Thyroid hormone concentrations in female baboons: Metabolic consequences of living in a highly seasonal environment.

How female mammals adapt metabolically in response to environmental variation remains understudied in the wild, because direct measures of metabolic activity are difficult to obtain in wild populations. However, recent advances in the non-invasive measurement of fecal thyroid hormones, triiodothyronine (T3), an important regulator of metabolism, provide an opportunity to understand how female baboons living in the harsh Amboseli ecosystem in southern Kenya adapt to environmental variability and escape strict reproductive seasonality. Specifically, we assessed how a female's activity budget, diet, and concentrations of fecal T3 metabolites (mT3) changed over the course of the year and between years. We then tested which of several environmental variables (season, rainfall, and temperature) and behavioral variables (female activity budget and diet) best predicted mT3 concentrations. Finally, we determined if two important reproductive events - onset of ovarian cycling and conception of an offspring - were preceded by changes in female mT3 concentrations. We found female baboons' mT3 concentrations varied markedly across the year and between years as a function of environmental conditions. Further, changes in a female's behavior and diet only partially mediated the metabolic response to the environment. Finally, mT3 concentrations increased in the weeks prior to menarche and cycling resumption, regardless of the month or season in which cycling started. This pattern indicates that metabolic activation may be an indicator of reproductive readiness in female baboons as their energy balance is restored.

Evaluating expert-based habitat suitability information of terrestrial mammals with GPS-tracking data.

Aim: Macroecological studies that require habitat suitability data for many species often derive this information from expert opinion. However, expert-based information is inherently subjective and thus prone to errors. The increasing availability of GPS tracking data offers opportunities to evaluate and supplement expert-based information with detailed empirical evidence. Here, we compared expert-based habitat suitability information from the International Union for Conservation of Nature (IUCN) with habitat suitability information derived from GPS-tracking data of 1,498 individuals from 49 mammal species. Location: Worldwide. Time period: 1998-2021. Major taxa studied: Forty-nine terrestrial mammal species. Methods: Using GPS data, we estimated two measures of habitat suitability for each individual animal: proportional habitat use (proportion of GPS locations within a habitat type), and selection ratio (habitat use relative to its availability). For each individual we then evaluated whether the GPS-based habitat suitability measures were in agreement with the IUCN data. To that end, we calculated the probability that the ranking of empirical habitat suitability measures was in agreement with IUCN's classification into suitable, marginal and unsuitable habitat types. Results: IUCN habitat suitability data were in accordance with the GPS data (> 95% probability of agreement) for 33 out of 49 species based on proportional habitat use estimates and for 25 out of 49 species based on selection ratios. In addition, 37 and 34 species had a > 50% probability of agreement based on proportional habitat use and selection ratios, respectively. Main conclusions: We show how GPS-tracking data can be used to evaluate IUCN habitat suitability data. Our findings indicate that for the majority of species included in this study, it is appropriate to use IUCN habitat suitability data in macroecological studies. Furthermore, we show that GPS-tracking data can be used to identify and prioritize species and habitat types for re-evaluation of IUCN habitat suitability data.

Effects of body size on estimation of mammalian area requirements.

Accurately quantifying species' area requirements is a prerequisite for effective area-based conservation. This typically involves collecting tracking data on species of interest and then conducting home-range analyses. Problematically, autocorrelation in tracking data can result in space needs being severely underestimated. Based on the previous work, we hypothesized the magnitude of underestimation varies with body mass, a relationship that could have serious conservation implications. To evaluate this hypothesis for terrestrial mammals, we estimated home-range areas with global positioning system (GPS) locations from 757 individuals across 61 globally distributed mammalian species with body masses ranging from 0.4 to 4000 kg. We then applied block cross-validation to quantify bias in empirical home-range estimates. Area requirements of mammals <10 kg were underestimated by a mean approximately15%, and species weighing approximately100 kg were underestimated by approximately50% on average. Thus, we found area estimation was subject to autocorrelation-induced bias that was worse for large species. Combined with the fact that extinction risk increases as body mass increases, the allometric scaling of bias we observed suggests the most threatened species are also likely to be those with the least accurate home-range estimates. As a correction, we tested whether data thinning or autocorrelation-informed home-range estimation minimized the scaling effect of autocorrelation on area estimates. Data thinning required an approximately93% data loss to achieve statistical independence with 95% confidence and was, therefore, not a viable solution. In contrast, autocorrelation-informed home-range estimation resulted in consistently accurate estimates irrespective of mass. When relating body mass to home range size, we detected that correcting for autocorrelation resulted in a scaling exponent significantly >1, meaning the scaling of the relationship changed substantially at the upper end of the mass spectrum.

