Behavioral thermoregulation in primates: A review of literature and future avenues.

Primates face severe challenges from climate change, with warming expected to increase animals' thermoregulatory demands. Primates have limited long-term options to cope with climate change, but possess a remarkable capacity for behavioral plasticity. This creates an urgency to better understand the behavioral mechanisms primates use to thermoregulate. While considerable information exists on primate behavioral thermoregulation, it is often scattered in the literature in a manner that is difficult to integrate. This review evaluates the status of the available literature on primate behavioral thermoregulation to facilitate future research. We surveyed peer-reviewed publications on primate thermoregulation for N = 17 behaviors across four thermoregulatory categories: activity budgeting, microhabitat use, body positioning, and evaporative cooling. We recorded data on the primate taxa evaluated, support for a thermoregulatory function, thermal variable assessed, and naturalistic/manipulative study conditions. Behavioral thermoregulation was pervasive across primates, with N = 721 cases of thermoregulatory behaviors identified across N = 284 published studies. Most genera were known to utilize multiple behaviors ( x ¯ = 4.5 ± 3.1 behaviors/genera). Activity budgeting behaviors were the most commonly encountered category in the literature (54.5% of cases), while evaporative cooling behaviors were the least represented (6.9% of cases). Behavioral thermoregulation studies were underrepresented for certain taxonomic groups, including lemurs, lorises, galagos, and Central/South American primates, and there were large within-taxa disparities in representation of genera. Support for a thermoregulatory function was consistently high across all behaviors, spanning both hot- and cold-avoidance strategies. This review reveals asymmetries in the current literature and avenues for future research. Increased knowledge of the impact thermoregulatory behaviors have on biologically relevant outcomes is needed to better assess primate responses to warming environments and develop early indicators of thermal stress.

Monkey business: Collaborating to grow an ecological physiology of primates.

The lab and field provide differing approaches to studying primate biology. We outline the challenges and benefits of these approaches and demonstrate how collaboration can help bridge these perspectives to provide complementary insight into primate adaptive pathways. With this aim, our collaboration has made tangible insights into the ecological physiology of several primate species, and also yielded more subtle, intangible professional benefits.

Do Common Marmosets (Callithrix jacchus) Use Scent to Communicate Information about Food Resources?

Many animals use olfactory cues to signal information about food resources; however, this particular use of scent has received little attention in primates. Common marmosets (Callithrix jacchus) are exudativores that gouge bark to elicit exudate production and frequently deposit scent marks at gouge holes. We conducted preliminary tests of the hypothesis that common marmosets use olfactory cues to communicate information about exudate value, with more desirable resources targeted for marking. We performed choice experiments on two captive male marmosets. The animals were presented with: (1) a urine scent-marked and unmarked food resource, and (2) a high and low value food resource (i.e., greater/lesser food volumes). Marmosets placed more scent marks on high, compared to low, value food resources. Animals also spent more time gouging, removed more bark and more frequently revisited high versus low value food resources. Lastly, scent-marked foods were gouged more often than unmarked foods. Our findings support the hypothesis that marmosets use scent marking and olfaction to convey information about food resources, although verification in a larger sample is needed. Nonetheless, the demonstrated link between food value and scent marking suggests that olfactory signals may aid marmoset foraging decisions.

Thyroid hormone fluctuations indicate a thermoregulatory function in both a tropical (Alouatta palliata) and seasonally cold-habitat (Macaca fuscata) primate.

