RESUMO
Social bonds increase fitness in a range of mammals. One pathway by which social bonds may increase fitness is by reducing the exposure to physiological stress, i.e. glucocorticoid (GC) hormones, that can be detrimental to health and survival. This is achieved through downregulating hypothalamic-pituitary-adrenal (HPA)-axis activity. Indeed, long-term measures of social (grooming) bonds are often negatively correlated with HPA-axis activity. However, the proximate role of physical touch through allogrooming remains an open question in the sociality-health-fitness debate. Demonstrating the potential anxiolytic benefits of grooming in the wild is hindered by methodological limitations. Here, we match accelerometer-identified grooming in wild female chacma baboons (Papio ursinus) to non-invasive faecal GC metabolite concentrations (fGCs). Consistent with previous work, we found a negative (but statistically non-significant) overall relationship between individual averaged fGCs and grooming rates. However, when time-matching grooming to fGCs, we found that both more giving and receiving grooming were followed by higher fGCs. This upregulation of HPA-axis activity suggests that maintaining social bonds (and its ultimate fitness benefits) may come at a shorter-term physiological cost. This finding sheds new light on a ubiquitous social behaviour typically considered 'relaxing' and suggests that sociopositive contact can trigger physiological stress.
Assuntos
Asseio Animal , Estresse Fisiológico , Animais , Feminino , Fezes/química , Glucocorticoides/metabolismo , Comportamento Social , Papio ursinus/fisiologia , Sistema Hipotálamo-Hipofisário/fisiologia , Sistema Hipófise-Suprarrenal/fisiologiaRESUMO
Animals have finite energy reserves for growth, survival, and reproduction and must maintain a stable energy balance. Measuring energy balance in the wild, however, is beset with methodological challenges. Quantification of urinary C-peptide (uCP), a proxy for insulin secretion, has enabled researchers to non-invasively estimate energy balance, and positive relationships between uCP levels and energy intake have been documented in numerous non-human primates. Comparatively few studies show that, consistent with insulin physiology, energy expenditure also alters levels of uCP. The timescale and extent of this relationship, however, remains unclear given the reliance on crude measures of activity and inferred energy expenditure. Here, for the first time, we test for effects of accelerometer-derived Vectorial Dynamic Body Acceleration (VeDBA) - a continuous measure of physical activity energy expenditure - on urinary C-peptide (uCP) levels in n = 12 wild chacma baboons (Papio ursinus). Applying a model selection approach, we show that VeDBA summed over short timescales (30 min to 1 h) prior to urine collection was negatively associated with uCP levels. Using the acceleration-based time individuals spent 'non-stationary' (i.e. locomoting) prior to urine collection as a predictor - instead of summed VeDBA - revealed similar but less clear results. Overall, the negative relationship between VeDBA and uCP levels highlights the importance of quantifying physical activity energy expenditure when using uCP measures to estimate energy balance and has potential implications for the field of energetics accelerometry.
Assuntos
Metabolismo Energético , Papio ursinus , Animais , Peptídeo C , Metabolismo Energético/fisiologia , Aceleração , AcelerometriaRESUMO
Collective behaviour has a critical influence on group social structure and organization, individual fitness and social evolution, but we know little about whether and how it changes in anthropogenic environments. Here, we show multiple and varying effects of urban space-use upon group-level processes in a primate generalist-the chacma baboon (Papio ursinus)-within a managed wild population living at the urban edge in the City of Cape Town, South Africa. In natural space, we observe baboon-typical patterns of collective behaviour. By contrast, in urban space (where there are increased risks, but increased potential for high-quality food rewards), baboons show extreme flexibility in collective behaviour, with changes in spatial cohesion and association networks, travel speeds and group coordination. However, leader-follower roles remain robust across natural and urban space, with adult males having a disproportionate influence on the movement of group members. Their important role in the group's collective behaviour complements existing research and supports the management tactic employed by field rangers of curbing the movements of adult males, which indirectly deters the majority of the group from urban space. Our findings highlight both flexibility and robustness in collective behaviour when groups are presented with novel resources and heightened risks.
