Stress behaviour and physiology of developing Arctic barnacle goslings ( Branta leucopsis) is affected by legacy trace contaminants.

Natural populations are persistently exposed to environmental pollution, which may adversely impact animal physiology and behaviour and even compromise survival. Responding appropriately to any stressor ultimately might tip the scales for survival, as mistimed behaviour and inadequate physiological responses may be detrimental. Yet effects of legacy contamination on immediate physiological and behavioural stress coping abilities during acute stress are virtually unknown. Here, we assessed these effects in barnacle goslings ( Branta leucopsis) at a historical coal mine site in the Arctic. For three weeks we led human-imprinted goslings, collected from nests in unpolluted areas, to feed in an abandoned coal mining area, where they were exposed to trace metals. As control we led their siblings to feed on clean grounds. After submitting both groups to three well-established stress tests (group isolation, individual isolation, on-back restraint), control goslings behaved calmer and excreted lower levels of corticosterone metabolites. Thus, legacy contamination may decisively change stress physiology and behaviour in long-lived vertebrates exposed at a young age.

The importance of the altricial - precocial spectrum for social complexity in mammals and birds - a review.

Various types of long-term stable relationships that individuals uphold, including cooperation and competition between group members, define social complexity in vertebrates. Numerous life history, physiological and cognitive traits have been shown to affect, or to be affected by, such social relationships. As such, differences in developmental modes, i.e. the 'altricial-precocial' spectrum, may play an important role in understanding the interspecific variation in occurrence of social interactions, but to what extent this is the case is unclear because the role of the developmental mode has not been studied directly in across-species studies of sociality. In other words, although there are studies on the effects of developmental mode on brain size, on the effects of brain size on cognition, and on the effects of cognition on social complexity, there are no studies directly investigating the link between developmental mode and social complexity. This is surprising because developmental differences play a significant role in the evolution of, for example, brain size, which is in turn considered an essential building block with respect to social complexity. Here, we compiled an overview of studies on various aspects of the complexity of social systems in altricial and precocial mammals and birds. Although systematic studies are scarce and do not allow for a quantitative comparison, we show that several forms of social relationships and cognitive abilities occur in species along the entire developmental spectrum. Based on the existing evidence it seems that differences in developmental modes play a minor role in whether or not individuals or species are able to meet the cognitive capabilities and requirements for maintaining complex social relationships. Given the scarcity of comparative studies and potential subtle differences, however, we suggest that future studies should consider developmental differences to determine whether our finding is general or whether some of the vast variation in social complexity across species can be explained by developmental mode. This would allow a more detailed assessment of the relative importance of developmental mode in the evolution of vertebrate social systems.

Long-term memory of hierarchical relationships in free-living greylag geese.

Animals may memorise spatial and social information for many months and even years. Here, we investigated long-term memory of hierarchically ordered relationships, where the position of a reward depended on the relationship of a stimulus relative to other stimuli in the hierarchy. Seventeen greylag geese (Anser anser) had been trained on discriminations between successive pairs of five or seven implicitly ordered colours, where the higher ranking colour in each pair was rewarded. Geese were re-tested on the task 2, 6 and 12 months after learning the dyadic colour relationships. They chose the correct colour above chance at all three points in time, whereby performance was better in colour pairs at the beginning or end of the colour series. Nonetheless, they also performed above chance on internal colour pairs, which is indicative of long-term memory for quantitative differences in associative strength and/or for relational information. There were no indications for a decline in performance over time, indicating that geese may remember dyadic relationships for at least 6 months and probably well over 1 year. Furthermore, performance in the memory task was unrelated to the individuals' sex and their performance while initially learning the dyadic colour relationships. We discuss possible functions of this long-term memory in the social domain.

Early development of gaze following into distant space in juvenile Greylag geese (Anser anser).