Thyroid hormones boost animals' basal metabolic rate and represent an important thermoregulatory pathway for mammals that face cold temperatures. Whereas the cold thermal pressures experienced by primates in seasonal habitats at high latitudes and elevations are often apparent, tropical habitats also display distinct wet and dry seasons with modest changes in thermal environment. We assessed seasonal and temperature-related changes in thyroid hormone levels for two primate species in disparate thermal environments, tropical mantled howlers (Alouatta palliata), and seasonally cold-habitat Japanese macaques (Macaca fuscata). We collected urine and feces from animals and used ELISA to quantify levels of the thyroid hormone triiodothyronine (fT3 ). For both species, fT3 levels were significantly higher during the cooler season (wet/winter), consistent with a thermoregulatory role. Likewise, both species displayed greater temperature deficits (i.e., the degree to which animals warm their body temperature relative to ambient) during the cooler season, indicating greater thermoregulatory pressures during this time. Independently of season, Japanese macaques displayed increasing fT3 levels with decreasing recently experienced maximum temperatures, but no relationship between fT3 and recently experienced minimum temperatures. Howlers increased fT3 levels as recently experienced minimum temperatures decreased, although demonstrated the opposite relationship with maximum temperatures. This may reflect natural thermal variation in howlers' habitat: wet seasons had cooler minimum and mean temperatures than the dry season, but similar maximum temperatures. Overall, our findings support the hypothesis that both tropical howlers and seasonally cold-habitat Japanese macaques utilize thyroid hormones as a mechanism to boost metabolism in response to thermoregulatory pressures. This implies that cool thermal pressures faced by tropical primates are sufficient to invoke an energetically costly and relatively longer-term thermoregulatory pathway. The well-established relationship between thyroid hormones and energetics suggests that the seasonal hormonal changes we observed could influence many commonly studied behaviors including food choice, range use, and activity patterns.

An assessment of skin temperature gradients in a tropical primate using infrared thermography and subcutaneous implants.

Infrared thermography has become a useful tool to assess surface temperatures of animals for thermoregulatory research. However, surface temperatures are an endpoint along the body's core-shell temperature gradient. Skin and fur are the peripheral tissues most exposed to ambient thermal conditions and are known to serve as thermosensors that initiate thermoregulatory responses. Yet relatively little is known about how surface temperatures of wild mammals measured by infrared thermography relate to subcutaneous temperatures. Moreover, this relationship may differ with the degree that fur covers the body. To assess the relationship between temperatures and temperature gradients in peripheral tissues between furred and bare areas, we collected data from wild mantled howling monkeys (Alouatta palliata) in Costa Rica. We used infrared thermography to measure surface temperatures of the furred dorsum and bare facial areas of the body, recorded concurrent subcutaneous temperatures in the dorsum, and measured ambient thermal conditions via a weather station. Temperature gradients through cutaneous tissues (subcutaneous-surface temperature) and surface temperature gradients (surface-ambient temperature) were calculated. Our results indicate that there are differences in temperatures and temperature gradients in furred versus bare areas of mantled howlers. Under natural thermal conditions experienced by wild animals, the bare facial areas were warmer than temperatures in the furred dorsum, and cutaneous temperature gradients in the face were more variable than the dorsum, consistent with these bare areas acting as thermal windows. Cutaneous temperature gradients in the dorsum were more closely linked to subcutaneous temperatures, while facial temperature gradients were more heavily influenced by ambient conditions. These findings indicate that despite the insulative properties of fur, for mantled howling monkeys surface temperatures of furred areas still demonstrate a relationship with subcutaneous temperatures. Given that most mammals possess dense fur, this provides insight for using infrared imaging in thermoregulatory studies of wild animals lacking bare skin.

Preference and consequences: A preliminary look at whether preference impacts oral processing in non-human primates.

Non-human primates demonstrate food preferences much like humans. We have little insight, however, into how those preferences impact oral processing in primates. To begin describing this relationship, we conducted a preliminary analysis measuring food preference in two tufted capuchins (Cebus apella) and comparing ranked preference to physiological variables during chewing of these foods. Food preference was assessed for each monkey across 12 foods, including monkey biscuits and 11 foods consumed by humans (e.g., various fruits and nuts). Animals chose from randomized pairs of foods to generate a ranked scale across the 12 foods. Contemporaneous with preference testing, electromyographic (EMG) activity was measured for the jaw-closing muscles to assess oral physiology during chewing of these foods. As expected, these capuchins exhibited clear preferences among these 12 foods. Based on their preferences, we identified sets of preferred and non-preferred brittle (i.e., almond versus monkey chow) and ductile (i.e., dates and prunes versus apricots) foods for physiological comparisons that broadly control variation in food mechanical properties (FMPs). As expected, oral physiology varied with FMPs in each animal. Within brittle and ductile groupings, we observed several significant differences in chewing cycle length and relative muscle activation levels that are likely related to food preference. These differences tended to be complex and individual specific. The two capuchins chewed non-preferred apricots significantly faster than preferred dates and prunes. Effect sizes for preference were smaller than those for FMPs, supporting the previous focus on FMPs in primate dietary research. Although preliminary, these results suggest that food preference may influence oral physiology in non-human primates. The prospect that this relationship exists in monkeys raises the possibility that a link between food preference and oral processing in humans may be based on shared tendencies with non-human primates, such as aversion to bitter items or preference for sweet foods.

