Summary Many aspects of the social environment affect hypothalamic‐pituitary‐adrenal (HPA) axis function and increase circulating glucocorticoid concentrations. In this review, we examine the relationships between the social environment and the function of the HPA axis in vertebrates. First, we explore the effects of the social environment on glucocorticoid secretion in territorial (primarily non‐social) species, with an emphasis on the effects of variation in population density, as modified by environmental factors such as predation risk and food availability. In general, high population density or frequent territorial intrusions are associated with increased glucocorticoid secretion in a wide range of taxa, including mammals, birds, fish and reptiles, although there is considerable variability across species. Second, we consider the effects of social interactions and dominance rank on glucocorticoid secretion in social species, mostly in birds and mammals. We review studies that have detected an association between social status and glucocorticoid levels – sometimes with higher glucocorticoid levels in low‐ranking individuals, and sometimes with higher glucocorticoid levels in dominant individuals. The relationship between dominance and glucocorticoid levels varies among species, populations and years, in a manner that depends on the stability of the social hierarchy, environmental conditions, the type of breeding system, and the manner in which high rank is obtained and maintained. Finally, we discuss the concept of allostasis and consider interactions between social effects and other environmental factors, noting that there is relatively little research on these interactions to date. For both non‐social and social species, we identify priorities of future research. These priorities include more complete descriptions of HPA function that move beyond measurements of basal glucocorticoid concentrations (which will generally require field experiments), to studies that examine organizational effects of social stressors, that directly test the relationship between HPA function and fitness, and that examine how glucocorticoid responses affect population dynamics. Although several lines of evidence suggest that glucocorticoid responses can affect the fitness of individuals and therefore can alter the dynamics of populations, the effect of glucocorticoid responses on population dynamics remains essentially unstudied.
Summary 1. Methods to measure metabolites of steroid hormones from faeces have become very popular in wildlife conservation and ecology, because they allow gathering physiological data without the necessity to capture the animals. However, this advantage comes at costs that are particularly relevant when studying free‐living animals in their natural environments. Previous methodological reviews have stressed the importance of validations to prove that real metabolites of the hormone in question are measured, but the research community has largely ignored further caveats relating to sex, diet, metabolic rate and individual differences in hormone metabolite formation. 2. Often the sexes differ in how they metabolize hormones. As a consequence, one may not be able to compare hormone metabolite concentrations between males and females of one species. 3. Diet can alter the way hormones are metabolized, and different diets can change the amount of faecal bulk. Both phenomena can result in measurement artefacts that may seriously distort the estimation of hormone metabolite concentrations. As a consequence, comparisons of hormone metabolite concentrations, for example, between seasons or populations, may become problematic. 4. Changes in ambient temperature and food availability may trigger large fluctuations in metabolic rate of free‐living animals. These fluctuations may then result in major distortions of faecal hormone metabolite concentrations without any change in bioactive hormone levels. 5. Bacteria metabolize hormones in the gut. Individual differences in bacterial composition can cause differences in how hormones are decomposed. Thus, individuals may differ with regard to what kind of hormone metabolites they form and with regard to the relative composition of these hormone metabolites. As only specific metabolites are measured, differences in metabolism may distort the results. 6. In summary, non‐invasive hormone research measures various end products of a hormone after its clearance from the circulation and extensive modification by bacteria. Not only does this increase random variance, it may also generate systematic noise, which may seriously distort the signal (i.e. the hormonal status of the individual) in a non‐random manner. Thus, we still need to learn much more about whether this widely used technique reliably measures the physiological status of animals in uncontrolled environments.
During the past several years, the noninvasive measurement of steroid metabolites from mammalian feces and bird droppings has become more and more popular. With an increasing acceptance of the method, investigators may become less aware of the need to validate their assays. It is shown why such validations are essential for each new species investigated and various ways to physiologically validate such noninvasive methods are described. Using the European stonechat (Saxicola torquata rubicola) as a model, it is explained why a validated method to measure androgen metabolites in males does not necessarily work in females. In addition the difficulties that may be neglected owing to the superficial ease of sampling and processing of excreta are investigated. Various issues that may arise during sampling, storage, and extraction of excreta are addressed. Finally, results suggesting that experimental manipulations of the diet may affect hormone metabolite levels in European stonechats are presented. So far, only a few studies have investigated the impact of diet on hormone metabolite levels, and these are the first data to report such an impact in birds. More studies are urgently needed to learn more about differences between the sexes, individuals, and populations and the impact of diet and energy metabolism on hormone metabolites.