Visual co-orientation with another's gaze direction (gaze following) may provide important information about the location of food, social interactions or predators. Gaze following has been shown in a variety of mammals, but only in few bird species, and has not been tested in precocial birds at all. It has been suggested that gaze following is an anti-predator behaviour, and in Common ravens (Corvus corax) and rooks (C. frugilegus), it emerges shortly after fledging, at a time when young birds leave the predator-safe nest. However, if gaze following is adaptive, the developmental pattern should differ between altricial and precocial birds. Greylag geese (Anser anser) are highly social birds with a precocial development. Goslings move and feed independently within 24 h post-hatching, and they are highly vulnerable to aerial predators. We therefore predicted that greylag geese are capable of gaze following and that they develop this skill already pre-fledging. We experimentally tested 19 hand-raised greylag goslings for their ability to follow a conspecific's gaze when they were between 10 days and 6 weeks old. In line with our predictions, first responses were already detectable in 10-day-old goslings. Our results therefore not only demonstrate that greylag geese follow the gaze of conspecifics into distant space, but that they also develop this ability much earlier than altricial birds.

Benefits of family reunions: social support in secondary greylag goose families.

Social interactions are among the most potent stressors. However, social allies may diminish stress, increase success in agonistic encounters and ease access to resources. We studied the role of social support as a major mechanism for individual stress management in families of free-ranging greylag geese (Anser anser). Greylag geese are long-term monogamous, live in a female-bonded social system, and fledged offspring stay with their parents until the next breeding season ('primary families'). Should parents then fail to fledge young, subadults might rejoin them in summer after molt is completed ('secondary families'). We have previously shown that primary greylag goose families reap benefits from active social support in agonistic encounters, and also excrete lower levels of immuno-reactive corticosterone metabolites (CORT, 'passive social support'). Here we investigated how far active and passive social support continues in secondary goose families. Although we found that active support in agonistic encounters was almost absent in secondary families, subadult male geese won an increased number of agonistic encounters due to the mere presence of their secondary family. Particularly adult and subadult females benefited from passive social support through decreased CORT, whereas males did not. Decrease in the hormonal stress response during challenging situations, induced by social allies, may help the females' long-term energy management, thereby improving the odds for successful future reproduction. We discuss whether joining a secondary family may be an alternative tactic for young geese towards optimizing their start into a complex social life.

Heart rate modulation in bystanding geese watching social and non-social events.

Simply observing other individuals interacting has been shown to affect subsequent behaviour and also hormones in 'bystander' individuals. However, immediate physiological responses of an observer have been hardly investigated. Here we present results on individuals' heart rate (HR) responses during various situations, which occur regularly in a flock of greylag geese (Anser anser, e.g. agonistic encounters, vehicles passing by). We recorded simultaneously HR and behaviour of 21 semi-tame free-roaming geese, equipped with fully implanted transmitters. We considered 304 social and 81 non-social events during which the focal individuals did not respond behaviourally. Independent of the spatial distance to the event, these HR responses were significantly greater in social contexts (e.g. departing or landing geese, agonistic interactions) than in non-social situations (e.g. vehicles passing by, thunder). Focal individuals showed a significantly higher maximum HR as well as a greater HR increase in response to agonistic interactions, in which the pair partner or a family member was involved, as compared with a non-affiliated goose. Also, HR was significantly higher when the bystander watched non-affiliated geese interacting, which were higher ranking than the focal. We conclude that these differences are due to different relevance of the recorded events for the focal individual, depending on the individuals involved in the observed interaction.

Diel pattern of corticosterone metabolites in Arctic barnacle goslings (Branta leucopsis) under continuous natural light.