Assuntos
Papio ursinus , Coesão Social , Animais , Cidades , Masculino , Papio , África do SulRESUMO
Glucocorticoids (GCs), a class of steroid hormones released through activation of the hypothalamic-pituitary-adrenal (HPA) axis, perform many vital functions essential for survival, including orchestrating an organism's response to stressors by modulating physiological and behavioural responses. Assessing changes and variation in GC metabolites from faecal or urine samples allows for the non-invasive monitoring of HPA-axis activity across vertebrates. The time lag of hormone excretion differs between these sample matrices, which has implications for their suitability for studying effects of different temporal nature on HPA-axis activity. However, simultaneous comparisons of predictors of faecal and urinary GC metabolites (fGCs and uGCs, respectively) are lacking. To address this gap, we employ frequent non-invasive sampling to investigate correlates of fGCs and uGCs in wild chacma baboons (Papio ursinus) (n = 17), including long-term (dominance rank, season, female reproductive state) and short-term (time of day, daily weather conditions) factors. Correlated with increasing day length, fGCs gradually decreased from winter to summer. No seasonal effect on uGCs was found but 'rain days' were associated with increased uGCs. Pregnant females had significantly higher fGCs compared to cycling and lactating females, whereas uGCs were not statistically different across reproductive states. A circadian effect was observed in uGCs but not in fGCs. Dominance rank did not affect either fGCs or uGCs. Our study highlights the difference in inherent fluctuation between uGCs and fGCs and its potential consequences for HPA-axis activity monitoring. While uGCs offer the opportunity to study short-term effects, they undergo more pronounced fluctuations, reducing their ability to capture long-term effects. Given the increasing use of urine for biological monitoring, knowledge of this potential limitation is crucial. Where possible, uGCs and fGCs should be monitored in tandem to obtain a comprehensive understanding of short- and long-term drivers of HPA-axis activity.
Assuntos
Glucocorticoides , Papio ursinus , Animais , Feminino , Glucocorticoides/metabolismo , Sistema Hipotálamo-Hipofisário/metabolismo , Lactação , Papio ursinus/metabolismo , Sistema Hipófise-Suprarrenal/metabolismoRESUMO
The authors investigated left-right turning preferences of n = 260 juvenile European sea bass (Dicentrarchus labrax) reared in ambient conditions and ocean acidification (OA) conditions or in ambient conditions but tested in OA water. Groups of 10 individuals were observed alone in a circular tank, and individuals' left and right turning during free-swimming was quantified using trajectory data from the video. The authors showed that near-future OA levels do not affect the number of turns made, or behavioural lateralization (turning preference), in juvenile D. labrax tested in groups.
Assuntos
Bass , Animais , Natação , Dióxido de Carbono , Concentração de Íons de Hidrogênio , Água do MarRESUMO
Humans have altered up to half of the world's land surface. Wildlife living within or close to these human-modified landscapes are presented with opportunities and risks associated with feeding on human-derived foods (e.g., agricultural crops and food waste). Understanding whether and how wildlife adapts to these landscapes is a major challenge, with thousands of studies published on the topic over the past 10 years. In the present article, we build on established theoretical frameworks to understand the behavioral causes of crop and urban foraging by wildlife. We then develop and extend this framework to describe the multifaceted ecological consequences of crop and urban foraging for the individuals and populations in which they arise, with emphasis on social species for which interactions with people are, on balance, negative (commonly referred to as raiding species). Finally, we discuss the management challenges faced by urban and rural land managers, businesses, and government organizations in mitigating human-wildlife conflicts and propose ways to improve the lives of both wildlife and humans living in human-modified landscapes and to promote coexistence.
RESUMO
Androgens, traditionally viewed as hormones that regulate secondary sexual characteristics and reproduction in male vertebrates, are often modulated by social stimuli. High levels of the 'social hormone' testosterone (T) are linked to aggression, dominance, and competition. Low T levels, in contrast, promote sociopositive behaviours such as affiliation, social tolerance, and cooperation, which can be crucial for group-level, collective behaviours. Here, we test the hypothesis that - in a collective context - low T levels should be favourable, using non-reproductive male and female stickleback fish (Gasterosteus aculeatus) and non-invasive waterborne hormone analysis. In line with our predictions, we show that the fishes' T levels were significantly lower during shoaling compared to when alone, with high-T individuals showing the largest decrease. Ruling out stress-induced T suppression and increased T conversion into oestradiol, we find evidence that shoaling directly affects androgen responsiveness. We also show that groups characterized by lower mean T exhibit less hierarchical leader-follower dynamics, suggesting that low T promotes egalitarianism. Overall, we show that collective action results in lower T levels, which may serve to promote coordination and group performance. Our study, together with recent complementary findings in humans, emphasizes the importance of low T for the expression of sociopositive behaviour across vertebrates, suggesting similarities in endocrine mechanisms.
