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Goymann W.,Max Planck Institute For Ornithologie | Wingfield J.C.,University of California at Davis
Behavioral Ecology | Year: 2014

Testosterone is a key hormone for the development of secondary sexual characters and dimorphisms in behavior and morphology of male vertebrates. Because females often express detectable levels of testosterone, testosterone has been suggested to also play a role in the modulation of secondary sexual traits in females. Previous comparative analyses in birds and fish demonstrated a relationship between male-to-female testosterone ratios and the degree of sexual dimorphism. Furthermore, female maximum testosterone was related to mating system and coloniality. Here, we reevaluate these previous ideas using phylogenetic analyses and effect size measures for the relationship between birds' male-to-female maximum testosterone levels. Further, we investigate the seasonal androgen response of female birds (the difference from baseline to maximum testosterone), which in males is strongly related to mating system. We could not confirm a relationship between male-to-female testosterone, maximum female testosterone, or the seasonal androgen response of females with any life-history parameter. We conclude that the expectation that testosterone regulates traits in females in a similar manner as in males should be reconsidered. This expectation may be partially due to hormone manipulation studies using pharmacological doses of testosterone that had similar effects in females than in males but may be of limited importance for the physiological range of testosterone concentrations occurring within ecological and evolutionary contexts. Thus, the assumption that circulating testosterone should covary with ecologically relevant secondary sexual traits in females may be misleading: selection pressures on females differ from those on males and females may regulate behavior differently. © 2014 The Author.

DuVal E.H.,Max Planck Institute for Ornithology (Seewiesen) | Goymann W.,Max Planck Institute For Ornithologie
Hormones and Behavior | Year: 2011

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations. © 2010 Elsevier Inc.

Fusani L.,University of Ferrara | Cardinale M.,Institute for Marine Research | Schwabl I.,Max Planck Institute For Ornithologie | Goymann W.,Max Planck Institute For Ornithologie
Hormones and Behavior | Year: 2011

A large number of passerine species migrate at night, although most of them are diurnal outside the migratory seasons. This diurnal-to-nocturnal transition is a major life-history event, yet little is known about its physiological control. Previous work showed that during the migratory periods captive birds showing nocturnal migratory restlessness (Zugunruhe) have reduced concentrations of circulating melatonin at night compared to non-migratory periods. This suggested that the hormone melatonin, a main component of the avian circadian system, is involved in the expression of Zugunruhe. Other studies demonstrated that the relationship between low melatonin levels and Zugunruhe is not a seasonal correlation. When Zugunruhe was interrupted by exposing birds to a fasting-and-refeeding protocol, melatonin levels increased. Here we studied whether melatonin and food availability influence the intensity of Zugunruhe in wild migrating garden warblers (Sylvia borin) at a stopover site. Birds were held in recording cages overnight, with or without food available, and either bled to determine melatonin concentrations or treated transdermally with melatonin. We found that melatonin levels at night were correlated with the intensity of diurnal locomotor activity and with condition, but were not correlated with Zugunruhe. Similarly, the melatonin treatment did not have effects on Zugunruhe, whereas food availability increased it. Our study shows that the nocturnal melatonin levels in migrating warblers depend on food availability and are correlated with condition. In addition, it suggests that melatonin does not control Zugunruhe and might rather be involved in energy conservation and/or clock synchronization during migration. © 2010 Elsevier Inc.

Goymann W.,Max Planck Institute For Ornithologie | Landys M.M.,Max Planck Institute For Ornithologie | Landys M.M.,Oregon State University
Journal of Avian Biology | Year: 2011

Past studies have suggested a fundamental difference in testosterone concentrations between tropical and northern latitude male birds, with the convention being that males in the tropics express much lower levels of testosterone. However, recent comparative studies have shown that tropical males with a short and synchronous breeding season (i.e. a breeding season typical of northern species) express maximum testosterone levels similar to those of northern latitude birds. Here, we ask the converse: do northern latitude songbirds that express a defining life-history characteristic typical of the tropics, i.e. year-round territoriality, have an annual testosterone profile similar to that of tropical songbirds? For the few year-round territorial species for which data are available, we found that seasonal testosterone profiles and seasonal maxima in plasma testosterone were similar between males of tropical and non-tropical species. For example, males of both groups expressed seasonal maxima during the period when females were fertile, and testosterone levels at this time were similar. In contrast, this and other studies show that species with seasonal territories typically express maximum testosterone levels earlier in the breeding cycle, when territories are first being established. Taken together, we suggest that specific life-history traits may play a more important role in determining testosterone profiles of tropical and non-tropical birds than breeding latitude and encourage further studies to allow for more formal comparisons. © 2011 The Authors.

Goymann W.,Max Planck Institute For Ornithologie | Spina F.,Instituto Nazionale per la Protezione e la Ricerca Ambientale | Ferri A.,Instituto Nazionale per la Protezione e la Ricerca Ambientale | Fusani L.,University of Ferrara
Biology Letters | Year: 2010

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. © 2010 The Royal Society.

Creel S.,Montana State University | Dantzer B.,Michigan State University | Goymann W.,Max Planck Institute For Ornithologie | Rubenstein D.R.,Columbia University
Functional Ecology | Year: 2013

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. © 2012 The Authors. Functional Ecology © 2012 British Ecological Society.