To pair or not to pair: Sources of social variability with white-faced saki monkeys (Pithecia pithecia) as a case study.

Intraspecific variability in social systems is gaining increased recognition in primatology. Many primate species display variability in pair-living social organizations through incorporating extra adults into the group. While numerous models exist to explain primate pair-living, our tools to assess how and why variation in this trait occurs are currently limited. Here I outline an approach which: (i) utilizes conceptual models to identify the selective forces driving pair-living; (ii) outlines novel possible causes for variability in social organization; and (iii) conducts a holistic species-level analysis of social behavior to determine the factors contributing to variation in pair-living. A case study on white-faced sakis (Pithecia pithecia) is used to exemplify this approach. This species lives in either male-female pairs or groups incorporating "extra" adult males and/or females. Various conceptual models of pair-living suggest that high same-sex aggression toward extra-group individuals is a key component of the white-faced saki social system. Variable pair-living in white-faced sakis likely represents alternative strategies to achieve competency in this competition, in which animals experience conflicting selection pressures between achieving successful group defense and maintaining sole reproductive access to mates. Additionally, independent decisions by individuals may generate social variation by preventing other animals from adopting a social organization that maximizes fitness. White-faced saki inter-individual relationships and demographic patterns also lend conciliatory support to this conclusion. By utilizing both model-level and species-level approaches, with a consideration for potential sources of variation, researchers can gain insight into the factors generating variation in pair-living social organizations.

Pitheciid research comes of age: Past puzzles, current progress, and future priorities.

For a long time, members of the Pitheciidae were among the least studied of all Neotropical primates. But times have changed. Here, we trace the trajectory of this change and show how the articles in this special edition illustrate new knowledge and developments in our understanding of pitheciid ecology, behavior, and conservation. We propose new directions and priorities for future research, especially to ensure the effective conservation of pitheciids, and demonstrate how studies of this family are now the focus of hypothesis-driven research that not only allows the details of this family's biology to be explored, but will allow its biology to be compared with other primate lineages.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both.

Body temperature and thermal environment in a generalized arboreal anthropoid, wild mantled howling monkeys (Alouatta palliata).

Free-ranging primates are confronted with the challenge of maintaining an optimal range of body temperatures within a thermally dynamic environment that changes daily, seasonally, and annually. While many laboratory studies have been conducted on primate thermoregulation, we know comparatively little about the thermal pressures primates face in their natural, evolutionarily relevant environment. Such knowledge is critical to understanding the evolution of thermal adaptations in primates and for comparative evaluation of humans' unique thermal adaptations. We examined temperature and thermal environment in free-ranging, mantled howling monkeys (Alouatta palliata) in a tropical dry forest in Guanacaste, Costa Rica. We recorded subcutaneous (Tsc ) and near-animal ambient temperatures (Ta ) from 11 animals over 1586.5 sample hours during wet and dry seasons. Howlers displayed considerable variation in Tsc , which was largely attributable to circadian effects. Despite significant seasonal changes in the ambient thermal environment, howlers showed relatively little evidence for seasonal changes in Tsc . Howlers experienced warm thermal conditions which led to body cooling relative to the environment, and plateaus in Tsc at increasingly warm Ta . They also frequently faced cool thermal conditions (Ta < Tsc ) in which Tsc was markedly elevated compared with Ta . These data add to a growing body of evidence that non-human primates have more labile body temperatures than humans. Our data additionally support a hypothesis that, despite inhabiting a dry tropical environment, howling monkeys experience both warm and cool thermal pressures. This suggests that thermal challenges may be more prevalent for primates than previously thought, even for species living in nonextreme thermal environments.

Non-monogamous copulations and potential within-group mating competition in white-faced saki monkeys (Pithecia pithecia).