Assuntos
Androgênios/farmacologia , Comportamento Animal/efeitos dos fármacos , Comportamento Cooperativo , Smegmamorpha/fisiologia , Comportamento Social , Agressão/efeitos dos fármacos , Androgênios/metabolismo , Animais , Feminino , Peixes/fisiologia , Abrigo para Animais , Masculino , Distribuição Aleatória , Reprodução/efeitos dos fármacos , Reprodução/fisiologia , Smegmamorpha/metabolismo , Meio Social , Testosterona/metabolismo , Testosterona/farmacologiaRESUMO
As human-modified landscapes encroach into natural habitats, wildlife face a reduction in natural food sources but also gain access to calorie-rich, human-derived foods. However, research into the energetics of wildlife living within and adjacent to urban and rural landscapes is lacking. C-peptide - a proxy for insulin production and a diagnostic tool for assessing pancreatic function in humans and domestic animals - can be quantified non-invasively from urine (uCP) and may provide a way to investigate the energetic correlates of living in human-altered landscapes. UCP is increasingly used in studies of primate energetics, and here we examine predictors of variation in uCP levels in nâ¯=â¯17 wild chacma baboons (Papio ursinus) living at the urban edge on the Cape Peninsula, South Africa. We find that uCP was positively associated with food provisioning and negatively with night fasting. UCP levels were comparable between winter and summer but significantly lower during spring, possibly driven by consumption of energy-rich seeds during summer and more human-derived foods during winter. UCP was elevated in pregnant females and similar for lactating and cycling females. We find no effect of dominance rank on uCP. Samples collected with synthetic Salivettes had significantly lower uCP levels than directly pipetted samples. Overall, our results indicate that uCP is a reliable, non-invasive measure of energy balance and intake in baboons, and suggest potential energetic benefits of living at the urban edge. More broadly, studies of uCP may offer unique insight into the environmental control of hormone-behaviour relationships in species crossing natural and urban environments.
Assuntos
Peptídeo C/urina , Ecossistema , Metabolismo Energético/fisiologia , Papio ursinus , Animais , Animais Selvagens , Peptídeo C/análise , Feminino , Alimentos , Interação Humano-Animal , Humanos , Lactação/fisiologia , Masculino , Papio ursinus/metabolismo , Papio ursinus/urina , População Rural , Estações do Ano , África do SulRESUMO
An extensive body of research exists on androgen secretion in males. Although androgens are also known to drive patterns of female reproductive physiology and behavior, little attention has been paid to these "male" hormones in females. Here, we examined female fecal androgen excretion in strictly seasonally breeding wild Assamese macaques (Macaca assamensis) and tested the hypothesis that changes in premating season fecal androgens vary with female readiness to resume ovarian cycling and thus to conceive. Across 2 years, 155 fecal samples were collected from seven reproductively quiescent (i.e., acyclic) females during the premating season months, August and September. Samples were analyzed for immunoreactive epiandrosterone (iEA), a major fecal metabolite of testosterone in macaques. Changes in iEA concentrations during the premating season were significantly negatively associated with (1) the presence of dependent offspring, i.e., lactating females showed a smaller change, and (2) with the timing of conceptions in the mating seasons, i.e., females that conceived early exhibited the greatest changes. These results provide strong evidence for a relationship between changes in androgens during the premating season and female readiness to conceive.
