Katharina Hirschenhauser

Testosterone in Tropical Birds: Effects of Environmental and Social Factors

Previous investigations suggest that male tropical birds have lower plasma testosterone concentrations than northern latitude species. To test whether this generalization is valid, we analyzed all currently available plasma testosterone data of tropical birds. We focused on peak breeding testosterone levels using phylogenetic and conventional statistics. Explanatory variables considered were social mating system, type of territoriality, breeding season length, and altitude. On average, tropical birds had lower mean peak testosterone levels than northern temperate birds. However, in several tropical species, testosterone levels were well within the range of northern latitude birds. Without controlling for phylogeny, breeding season length, type of territoriality, and altitude explained a significant proportion of the variance in testosterone levels. The shorter the breeding season, the higher the testosterone levels. Tropical birds that defend a breeding season territory had higher testosterone levels than birds that were year‐round territorial or colonial, and testosterone levels were positively correlated with altitude. When controlling for phylogeny, only breeding season length predicted testosterone levels. In conclusion, we propose to refine previous notions of low plasma testosterone levels in tropical birds: short breeding seasons and perhaps environmental conditions at high altitudes precipitate conditions under which high testosterone levels are beneficial in the tropics.

A test of the ‘challenge hypothesis’ in cichlid fish: simulated partner and territory intruder experiments

In male birds, the responsiveness of androgens to sexual and territorial behaviour is predicted to vary with mating system and the degree of paternal investment (‘challenge hypothesis’, CH; Wingfield et al. 1990, American Naturalist, 136, 829–846). The CH predicts a higher and longer lasting ‘breeding baseline’ androgen level in males of polygynous species with no or only short-term paternal investment than in males of monogamous species with a high degree of paternal investment. Since the applicability of the CH to nonavian vertebrates has been unclear, we experimentally tested its predictions in several cichlid fish (Neolamprologus pulcher, Lamprologus callipterus, Tropheus moorii, Pseudosimochromis curvifrons and Oreochromis mossambicus) using a simulated territorial intruder protocol. Androgens (11-ketotestosterone: 11-KT; testosterone: T) were measured from fish-holding water. In all species sampled, the 11-KT patterns confirmed the predictions of the CH originating from the avian literature, but T patterns did not. Males of all species sampled were highly responsive to territorial intrusions; however, the magnitude and duration of this response, that is, the rapid return to baseline 11-KT levels, could not clearly be explained by the degree of paternal care. 11-KT responses to interactions with ovulating females were observed in maternal mouthbrooders but not in biparental species (e.g. Lamprologini). At the interspecific level, androgen responsiveness was greater among males of monogamous species, as predicted, but also in species with more intense pair bonding (e.g. Tropheus moorii). Thus, this study confirms the predictions of the CH in cichlid fish at both the intraspecific and the interspecific levels.

Hormonal mechanisms of cooperative behaviour

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.

Non-invasive measurement of steroids in fish-holding water: important considerations when applying the procedure to behaviour studies

Fish behaviourists are increasingly turning to non-invasive measurement of steroid hormones in holding water, as opposed to blood plasma. When some of us met at a workshop in Faro, Portugal, in September, 2007, we realised that there were still many issues concerning the application of this procedure that needed resolution, including: Why do we measure release rates rather than just concentrations of steroids in the water? How does one interpret steroid release rates when dealing with fish of different sizes? What are the merits of measuring conjugated as well as free steroids in water? In the ‘static’ sampling procedure, where fish are placed in a separate container for a short period of time, does this affect steroid release—and, if so, how can it be minimised? After exposing a fish to a behavioural stimulus, when is the optimal time to sample? What is the minimum amount of validation when applying the procedure to a new species? The purpose of this review is to attempt to answer these questions and, in doing so, to emphasize that application of the non-invasive procedure requires more planning and validation than conventional plasma sampling. However, we consider that the rewards justify the extra effort.

Habituation to humans affects yolk steroid levels and offspring phenotype in quail.

In the field as well as in the laboratory, human-generated stress responses are reduced in adult animals previously habituated to humans in comparison to non-habituated individuals. In birds, yolk steroid levels vary with maternal environment and condition. We tested the hypothesis that the experience of female birds with humans could affect yolk steroids levels and offspring phenotype. Two groups of Japanese quail, one habituated to humans (H) and a second non-habituated (NH), were exposed daily to brief human disturbances. We analysed egg quality, offspring growth, and offspring emotional reactivity. NH females produced eggs with less androgens (testosterone and androstenedione) and more immunoreactive progesterone compared to birds habituated to humans. NH females produced eggs with less yolk, heavier shell and chicks hatching later and being smaller as compared to habituated individuals. A lower emotional reactivity was found in young of NH females compared to young of H females. Thus, human disturbance of the mother triggered different effects on chick phenotype depending on previous experience of mother birds with humans. In addition, we describe for the first time the influence of environmental stimuli on yolk immunoreactive progesterone levels. Our results show that a relatively minor difference in behavioral habituation may have substantial effects on eggs and offspring. This has obvious implications for keeping and handling laboratory animals, for conservation biology and for animal welfare.