Here we describe the excretion pattern of corticosterone metabolites collected from droppings in barnacle goslings (Branta leucopsis) raised under 24 hours of continuous natural light in the Arctic. In lower latitudes, circulating corticosterone peaks around waking and shows a nadir between midnight and 4:00, whereas the peak and nadir are time-delayed slightly when measuring corticosterone metabolites from droppings. Photoperiod, along with other environmental factors, helps to entrain an animal's endogenous rhythm to that of the natural world. North of the Arctic Circle, photoperiod may not be a reliable cue as light is continuously absent during the winter and continuously present during the summer. Here, for the first time, we used droppings to describe a 24-hour excretion pattern of corticosterone metabolites (CORTm). By applying circular statistics for dependent data, we found a diel rhythmic pattern even under continuous natural light. We discuss potential alternative 'Zeitgeber' that may function even in the polar regions, focusing on melatonin. We propose a line of research to measure melatonin non-invasively from droppings. We also provide a validation of the adopted enzyme immunoassay (EIA) that was originally developed for greylag geese.

Indices of stress and immune function in Arctic barnacle goslings (Branta leucopsis) were impacted by social isolation but not a contaminated grazing environment.

In many areas around the Arctic remains and spoil heaps of old mines can be found, which have been abandoned after their heydays. Runoff from tailings of these abandoned mines can directly contaminate the local environment with elevated concentrations of trace metals. Few studies have investigated the possible negative effects of contaminants on Arctic terrestrial animals that use these areas. Trace metals can accumulate in animals and this accumulation has been linked to negative effects on fitness. Both, the hypothalamus-pituitary-adrenal (HPA) axis and/or the immune system have been named as possible underlying causes for these observations. Free-living animals are often exposed to multiple stressors simultaneously, however, and this is often not considered in studies on the effects of contaminants on animal physiology. Here, we performed a study on Spitsbergen (Svalbard) taking both potential effects of trace metal contamination and social stress into account. We investigated experimentally effects of exposure to contaminants from a historic coal mine area on plasma corticosterone levels and on four innate immune parameters (haemolysis, haemagglutination, haptoglobin-like activity and nitric oxide) before and after social isolation in human-raised barnacle goslings (Branta leucopsis). Baseline corticosterone and immune parameters were not affected by mine-exposure. After social isolation, mine goslings tended to show decreased haemagglutination in comparison with control goslings, but we detected no difference in the other measures. Social isolation increased corticosterone and decreased haptoglobin-like activity in all goslings. Immunology and corticosterone levels of barnacle goslings thus seem unaffected, at least on the short term, by Arctic coal mining contamination.

Sampling effort/frequency necessary to infer individual acute stress responses from fecal analysis in Greylag geese (Anser anser).

Measuring hormone metabolites from excreta is a powerful method to study hormone-behavior relationships. Currently, fecal corticosterone metabolite concentrations are used to estimate individual short-term stress responses. From the free-roaming, semitame flock of greylag geese (Anser anser), as many fecal samples as possible were collected over 3 h following a challenge (social density stress) or in a control situation. This time span corresponds to the gut passage time of geese. It was asked how many samples were necessary to determine differences in excreted corticosterone immunoreactive metabolites (CORTs) between control and social density stress and which parameters (means, maxima, range) reliably showed this difference. A large variation of CORT was found between consecutive samples. Still, means, maxima, and ranges of the samples in a fecal series consistently showed the response to a stressor both within and between individuals. Three samples sufficed if the maximum value of CORT was used, whereas four or more samples were necessary to work with the mean. It was concluded that by increasing the number of fecal samples collected, the course of CORT could be measured more precisely and an individual's acute stress response inferred more reliably.

Juvenile greylag geese (Anser anser) discriminate between individual siblings.