Efectos del Tamaño Corporal sobre la Estimación de los Requerimientos de Área de Mamíferos Resumen La cuantificación precisa de los requerimientos de área de una especie es un prerrequisito para que la conservación basada en áreas sea efectiva. Esto comúnmente implica la recolección de datos de rastreo de la especie de interés para después realizar análisis de la distribución local. De manera problemática, la autocorrelación en los datos de rastreo puede resultar en una subestimación grave de las necesidades de espacio. Con base en trabajos previos, formulamos una hipótesis en la que supusimos que la magnitud de la subestimación varía con la masa corporal, una relación que podría tener implicaciones serias para la conservación. Para probar esta hipótesis en mamíferos terrestres, estimamos las áreas de distribución local con las ubicaciones en GPS de 757 individuos de 61 especies de mamíferos distribuidas mundialmente con una masa corporal entre 0.4 y 4,000 kg. Después aplicamos una validación cruzada en bloque para cuantificar el sesgo en estimaciones empíricas de la distribución local. Los requerimientos de área de los mamíferos <10 kg fueron subestimados por una media ∼15% y las especies con una masa ∼100 kg fueron subestimadas en ∼50% en promedio. Por lo tanto, encontramos que la estimación del área estaba sujeta al sesgo inducido por la autocorrelación, el cual era peor para las especies de talla grande. En combinación con el hecho de que el riesgo de extinción incrementa conforme aumenta la masa corporal, el escalamiento alométrico del sesgo que observamos sugiere que la mayoría de las especies amenazadas también tienen la probabilidad de ser aquellas especies con las estimaciones de distribución local menos acertadas. Como corrección, probamos si la reducción de datos o la estimación de la distribución local informada por la autocorrelación minimizan el efecto de escalamiento que tiene la autocorrelación sobre las estimaciones de área. La reducción de datos requirió una pérdida de datos del ∼93% para lograr la independencia estadística con un 95% de confianza y por lo tanto no fue una solución viable. Al contrario, la estimación de la distribución local informada por la autocorrelación resultó en estimaciones constantemente precisas sin importar la masa corporal. Cuando relacionamos la masa corporal con el tamaño de la distribución local, detectamos que la corrección de la autocorrelación resultó en un exponente de escalamiento significativamente >1, lo que significa que el escalamiento de la relación cambió sustancialmente en el extremo superior del espectro de la masa corporal.

Estimation of energetic condition in wild baboons using fecal thyroid hormone determination.

Understanding how environmental and social factors affect reproduction through variation in energetic condition remains understudied in wild animals, in large part because accurately and repeatedly measuring energetic condition in the wild is a challenge. Thyroid hormones (THs), such as triiodothyronine (T3) and thyroxine (T4), have a key role in mitigating metabolic responses to energy intake and expenditure, and therefore are considered important biomarkers of an animal's energetic condition. Recent method development has shown that T3 and T4 metabolites can be measured in feces, but studies measuring THs in wild populations remain rare. Here we measured fecal T3 metabolites (mT3) in baboons, and tested whether the conditions of collection and storage used for steroid hormones could also be used for mT3; we focused on mT3 as it is the biologically active form of TH and because fecal T4 metabolites (mT4) were below detection levels in our samples. We also tested if mT3 could be determined in freeze-dried samples stored for long periods of time, and if these concentrations reflected expected biological variations across seasons and reproductive states. Our results show that mT3 can be measured with accuracy and precision in baboon feces. The conditions of collection and storage we use for steroid hormones are appropriate for mT3 determination. In addition, mT3 concentrations can be determined in samples stored at -20 °C for up to 9 years, and are not predicted by the amount of time in storage. As expected, wild female baboons have lower mT3 concentrations during the dry season. Interestingly, mT3 concentrations are lower in pregnant and lactating females, possibly reflecting an energy sparing mechanism. Retroactive determination of mT3 concentration in stored, freeze-dried feces opens the door to novel studies on the role of energetic condition on fitness in wild animals.

