Does the stress axis mediate behavioural flexibility in a social cichlid, Neolamprologus pulcher?

Behavioural flexibility plays a major role in the way animals cope with novel situations, and physiological stress responses are adaptive and highly efficient mechanisms to cope with unpredictable events. Previous studies investigating the role of stress responses in mediating behavioural flexibility were mostly done in laboratory rodents using stressors and cognitive challenges unrelated to the ecology of the species. To better understand how stress mediates behavioural flexibility in a natural context, direct manipulations of the stress response and cognitive tests in ecologically relevant contexts are needed. To this aim, we pharmacologically blocked glucocorticoid receptors (GR) in adult Neolamprologus pulcher using a minimally invasive application of a GR antagonist. GR blockade prevents the recovery after a stressful event, which we predicted to impair behavioural flexibility. After the application of the GR antagonist, we repeatedly exposed fish to a predator and tested their behavioural flexibility using a detour task, i.e. fish had to find a new, longer route to the shelter when the shortest route was blocked. While the latencies to find the shelter were not different between treatments, GR blocked fish showed more failed attempts during the detour tasks than control fish. Furthermore, weak performance during the detour tasks was accompanied by an increase of fear related behaviours. This suggests that blocking GR changed the perception of fear and resulted in an impaired behavioural flexibility. Therefore, our results support a potential link between the capacity to recover from stressors and behavioural flexibility in N. pulcher with potential consequences for an effective and adaptive coping with changing environments.

Children's Relationships with a Non-Vertebrate Animal: The Case of a Giant African Land Snail (Achatina fulica) at School.

Employing living animals in educational settings is popular and may assist learning. Human-animal relationships are considered fundamental for the effects of animal-assisted interventions (AAI) on successful learning. Key studies on AAI emphasize dogs, or other large-brained vertebrates, while AAI with non-vertebrate species is a yet rather unexplored field. However, bringing non-vertebrate species to school has ethical and practical advantages. In an exploratory study, we tested whether seven-years-old children would form caregiving relationships with a Giant African land snail (Achatina fulica). Prior to the survey, the snail had been kept inside a terrarium in the classroom for seven months. We employed a questionnaire for measuring children's pet attachment to assess the children's relationships with the snail. The observed relationship scores with the snail were intermediate to high and did not differ from same-aged children's attachment scores with their dogs, cats, and rabbits. No differences due to gender were observed. Children potentially developed caregiving attitudes and empathy towards the snail, and thus, the presented results indicate potential benefits from employing a non-vertebrate species in educational settings, as well as for animal-assisted therapy. The specific features of A. fulica are discussed in the frame of human-animal interactions, learning, and anthropomorphism.

Monitoring public awareness about the endangered northern bald ibis: a case study involving primary school children as citizen scientists.

BACKGROUND: Citizen science has evolved over the past decades by motivating members of the public to interact with scientists and actively participate in scientific research and monitoring. For this purpose, a proficient communication is mandatory in order to efficiently convey messages and reduce the gap of knowledge between scientists and lay people. In the present study, we aimed at evaluating the multiplying effect of children, who were trained to communicate their knowledge on an endangered bird species in order to engage the local community in the long-term ornithological monitoring of the free flying and individually marked colony of northern bald ibis (NBI, Geronticus eremita), which was established at the research station in 1997. METHODS: Pupils of the local primary schools were in regular contact with researchers, enjoyed outdoor encounters with the birds, and were invited to talk about their experience with as many people as possible. Later on, they acted as surveyors to assess the knowledge of the public on (i) the general knowledge about the species, (ii) specific knowledge about the local colony, and (iii) attitudes towards science. In two different years of evaluation (2012 and 2016) a total number of 387 persons were surveyed. The questions were generated together with the pupils and their teachers and the questionnaires were similar for both years of evaluation. All queries were in a closed format. RESULTS: Our results show an increase in the proportion of correct answers provided by the surveyed persons between the two years of evaluation. Education-based activities may encourage children to effectively act as multipliers of information and attitudes. This has the potential to induce sustainable changes with respect to attitude towards science, at least among local communities. Furthermore, the study suggests caution with the quality of some information reported by citizen scientists, which might be solved by more careful training actions and more specific information about local particularities. Even though the study would have gained more informative power with some additional precautions than in its current form, our findings recommend the empowerment of pupils as multipliers of scientific knowledge.