Social species that maintain individualised relationships with certain others despite continuous changes in age, reproductive status and dominance rank between group members ought to be capable of individual recognition. Tests of "true" individual recognition, where an individual recognises unique features of another, are rare, however. Often kinship and/or familiarity suffice to explain dyadic interactions. The complex relationships within a greylag goose flock suggest that they should be able to recognise individuals irrespective of familiarity or kinship. We tested whether six-week-old hand-raised greylags can discriminate between two of their siblings. We developed a new experimental protocol, in which geese were trained to associate social siblings with geometrical symbols. Subsequently, focals were presented with two geometrical symbols in the presence of a sibling associated with one of the symbols. Significant choice of the geometrical symbol associated with the target present indicated that focals were able to distinguish between individual targets. Greylag goslings successfully learned this association-discrimination task, regardless of genetic relatedness or sex of the sibling targets. Social relationships within a goose flock thus may indeed be based on recognition of unique features of individual conspecifics.

Heart rate responses to induced challenge situations in greylag geese (Anser anser).

Adequate short-term responses to stressors are of great importance for the health and well-being of individuals and factors modulating the physiological stress response (e.g., controllability, suddenness, familiarity) of a stimulus are well described under laboratory conditions. In the present study we aimed at investigating the stress response in greylag geese (Anser anser) in the field, confronting individuals with naturally occurring stressors. We measured beat-to-beat heart rate (HR) via fully implanted transmitters during three different experimental challenges: (1) catching and holding, (2) confrontation with a model predator, and (3) approach by different humans. We compared this to a control period and HR during agonistic encounters, a naturally occurring stressor. All three experimental situations evoked a HR increase. Highest HR responses were elicited by catching and holding the animals. In the third experiment, HR responses were greatest when the geese were approached by a human stranger (i.e., somebody the geese have never seen before). Hence, geese discriminated between different kinds of stressors and adjusted their physiological response depending on the type of stressor. Our results show that geese were able to discriminate between individual humans. In line with a number of lab studies, we suggest that particularly the controllability of certain situation determines the intensity of the HR response, also in a natural setting in the field.

Glucocorticoids enhance and suppress heart rate and behaviour in time dependent manner in greylag geese (Anser anser).

Stress responses involve autonomic, endocrine and behavioural changes. Each of these responses has been studied thoroughly in avian species, but hardly in an integrative way, in free-living birds. This is necessary to reveal the temporal dynamics of the stress response. Towards that goal, we recorded heart rate (HR) and behaviour in free-ranging male greylag geese (Anser anser) simultaneously over 2h. The geese were subjected to (a) unmanipulated control condition, (b) capture, handling and injection of ACTH, and (c) capture, handling and injection of a saline solution (SHAM). Fecal samples for the non-invasive determination of immuno-reactive glucocorticoid metabolite (BM) concentrations were collected for 7h thereafter. The SHAM control caused a significant BM increase, a transient increase in HR, an initial increase of preening behaviour and a delay in feeding. ACTH treatment, relative to SHAM, produced significantly higher BM concentrations, and activation of "displacement behaviours" such as wing flapping, body shaking and preening. Also, feeding activity as well as resting was postponed and/or lower for a longer period of time after ACTH than after SHAM. ACTH injection had a greater effect than SHAM injection on HR increase in the first hour, but particularly on HR decline in the second hour following the injection. Hence, glucocorticoids had time- and dose-dependent stimulatory and suppressive effects on cardiovascular activity and behaviour. HR dynamics after ACTH actually matched with behavioural dynamics: both were first enhanced and later suppressed, which is in alignment with adaptive stress management involving the fight-flight response and recovery from stress, respectively.

Serial agonistic attacks by greylag goose families, Anser anser, against the same opponent.

It is known from primates that alliance partners may support each other's interests in competition with others, for example, through repeated agonistic attacks against a particular individual. We examined serial aggressive interactions between greylag goose families and other flock members. We found that repeated attacks towards the same individual were common and that up to five serial attacks by family members followed an initial attack. Family size did not affect the frequency of such serial attacks. Juvenile geese evidently benefited most from active social support through serial attacks. About 60% of the juveniles' lost primary interactions were subsequently reversed by another family member. This may be one of the reasons why juveniles rank higher in the social hierarchy than would be expected from their age and size alone. Losses in serial attacks predominantly occurred against other, presumably higher-ranking, family geese and ganders. We propose three major functions/consequences of serial attacks. Analogous to primates, serial attacks in greylag geese may serve to reinforce a losing experience of an opponent defeated in a preceding attack. On the side of the winning family, serial attacks may reinforce the experience of winning. Both winning and losing experiences are linked with physiological consequences in higher vertebrates, affecting the future social performance of winners or losers. Finally, serial attacks may signal the agonistic potential of a family to other flock members. This is supported by heart rate data, which indicate that greylags are competent to interpret third-party relationships.