Assuntos
Androgênios/análise , Macaca/metabolismo , Comportamento Sexual Animal/fisiologia , Androsterona/análise , Animais , Antropologia Física , Ensaio de Imunoadsorção Enzimática , Fezes/química , Feminino , Macaca/fisiologia , Reprodução/fisiologia , Estações do Ano , Predomínio SocialRESUMO
Species with slow life history strategies that invest in few offspring with extended parental care need to adapt their behavior to cope with anthropogenic changes that occur within their lifetime. Here we show that a female chacma baboon (Papio ursinus) that commonly ranges within urban space in the City of Cape Town, South Africa, stops using urban space after giving birth. This change of space use occurs without any significant change in daily distance traveled or social interactions that would be expected with general risk-sensitive behavior after birth. Instead, we suggest this change occurs because of the specific and greater risks the baboons experience within the urban space compared to natural space, and because leaving the troop (to enter urban space) may increase infanticide risk. This case study can inform methods used to manage the baboons' urban space use in Cape Town and provides insight into how life history events alter individuals' use of anthropogenic environments.
RESUMO
Most studies of collective animal behaviour rely on short-term observations, and comparisons of collective behaviour across different species and contexts are rare. We therefore have a limited understanding of intra- and interspecific variation in collective behaviour over time, which is crucial if we are to understand the ecological and evolutionary processes that shape collective behaviour. Here, we study the collective motion of four species: shoals of stickleback fish (Gasterosteus aculeatus), flocks of homing pigeons (Columba livia), a herd of goats (Capra aegagrus hircus) and a troop of chacma baboons (Papio ursinus). First, we describe how local patterns (inter-neighbour distances and positions), and group patterns (group shape, speed and polarization) during collective motion differ across each system. Based on these, we place data from each species within a 'swarm space', affording comparisons and generating predictions about the collective motion across species and contexts. We encourage researchers to add their own data to update the 'swarm space' for future comparative work. Second, we investigate intraspecific variation in collective motion over time and provide guidance for researchers on when observations made over different time scales can result in confident inferences regarding species collective motion. This article is part of a discussion meeting issue 'Collective behaviour through time'.
Assuntos
Columbidae , Smegmamorpha , Animais , Comportamento Animal , Movimento (Física) , Evolução BiológicaRESUMO
Quantification of activity budgets is pivotal for understanding how animals respond to changes in their environment. Social grooming is a key activity that underpins various social processes with consequences for health and fitness. Traditional methods use direct (focal) observations to calculate grooming rates, providing systematic but sparse data. Accelerometers, in contrast, can quantify activity budgets continuously but have not been used to quantify social grooming. We test whether grooming can be accurately identified using machine learning (random forest model) trained on labelled acceleration data from wild chacma baboons (Papio ursinus). We successfully identified giving and receiving grooming with high precision (81% and 91%) and recall (87% and 79%). Giving grooming was associated with a distinct rhythmical signal along the surge axis. Receiving grooming had similar acceleration signals to resting, and thus was more difficult to assign. We applied our machine learning model to n = 680 collar data days from n = 12 baboons and found that grooming rates obtained from accelerometers were significantly and positively correlated with direct observation rates for giving but not receiving grooming. The ability to collect continuous grooming data in wild populations will allow researchers to re-examine and expand upon long-standing questions regarding the formation and function of grooming bonds.
RESUMO
In placental mammals, pregnancy usually is associated with an increase in maternal androgens, which may significantly impact fetal growth and differentiation, and affect postnatal development and behavior. Owing to their slow life histories and challenging social conditions, determination of maternal androgens and potential interference effects of fetal androgen production are of particular interest in wild primates. However, androgen production has been rarely investigated in wild female primates, and studies on maternal androgens during gestation in particular often do not span the entire pregnancy. Here, we characterize fecal androgen production throughout gestation in wild Assamese macaques (Macaca assamensis) using noninvasive hormone analysis and, furthermore, examine fetal sex effects on maternal androgen excretion. A total of 207 fecal samples were analyzed from seven females for concentrations of immunoreactive epiandrosterone (iEA). Fecal iEA concentrations, as predicted based on cercopithecine blood-serum patterns, increased during early gestation and were significantly higher during the first trimester compared with preconception concentrations and those recorded during later stages of gestation. Further, during the third trimester, male-carrying mothers showed significantly higher iEA concentrations compared with female-carrying mothers. This first characterization of fecal androgen excretion during gestation in Assamese macaques indicates both a maternal and fetal effect on androgen production. Although our sample size is small, our results, nevertheless, provide the basis for assessing potential influences of maternal androgens on postnatal offspring development and behavior.
