Growing up in a crowd: social environment shapes the offspring's early exploratory phenotype in a colonial breeding species

Abstract

In colonial breeding species, the number of adverse social interactions during early life typically varies with breeding density. Phenotypic plasticity can help deal with this social context, by allowing offspring to adjust their behaviour. Furthermore, offspring may not be unprepared since mothers can allocate resources to their embryos that may pre-adjust them to the post-hatching conditions. Thus, we hypothesize that lesser black-backed gull chicks raised in dense breeding areas, with greater exposure to intra-specific aggression, show higher levels of anxiety and lower levels of exploration compared to chicks in low-density areas, and that this is facilitated by prenatal effects. To test this, we cross-fostered clutches within and across pre-defined high- and low-breeding density areas. We measured chicks' anxiety and exploration activity in an open-field test that included a novel and a familiar object. We found that both pre- and post-natal social environment contributed nearly equally and shaped the offspring's exploratory behaviour, but not its anxiety, in an additive way. Post-natal effects could reflect a learned avoidance of intra-specific aggression, yet identifying the pathways of the prenatal effects will require further study.

Breeding density affects the movements of gull chicks, the size of their home ranges and their association with neighbours

“…However, chicks do not necessarily hatch unprepared for this environment, as mothers can allocate hormones or other components to their eggs that can prepare their offspring for the conditions they are likely to encounter after hatching [40–42]. In support of this, pre-natal breeding density significantly predicted chick exploration behaviour in the open field test with chicks from the same colony, including individuals from this study [32], with pre- and post-natal social environment contributing almost equally to chick exploration behaviour. While this suggests that offspring may indeed benefit from pre-natal programming when post-natal conditions match pre-natal conditions, we can only speculate why we did not find a similar pre-natal effect when we directly tracked chicks in their post-natal social environment.…”

“…On the one hand, lower movement activity would reduce the likelihood of crossing territorial boundaries, and as such, reduce the probability of an aggressive encounter. Consistent with this idea, we have recently shown that gull chicks reared at high breeding densities in a colony exhibit less exploratory activity in novel environments [32]. Furthermore, the early-life social environment may affect resilience to (social) stress [33] or anxiety, with the latter again facilitating avoidance of aggressive interactions [33,34] (but see [32]).…”

“…Consistent with this idea, we have recently shown that gull chicks reared at high breeding densities in a colony exhibit less exploratory activity in novel environments [32]. Furthermore, the early-life social environment may affect resilience to (social) stress [33] or anxiety, with the latter again facilitating avoidance of aggressive interactions [33,34] (but see [32]). On the other hand, the early experience of aggression may enhance the expression of aggressive behaviour [35], which in turn may increase a chick’s competitive ability, for example, by upregulating testosterone production (i.e.…”

“…The fenced-off colony in which this study took place is located in the outer harbour of Zeebrugge, Belgium (51°20′56.2″ N, 3°10′25.0″ E) and hosted 282 pairs of lesser black-backed gulls during the study year (2021). To experimentally create variation in social density within the colony, 221 U-shaped concrete blocks (preferred breeding sites for gulls in this colony) were unequally distributed across eight equally sized (850 m 2 ) plots separated by 50 cm high plastic mesh fences in 2020 (for details see [ 32 ]). From the onset of egg laying onwards (around 25 April), we determined the laying date of each egg during three visits per week.…”

“…In this study, we examine the effects of the early-life social environment on movement activity, home range size and social associations with neighbours in chicks of the lesser black-backed gull ( Larus fuscus ), a semi-precocial species whose chicks begin to move at approximately 5–7 days of age. Early life movement forms the basis of exploratory behaviour, which has also been shown to be influenced by the early social environment [ 32 ], and thus potentially the level of aggression to which chicks are exposed. While until recently it was virtually impossible to study the movements and social interactions of chicks under natural conditions, recent developments in tracking technology now allow one to follow free-ranging individuals with high temporal and spatial accuracy.…”