The relationship between social play and developmental milestones in wild chimpanzees (Pan troglodytes schweinfurthii).

Social play is common among many group-living animals, but the benefits are not well understood. Proposed benefits include increased muscle coordination as the result of increased locomotor versatility and development, and strengthened social bonds through interactions with like-aged individuals. In this study, we used 33 years of long-term behavioral data on infant chimpanzees in Gombe National Park, Tanzania, to examine these potential benefits of social play, specifically how the percentage of time engaged in social play relates to motor and social developmental milestones. We predicted that infants who engaged in more social play would achieve motor and social milestones at younger ages. We found that individuals that spent more time engaging in social play achieved the motor milestones of riding dorsally and traveling independently at earlier ages. Additionally, we found that the amount of play was correlated with earlier ages for reaching the social milestones of spatial independence from mother, first grooming of non-maternal kin, and first observed mating attempt. This is the first study in great apes to demonstrate a relationship between play behavior and developmental milestones, supporting the hypotheses that play provides motor, and social benefits.

Limited evidence for third-party affiliation during development in wild chimpanzees (Pan troglodytes schweinfurthii).

Examining the ontogeny of conflict-mitigating behaviours in our closest living relatives is an important component of understanding the evolutionary origins of cooperation in our species. In this study, we used 26 years of data to investigate the emergence of third-party affiliation (TPA), defined as affiliative contact given to recipients of aggression by uninvolved bystanders (regardless of initiation), in wild immature eastern chimpanzees (Pan troglodytes schweinfurthii) of Gombe National Park, Tanzania. We also characterized TPA by mothers in the same dataset as an adult benchmark for interpreting immature TPA patterns. In summary, we found that immatures did not express TPA as measured by grooming between the ages of 1.5 and 12.0 years, and that there was limited evidence that immatures expressed TPA via play. We also found that mothers did express TPA to offspring, although mothers did not show TPA towards non-offspring. Cases of TPA by mothers to other adults were too few to analyse separately. These results contrast with findings from captive studies which found that chimpanzees as young as 6 years of age demonstrated TPA. We argue that within-species variation in the expression of TPA, both in immatures and adulthood, provides evidence that the conflict management behaviours of young chimpanzees may be heavily influenced by social, ecological and demographic factors.

Costs and benefits of group living in primates: an energetic perspective.

Group size is a fundamental component of sociality, and has important consequences for an individual's fitness as well as the collective and cooperative behaviours of the group as a whole. This review focuses on how the costs and benefits of group living vary in female primates as a function of group size, with a particular emphasis on how competition within and between groups affects an individual's energetic balance. Because the repercussions of chronic energetic stress can lower an animal's fitness, identifying the predictors of energetic stress has important implications for understanding variation in survivorship and reproductive success within and between populations. Notably, we extend previous literature on this topic by discussing three physiological measures of energetic balance-glucocorticoids, c-peptides and thyroid hormones. Because these hormones can provide clear signals of metabolic states and processes, they present an important complement to field studies of spatial and temporal changes in food availability. We anticipate that their further application will play a crucial role in elucidating the adaptive significance of group size in different social and ecological contexts.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Reproductive state and rank influence patterns of meat consumption in wild female chimpanzees (Pan troglodytes schweinfurthii).