Assuntos
Androgênios/análise , Fezes/química , Feto/fisiologia , Macaca/fisiologia , Prenhez/fisiologia , Androsterona/análise , Animais , Feminino , Masculino , Gravidez , Fatores Sexuais , Estatísticas não ParamétricasRESUMO
Studies of self-organizing groups like schools of fish or flocks of birds have sought to uncover the behavioral rules individuals use (local-level interactions) to coordinate their motion (global-level patterns). However, empirical studies tend to focus on short-term or one-off observations where coordination has already been established or describe transitions between different coordinated states. As a result, we have a poor understanding of how behavioral rules develop and are maintained in groups. Here, we study the emergence and repeatability of coordinated motion in shoals of stickleback fish (Gasterosteus aculeatus). Shoals were introduced to a simple environment, where their spatio-temporal position was deduced via video analysis. Using directional correlation between fish velocities and wavelet analysis of fish positions, we demonstrate how shoals that are initially uncoordinated in their motion quickly transition to a coordinated state with defined individual leader-follower roles. The identities of leaders and followers were repeatable across two trials, and coordination was reached more quickly during the second trial and by groups of fish with higher activity levels (tested before trials). The rapid emergence of coordinated motion and repeatability of social roles in stickleback fish shoals may act to reduce uncertainty of social interactions in the wild, where individuals live in a system with high fission-fusion dynamics and non-random patterns of association.
RESUMO
Many animal personality traits have implicit movement-based definitions and can directly or indirectly influence ecological and evolutionary processes. It has therefore been proposed that animal movement studies could benefit from acknowledging and studying consistent interindividual differences (personality), and, conversely, animal personality studies could adopt a more quantitative representation of movement patterns.Using high-resolution tracking data of three-spined stickleback fish (Gasterosteus aculeatus), we examined the repeatability of four movement parameters commonly used in the analysis of discrete time series movement data (time stationary, step length, turning angle, burst frequency) and four behavioral parameters commonly used in animal personality studies (distance travelled, space use, time in free water, and time near objects).Fish showed repeatable interindividual differences in both movement and behavioral parameters when observed in a simple environment with two, three, or five shelters present. Moreover, individuals that spent less time stationary, took more direct paths, and less commonly burst travelled (movement parameters), were found to travel farther, explored more of the tank, and spent more time in open water (behavioral parameters).Our case study indicates that the two approaches-quantifying movement and behavioral parameters-are broadly equivalent, and we suggest that movement parameters can be viewed as "micropersonality" traits that give rise to broad-scale consistent interindividual differences in behavior. This finding has implications for both personality and movement ecology research areas. For example, the study of movement parameters may provide a robust way to analyze individual personalities in species that are difficult or impossible to study using standardized behavioral assays.
RESUMO
The earliest studies of collective animal behaviour were inspired by and conducted in the wild. Over the past decades much of the research in this field has shifted to the laboratory, combining high-resolution tracking of individuals with mathematical simulations or agent-based models. Today we are beginning to see a 're-wilding' of collective behaviour thanks to technological advances, providing researchers with the opportunity to quantify and model the heterogeneity that exists within the social groupings they study and within the environments in which these groups live. The perspective we present here aims to inspire and steer this research toward answering fundamental and outstanding behavioural and ecological questions, while also tackling pertinent conservation challenges.
Assuntos
Ecologia/métodos , Etologia/métodos , Comportamento Social , Vertebrados/fisiologia , Animais , Comportamento Animal , Ecologia/instrumentação , Etologia/instrumentaçãoRESUMO
Cortisol coregulation, which is the up- or down-regulation of partners' physiological stress responses, has been described for individuals with strong attachment bonds, e.g. parents and their children, and romantic relationship partners. Research into moderating effects on cortisol coregulation suggests stronger covariation among distressed partners. Whether cortisol coregulation is unique to humans or can also be found in other species that share universal features of the vertebrate stress response remains unexplored. Using a repeated measures approach and non-invasive waterborne hormone analysis, we test the hypothesis that dyads of three-spined stickleback fish (Gasterosteus aculeatus) coregulate their cortisol levels in shared environments. Dyadic cortisol levels were unrelated when cohabiting (home tank), but significantly covaried when sharing a more stressful (as indicated by higher cortisol levels) environment (open field). Time-lag analysis further revealed that open field cortisol levels were predicted by partner's cortisol levels prior to the shared experience. To our knowledge, this study provides the first evidence for coregulatory processes on cortisol responses in a non-human animal that lacks strong bonds and social attachment relationships, suggesting a shared evolutionary origin of cortisol coregulation in vertebrates. From an adaptive perspective, cortisol coregulation may serve to reduce risk in challenging, potentially threatening situations.
