RESUMEN
For males of gregarious species, dominance status and the strength of affiliative relationships can have major fitness consequences. Social dynamics also impose costs by affecting glucocorticoids, mediators of homeostasis and indicators of the physiological response to challenges and within-group competition. We investigated the relationships between dominance, social bonds, seasonal challenges, and faecal glucocorticoid metabolite (fGC) measures in wild Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, Thailand, combining behavioural data with 4129 samples from 62 adult males over 15 years. Our previous work on this population suggested that increased competition during the mating season was associated with elevated fGC levels and that, unusually for male primates, lower rank position correlated with higher fGC levels. With a much larger dataset and dynamic measures of sociality, we re-examined these relationships and additionally tested the potentially fGC-attenuating effect of social support. Contrary to our previous study, yet consistent with the majority of work on male primates, dominance rank had a positive relationship with fGC levels, as high status correlated with elevated glucocorticoid measures. fGC levels were increased at the onset of the mating season. We demonstrated an fGC-reducing effect of supportive relationships in males and showed that dynamics in affiliation can correlate with dynamics in physiological responses. Our results suggest that in a system with intermediate contest potential, high dominance status can impose physiological costs on males that may potentially be moderated by social relationships. We highlight the need to consider the dynamics of sociality and competition that influence hormonal processes.
Asunto(s)
Heces , Glucocorticoides , Macaca , Conducta Social , Predominio Social , Animales , Masculino , Glucocorticoides/metabolismo , Glucocorticoides/análisis , Heces/química , Macaca/fisiología , Estaciones del Año , Animales Salvajes/fisiología , Tailandia , Conducta Animal/fisiologíaRESUMEN
Female fertility signals are found across taxa, and the precision of such signals may be influenced by the relative strength of different sexual selection mechanisms. Among primates, more precise signals may be found in species with stronger direct male-male competition and indirect female mate choice, and less precise signals in species with stronger indirect male-male competition (e.g. sperm competition) and direct female mate choice. We tested this hypothesis in a wild population of Kinda baboons in Zambia, combining data on female signals with reproductive hormones (estrogen and progesterone metabolites) and intra- and inter-cycle fertility. We predicted that Kinda baboons will exhibit less precise fertility signals than other baboon species, as they experience weaker direct and stronger indirect male-male competition. The frequency of copulation calls and proceptive behavior did not vary with hormones or intra- or inter-cycle fertility in almost all models. Sexual swelling size was predicted by the ratio of estrogen to progesterone metabolites, and was largest in the fertile phase, but differences in size across days were small. Additionally, there was variability in the timing of ovulation relative to the day of sexual swelling detumescence across cycles and swelling size did not vary with inter-cycle fertility. Our results suggest that female Kinda baboon sexual swellings are less precise indicators of fertility compared to other baboon species, while signals in other modalities do not reflect variation in intra- and inter-cycle fertility. Female Kinda baboon sexual signals may have evolved as a strategy to reduce male monopolizability, allowing for more female control over reproduction by direct mate choice.
RESUMEN
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.
Asunto(s)
Aseo Animal , Estrés Fisiológico , Animales , Femenino , Heces/química , Glucocorticoides/metabolismo , Conducta Social , Papio ursinus/fisiología , Sistema Hipotálamo-Hipofisario/fisiología , Sistema Hipófiso-Suprarrenal/fisiologíaRESUMEN
Glucocorticoid and androgen hormones play a prominent role in male reproductive effort. Their production usually increases in non-human primates during mating competition, which may include rivalry for access to receptive females, struggles for high dominance rank, or social pressure on low-ranking individuals. It is generally assumed that glucocorticoids and androgens are associated with mating challenges rather than dominance status, but the involvement of multiple factors makes it difficult to disentangle the two. In this regard, Tonkean macaques provide a suitable model because they are characterized by relaxed dominance and year-round breeding, meaning that there is typically no more than one receptive female in a group, and thus first-ranking males can easily monopolize her. We studied two captive groups of Tonkean macaques over an 80-month period, recording the reproductive status of females, collecting urine from males and sampling behaviors in both sexes. Male urinary hormone concentrations could be affected by increased competition caused by the mating period, the number of males and the degree of female attractiveness. The highest increases in androgens were recorded in males performing female mate-guarding. Despite the importance of dominance status in determining which males can mate, we found no significant effect of male rank on glucocorticoids and only a marginal effect on androgens during mate-guarding. Both types of hormones were more directly involved in the mating effort of males than in their dominance status. Our results show that their function can be understood in light of the particular competitive needs generated by the species-specific social system.
