Coping with extreme free cortisol levels: Seasonal stress axis changes in sympatric North American flying squirrels.

Most environments exhibit predictable yearly changes, permitting animals to anticipate them. The hypothalamic-pituitary-adrenal (HPA) axis is a key physiological pathway that enables animals to cope with such changes. Monitoring glucocorticoid (the end products of the HPA axis) levels in wild animals throughout the year can improve our understanding of how this pathway responds to different conditions. For this study, we collected 18 months of data on two species of North American flying squirrels (Glaucomys sabrinus and G. volans) living in a southern Ontario forest where temperature and food availability fluctuate dramatically throughout the year. These squirrels are active year-round, nest communally, and rely on scatter hoarded foods in the winter months. Flying squirrels have extremely high levels of free plasma cortisol relative to other mammals, but it is unknown how these levels are affected by environmental and reproductive factors. For both species, our goals were to (1) validate an enzyme immunoassay (EIA) to measure their fecal glucocorticoid metabolite (FGM) concentrations and (2) assess yearly differences, seasonal changes, and the influence of sex, reproduction, and ambient temperature on FGM concentrations in each species. In the lab, we successfully validated the use of antibody 5α-pregnane-3ß, 11ß, 21-triol-20-one EIA for FGM analysis in both species. In the field, neither sex nor reproductive status (breeding condition or not) were linked to FGM concentrations in either species. FGM concentrations were higher in autumn compared to the spring and summer. There were no other seasonal differences. We discuss possible explanations for the autumn peak in FGM concentrations (increased energy expenditure and social nesting changes), as well as outline possible avenues for future research. Understanding how individuals and populations respond to environmental change is a critical goal in evolutionary ecology, particularly in the context of a rapidly changing Anthropocene.

How can we apply decision-making theories to wild animal behavior? Predictions arising from dual process theory and Bayesian decision theory.

Our understanding of decision-making processes and cognitive biases is ever increasing, thanks to an accumulation of testable models and a large body of research over the last several decades. The vast majority of this work has been done in humans and laboratory animals because these study subjects and situations allow for tightly controlled experiments. However, it raises questions about how this knowledge can be applied to wild animals in their complex environments. Here, we review two prominent decision-making theories, dual process theory and Bayesian decision theory, to assess the similarities in these approaches and consider how they may apply to wild animals living in heterogenous environments within complicated social groupings. In particular, we wanted to assess when wild animals are likely to respond to a situation with a quick heuristic decision and when they are likely to spend more time and energy on the decision-making process. Based on the literature and evidence from our multi-destination routing experiments on primates, we find that individuals are likely to make quick, heuristic decisions when they encounter routine situations, or signals/cues that accurately predict a certain outcome, or easy problems that experience or evolutionary history has prepared them for. Conversely, effortful decision-making is likely in novel or surprising situations, when signals and cues have unpredictable or uncertain relationships to an outcome, and when problems are computationally complex. Though if problems are overly complex, satisficing via heuristics is likely, to avoid costly mental effort. We present hypotheses for how animals with different socio-ecologies may have to distribute their cognitive effort. Finally, we examine the conservation implications and potential cognitive overload for animals experiencing increasingly novel situations caused by current human-induced rapid environmental change.

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus.