Many primates display within-species variation in social organization and mating system. Individuals of these species may be confronted with both the challenges of between-group competition to exclude same-sex competitors as well as within-group competition for mating opportunities. Free-ranging white-faced saki monkeys (Pithecia pithecia) live in both male-female pairs and small multi-male, multi-female groups. Despite commonly held views that this species is monogamous, there are currently no published accounts of mating patterns in the genus Pithecia. I recorded copulations and sexual behavior from three free-ranging groups of white-faced sakis at Brownsberg Naturepark, Suriname over a period of 17 months. Groups displayed both monogamous and polygynandrous mating. Individuals in polygynandrous groups were not observed to mate more frequently with certain partners. Copulation harassment occurred in 8.6% of copulations (total N = 81) and was performed by both sexes. This harassment successfully prevented ejaculation in six out of seven instances and harassment by males resulted in male-male aggression on four occasions. Two cases of female-directed sexual aggression by males were also observed, which may indicate that males use sexual coercion to influence female mating behavior. Although based on a small number of groups, these data show that white-faced sakis display variability in mating system and that this variability is not directly dictated by social organization. Furthermore, groups with promiscuous copulations exhibit behaviors indicative of within-group mating competition.

Terrestrial activity in pitheciins (Cacajao, Chiropotes, and Pithecia).

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a "local pattern" of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types.

Back to the Future: Reintegrating Biology to Understand How Past Eco-evolutionary Change Can Predict Future Outcomes.

During the last few decades, biologists have made remarkable progress in understanding the fundamental processes that shape life. But despite the unprecedented level of knowledge now available, large gaps still remain in our understanding of the complex interplay of eco-evolutionary mechanisms across scales of life. Rapidly changing environments on Earth provide a pressing need to understand the potential implications of eco-evolutionary dynamics, which can be achieved by improving existing eco-evolutionary models and fostering convergence among the sub-fields of biology. We propose a new, data-driven approach that harnesses our knowledge of the functioning of biological systems to expand current conceptual frameworks and develop corresponding models that can more accurately represent and predict future eco-evolutionary outcomes. We suggest a roadmap toward achieving this goal. This long-term vision will move biology in a direction that can wield these predictive models for scientific applications that benefit humanity and increase the resilience of natural biological systems. We identify short, medium, and long-term key objectives to connect our current state of knowledge to this long-term vision, iteratively progressing across three stages: (1) utilizing knowledge of biological systems to better inform eco-evolutionary models, (2) generating models with more accurate predictions, and (3) applying predictive models to benefit the biosphere. Within each stage, we outline avenues of investigation and scientific applications related to the timescales over which evolution occurs, the parameter space of eco-evolutionary processes, and the dynamic interactions between these mechanisms. The ability to accurately model, monitor, and anticipate eco-evolutionary changes would be transformational to humanity's interaction with the global environment, providing novel tools to benefit human health, protect the natural world, and manage our planet's biosphere.

Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference.

White-faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999]. In order to determine if social bonds in this species reflect patterns displayed by pair-bonded groups or larger multimale-multifemale groups, we draw on 17 months of data collected on wild white-faced sakis at Brownsberg Nature Park, Suriname. We analyzed within-group social bonds for three habituated groups (one two-adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two-adult and multiadult groups showed significantly stronger social bonds between a single male-female dyad within each group (deemed "primary dyads"). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within-group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white-faced sakis do not show behavioral and physical traits typical of monogamy or pair-bonding, social bonds are strongest between a single male-female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale-multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white-faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates.

What smells? Developing in-field methods to characterize the chemical composition of wild mammalian scent cues.

Olfactory cues play an important role in mammalian biology, but have been challenging to assess in the field. Current methods pose problematic issues with sample storage and transportation, limiting our ability to connect chemical variation in scents with relevant ecological and behavioral contexts. Real-time, in-field analysis via portable gas chromatography-mass spectrometry (GC-MS) has the potential to overcome these issues, but with trade-offs of reduced sensitivity and compound mass range. We field-tested the ability of portable GC-MS to support two representative applications of chemical ecology research with a wild arboreal primate, common marmoset monkeys (Callithrix jacchus). We developed methods to (a) evaluate the chemical composition of marmoset scent marks deposited at feeding sites and (b) characterize the scent profiles of exudates eaten by marmosets. We successfully collected marmoset scent marks across several canopy heights, with the portable GC-MS detecting known components of marmoset glandular secretions and differentiating these from in-field controls. Likewise, variation in the chemical profile of scent marks demonstrated a significant correlation with marmoset feeding behavior, indicating these scents' biological relevance. The portable GC-MS also delineated species-specific olfactory signatures of exudates fed on by marmosets. Despite the trade-offs, portable GC-MS represents a viable option for characterizing olfactory compounds used by wild mammals, yielding biologically relevant data. While the decision to adopt portable GC-MS will likely depend on site- and project-specific needs, our ability to conduct two example applications under relatively challenging field conditions bodes well for the versatility of in-field GC-MS.