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Andrógenos , Glucocorticoides , Animales , Femenino , Masculino , Conducta Sexual Animal/fisiología , Macaca/fisiología , Predominio SocialRESUMEN
Thyroid hormones are key modulators of development, as well as mediators of environmental conditions, by regulating developmental processes and metabolism in primates. Hormone measurement in noninvasively collected samples, that is, feces and urine, is a valuable tool for studying the endocrine function of wildlife, and recent studies have demonstrated the feasibility of measuring thyroid hormones in fecal samples of zoo-housed and wild nonhuman primates. Our study aimed to (i) validate the measurement of immunoreactive fecal total triiodothyronine (IF-T3) in wild Assamese macaques (Macaca assamensis) and (ii) to investigate its developmental changes and its response to environmental changes, including stress responses, in immature individuals. Fecal samples and environmental parameters were collected from individuals of three social groups of wild Assamese macaques living at Phu Khieo Wildlife Sanctuary, Northeastern Thailand. Our study confirmed the methodological feasibility and biological validity of measuring IF-T3 in this population. Specifically, the biological validation demonstrated higher IF-T3 levels in immatures compared to adults, and higher levels in females during late gestation compared to the preconception stage. Our analysis of IF-T3 levels in developing immature macaques revealed a significant increase with age. Furthermore, we found a positive association between IF-T3 and immunoreactive fecal glucocorticoid levels, an indicator of the physiological stress response. Neither minimum temperature nor fruit abundance predicted variation in IF-T3 levels in the immatures. Our findings indicate the possibility for differing effects of climatic factors and food availability on thyroid hormone level changes in immature versus adult animals and in wild compared to experimental conditions. Overall, our study provides the basis for further investigations into the role of thyroid hormones in shaping species-specific traits, growth, and overall primate development.
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Animales Salvajes , Macaca , Femenino , Animales , Embarazo , Macaca/fisiología , Hormonas Tiroideas , Fenotipo , HecesRESUMEN
Measurement of the health and disease status of free-ranging primates is often limited by a lack of available biomarkers of immune activation and inflammation that can be applied noninvasively via the measurement of urine or fecal samples. Here, we evaluate the potential usefulness of noninvasive urinary measurements of a number of cytokines, chemokines, and other markers of inflammation and infection. We took advantage of surgery-associated inflammation in seven captive rhesus macaques, collecting urine samples before and after the medical interventions. We measured these urine samples for 33 different markers of inflammation and immune activation that are known to be responsive to inflammation and infection in rhesus macaque blood samples, via the Luminex platform. We also measured all samples for concentrations of the soluble urokinase plasminogen activator receptor (suPAR), which we had validated in a prior study as an effective biomarker of inflammation. Despite urine samples being collected in captivity under ideal conditions (clean, no contamination with feces or soil, frozen quickly), 13/33 biomarkers measured via Luminex were found at concentrations below detection limits in >50% of samples. Of the remaining 20 markers, only 2 showed significant increases in response to surgery-IL18 and MPO (myeloperoxidase). However, suPAR measurements of the same samples show a consistent marked increase in response to surgery that is absent from the patterns of IL18 and MPO measurement. Given that our samples were collected under conditions that are greatly preferable to those usually encountered in the field, urinary cytokine measurements via the Luminex platform seem overall unpromising for primate field studies.