Anogenital distance (AGD) is positively correlated to fetal androgen exposure and developmental masculinization in mammals. Independent of overall body size, AGD shows a strong positive correlation with male fertility and in rodents, AGD is a good indicator of male competitive ability and is associated with female choice. We hypothesized that AGD will also predict male competitive ability in non-human primates. To test this, we measured AGD noninvasively with a parallel laser in a wild population of Angolan colobus monkeys (Colobus angolensis ruwenzorii) in Uganda and correlated to it to their social structure. C. angolensis ruwenzorii form a multilevel society with both one-male/multifemale units (OMUs) and multimale/multifemale units (MMUs). We compared AGD in males from five OMUs and six MMUs and related it to their fecal androgen metabolite concentrations, dominance rank and body size, and to the number of females in their unit. Males in OMUs had greater access to females, so were predicted to have longer AGDs, but this was not found. AGD also did not correlate overall with mean fecal androgen metabolites in MMUs. However, AGD was correlated with dominance rank in MMUs, demonstrating that higher-ranking males in these multimale units had longer AGDs. Body size did not show the same relationship with dominance rank, suggesting that male rank was not just a reflection of absolute male size. Our findings indicate that AGD predicts male competitive ability in this species and that it may be a useful correlate throughout the non-human primates. These results also support the idea that prenatal androgen exposure increases the likelihood of the expression of behaviors that maintain high dominance rank.

Temporal patterns in the social network of core units in Rwenzori Angolan colobus monkeys: Effects of food availability and interunit dispersal.

Multi-level societies are complex, nested social systems where basic social groups (i.e., core units) associate in a hierarchical manner, allowing animals to adjust their group sizes in response to variables such as food availability, predation, or conspecific threat. These pressures fluctuate over time and examining the extent to which this variation affects the clustering of core units into different tiers may be instrumental in understanding the evolution of multi-level societies.The goal of our study was to determine the degree of temporal variability in interunit associations in a multi-level society of Rwenzori Angolan colobus monkey (Colobus angolensis ruwenzorii), and to determine the social and ecological factors that underlie association patterns. The C. a. ruwenzorii multi-level society consists of at least three tiers, with core units clustering into clans that share a home range in a band tier.We performed social network analyses on 21 months of association data from 13 core units (totaling 139 identifiable individuals) at Lake Nabugabo, Uganda. We described the patterns of variation in core-unit associations over time and investigated how changes in rainfall, food availability, and interunit dispersals were correlated with these associations over the short-term (month to month) and long-term (year to year).Although clans were relatively stable, larger-scale changes in association patterns included the formation of an all-male unit and the transfer of one core unit between clans (within the band tier). Seasonally, core units associated significantly more when fruit, their preferred food source, was abundant (i.e., social networks were denser and more clustered) and there was no direct effect of rainfall seasonality or young leaf availability. Male dispersals also occurred more during periods of high fruit availability, suggesting that greater band cohesion allowed males to prospect and transfer between core units. Once males transferred, their previous and new units associated significantly more with one another than with other core units for 1-2 months postdispersal. The dispersal of five males from one core unit to another in a different clan co-occurred with this core unit switching its clan affiliation.By examining temporal shifts in social network structure among core units, this study shows the interconnected roles that food availability and dispersal have in shaping the C. a. ruwenzorii multi-level social system. Our findings highlight how ecological conditions can drive association patterns, impact interunit relationships, and influence social organization.

High levels of infant handling by adult males in Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) compared to two closely related species, C. guereza and C. vellerosus.

Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels have been reported in some primates. Though infant handling is a costly behaviour, there are many benefits that male handlers can accrue. Infant handling by males is most conspicuous in platyrrhines and tends to be uncommon in catarrhines. In the latter species, research on male-infant interactions has focused on low-cost behaviours, such as proximity and grooming. However, to better understand the evolution of infant handling by males, more data on its occurrence across the Primate order are essential, even in species where it is relatively uncommon. We compare the occurrence of infant handling by males in three closely related species of catarrhine: Colobus vellerosus, C. guereza, and C. angolensis ruwenzorii. We collected focal animal samples on infants to quantify infant handling rates and durations, and found that adult male C. a. ruwenzorii handled infants much more frequently and for much longer than males in the other two species. We discuss how C. a. ruwenzorii's unique social organization may explain high levels of infant handling by adult males in this species. More long-term and detailed comparisons of infant handling across species and populations will shed light on how sociality has shaped the evolution of this behaviour in the Primate order.

