors is mixed among primates. We investigate whether infant handling behaviors exhibit paternal kin biases in wild white-faced capuchins monkeys (Cebus capucinus) by comparing interactions between infants and genetic sires, potential sires, siblings (full sibling, maternal, and paternal half-siblings) and unrelated handlers. We used a linear mixed model approach to analyze data collected on 21 focal infants from six groups in Sector Santa Rosa, Costa Rica. Our analyses suggest that the best predictor of adult and subadult male interactions with an infant is the male's dominance status, not his paternity status. We found that maternal siblings but not paternal siblings handled infants more than did unrelated individuals. We conclude that maternal but not paternal kinship influence patterns of infant handling in white-faced capuchins, regardless of whether or not they can recognize paternal kin. Am. J. Primatol. 78:659-668, 2016. © 2016 Wiley Periodicals, Inc.

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus.

OBJECTIVE: Circannual variation in reproduction is pervasive in birds and mammals. In primates, breeding seasonality is variable, with seasonal birth peaks occurring even in year-round breeders. Environmental seasonality is reportedly an important contributor to the observed variation in reproductive seasonality. Given that food availability is the primary factor constraining female reproduction, predictions concerning responsiveness to environmental seasonality focus on females, with studies of males focusing primarily on social factors. We examined the influence of both environmental and social factors on male fecal testosterone (fT) and glucocorticoids (fGC) in moderately seasonally breeding white-faced capuchin monkeys (Cebus capucinus) in Costa Rica. METHODS: Over 17 months, we collected 993 fecal samples from 14 males in three groups. We used LMM to simultaneously examine the relative effects of photoperiod, fruit biomass, rainfall, temperature, female reproductive status (i.e., number of periovulatory periods, POPs), and male age and dominance rank on monthly fT and fGC levels. RESULTS: Male age and rank had large effects on fT and fGC. Additionally, some hormone variation was explained by environmental factors: photoperiod in the previous month (i.e., lagged photoperiod) was the best environmental predictor of monthly fT levels, whereas fGC levels were best explained by lagged photoperiod, fruit biomass, and rainfall. POPs predicted monthly fT and fGC, but this effect was reduced when all variables were considered simultaneously, possibly because lagged photoperiod and POP were highly correlated. CONCLUSIONS: Males may use photoperiod as a cue predicting circannual trends in the temporal distribution of fertile females, while also fine-tuning short-term hormone increases to the actual presence of ovulatory females, which may occur at any time during the year.

Edge effects in the primate community of the biological dynamics of Forest Fragments Project, Amazonas, Brazil.

While much is known about abiotic and vegetative edge effects in tropical forests, considerably less is known about the impact of forest edges on large mammals. In this study, we examine edge effects in a primate community to determine: 1) the distance from the edge over which edge effects in primate density are detectable, 2) whether individual species exhibit edge effects in their density, and 3) whether biological characteristics can be used to predict primate presence in edge habitats. Given their importance to many primate species, we also examine the influence of the number of large trees. We found edge penetration distances of 150 m for the five species that experienced edge effects, suggesting that primates respond to edge-related changes in the plant community that are known to be strongest over the first 150 m. Four species had higher edge densities: Alouatta macconnelli (folivore-frugivore), Chiropotes chiropotes (frugivorous seed predator), Saguinus midas (frugivore-faunivore), and Sapajus apella apella (frugivore-faunivore); one species' density was lower: Ateles paniscus (frugivore); and the final species, Pithecia chrysocephala (frugivorous seed predator), did not show an edge-related pattern. The lone significant relationship between the biological characteristics examined (body weight, diet, group size, and home range size) and primate presence in edge habitats was a negative relationship with the amount of fruit consumed. Though we did not examine primate responses to edges that border a denuded matrix, we have shown that edges influence primate distribution even following decades of secondary forest regeneration at habitat edges.

Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus).

Much attention has been paid to hormonal variation in relation to male dominance status and reproductive seasonality, but we know relatively little about how hormones vary across life history stages. Here we examine fecal testosterone (fT), dihydrotestosterone (fDHT), and glucocorticoid (fGC) profiles across male life history stages in wild white-faced capuchins (Cebus capucinus). Study subjects included 37 males residing in three habituated social groups in the Área de Conservacíon Guanacaste, Costa Rica. Male life history stages included infant (0 to <12months; N=3), early juvenile (1 to <3years; N=10), late juvenile (3 to <6years; N=9), subadult (6 to <10years; N=8), subordinate adult (⩾10years; N=3), and alpha adult (⩾10years; N=4, including one recently deposed alpha). Life history stage was a significant predictor of fT; levels were low throughout the infant and juvenile phases, doubled in subadult and subordinate adults, and were highest for alpha males. Life history stage was not a significant predictor of fDHT, fDHT:fT, or fGC levels. Puberty in white-faced capuchins appears to begin in earnest during the subadult male phase, indicated by the first significant rise in fT. Given their high fT levels and exaggerated secondary sexual characteristics, we argue that alpha adult males represent a distinctive life history stage not experienced by all male capuchins. This study is the first to physiologically validate observable male life history stages using patterns of hormone excretion in wild Neotropical primates, with evidence for a strong association between fT levels and life history stage.