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Interleucina-18 , Receptores del Activador de Plasminógeno Tipo Uroquinasa , Animales , Macaca mulatta , Inflamación/veterinaria , Biomarcadores , CitocinasRESUMEN
In male vertebrates, testosterone is generally known to coordinate reproductive trade-offs, in part by promoting the transition to the next reproduction at the expense of current parental care. The role of testosterone in reproductive transitions has been little tested in female vertebrates, especially in mammals. The present study sought to fill this gap, by first undertaking an experimental study, in which we identified DHT, androstenediol, and in particular etiocholanolone, as fecal androgen metabolites which reflect serum testosterone concentration in female rhesus macaques (Macaca mulatta). Using concentrations of fecal etiocholanolone as proxy for circulating testosterone, we then conducted a field study on 46 free-ranging rhesus macaques of Cayo Santiago, Puerto Rico, to test if testosterone mediates the trade-off between reproductive transition (a higher chance of reproducing in the next year) and current reproduction (providing more care to current offspring). While the evidence for testosterone was weak, the testing of fecal immunoreactive estrogen metabolites suggested a potential role of estrogen in reproductive trade-offs. We found large individual differences in fecal etiocholanolone concentrations during the early postpartum period that were unexplained even after accounting for sociodemographic factors such as age and dominance rank. Further investigation is needed to understand this variation. Our study suggests that the actions of testosterone in females may not have evolved to fulfil the same role in primate reproductive transitions as it does in males, and we encourage more studies to consider the function of testosterone in reproductive behaviors and life history transitions in females of mammalian taxa.
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Estrógenos , Testosterona , Animales , Etiocolanolona , Femenino , Macaca mulatta , Masculino , Mamíferos , ReproducciónRESUMEN
Androgens offer a window into the timing of important male life history events such as maturation. However, when males are the dispersing sex, piecing together normative androgen profiles across development is challenging because dispersing males are difficult to track. Here, we examined the conditions that may be associated with male androgen status (via fecal androgen metabolites, fAMs) and age at dispersal in wild male geladas (Theropithecus gelada). Gelada male life histories are highly variable - dispersal may occur before sexual maturation, dispersal itself can be immediate or drawn out, and, due to their multi-leveled society, social conditions affecting dispersal can vary for juveniles living in different reproductive units within the same band. Using longitudinal data from known natal males, we examined how androgen levels and age at dispersal were associated with: (1) access to maternal resources (i.e., maternal rank, birth of a younger sibling, experiencing maternal loss), and (2) access to male peers (i.e., number of similar-aged males in their unit). We found that androgens were significantly lower in males with high-ranking mothers (in males >2.5 years of age; infant androgens were unrelated) and that having more male peers in their social group and larger groups overall predicted an earlier age at dispersal. Moreover, dispersal in geladas was not preceded or followed by a surge in androgen levels. Taken together, results suggest that social environments can cause individual variation in androgens and dispersal age. Whether this variation leads to differences in male fitness in later life remains to be determined.
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Theropithecus , Animales , Masculino , Humanos , Anciano , Andrógenos , ReproducciónRESUMEN
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.