Primary pupils, science and a model bird species: Evidence for the efficacy of extracurricular science education.

Beyond subject matter learning, primary science teaching aims at encouraging positive attitudes toward, and lasting interest in, science. This study tested whether the learning and science commitment of 8- to 10-year old pupils was affected by extracurricular learning opportunities involving repeated interactions with free-living northern bald ibis (Geronticus eremita; an endangered bird species) and professional researchers. To examine the project's efficacy, pupils' learning progress was monitored by repeated measures of knowledge (i) about northern bald ibises in specific, and (ii) of bird diversity in general. In addition, the children's attitudes toward science were monitored and their dynamic mental models of northern bald ibis' morphology and size were assessed from drawings. A total of 55 pupils from two schools were tested for eight months (before, during and after the experience). Control groups went through regular (curricular) science lessons with similar content and time investment. The extracurricular experience produced a clear learning progress with large effect sizes, which was particularly evident on a long timescale. In addition to subject matter knowledge, the project group pupils could name more bird species and expressed their views about the importance of scientific research for society in a higher proportion than control groups. Differences between schools suggest that project participation also changed the teacher's own interest in northern bald ibises, which affected learning in the control group taught by the same teacher. Beyond the pupils' language and reading skills, learning progress was also visible by scoring ibis-typical features in drawings; their mental models of relative size were not changed due to project participation, however. The results are discussed in reference to inducing and maintaining pupils' attitude and interest in a topic. The study adds empirical evidence for the potentials of advancing primary science education e. g. by fostering the collaboration of schools with scientists.

Neural activation following offensive aggression in Japanese quail.

Aggression is a fundamental part of animal social behaviour. In avian species, little is known about its neural representation. In particular, neural activity following offensive aggression has not been studied in detail. Here, we investigated the patterns of brain activation using immediate-early gene (IEG) expression in male Japanese quail that showed pronounced aggressive behaviours during a 30 min male-male interaction and compared them to those of males that did not interact with a conspecific. In aggressive males, we found a massive induction of the IEG ZENK in pallial brain structures such as the intermediate medial mesopallium, the caudomedial mesopallium and the intermediate medial nidopallium. To a lesser extent, activation was observed in subpallial areas such as the nucleus taeniae of the amygdala and in the medial portion of the bed nucleus of the stria terminalis. Our data suggest that the modulation of aggressive behaviour involves the integration of multisensory information.

Winning and losing in public: audiences direct future success in Japanese quail.

Among vertebrates, winning a fight enhances the probability of future victories and vice versa and the role of post-conflict testosterone in mediating this 'winner effect' is widely accepted. In a series of staged fights of Japanese quail (Coturnix japonica) we tested both opponents' pre-fight and post-conflict testosterone, behavior and dominance status after returning to their social groups. We found that the presence of a familiar mixed-sex audience during the encounter modulated both the testosterone response and the long-term success after a fighting experience. 'Public losers' but not 'public winners' lacked a post-conflict testosterone response, whereas without an audience both winners and losers increased testosterone metabolite levels. Long-lasting winner and loser effects exclusively occurred when the performance information was perceived by a mixed-sex audience. In further experiments we manipulated the testosterone responsiveness of either the loser or the winner. An artificial post-conflict testosterone surge after having lost a fight effectively reversed the loser effect in Japanese quail. In contrast, the 'winner effect' was not changed by blocking testosterone after the fight. Overall, male Japanese quails' post-conflict testosterone was connected to the audiences and thus, own or the observers' perception of the challenge rather than to winning or losing a fight.

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.

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.

Does 'Relationship Intelligence' Make Big Brains in Birds?

Lately, Emery et al. developed a bird-specific modification of the "social brain hypothesis", termed "relationship intelligence hypothesis". Although the idea may be valuable, we doubt that it is supported by sufficient evidence and critically discuss some of the arguments raised by the authors in favour of their new idea.

Synthesis of measuring steroid metabolites in goose feces.