An increase in faunivory is a consistent component of human evolutionary models. Animal matter is energy- and nutrient-dense and can provide macronutrients, minerals, and vitamins that are limited or absent in plant foods. For female humans and other omnivorous primates, faunivory may be of particular importance during the costly periods of pregnancy and early lactation. Yet, because animal prey is often monopolizable, access to fauna among group-living primates may be mediated by social factors such as rank. Wild chimpanzees (Pan troglodytes) across Africa habitually consume insects and/or vertebrates. However, no published studies have examined patterns of female chimpanzee faunivory during pregnancy and early lactation relative to non-reproductive periods, or by females of different rank. In this study, we assessed the influence of reproductive state and dominance rank on the consumption of fauna (meat and insects) by female chimpanzees of Gombe National Park, Tanzania. Using observational data collected over 38 years, we tested (a) whether faunivory varied by reproductive state, and (b) if high-ranking females spent more time consuming fauna than lower-ranking females. In single-factor models, pregnant females consumed more meat than lactating and baseline (meaning not pregnant and not in early lactation) females, and high-ranking females consumed more meat than lower-ranking females. A two-factor analysis of a subset of well-sampled females identified an interaction between rank and reproductive state: lower-ranking females consumed more meat during pregnancy than lower-ranking lactating and baseline females did. High-ranking females did not significantly differ in meat consumption between reproductive states. We found no relationships between rank or reproductive state with insectivory. We conclude that, unlike insectivory, meat consumption by female chimpanzees is mediated by both reproductive state and social rank. We outline possible mechanisms for these patterns, relate our findings to meat-eating patterns in women from well-studied hunter-gatherer societies, and discuss potential avenues for future research.

Optimal group size in a highly social mammal.

Group size is an important trait of social animals, affecting how individuals allocate time and use space, and influencing both an individual's fitness and the collective, cooperative behaviors of the group as a whole. Here we tested predictions motivated by the ecological constraints model of group size, examining the effects of group size on ranging patterns and adult female glucocorticoid (stress hormone) concentrations in five social groups of wild baboons (Papio cynocephalus) over an 11-y period. Strikingly, we found evidence that intermediate-sized groups have energetically optimal space-use strategies; both large and small groups experience ranging disadvantages, in contrast to the commonly reported positive linear relationship between group size and home range area and daily travel distance, which depict a disadvantage only in large groups. Specifically, we observed a U-shaped relationship between group size and home range area, average daily distance traveled, evenness of space use within the home range, and glucocorticoid concentrations. We propose that a likely explanation for these U-shaped patterns is that large, socially dominant groups are constrained by within-group competition, whereas small, socially subordinate groups are constrained by between-group competition and predation pressures. Overall, our results provide testable hypotheses for evaluating group-size constraints in other group-living species, in which the costs of intra- and intergroup competition vary as a function of group size.

Maternal rank influences the outcome of aggressive interactions between immature chimpanzees.

For many long-lived mammalian species, extended maternal investment has a profound effect on offspring integration in complex social environments. One component of this investment may be aiding young in aggressive interactions, which can set the stage for offspring social position later in life. Here we examined maternal effects on dyadic aggressive interactions between immature (<12 years) chimpanzees. Specifically, we tested whether relative maternal rank predicted the probability of winning an aggressive interaction. We also examined maternal responses to aggressive interactions to determine whether maternal interventions explain interaction outcomes. Using a 12-year behavioural data set (2000-2011) from Gombe National Park, Tanzania, we found that relative maternal rank predicted the probability of winning aggressive interactions in male-male and male-female aggressive interactions: offspring were more likely to win if their mother outranked their opponent's mother. Female-female aggressive interactions occurred infrequently (two interactions), so could not be analysed. The probability of winning was also higher for relatively older individuals in male-male interactions, and for males in male-female interactions. Maternal interventions were rare (7.3% of 137 interactions), suggesting that direct involvement does not explain the outcome for the vast majority of aggressive interactions. These findings provide important insight into the ontogeny of aggressive behaviour and early dominance relationships in wild apes and highlight a potential social advantage for offspring of higher-ranking mothers. This advantage may be particularly pronounced for sons, given male philopatry in chimpanzees and the potential for social status early in life to translate more directly to adult rank.

Sex differences in wild chimpanzee behavior emerge during infancy.