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Glucocorticoides , Papio ursinus , Animales , Femenino , Glucocorticoides/metabolismo , Sistema Hipotálamo-Hipofisario/metabolismo , Lactancia , Papio ursinus/metabolismo , Sistema Hipófiso-Suprarrenal/metabolismoRESUMEN
Energy availability drives an individual's fitness and can be affected by diverse energetic challenges. The assessment of hormones involved in metabolic activity and energy mobilization provides a gateway to the study of physiological adaptations in response to changes in energy availability. Here, we investigated immunoreactive urinary total triiodothyronine (uTT3, thyroid hormone secreted through the hypothalamus-pituitary-thyroid axis and regulating the basal metabolic rate) alongside glucocorticoids (i.e. urinary cortisol, uCort, secreted through the hypothalamus-pituitary-adrenal axis and mediating energy mobilization) in wild female Assamese macaques (Macaca assamensis). Combining more than 2900; of behavioral data from 42 adult females with physiological data from 382 urine samples, we evaluated both uTT3 and uCort in relation to potential energetic challenges encountered by a female, namely fluctuations in energy intake, travel distance, reproductive state and minimum ambient temperature. As predicted, levels of both hormones changed in response to variation in energy intake with a tendency toward a positive effect on uTT3 and a significant negative effect on uCort levels. Unexpectedly, neither hormone was influenced by variation in travel distance. Reproductive state affected both hormones with higher levels of uTT3 and uCort in the second half of gestation. Finally, a decrease of minimum temperature triggered an increase in uCort but unexpectedly not in uTT3. Collectively, our results highlight the respective contribution of two endocrine axes when facing energetic challenges and the underlying metabolic strategies to cope with them. Overall, assessing thyroid hormones together with glucocorticoids provides an integrative picture in the evaluation of an individual's energy status.
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Macaca , Triyodotironina , Animales , Regulación de la Temperatura Corporal , Ingestión de Alimentos , Femenino , Hidrocortisona , ReproducciónRESUMEN
Regulation of energy allocation and metabolic rate plays an important role in determining behavior and fitness in wild animals, calling for the validation of non-invasive markers of energetic condition. Recently, the thyroid hormone triiodothyronine (T3) has emerged as a promising marker as concentrations decrease to lower the metabolic rate during energetically challenging periods. However, it remains largely unclear whether T3 merely represents an alternative or provides additional information compared to other compounds involved in the regulation of energy acquisition and allocation, like cortisol and C-peptide, as few joint measurements have been conducted to date in non-invasively collected samples. We aimed to validate the non-invasive measurement of immunoreactive urinary total T3 (uTT3), in comparison to urinary cortisol (uCort) and urinary C-peptide (uCP), as a marker of metabolic response to variation in food intake in macaques, and to address a number of issues regarding the collection, storage and processing of samples which are important for application of uTT3 measurements under field conditions. We used daily samples and body mass measures from a prior food restriction-refeeding experiment over 4 weeks with six captive macaques and analyzed concentrations of uTT3 and uCort in samples collected prior to (fasting) and after morning feeding (non-fasting). Concentrations of uTT3 decreased in response to restriction in food supply and were also lower during weeks of food restriction compared to weeks of refeeding. Variation in uTT3 also correlated positively with variation in body mass and concentrations of uCP. As expected, uCort showed the reverse pattern, increasing during food restriction and decreasing following refeeding, but was not associated with variation in body mass. Generally, compared to fasting samples, concentrations were higher in post-morning feeding, i.e. non-fasting, samples for uTT3 but not uCort. Contamination of urine samples with fecal matter, but not soil, and exposure to UV light led to a decrease in uTT3. uTT3 was largely unaffected by repeated freeze-thaw cycles and by refrigeration for medium-term storage (2 days) but degraded substantially when stored at ambient temperature for the same period. In conclusion, uTT3 measurements inform on the effect of food intake and its associated metabolic response to variation in energetic status. Since uTT3 is reasonably robust to many issues associated with collection and storage of urine samples under field conditions, it is a promising biomarker for studies of energetic condition and basal metabolic rate in wild macaques.