Callitrichid responses to dead and dying infants: the effects of paternal bonding and cause of death.

Many primates show responses to dead infants, yet testing explanations for these behaviors has been difficult. Callitrichids present a unique opportunity to delineate between hypotheses, since unlike most species, male caretakers form closer social bonds with infants than mothers. Callitrichids are also known to commit infanticide, leaving obvious wounds that may enable them to more readily recognize death. We present: (1) a case study of a wild common marmoset (Callithrix jacchus) group responding to an infant's natural death, and (2) a review of published infant deaths across callitrichids (N = 16), testing for trends in the sex of reacting individuals and cause of death. In our case study, several group members frequently interacted with the dead infant, attempting to carry it. However, the strongest response was from a male that remained with the corpse for ~ 3 h, despite his group leaving the area. Across callitrichid species, corpse interactions were significantly sex-biased: 100% (N = 6) of accidental deaths involved corpse interaction by males (p = 0.007), compared to 60% (N = 3 of 5) by females (p = 0.095). Cause of death also played a significant role, with individuals attempting to carry dead infants in 100% (N = 6) of accidental deaths, but only 11.1% (N = 1 of 9) of infanticides (p = 0.001). Although the available literature is small and potentially subject to publication biases, these data support the idea that visually obvious wounds may influence callitrichids' perception of dead conspecifics. Additionally, male-biased patterns of corpse interaction in callitrichids indicate that social bonds likely shape reactions to the dead, in addition to kinship. While published data on primate thanatology are limited, this study demonstrates quantitative approaches that can provide empirical insights into primates' responses to dead conspecifics.

Getting Humans Off Monkeys' Backs: Using Primate Acclimation as a Guide for Habitat Management Efforts.

Wild primates face grave conservation challenges, with habitat loss and climate change projected to cause mass extinctions in the coming decades. As large-bodied Neotropical primates, mantled howling monkeys (Alouatta palliata) are predicted to fare poorly under climate change, yet are also known for their resilience in a variety of environments, including highly disturbed habitats. We utilized ecophysiology research on this species to determine the morphological, physiological, and behavioral mechanisms howlers employ to overcome ecological challenges. Our data show that howlers at La Pacifica, Costa Rica are capable of modifying body size. Howlers displayed reduced mass in warmer, drier habitats, seasonal weight changes, frequent within-lifetime weight fluctuations, and gradual increases in body mass over the past four decades. These within-lifetime changes indicate a capacity to modify morphology in a way that can impact animals' energetics and thermodynamics. Howlers are also able to consume foods with a wide variety of food material properties by altering oral processing during feeding. While this capability suggests some capacity to cope with the phenological shifts expected from climate change and increased habitat fragmentation, data on rates of dental microwear warn that these acclimations may also cost dental longevity. Lastly, we found that howlers are able to acclimate to changing thermal pressures. On shorter-term daily scales, howlers use behavioral mechanisms to thermoregulate, including timing activities to avoid heat stress and utilizing cool microhabitats. At the seasonal scale, animals employ hormonal pathways to influence heat production. These lines of evidence cumulatively indicate that howlers possess morphological, physiological, and behavioral mechanisms to acclimate to environmental challenges. As such, howlers' plasticity may facilitate their resilience to climate change and habitat loss. While habitat loss in the tropics is unlikely to abate, our results point to a potential benefit of active management and selective cultivation to yield large, interconnected forest fragments with targeted phenology that provides both a complex physical structure and a diversity of food sources. These steps could assist howlers in using their natural acclimation potential to survive future conservation threats.