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 gut-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; 17beta-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.

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.

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation.

Male androgen responses to social challenges have been predicted to vary with mating system, male-male aggressiveness, and the degree of paternal investment in birds ("challenge hypothesis," Am. Nat. 136 (1990), 829). This study focused on the interspecific predictions of the challenge hypothesis. Comparative methods were used to control for effects of the phylogenetic relatedness among the sampled species. Male androgen data of 84 bird species were collected from literature records on seasonal androgen patterns. From these, the androgen responsiveness (AR) was calculated as described in the original challenge hypothesis (i.e., maximum physiological level/breeding baseline). Scatterplots of AR versus mating strategy, male-male aggressiveness, and the degree of paternal care confirmed the expected interspecific patterns. When phylogenetic analyses were performed among all of the sampled species, the effects of paternal investment disappeared while the AR remained covarying to a high degree with mating system and male-male aggressiveness. Although these mechanisms may be different at the intraspecific level, this suggests that interspecific differences of AR in male birds may have evolved in response to changes of mating strategies, rather than in response to altered paternal duties. However, control for phylogeny among the subsample of 32 passerine species revealed that if any paternal investment contributed to the observed variance in AR, then the change from "no male incubation" to "male shares incubation duties" represented the most effective, whereas the male's contribution to feeding offspring did not explain the observed variation of AR.

Monthly patterns of testosterone and behavior in prospective fathers.

The individual time patterns of salivary testosterone of adult healthy men, self-reported sexual behavior and their co-occurrence with regular weekly or monthly intervals were studied. Twenty-seven volunteer males (mean age 33 +/- 1 years) collected daily morning saliva over a period of 90 days. Evening questionnaires provided daily information on sexual activity. From the saliva, testosterone immunoreactive substances were determined using enzyme immunoassay. To detect events in which increases of testosterone were associated with sexual activity and at the same time controlling for regular internal patterns in men, data were analyzed using Theme software. First results indicated a varying number of complex nonrandom interaction patterns of testosterone with sexual activity, but also with weekly (i.e., Saturdays) and monthly intervals (i.e., 28-day full-moon intervals). The social context of the occurrence of specific pattern combinations was elaborated using parameters from the men's self-reported general life history profiles. Peak hormone levels occurred around weekends in the majority of the males. The 28-day monthly interval coincided with testosterone peaks only in those of the paired men who reported a current wish for children ("prospective fathers"), but not in unpaired men or in those who did not wish to have children with their current partner. Rather than representing a direct regular pattern of the male testosterone per se, the observed patterns suggest that men have the facultative potential to adjust their testosterone responses to their female partner's cycle. In line with the interactions between behavior and androgens observed in vertebrates in general, this study adds an example of the mutual character of hormone-behavior interactions and, thus, for the social context of testosterone patterns in human males.

Social modulation of androgen levels in male teleost fish.

Androgens are classically thought of as the sex steroids controlling male reproduction. However, in recent years evidence has accumulated showing that androgens can also be affected by the interactions between conspecifics, suggesting reciprocal interactions between androgens and behaviour. These results have been interpreted as an adaptation for individuals to adjust their agonistic motivation and to cope with changes in their social environment. Thus, male-male interactions would stimulate the production of androgens, and the levels of androgens would be a function of the stability of its social environment ['challenge hypothesis', Gen. Comp. Endocrinol. 56 (1984) 417]. Here the available data on social modulation of androgen levels in male teleosts are reviewed and some predictions of the challenge hypothesis are addressed using teleosts as a study model. We investigate the causal link between social status, territoriality and elevated androgen levels and the available evidence suggests that the social environment indeed modulates the endocrine axis of teleosts. The association between higher androgen levels and social rank emerges mainly in periods of social instability. As reported in the avian literature, in teleosts the trade-off between androgens and parental care is indicated by the fact that during the parental phase breeding males decreased their androgen levels. A comparison of androgen responsiveness between teleost species with different mating and parenting systems also reveals that parenting explains the variation observed in androgen responsiveness to a higher degree than the mating strategy. Finally, the adaptive value of social modulation of androgens and some of its evolutionary consequences are discussed.