Infanticide and partial cannibalism in free-ranging Coquerel's sifaka (Propithecus coquereli).

Infanticide has been observed across many primate taxa, but the extent of its occurrence is not fully understood due to difficulty in observation and uneven reporting. Several hypotheses have been proposed to explain why infanticide occurs in primates and whether it benefits some individuals within a social group. Here we report on a case of infanticide, followed by partial consumption of the infant, in a population of Coquerel's sifaka (Propithecus coquereli) at Mariarano, Northwest Madagascar. We witnessed an adult male sifaka kill and consume part of an infant, a member of his own social group, as well as the mother's reaction to the infanticide. Following the infanticide, the mother of the deceased infant left the social group after repeated agonistic encounters with the other group members. We evaluate how this event relates to the predictions of four common hypotheses. Further research on Coquerel's sifaka is needed to determine the frequency of infanticide in this species, and in lemurs more generally, because infanticide is currently poorly understood in this taxon.

A multi-level society comprised of one-male and multi-male core units in an African colobine (Colobus angolensis ruwenzorii).

Several mammalian species exhibit complex, nested social organizations, termed multi-level or modular societies. Multi-level societies comprise stable core units that fission and fuse with one another in a hierarchical manner, forming groups that vary in size over time. Among nonhuman primates, these social systems have been confirmed in several African papionin and Asian colobine species. We use data from August 2017 to July 2018 on individually-recognized Rwenzori Angolan colobus living near Lake Nabugabo, Uganda to document the first multi-level society in an African colobine. The study band comprised up to 135 individuals organized into 12 socially and spatially distinct core units that ranged in size from 4 to 23 individuals. These core units showed a strong affinity to one another, spending roughly 75% of their time together. Core units fissioned and fused non-randomly with one another throughout the day, leading to different combinations of core units being observed. Using association indices between core units, we employed hierarchical cluster analyses and permutation tests to show that some core units associated preferentially into clans. Thus, we confirm three tiers of social organization for Rwenzori Angolan colobus: core unit, clan, and band. The social organization of this subspecies is unlike any reported previously in a nonhuman primate, with about half the core units containing a single adult male and the others containing multiple reproductive adult males. The discovery of a unique primate multi-level society in a novel lineage could allow for a better understanding of the evolution of these complex social systems across the Animal Kingdom. Preliminary data show males transfer within the band and females transfer outside of the band, which is proposed for hominin multi-level societies. This subspecies could thus also provide insight into the selective pressures underlying multi-level societies in our own lineage.

Proximity and grooming patterns reveal opposite-sex bonding in Rwenzori Angolan colobus monkeys (Colobus angolensis ruwenzorii).

Close proximity and social grooming are important bonding mechanisms in primates. These behaviors show the social structure of a species and many studies have found positive correlations between the degree of kinship and grooming and proximity. We used 1 year of data collected via instantaneous scan sampling on a large "supertroop" of Colobus angolensis ruwenzorii at Lake Nabugabo, Uganda, to examine partner preferences for grooming and nearest neighbors in each age-sex class. Little is known about this species, so we based our hypotheses on congeners. Of the five species of black-and-white colobus, data on sex-biased dispersal patterns are available for three (C. guereza, C. vellerosus, and C. polykomos), all of which show male-biased dispersal with occasional female dispersal. We thus predicted that female C. a. ruwenzorii would be more strongly bonded than males, showing greater proximity and grooming. We did not expect bonding between the sexes since congeners do not show this pattern. We found that among adult dyads, males and females were more likely to be found in loose proximity, and to groom, than would be expected given group composition. Conversely, both males and females had relatively weak same-sex relationships. Between the sexes, adult males had higher proximity and grooming indices with adult females without infants than with females with infants. These observations indicate that this subspecies is cross-bonded and that both sexes may disperse. Furthermore, our findings suggest that the social organization and social structure of C. a. ruwenzorii differ greatly from other black-and-white colobus species.