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Macaca , Triyodotironina , Animales , Animales Salvajes , Hidrocortisona , Hormonas TiroideasRESUMEN
Selection-pressures differ with population density, but few studies investigate how this can affect reproductive physiology. European badger (Meles meles) density varies from solitary to group-living across their range, with reported mating periods throughout the entire year to specific seasonal periods. Badger reproduction is evolutionarily distinct, interrupting the direct progression from conception to gestation with delayed implantation (DI), allowing for superfecundation (SF). To establish the tactical mating flexibility afforded by DI*SF, we used cross-sectional population-level seasonal variation of circulating sex-steroids for 97 females from a high-density population. Oestradiol was highest in spring among non-parous females, then lower in summer, and remained low during following seasons, suggesting that the mating period was restricted to just spring. Oestrone was consistently higher than oestradiol; it was elevated in spring, lowest during summer, peaked in autumn, and remained elevated for pregnant females in winter. This suggests that oestrone sustains pre-implanted blastocysts throughout DI. Progesterone was low throughout, except during winter pregnancy, associated with implantation and luteal development. In contrast to multiple mating periods reported by lower-density studies, our oestradiol data suggest that, at high-density, females exhibit only one mating period (congruent with testosterone patterns in males studied previously in this same population). While additional mating periods during DI enhance fertility assurance at low-density, at high-density, we propose that when coitus is frequent, fertilisation is assured, precluding the need for further cycles and associated mating risks. This endocrinologically flexible DI*SF mating strategy likely represents a form of balancing selection, allowing badgers to succeed at a range of regional densities.
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Mustelidae , Animales , Estudios Transversales , Femenino , Fertilidad , Masculino , Mustelidae/fisiología , Embarazo , Reproducción , Estaciones del AñoRESUMEN
Wildlife ecotourism can offer a source of revenue which benefits local development and conservation simultaneously. However, habituation of wildlife for ecotourism can cause long-term elevation of glucocorticoid hormones, which may suppress immune function and increase an animal's vulnerability to disease. We have previously shown that western lowland gorillas (Gorilla gorilla gorilla) undergoing habituation in Dzanga-Sangha Protected Areas, Central African Republic, have higher fecal glucocorticoid metabolite (FGCM) levels than both habituated and unhabituated gorillas. Here, we tested the relationship between FGCM levels and strongylid infections in the same gorillas. If high FGCM levels suppress the immune system, we predicted that FGCM levels will be positively associated with strongylid egg counts and that gorillas undergoing habituation will have the highest strongylid egg counts, relative to both habituated and unhabituated gorillas. We collected fecal samples over 12 months in two habituated gorilla groups, one group undergoing habituation and completely unhabituated gorillas. We established FGCM levels and fecal egg counts of Necator/Oesophagostomum spp. and Mammomonogamus sp. Controlling for seasonal variation and age-sex category in strongylid infections we found no significant relationship between FGCMs and Nectator/Oesophagostomum spp. or Mammomonogamus sp. egg counts in a within group comparison in either a habituated group or a group undergoing habituation. However, across groups, egg counts of Nectator/Oesophagostomum spp. were lowest in unhabituated animals and highest in the group undergoing habituation, matching the differences in FGCM levels among these gorilla groups. Our findings partially support the hypothesis that elevated glucocorticoids reduce a host's ability to control the extent of parasitic infections, and show the importance of non-invasive monitoring of endocrine function and parasite infection in individuals exposed to human pressure including habituation process and ecotourism.
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Enfermedades del Simio Antropoideo , Parásitos , Enfermedades Parasitarias , Animales , Enfermedades del Simio Antropoideo/parasitología , Heces , Glucocorticoides , Gorilla gorillaRESUMEN
The assessment of mucosal immunity as a component of animal health is an important aspect for the understanding of variation in host immunity, and its tradeoff against other life-history traits. We investigated immunoglobulin A (IgA), the major type of antibody associated with mucosal immunity, in relation to changes in parasitic burden following anthelminthic treatment in noninvasively collected fecal samples in a semi-free ranging group of Barbary macaques (Macaca sylvanus). We measured IgA in 340 fecal samples of fourteen females and nine males. As IgA has been found to be responsive to stressors, we also related fecal IgA (fIgA) levels to fecal glucocorticoid metabolites (fGCM) measured in the same samples as part of a previous study. We found a high variability within and between individual fIgA levels over time. Running generalized additive mixed models, we found that fIgA levels were higher in males than in females, but did not change in response to the anthelmintic treatment and the resulting reduction in worm burden. Instead, fIgA level changes were significantly correlated to changes in fGCM levels. Our findings indicate that due to the strong responsiveness of fIgA to HPA-axis activity, the measurement of fIgA may have certain limitations with respect to reflecting gastrointestinal parasitic burden. Moreover, the responsiveness of fIgA to stressors interferes with the interpretation of IgA levels in fecal samples as a measure of mucosal immunity, at least in our study population of the Barbary macaques.