Assuntos
Hidrocortisona/metabolismo , Smegmamorpha/metabolismo , Animais , Comportamento Animal , Ecossistema , Smegmamorpha/fisiologiaRESUMO
While the literature on consistent individual differences in correlated suites of physiological and behavioural traits is steadily growing for vertebrates, invertebrates have received less attention. The few studies that do exist have measured temporary physiological states (or responses), rather than consistent individual physiological traits. Here, I explore the consistency of individual differences in physiology and behaviour of n=53 shore crabs (Carcinus maenas) by repeatedly measuring haemolymph density (HD) and the crabs' responses to a novel environment. In crustaceans, HD is directly proportional to protein concentrations, and thus indicative of physiological condition. HD was highly repeatable, and crabs showed consistent individual differences in their behavioural responses to a novel environment, thus indicating individual consistency in both physiology and behaviour. Furthermore, HD was significantly correlated with the crabs' risk propensity, i.e. individuals with higher HD spent more time near shelter. Overall, this provides the first evidence for consistency in an endogenous physiological trait in an invertebrate. The link between consistent physiology and behaviour, i.e. coping styles, analogous to those found in vertebrates, suggests metabolic and/or immunological correlates of personality which offer great potential for future studies.
RESUMO
Social density processes impact the activity and order of collective behaviours in a variety of biological systems. Much effort has been devoted to understanding how density of people affects collective human motion in the context of pedestrian flows. However, there is a distinct lack of empirical data investigating the effects of social density on human behaviour in cooperative contexts. Here, we examine the functioning and performance of human teams in a central-place foraging arena using high-resolution GPS data. We show that team functioning (level of coordination) is greatest at intermediate social densities, but contrary to our expectations, increased coordination at intermediate densities did not translate into improved collective foraging performance, and foraging accuracy was equivalent across our density treatments. We suggest that this is likely a consequence of foragers relying upon visual channels (local information) to achieve coordination but relying upon auditory channels (global information) to maximise foraging returns. These findings provide new insights for the development of more sophisticated models of human collective behaviour that consider different networks for communication (e.g. visual and vocal) that have the potential to operate simultaneously in cooperative contexts.
Assuntos
Comportamento Cooperativo , Comportamento Alimentar/fisiologia , Relações Interpessoais , Comportamento Social , Adolescente , Adulto , Algoritmos , Análise de Variância , Tomada de Decisões/fisiologia , Feminino , Processos Grupais , Humanos , Masculino , Pessoa de Meia-Idade , Desempenho Psicomotor/fisiologia , Adulto JovemRESUMO
The social environment can have a powerful impact on an individual's stress response and thus affect health and biological fitness. Positive social interactions are particularly important for females of species living in complex societies, e.g. humans and non-human primates. Existing studies have mainly focussed on the effect of same-sex social interaction on the stress response, rather than both same- and opposite-sex social interaction simultaneously. However, consideration of both may be crucial since females may have different 'social needs' across different life-history stages. Applying the conceptual framework of allostasis, we tested the hypothesis that female allostatic load (measured through faecal glucocorticoid levels [fGCs]), of wild seasonally breeding Assamese macaques (Macaca assamensis), would increase if their social needs were not maintained in accordance with season. We found significant seasonal differences in same- and opposite-sex sociality which, depending on season, predicted female fGCs. In the mating season, females which spent more time close to males and more frequently groomed with them exhibited lower fGCs. In the non-mating season, when female-male interaction was infrequent, positive female-female sociality predicted lower fGCs. Our results support the hypothesis that same- and opposite-sex sociopositive interactions, specific to certain life-history stages, can mediate fGCs. We interpret this as a consequence of the positive direct and/or indirect effects of social contact in accordance with interactions pertaining to a given life-history stage, which are likely to impact positively upon fitness.