Mareike Stöwe

Ravens, Corvus corax, follow gaze direction of humans around obstacles

The ability to follow gaze (i.e. head and eye direction) has recently been shown for social mammals, particularly primates. In most studies, individuals could use gaze direction as a behavioural cue without understanding that the view of others may be different from their own. Here, we show that hand–raised ravens not only visually co–orient with the look–ups of a human experimenter but also reposition themselves to follow the experimenters gaze around a visual barrier. Birds were capable of visual co–orientation already as fledglings but consistently tracked gaze direction behind obstacles not before six months of age. These results raise the possibility that sub–adult and adult ravens can project a line of sight for the other person into the distance. To what extent ravens may attribute mental significance to the visual behaviour of others is discussed.

The ontogeny of caching in ravens, Corvus corax

Ravens scavenging on carcasses devote much of their time to carrying off loads of food for temporary storage in caches. Ways of reducing conspecific pilfering of these caches include camouflaging caches with debris and positioning caches at a distance from and/or out of sight of potential competitors. We examined the acquisition and improvement of these caching skills in young captive ravens. We identified a hierarchy of elements in the caching behaviour, ranging from simply pressing the caching items towards solid structures to the appropriate covering of them with surrounding material. The development of these elements was closely linked with the birds’ acquisition of Piagetian Stages of object permanence. Furthermore, we distinguished between the young ravens’ initial caching of edible and inedible items. We tracked the individuals’ temporal development of placing their caches at a distance from and out of sight of conspecifics and their social interactions over caches. Behaviours aimed at preventing pilfering were associated with competitive interactions and were manifested only with edible items. We conclude that the skills for camouflaging caches are primarily affected by maturation of representational capacities for hidden (i.e. not visible) items, whereas the skills for the positioning of caches are strongly affected by experience gained through social interactions.

Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax)

Averse effects of social stress may be buffered by the presence of social allies, which mainly has been demonstrated in mammals and recently also in birds. However, effects of socio-positive behavior prior to fledging in relation to corticosterone excretion in altricial birds have not been investigated yet. We here monitored corticosterone excretion patterns in three groups of hand raised juvenile ravens (n=5, 6 and 11) in the nest, post-fledging (May-July) and when ravens would be independent from their parents (September-November). We related these corticosterone excretion patterns to socio-positive behavior. Behavioral data were collected via focal sampling in each developmental period considered. We analyzed amounts of excreted immunoreactive corticosterone metabolites (CM) using enzyme immuno assays. We collected fecal samples in each developmental period considered and evaluated the most appropriate assay via an isolation stress experiment. Basal CM was significantly higher during the nestling period than post-fledging or when birds were independent. The time nestlings spent allopreening correlated negatively with mean CM. Post-fledging, individuals with higher CM levels sat close to (distance <50 cm) conspecifics more frequently and tended to preen them longer. When birds were independent and a stable rank hierarchy was established, dominant individuals were preened significantly longer than subordinates. These patterns observed in ravens parallel those described for primates, which could indicate that animal species living in a complex social environment may deal with social problems in a similar way that is not restricted to mammals or primates.

Behavioural phenotypes may determine whether social context facilitates or delays novel object exploration in ravens (Corvus corax)

Individuals consistently differ in behavioural phenotypes. Here we examine the interaction between behavioural phenotype and response to social context during novel object exploration in a neophobic corvid species, the raven (Corvus corax). The presence of conspecifics tends to encourage object exploration and learning but may also delay or even inhibit exploratory behaviour. Factors such as individual differences in response to social context may determine whether the presence of a conspecific facilitates or inhibits approach to novel objects. We confronted eleven six-month-old hand-raised ravens with novel objects, both individually and in dyadic combinations. We defined individuals as “fast” and “slow” explorers on the basis of their approach latency to novel objects when tested individually. The presence of a conspecific delayed the approach of fast birds to novel objects. Slow birds, in contrast, approached the novel objects with lower latencies and spent more time close to them when in dyads with fast siblings than when alone. The individuals’ approach behaviour seemed to determine whether social context facilitated or delayed exploratory behaviour. This may contribute to explaining ambiguous results concerning the effects of social context in previous studies.