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Inmunidad Mucosa , Inmunoglobulina A , Animales , Heces , Femenino , Glucocorticoides , MasculinoRESUMEN
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.
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Andrógenos/farmacología , Conducta Animal/efectos de los fármacos , Conducta Cooperativa , Smegmamorpha/fisiología , Conducta Social , Agresión/efectos de los fármacos , Andrógenos/metabolismo , Animales , Femenino , Peces/fisiología , Vivienda para Animales , Masculino , Distribución Aleatoria , Reproducción/efectos de los fármacos , Reproducción/fisiología , Smegmamorpha/metabolismo , Medio Social , Testosterona/metabolismo , Testosterona/farmacologíaRESUMEN
Glucocorticoids have wide-ranging effects on animals' behaviour, but many of these effects remain poorly understood because numerous confounding factors have often been neglected in previous studies. Here, we present data from a 2-year study of 7 groups of wild Verreaux's sifakas (Propithecus verreauxi), in which we examined concentrations of faecal glucocorticoid metabolites (fGCMs, n = 2350 samples) simultaneously in relation to ambient temperatures, food intake, rank, reproduction, adult sex ratios, social interactions, vigilance and self-scratching. Multi-variate analyses revealed that fGCM concentrations were positively correlated with increases in daily temperature fluctuations and tended to decrease with increasing fruit intake. fGCM concentrations increased when males were sexually mature and began to disperse, and dominant males had higher fGCM concentrations than subordinate males. In contrast to males, older females showed a non-significant trend to have lower fGCM levels, potentially reflecting differences in male and female life-history strategies. Reproducing females had the highest fGCM concentrations during late gestation and had higher fGCM levels than non-reproducing females, except during early lactation. Variation in fGCM concentrations was not associated with variation in social interactions, adult sex ratios, vigilance and self-scratching. Altogether, we show that measures of glucocorticoid output constitute appropriate tools for studying energetic burdens of ecological and reproductive challenges. However, they seem to be insufficient indicators for immediate endocrinological responses to social and nonsocial behaviours that are not directly linked to energy metabolism.
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Glucocorticoides/metabolismo , Indriidae/fisiología , Animales , Conducta Animal/fisiología , Dominación-Subordinación , Ingestión de Alimentos/fisiología , Metabolismo Energético/fisiología , Heces/química , Femenino , Glucocorticoides/análisis , Indriidae/metabolismo , Masculino , Embarazo , Reproducción/fisiología , Estaciones del Año , Conducta SocialRESUMEN
Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, older juveniles, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.
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Alostasis/fisiología , Cercopithecus , Metabolismo Energético/fisiología , Crecimiento y Desarrollo/fisiología , Medio Social , Animales , Conducta Animal/fisiología , Péptido C/orina , Cercopithecidae/crecimiento & desarrollo , Cercopithecidae/metabolismo , Cercopithecus/crecimiento & desarrollo , Cercopithecus/metabolismo , Conducta Competitiva/fisiología , Heces/química , Femenino , Glucocorticoides/análisis , Glucocorticoides/metabolismo , Aseo Animal/fisiología , Humanos , Masculino , Conducta SocialRESUMEN
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.