Androgen levels show strong patterns throughout the year in male vertebrates and play an important role in the seasonal modulation of the frequency, intensity and persistence of aggression. The Challenge Hypothesis (Wingfield, J.C., Hegner, R.E., Dufty, A.M., Ball, G.F., 1990. The "Challenge Hypothesis": Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136, 829-846) predicts that seasonal patterns in androgen levels vary as a function of mating system, male-male aggression and paternal care. Although many studies have addressed these predictions, investigators have often assumed that the ratio of the breeding season maximum and breeding baseline concentrations (termed "androgen responsiveness") reflects hormonal responses due to social stimulation. However, increasing evidence suggests that seasonal androgen elevations are not necessarily caused by social interactions between males. Here, we separate the seasonal androgen response (R(seasonal)) and the androgen responsiveness to male-male competition (R(male-male)) to begin to distinguish between different kinds of hormonal responses. We demonstrate that R(seasonal) and R(male-male) are fundamentally different and should be treated as separate variables. Differences are particularly evident in single-brooded male birds that show no increase in plasma androgen levels during simulated territorial intrusions (STIs), even though R(seasonal) is elevated. In multiple-brooded species, STIs typically elicit a rise in androgens. We relate these findings to the natural history of single- and multiple-brooded species and suggest a research approach that could be utilized to increase our understanding of the factors that determine different types of androgen responses. This approach does not only include R(seasonal) and R(male-male), but also the androgen responsiveness to receptive females (R(male-female)) and to non-social environmental cues (R(environmental)), as well as the physiological capacity to produce and secrete androgens (R(potential)). Through such studies, we can begin to better understand how social and environmental factors may lead to differences in androgen responses.
Vocal signals such as calls play a crucial role for survival and successful reproduction, especially in group-living animals. However, call interactions and call dynamics within groups remain largely unexplored because their relation to relevant contexts or life-history stages could not be studied with individual-level resolution. Using on-bird microphone transmitters, we recorded the vocalisations of individual zebra finches (Taeniopygia guttata) behaving freely in social groups, while females and males previously unknown to each other passed through different stages of the breeding cycle. As birds formed pairs and shifted their reproductive status, their call repertoire composition changed. The recordings revealed that calls occurred non-randomly in fine-tuned vocal interactions and decreased within groups while pair-specific patterns emerged. Call-type combinations of vocal interactions changed within pairs and were associated with successful egg-laying, highlighting a potential fitness relevance of calling dynamics in communication systems.DOI: http://dx.doi.org/10.7554/eLife.07770.001
).Migration remains one of the great mysteries of animal life. Small migratory birds rely on refuelling stopovers after crossing ecological barriers such as deserts or seas. Previous studies have suggested that fuel reserves may determine stopover duration but this hypothesis could not be tested because of methodological limitations. Here, we provide evidence that subcutaneous fat stores determine stopover duration by measuring the permanence of migratory garden warblers (Sylvia borin) on a small Mediterranean island during spring migration with telemetry methods. Garden warblers with large amounts of fat stores departed the island significantly sooner than lean birds. All except one fat bird left the island on the same evening after capture, with a mean total stopover estimate of 8.8 hours. In contrast, the mean estimated total stopover duration of lean birds was 41.3 hours. To our knowledge, this is the first study that measures the true minimum stopover duration of a songbird during migration.
Research on the diversity, evolution and stability of cooperative behaviour has generated a considerable body of work. As concepts simplify the real world, theoretical solutions are typically also simple. Real behaviour, in contrast, is often much more diverse. Such diversity, which is increasingly acknowledged to help in stabilizing cooperative outcomes, warrants detailed research about the proximate mechanisms underlying decision-making. Our aim here is to focus on the potential role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviour in vertebrates. We first provide a brief introduction into the neuroendocrine basis of social behaviour. We then evaluate how hormones may influence known cognitive modules that are involved in decision-making processes that may lead to cooperative behaviour. Based on this evaluation, we will discuss specific examples of how hormones may contribute to the variability of cooperative behaviour at three different levels: (i) within an individual; (ii) between individuals and (iii) between species. We hope that these ideas spur increased research on the behavioural endocrinology of cooperation.
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