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.

Individualities in a flock of free-roaming greylag geese: behavioral and physiological consistency over time and across situations.

The concept of personality implies individual differences in behavior and physiology that show some degree of repeatability/consistency over time and across contexts. Most studies of animal personality, particularly studies of individuals' variation in physiological mechanisms, have been conducted on selected individuals in controlled conditions. We attempted to detect consistent behaviors as well as physiological patterns in greylag ganders (Anser anser) from a free-roaming flock living in semi-natural conditions. We tested 10 individuals repeatedly, in a handling trial, resembling tests for characterization of "temperaments" in captive animals. We recorded the behavior of the same 10 individuals during four situations in the socially intact flock: (1) a "low density feeding condition", (2) a "high density feeding condition", (3) a "low density post-feeding situation" and (4) while the geese rested. We collected fecal samples for determination of excreted immuno-reactive corticosterone (BM) and testosterone metabolites (TM) after handling trials, as well as the "low density feeding" and the "high density feeding" conditions. BM levels were very highly consistent over the repeats of handling trials, and the "low density feeding condition" and tended to be consistent over the first two repeats of the "high density feeding condition". Also, BM responses tended to be consistent across contexts. Despite seasonal variation, there tended to be inter-test consistency of TM, which pointed to some individual differences in TM as well. Aggressiveness turned out to be a highly repeatable trait, which was consistent across social situations, and tended to correlate with an individual's resistance during handling trials. Also, "proximity to the female partner" and "sociability" - the average number of neighboring geese in a close distance while resting - were consistent. We conclude that aggressiveness, "affiliative tendencies" and levels of excreted corticosterone and testosterone metabolites may be crucial factors of personality in geese.

Active and passive social support in families of greylag geese (Anser anser).

In general, support by social allies may reduce stress, increase success in agonistic encounters and ease access to resources. Social support was mainly known from mammals, particularly primates, and has been studied in birds only recently. Basically two types are known: (i) 'active social support', which describes the participation of a social ally in agonistic encounters, and (ii) 'passive social support' in which the mere presence of a social ally reduces behavioural and physiological stress responses. In greylag geese (Anser anser) offspring stay with their parents for an entire year or even longer and therefore are a candidate avian model to study support by social allies. We investigated the effects of active and passive social support in ten families (ten males, ten females, 33 juveniles) in a free-roaming, semi-tame flock of greylag geese. Focal individuals were observed during three time periods: (i) re-establishment of the flock in the fall, (ii) stable winter flock, and (iii) disintegration of the flock and break-up of family bonds. We recorded all agonistic interactions of the members of one focal family during morning feedings for two consecutive days: a control day, in which food was distributed widely, and a social density stress situation, in which the same amount of food was spread over a much smaller area. In addition, we collected faeces of all individuals within this family for three hours from the beginning of the feeding situation for determining excreted corticosterone immuno-reactive metabolites by enzyme immuno assay. We found that the small families, i.e. pairs with one or two accompanying young, were involved in more agonistic interactions, mainly through the lack of active social support, as compared to large families in the same situation. Members of greylag goose families lost agonistic encounters significantly less often when actively supported. In addition, the excretion of corticosterone metabolites was significantly decreased in large families during a social density stress situation, probably as an effect of passive social support. Via such a socially induced decrease in hormonal stress response during challenging situations, an individual's long term energy management may benefit.