The role of biological and social influences on sex differences in human child development is a persistent topic of discussion and debate. Given their many similarities to humans, chimpanzees are an important study species for understanding the biological and evolutionary roots of sex differences in human development. In this study, we present the most detailed analyses of wild chimpanzee infant development to date, encompassing data from 40 infants from the long-term study of chimpanzees at Gombe National Park, Tanzania. Our goal was to characterize age-related changes, from birth to five years of age, in the percent of observation time spent performing behaviors that represent important benchmarks in nutritional, motor, and social development, and to determine whether and in which behaviors sex differences occur. Sex differences were found for indicators of social behavior, motor development and spatial independence with males being more physically precocious and peaking in play earlier than females. These results demonstrate early sex differentiation that may reflect adult reproductive strategies. Our findings also resemble those found in humans, which suggests that biologically-based sex differences may have been present in the common ancestor and operated independently from the influences of modern sex-biased parental behavior and gender socialization.

Rank effects on social stress in lactating chimpanzees.

Given the deleterious consequences associated with chronic stress, individual differences in stress susceptibility can have important fitness implications. These differences may be explained in part by dominance status because high rank is typically associated with decreased aggression and improved nutrition. Here, we examined the relationship between dominance and social stress in lactating chimpanzees, Pan troglodytes schweinfurthii, at Gombe National Park, Tanzania. We did so by pairing daily demographic and behavioural data with faecal glucocorticoid metabolite (FGM) concentrations collected over 37 months. While there was no main effect of rank, interesting differences emerged by adult subgroup size and adult sex ratio (males/females). We found that differences in FGM concentrations between high- and low-ranking females were most pronounced as adult subgroup size and sex ratio increased. Low-ranking females had higher FGM concentrations in larger subgroups and in subgroups biased towards adult males; we observed no comparable change in FGM concentrations amongst high-ranking females. Because low-ranking females were the recipient of significantly more male aggression relative to females of high rank, these patterns may be driven by psychosocial stress in low-ranking females. There was no significant change in diet quality across subgroup sizes; this finding suggests that nutritional stressors were not driving differences in female FGM concentrations. Being susceptible to social stress has important fitness implications as it may constrain low-ranking females from 'choosing' optimal subgroups to take advantage of food resources and/or for the socialization of their offspring.

Competing for space: female chimpanzees are more aggressive inside than outside their core areas.

Female space use can have important fitness consequences, which are likely due to differential access to food resources. Many studies have explored spatial competition in solitary species, but little is known about how individuals in social species compete over shared space. In this study, we investigate spatial patterns of aggression among female East African chimpanzees, Pan troglodytes schweinfurthii. This species provides an excellent opportunity to study spatial competition since (1) female chimpanzees occupy overlapping core areas (small areas of the community range in which individuals concentrate their space use) and (2) female core area quality is correlated with reproductive success, suggesting that females compete over long-term access to core areas. Here, we examine how female aggression towards other females varies inside and outside individual female core areas during a 14-year period at Gombe National Park, Tanzania. Overall, females showed higher rates of aggression inside than outside their own core areas. This pattern was driven by spatial variation in aggression in nonfeeding contexts. While food-related aggression did not vary spatially, females were more aggressive in nonfeeding contexts inside their core areas than they were outside their core areas. These results suggest that female chimpanzees follow a mixed strategy in which they compete for long-term access to resources in their core areas as well as for immediate access to food throughout the community range.

When good neighbors don't need fences: Temporal landscape partitioning among baboon social groups.

