Maternal corticosterone deposition in avian yolk: Influence of laying order and group size in a joint-nesting, cooperatively breeding species

Abstract

Glucocorticoid hormones play a key role in day-to-day adjustments to fluctuating metabolic needs. These hormones also mediate physiological and behavioral responses to stressful events, allowing individuals to cope with stressors. Various environmental insults, such as a food shortages, predation attempts, and agonistic encounters often elevate plasma glucocorticoid levels in vertebrates. Because exposure to maternally-derived (via circulation or egg) glucocorticoids may be detrimental to the developing embryo, maternal stress can have negative carryover effects on offspring fitness. We examined corticosterone, the primary avian glucocorticoid, concentrations in egg yolk in a plural-breeding, joint-nesting species, the smooth-billed ani (Crotophaga ani), in which females compete among themselves to lay eggs in the final incubated clutch. We investigated whether yolk corticosterone levels varied with laying order and group size. Because egg-laying competition leads to physiological and social stress that is intensified with group size and laying order, we predicted that yolk corticosterone levels should increase from the early to the late egg-laying period and from single female to multi-female groups. In this two-year field study, we found that yolk corticosterone levels of late-laid eggs within the communal clutch were higher in multi-female groups than in single female groups. Results from this study suggest that laying females experience higher levels of stress in multi-female groups and that this maternal stress influences yolk corticosterone concentrations. This study identifies a novel cost of group-living in plural-breeding cooperatively breeding birds, namely an increase in yolk corticosterone levels with group size that may result in detrimental effects on offspring development.

The effect of social group size on feather corticosterone in the co-operatively breeding Smooth-billed Ani (Crotophaga ani): An assay validation and analysis of extreme social living

“…Competitive interactions have long been known to elevate baseline glucocorticoids in socially living species [19, 28, 65–67] and competitive interactions behind egg burial and tossing are likely to follow suit. Indeed, Schmaltz et al [34] reported higher CORT deposited in yolk of Smooth-billed Ani eggs laid in multi-female groups when compared to single female pairs. Similarly, yolk CORT deposited in late laid eggs of multi-female groups (after ovicidal competition had taken place) was reportedly higher than that of early laid eggs [34], highlighting the influence of ovicide on stress physiology in female breeders.…”

“…Indeed, Schmaltz et al [34] reported higher CORT deposited in yolk of Smooth-billed Ani eggs laid in multi-female groups when compared to single female pairs. Similarly, yolk CORT deposited in late laid eggs of multi-female groups (after ovicidal competition had taken place) was reportedly higher than that of early laid eggs [34], highlighting the influence of ovicide on stress physiology in female breeders. Aside from at-the-nest dynamics, enhanced competition for access to mates and resources in large social groups may also act to increase glucocorticoids in both sexes.…”

“…While all laying females are likely to experience elevations in baseline glucocortoids during breeding seasons, females in larger groups partake in compensatory egg production, therefore increasing annual oviposition and likely exacerbating physiological costs. Female Smooth-billed Anis from multi-female social groups have been shown to lay more eggs and deposit higher concentrations of CORT in yolk than those in single female groups [34, 35]—an action thought to occur by passive diffusion and therefore reflect circulating maternal CORT [72–74]. In males, heightened feather-CORT in atypically large social clusters is more likely explained by an exaggeration of intra-male competition for mating opportunities.…”

“…Chronic HPA activation, however, presents considerable metabolic demands and can yield detrimental effects on reproduction and survival [19, 28–31]. While numerous studies have examined the effects of social hierarchy on circulating CORT titers in birds [25, 32, 33], few have investigated the influence of social group size on stress physiology [17, 34] and fewer still in joint-nesting species [34]. …”

“…Alternatively, solitary nesting is not uncommon and presents an opportunity to capitalize on genetic contribution to a brood, though direct benefits of group living must be forgone. Trends of social group size and CORT deposited in yolk have been explored in Smooth-billed Ani eggs [34] and have elucidated a positive correlation between maternal group size and CORT deposition. Similar analyses, however, are lacking for breeding adults and may shed light on the desirability of grouping behaviour and social group maintenance.…”