Effects of physiological and social challenges in different seasons on fecal testosterone and corticosterone in male domestic geese (Anser domesticus)

Abstract We investigated the reliability of the non-invasive approach of measuring steroid hormones from feces in the domestic goose (Anser domesticus), a mainly herbivorous bird with a short gut passage time (2–3 h). Groups of eight outdoor-housed male domestic geese were subjected to three different experiments, injection of either GnRH analogue or ACTH, or ”social stimulation” by confrontation with two alien males or females. These experiments were replicated in three different seasons, in spring, during peak reproductive activity, in summer, during long-day photorefractoriness and postnuptial molt, and in fall, during sexual reactivation. GnRH stimulation resulted in significant increases of mean response and peak fecal testosterone metabolites (TM) in spring and fall. Response TM concentrations excreted in spring were generally higher than in summer and fall. Social confrontation with two females, but not with two males, increased mean and peak TM in all seasons. In general, ACTH treatment resulted in a proportionally higher increase of fecal corticosterone metabolites (BM) than GnRH did in fecal TM (80- to 140-fold vs 6- to 8-fold). ACTH significantly increased mean and peak BM in all seasons. Social confrontation with two males significantly increased fecal BM in spring, but confrontation with two females increased fecal BM in fall. Our results indicate that determining steroids from feces is a generally valid approach. However, the sensitivity of the method may vary between different hormones and results may differ between seasons. BM results seemed more sensitive and seasonally robust than did TM.

Synthesis of Measuring Steroid Metabolites in Goose Feces

Abstract: The reliability of noninvasively measuring steroid hormones from feces in greylag geese (Anser anser) and domestic geese (A. domesticus), both qualitatively and quantitatively, was tested experimentally. Geese are mainly herbivorous birds with a short gu‐passage time (2–3 h). Groups of eight outdoor‐housed male domestic geese were subjected to two different experiments, injection of either GnRH or ACTH, which were replicated in three different seasons (spring, summer, and fall). GnRH stimulation resulted in significant increases of response fecal testosterone metabolites (TM; 17β‐OH‐androgens) in spring and fall, but not during the summer photorefractoriness. Testosterone response patterns obtained from plasma samples paralleled those from feces; however, no direct correlation between individual immunoreactive plasma and feces contents was observed. To improve the sample handling during extraction and the assay sensitivity, we promote the use of a group‐specific antibody against 17‐oxoandrogens that does not require deconjugation prior to the analysis. ACTH robustly increased fecal corticosterone in all seasons. The polar nature of glucocorticoids, however, seems to make a distinction between conjugated and nonconjugated types difficult, and the available avian literature on this topic is discussed.

Social context may affect urinary excretion of 11-ketotestosterone in African cichlids

Summary We previously investigated the androgen responsiveness of males to simulated partner and territory intrusions in five African cichlid species (Neolamprologus pulcher, Lamprologus callipterus, Tropheus moorii, Pseudosimochromis curvifrons, Oreochromis mossambicus; Hirschenhauser et al., 2004). Here we re-analysed data on 11-ketotestosterone (11-KT) levels in holding water to compare the free (presumably from the gills) and conjugated (presumably from urine and faeces) 11-KT fractions. We sampled (i) pre-test baseline control levels from individual males in social isolation and (ii) response levels released after social interactions, either with an ovulating female or a male territory intruder. In four out of five species, conjugated metabolites contributed to the observed total 11-KT responses in water during social context, which was particularly apparent in peak responsive individuals exposed to male intruders. Thus, in water from males sampled in isolation immunoreactive 11-KT seemed to derive both from gills and urine, whereas the urinary 11-KT component apparently increased in the social context, particularly when a male was challenged by a same-sex intruder. These results suggest that (i) the social context may affect urine release patterns of males and (ii) 11KT data acquired by using fish-holding water may not simply reflect the passive transmission of steroid hormones via the gills.

Individual performance in complex social systems: the greylag goose example

Convergent social structures can be found in taxa that split a long time ago, for example more than 230 Mio years ago as in the case of mammals and birds. Such convergence is explained by common selection regimes, as all social systems are shaped by sex-specific tactics and strategies to optimise their reproductive success. In addition, the major social mechanisms, brain and physiology, are highly conserved throughout the vertebrates. Manoeuvring social contexts tends to be energetically costly and, hence, favours efficient decision-making. Therefore, at least in vertebrates, complex social systems generally select for social cognition. As an example for social convergence between mammals and birds, we introduce the surprisingly complex social system of greylag geese, featuring components such as a female-bonded clan structure, long parent-offspring relationships, as well as elaborate and highly functional patterns of mutual social support. Our results show that partners in reproductively successful goose pairs are in hormonal synchrony and provide social support to each other. We suggest that social support may be a major structuring principle of other social systems with long-term individualized and valuable partnerships as well. In general, individual performance in social systems is determined by the interplay between proximate mechanisms and ultimate functions.

Isolation and characterization of microsatellite marker loci in the greylag goose (Anser anser)

Ten novel polymorphic microsatellite loci were isolated and characterized from the greylag goose, Anser anser, a long‐term monogamous and biparental bird. Additionally, five new primers pairs were designed based on previously published microsatellite locus sequences from closely related species. Multiplex polymerase chain reactions conditions were optimized for all 15 primer pairs. The number of alleles ranged from two to 12 per locus with an observed heterozygosity ranging from 0.07 to 0.85. This marker set will be used to determine rates and origins of extra‐pair and parasitic young in a population of individually banded greylag geese with known life histories.