Goymann W.,Max Planck Institute For Ornithologie | Trappschuh M.,Max Planck Institute For Ornithologie
Journal of Biological Rhythms | Year: 2011

Most vertebrates living in seasonal environments show seasonal reproductive cycles and diel rhythms. The rhythmicity in behavior and morphology is accompanied by diel and seasonal patterns of hormone secretions. In small animals, the investigation of diel patterns of hormones has been hampered because repeated blood sampling is difficult and may influence subsequent measurements. A possibility to avoid these caveats is to investigate excreted hormone metabolites instead. Here, we describe the diel excretion patterns of testosterone and corticosterone metabolites in a small captive songbird during 4 seasons: winter, early spring (Zugunruhe), summer, and autumn molt. Our approach is quite unique, because the diel patterns of steroids have rarely-if at all-been investigated in the same individuals within several seasons. Small birds should be ideal to investigate diel patterns of hormone metabolites, because they defecate frequently enough to establish a diel profile. However, concentration measurements of hormone metabolites rely on the assumptions that hormone metabolites are placed into droppings of similar mass (the "dropping amount assumption") and are excreted in constant time intervals (the "constant interval assumption"). These assumptions were clearly violated in our study, as the dropping mass per time interval and the defecation intervals varied depending on the time of day and season. We thus used the rate of hormone metabolite excretion as an alternative measure to concentration. Both testosterone and corticosterone metabolites showed diel and seasonal rhythmicity. Furthermore, the diel pattern varied depending on season. Concentration and rate measurements gave similar results when the differences between hormone metabolite levels were large-for example, when testosterone metabolites were compared across seasons. When the differences were more subtle, though, the 2 measures did not always correspond well, indicating that the violation of the 2 basic assumptions affected the comparability of concentration measurements. We conclude that diel and seasonal comparisons of hormone metabolites potentially give biologically meaningful results, especially when rates instead of concentrations are measured. However, such studies require awareness of the limitations and pitfalls of noninvasive hormone measurements, a carefully designed experiment, and very cautious interpretation of the data. © 2011 SAGE Publications.

Apfelbeck B.,Max Planck Institute For Ornithologie | Stegherr J.,Max Planck Institute For Ornithologie | Goymann W.,Max Planck Institute For Ornithologie
Hormones and Behavior | Year: 2011

In many vertebrates testosterone increases during aggressive interactions and the surges in this hormone may be responsible for the winner effect. So far studies on this relationship have been done in captivity only, because simulating a winning situation for a territory owner in the field is difficult. However, an increasing number of studies show that territorial aggression is not necessarily accompanied by elevated testosterone after a single simulated territorial intrusion (STI) and therefore it has been proposed that STIs may even create a losing experience. We examined whether free-living male black redstarts (Phoenicurus ochruros) show changes in androgens, corticosterone and behavior following repeated STIs of high or low intensity and in contrast to being challenged only once. Repeated intrusions had no influence on androgen and corticosterone levels regardless of intrusion intensity. In contrast, the behavioral response changed over days depending on the intensity of the intrusion. Only birds challenged with high-level intruders approached the decoy significantly faster during the third intrusion than during the first one, stayed closer to the decoy, and sang more songs than males challenged with low-level intruders. Thus, although black redstarts reacted differently to STIs varying in frequency and intensity, these behavioral differences were not reflected in androgen or corticosterone levels. Our data show that it is unlikely that STIs induce a losing experience. Furthermore, they indicate that a hormonal effect of winning an encounter may not be universal in vertebrates and may depend on the ecological or life-history context. © 2011 Elsevier Inc.

Apfelbeck B.,Max Planck Institute For Ornithologie | Goymann W.,Max Planck Institute For Ornithologie
Proceedings of the Royal Society B: Biological Sciences | Year: 2011

Competition elevates plasma testosterone in a wide variety of vertebrates, including humans. The 'challenge hypothesis' proposes that seasonal peaks in testosterone during breeding are caused by social challenges from other males. However, during experimentally induced male-male conflicts, testosterone increases only in a minority of songbird species tested so far. Why is this so? Comparative evidence suggests that species with a short breeding season may not elevate testosterone levels during territory defence. These species may even be limited in their physiological capability to increase testosterone levels, which can be tested by injecting birds with gonadotropin-releasing hormone (GnRH). We studied two populations of black redstarts that differ in breeding altitude, morphology and the length of their breeding season. Unexpectedly, males of neither population increased testosterone in response to a simulated territorial intrusion, but injections with GnRH resulted in a major elevation of testosterone. Thus, black redstarts would have been capable of mounting a testosterone response during the male-male challenge. Our data show, for the first time, that the absence of an androgen response to male-male challenges is not owing to physiological limitations to increase testosterone. Furthermore, in contrast to comparative evidence between species, populations of black redstarts with a long breeding season do not show the expected elevation in testosterone during male-male challenges. © 2011 The Royal Society.

Goymann W.,Max Planck Institute For Ornithologie
Methods in Ecology and Evolution | Year: 2012

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 metabolismmay 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. © 2012 The Authors. Methods in Ecology and Evolution © 2012 British Ecological Society.

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