Intraspecific competition is a key factor shaping space-use strategies and movement decisions in many species, yet how and when neighbors utilize shared areas while exhibiting active avoidance of one another is largely unknown. Here we investigated temporal landscape partitioning in a population of wild baboons (Papio cynocephalus). We used global positioning system (GPS) collars to synchronously record the hourly locations of 5 baboon social groups for ~900 days, and we used behavioral, demographic, and life history data to measure factors affecting use of overlap areas. Annual home ranges of neighboring groups overlapped substantially, as predicted (baboons are considered non-territorial), but home ranges overlapped less when space use was assessed over shorter time scales. Moreover, neighboring groups were in close spatial proximity to one another on fewer days than predicted by a null model, suggesting an avoidance-based spacing pattern. At all time scales examined (monthly, biweekly, and weekly), time spent in overlap areas was greater during time periods when groups fed on evenly dispersed, low-quality foods. The percent of fertile females in social groups was negatively correlated with time spent in overlap areas only during weekly time intervals. This suggests that broad temporal changes in ecological resources are a major predictor of how intensively overlap areas are used, and groups modify these ecologically driven spacing patterns at short time scales based on female reproductive status. Together these findings offer insight into the economics of territoriality by highlighting the dynamics of spacing patterns at differing time scales.

Intergroup conflict: Ecological predictors of winning and consequences of defeat in a wild primate population.

In many social species, competition between groups is a major factor proximately affecting group-level movement patterns and space use and ultimately shaping the evolution of group living and complex sociality. Here we evaluated the factors influencing group-level dominance among 5 social groups of wild baboons (Papio cynocephalus), in particular focusing on the spatial determinants of dominance and the consequences of defeat. When direct conflict occurred between conspecific baboon groups, the winning group was predicted by differences in the number of adult males in each group and/or groups that had used the areas surrounding the encounter location more intensively than their opponent in the preceding 9 or 12 months. Relative intensity of space use over shorter timescales examined (3 and 6 months) was a poor predictor of the interaction's outcome. Losing groups but not winning groups experienced clear short-term costs. Losing groups used the area surrounding the interaction less following an agonistic encounter (relative to their intensity of use of the area prior to the interaction). These findings offer insight into the influences and consequences of intergroup competition on group-level patterns of space use.

White monkey syndrome and presumptive copper deficiency in wild savannah baboons.

In immature wild savannah baboons (Papio cynocephalus), we observed symptoms consistent with copper (Cu) deficiency and, more specifically, with a disorder referred to as white monkey syndrome (WMS) in laboratory primates. The objectives of this study were to characterize this pathology, and test three hypotheses that (1) Cu deficiency may have been induced by zinc (Zn) toxicity, (2) it may have been induced by molybdenum (Mo) toxicity, and (3) cumulative rainfall during the perinatal period and particularly during gestation is an ecological factor distinguishing infants afflicted with WMS from non-WMS infants. During 2001-2009, we observed 22 instances of WMS out of a total 377 live births in the study population. Visible symptoms exhibited by WMS infants included whitening of the animal's fur and/or impaired mobility characterized by an apparent "stiffening" of the hindlimbs. Occurrence of WMS did not vary significantly by gender. However, among individuals that survived at least 180 days, WMS males had a significantly lower survivorship probability than non-WMS males. Zn/Cu ratios assessed from hair samples of adult female baboons were higher in females who had produced at least one WMS offspring relative to females who had not had a WMS offspring. This was true even when the hair sample was collected long after the birth of the female's afflicted infant. We consider this potentially indicative of a robust tendency for low Cu levels induced by elevated Zn intake in some individuals. No significant differences of Mo/Cu ratios were observed. Cumulative rainfall during gestation (∼179 days) was 50% lower for WMS infants relative to non-WMS infants. In contrast, rainfall for the two classes of infants did not differ in the 180 days before conception or in the 180 days following birth. This finding highlights the importance of prenatal ecological conditions in healthy fetal development with regard to WMS.

Remote monitoring of primates using automated GPS technology in open habitats.

Automated tracking using a satellite global position system (GPS) has major potential as a research tool in studies of primate ecology. However, implementation has been limited, at least partly because of technological difficulties associated with the dense forest habitat of many primates. In contrast, primates inhabiting relatively open environments may provide ideal subjects for use of GPS collars, yet no empirical tests have evaluated this proposition. Here, we used an automated GPS collar to record the locations, approximate body surface temperature, and activity for an adult female baboon during 90 days in the savannah habitat of Amboseli, Kenya. Given the GPS collar's impressive reliability, high spatial accuracy, other associated measurements, and low impact on the study animal, our results indicate the great potential of applying GPS technology to research on wild primates.