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Péptido C/orina , Ecosistema , Metabolismo Energético/fisiología , Papio ursinus , Animales , Animales Salvajes , Péptido C/análisis , Femenino , Alimentos , Interacción Humano-Animal , Humanos , Lactancia/fisiología , Masculino , Papio ursinus/metabolismo , Papio ursinus/orina , Población Rural , Estaciones del Año , SudáfricaRESUMEN
Integrative behavioral ecology requires accurate and non-invasive measures of hormone mediators for the study of wild animal populations. Biologically sensitive assay systems for the measurement of hormones and their metabolites need to be validated for the species and sample medium (e.g. urine, feces, saliva) of interest. Where more than one assay is available for hormone (metabolite) measurement, antibody selection is useful in identifying the assay that tracks changes in an individuals endocrine activity best, i.e., the most biologically sensitive assay. This is particularly important when measuring how glucocorticoids (GCs) respond to the subtle, additive effects of acute stressors during a predictable metabolic challenge, such as gestation. Here, we validate a group-specific enzyme immunoassay, measuring immunoreactive 11ß-hydroxyetiocholanolone, for use in a wild primate, geladas (Theropithecus gelada). This group-specific assay produced values correlated with those from a previously validated double-antibody, corticosterone 125I radioimmunoassay. However, the results with the group-specific assay showed a stronger response to an ACTH challenge and identified greater variation in gelada immunoreactive fecal glucocorticoid metabolites (iGCMs) compared with the corticosterone assay, indicating a higher biological sensitivity for assessing adrenocortical activity. We then used the group-specific assay to: (1) determine the normative pattern of iGCM levels across gelada gestation, and (2) identify the ecological, social, and individual factors that influence GC output for pregnant females. Using a general additive mixed model, we found that higher iGCM levels were associated with low rank (compared to high rank) and first time mothers (compared to multiparous mothers). This study highlights the importance of assay selection and the efficacy of group-specific assays for hormonal research in non-invasively collected samples. Additionally, in geladas, our results identify some of the factors that increase GC output over and above the already-elevated GC concentrations associated with gestation. In the burgeoning field of maternal stress, these factors can be examined to identify the effects that GC elevations may have on offspring development.
Asunto(s)
Heces/química , Glucocorticoides/metabolismo , Metaboloma , Paridad , Theropithecus/metabolismo , Animales , Animales Salvajes/metabolismo , Corticosterona/metabolismo , Femenino , Técnicas para Inmunoenzimas , Masculino , Modelos Biológicos , Embarazo , Radioinmunoensayo , Reproducibilidad de los ResultadosRESUMEN
Across mammals, prenatal maternal stress (PREMS) affects many aspects of offspring development, including offspring growth. However, how PREMS translates to offspring growth is inconsistent, even within species. To explain the full range of reported effects of prenatal adversity on offspring growth, we propose an integrative hypothesis: developmental constraints and a counteracting adaptive growth plasticity work in opposition to drive PREMS effects on growth. Mothers experiencing adversity reduce maternal investment leading to stunted growth (developmental constraints). Concomitantly, the pace of offspring life history is recalibrated to partly compensate for these developmental constraints (adaptive growth plasticity). Moreover, the relative importance of each process changes across ontogeny with increasing offspring independence. Thus, offspring exposed to PREMS may grow at the same rate as controls during gestation and lactation, but faster after weaning when direct maternal investment has ceased. We tested these predictions with a comparative analysis on the outcomes of 719 studies across 21 mammal species. First, the observed growth changes in response to PREMS varied across offspring developmental periods as predicted. We argue that the observed growth acceleration after weaning is not "catch-up growth," because offspring that were small for age grew slower. Second, only PREMS exposure early during gestation produced adaptive growth plasticity. Our results suggest that PREMS effects benefit the mother's future reproduction and at the same time accelerate offspring growth and possibly maturation and reproductive rate. In this sense, PREMS effects on offspring growth allow mother and offspring to make the best of a bad start.