Corticosterone, food intake and refueling in a long-distance migrant.

Elevated baseline corticosterone levels function to mobilize energy in predictable life-history stages, such as bird migration. At the same time, baseline corticosterone has a permissive effect on the accumulation of fat stores (fueling) needed for migratory flight. Most migrants alternate flight bouts with stopovers, during which they replenish the fuel used during the preceding flight (refueling). The role of corticosterone in refueling is currently unclear. In a fasting-re-feeding experiment on northern wheatears (Oenanthe oenanthe) in autumn we found that baseline total and free corticosterone levels were negatively related with both food intake and the rate of fuel deposition after fasting. This confirms our earlier findings in wild conspecifics in spring and indicates that corticosterone does not stimulate stopover refueling. Whether the negative relationship between baseline corticosterone level and fuel deposition rate is causal is questionable, because within-individual comparison of corticosterone metabolite levels in droppings did not reveal differences between refueling and control periods. In other words, corticosterone does not appear to be down-regulated during refueling, which would be expected if it directly hampers refueling. We discuss possible correlates of corticosterone level that may explain the negative association between corticosterone and stopover refueling. Additionally, we found that fasting decreases total corticosterone level, which contrasts with previous studies. We propose that the difference is due to the other studies being conducted outside of the migration life-history stage, and provide a possible explanation for the decrease in corticosterone during fasting in migrating birds.

Corticosterone predicts nocturnal restlessness in a long-distance migrant.

The decision made by migrating birds to stop refueling and to depart from stopover depends on cues from innate rhythms, intrinsic factors such as fuel reserves, and extrinsic factors such as weather conditions. The physiological mechanism behind this decision, however, is largely unexplored. The transition from refueling to flight involves an increase in both locomotion and energetic demands. Because, at baseline levels, corticosterone stimulates locomotion and is involved in the mobilization of energy, this hormone could encourage departure of migrants. We collected field data on baseline corticosterone, migratory restlessness, and actual departure in northern wheatears at stopover. Additionally, in refueling long-term captive conspecifics, we measured migratory restlessness while simultaneously collecting droppings to determine glucocorticoid metabolite (GCM) levels. We found that migratory restlessness at stopover was positively correlated with corticosterone level. Similarly, in refueling long-term captive birds, migratory restlessness was positively correlated with concurrently measured GCM levels in droppings. To our best knowledge, our study is the first to simultaneously measure a hormonal signal and migratory restlessness. In conclusion, our results are consistent with the hypothesis that, by increasing locomotor activity, baseline corticosterone is involved in the regulation of departure of migrants at stopover. Future studies could reveal how corticosterone is up-regulated in migrants that are ready to depart.

Loner or socializer? Ravens’ adrenocortical response to individual separation depends on social integration

Non-breeding common ravens (Corvus corax) live in complex social groups with a high degree of fission–fusion dynamics. They form valuable relationships and alliances with some conspecifics, while taking coordinated action against others. In ravens, affiliates reconcile their conflicts, console each other after conflicts with a third party, and provide each other with social support — all behaviors that presumably reduce corticosterone levels and alleviate stress. However, how well an individual is socially integrated in a (sub)group might vary substantially. This raises the question whether the social integration of a raven affects its stress responses to fission–fusion dynamics. The present study aims to investigate this effect experimentally by separating single ravens (n = 16) individually from their group for four days and subsequently reintroducing them. To determine stress response patterns in the separated individuals we measured the amounts of immunoreactive corticosterone metabolites (CM) in droppings. We compared two enzyme immunoassays, which we validated by conducting an ACTH challenge, and finally decided to apply an 11-oxoetiocholanolone enzyme immunoassay. Additionally, we determined levels of social integration using focal observations. Our findings suggest that a strong social integration is related to low CM levels when the individuals are within the group and high levels during separations, implying that separation leads to stress in these birds. In contrast, poorly socially integrated ravens seem to exhibit the opposite pattern, indicating that to them group living is more stressful than being temporarily separated. We, therefore, conclude that the birds’ adrenocortical activity is modulated by their social integration.