Family-transmitted stress in a wild bird

Abstract

Recent data suggest that, in animals living in social groups, stress-induced changes in behavior have the potential to act as a source of information, so that stressed individuals could themselves act as stressful stimuli for other individuals with whom they interact repeatedly. Such form of cross-over of stress may be beneficial if it enhances adaptive responses to ecological stressors in the shared environment. However, whether stress can be transferred among individuals during early life in natural populations remains unknown. Here we tested the effect of living with stressed siblings in a gull species where, as in many vertebrates, family represents the basic social unit during development. By experimentally modifying the level of stress hormones (corticosterone) in brood mates, we demonstrate that the social transfer of stress level triggers similar stress responses (corticosterone secretion) in brood bystanders. Corticosterone-implanted chicks and their siblings were faster in responding to a potential predator attack than control chicks. In gulls, fast and coordinated reactions to predators may increase the chances of survival of the whole brood, suggesting a beneficial fitness value of cross-over of stress. However, our data also indicate that living with stressed brood mates early in life entails some long-term costs. Near independence, fledglings that grew up with stressed siblings showed reduced body size, high levels of oxidative damage in lipids and proteins, and a fragile juvenile plumage. Overall, our results indicate that stress cross-over occurs in animal populations and may have important fitness consequences.

Keywords: glucocorticoids; group living; phenotypic programming; social environment; stress cross-over.

Fig. S1.

Photographs of gull chicks during their postnatal development. (A and B) Chicks brooding (A) and showing antipredator response (B), crouching together during the first week of life. (C) Full-grown chick recaptured at 30 d of age.

Fig. 1.

Brood mates of corticosterone-implanted chicks showed reduced growth, increased basal glucocorticoid secretion, and a faster reaction time to predation risk. Tarsus length (A), body mass (B), and basal corticosterone level (root-squared) (C) at 8 d of age, and antipredator behavior (log-transformed time to crouch) (D) at 9 d of age in implanted (dark bars) and nonimplanted (light bars) yellow-legged gull chicks from control (blue) and stress (orange) broods. In each brood, two of three chicks were s.c. implanted between the shoulders with a surgical silastic implant filled with corticosterone (stress broods) or left empty (control broods), and the remaining sibling was left without being manipulated (nonimplanted). Data show estimated marginal mean ± SE (Fig. S2 for the comparison between initial and final values of each variable).

Fig. S2.

Brood mates of corticosterone-implanted chicks showed reduced growth, increased basal glucocorticoid secretion, and shortened time to respond to predation risk. Tarsus length (A), body mass (B), and basal corticosterone level (square root-transformed) (C) during the first 8 d after hatching in yellow-legged gull chicks from control (blue circles) and stress (orange triangles) broods. Within broods, implanted chicks are represented by dark symbols whereas nonimplanted chicks are represented by light symbols. In all analyses, age × brood treatment × chick manipulation was not significant (tarsus length: F_1,127.24 = 0.125, P = 0.724; body mass: F_1,125.04 = 0.056, P = 0.814; corticosterone level: F_1,73.30 = 0.086, P = 0.770). Data show the estimated marginal mean ± SE. Significant differences between groups: *P ≤ 0.05, **P ≤ 0.01.

Fig. 2.

Brood mates of corticosterone-implanted chicks were smaller, had increased levels of oxidative damage, and developed a more fragile juvenile plumage. Tarsus length (A), body mass (B), lipid peroxidation level (MDA) (C), advanced oxidation protein product (AOPP) level (D), barb density (E), and barbule density (F) in nonimplanted yellow-legged gull fledglings (30 d of age) from control (blue) and stress (orange) broods; note that none of these birds received an implant. Data show the estimated marginal mean ± SE. TBA, thiobarbituric acid reactive substances.

Fig. S3.

Corticosterone implants increased basal corticosterone levels in yellow-legged gull chicks (pilot study). Basal corticosterone levels (square root-transformed; mean ± SE) during the first 8 d after hatching in yellow-legged gull chicks from control (blue) and stress (orange) broods. Significant differences between groups: *P ≤ 0.05, **P ≤ 0.01.