Age and the timing of breeding in a long‐lived bird: a role for stress hormones?

Abstract

Summary1. Young birds often reproduce later in the season than older ones, with poorer breeding success, but the proximate mechanisms involved in such a pattern remain poorly studied, especially in long-lived species. One possible mechanism is the endocrine stress response which is accompanied by the release of corticosterone. Elevated corticosterone levels can trigger physiological and behavioural responses that may delay or even suppress reproduction. 2. We tested the hypothesis that the delayed timing of breeding of young birds may be related to a greater susceptibility to stress compared with older ones during the pre-laying period of the breeding season. For this purpose, known-age (7-44 years old) pre-laying snow petrels, Pagodroma nivea, were monitored for baseline and acute stress-induced corticosterone levels. We examined whether baseline and stress-induced corticosterone levels were related to age, and whether they could influence the decision to breed and egg-laying date. 3. Young snow petrels were more likely to skip the breeding season and to breed later than middle-aged birds. In addition, the oldest birds bred later than middle-aged ones, suggesting a possible senescence on laying dates. Baseline corticosterone levels were independent of age but young and very old birds were more sensitive to stress than middle-aged ones. However, there was no effect of stress-induced corticosterone levels on breeding decision and egg-laying date. Elevated baseline corticosterone levels during the pre-laying period were associated with a higher probability of skipping breeding in females and a delayed timing of egg-laying in both sexes. 4. These results suggest that the greater susceptibility of young breeders to stress was not the functional mechanism explaining their delayed timing of breeding. Baseline corticosterone levels, although independent of age, appear to be a more likely mediator of breeding decision and egglaying date. In long-lived birds, the relationship between age and timing of breeding may be rather indirect, as other age-related factors such as breeding experience or foraging skills may have a deeper impact on baseline corticosterone than age per se.

Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses

“…Furthermore, the low P4 and T levels in deferring birds is a hormonal profile that has 297 been linked to poor condition in seabirds [13,14,15]. These finding support our first prediction: 298 breeding deferral is characterized by low body mass, low blood hematocrit, and a generally 299 compromised condition upon arrival at the breeding colony after overwinter migration.…”

“…The initial breeding decision (breed/defer) was very strongly associated 316 with body mass, independent of age or quality, and the simplest explanation for this pattern is 317 that returning females can assess their post-migratory physiological state, and if some relative 318 threshold of condition has not been attained they will forgo reproduction thereby minimizing 319 fitness costs (as per life-history theory, [29]). This might be mediated in part by the effect of 320 body condition on hormonal processes which affect HPG functioning [13,14,15], and in our study 321 P4 and T were not up-regulated in deferring females to a degree that would support gamete 322 production. Previous studies of carryover effects in migratory animals, including seabirds, 323 provide some evidence for this by arguing that the environmental conditions experienced during 324 the non-breeding period can influence resource state at the onset of reproduction ([16] and 325 references therein).…”

“…For example, Goutte et al 67 [13] showed that in an annually-breeding seabird, elevated baseline corticosterone levels during 68 the pre-laying period after migration were associated with a higher probability of deferred 69 breeding, and speculated that elevated corticosterone might inhibit luteinizing hormone (LH) and 70 the downstream secretion of sex-steroids necessary for reproduction. Other studies have shown 71 that non-breeding or deferring birds are fully capable of elevating LH, when presented with a 72 4 luteinizing hormone releasing hormone (LHRH) challenge, but they do not or cannot sustain 73 gonadal steroid production [5,14,15].…”

Manipulating individual state during migration provides evidence for carry-over effects modulated by environmental conditions

“…In birds, chronic stress can reduce body condition [37,38] and thus, it is probable that birds stressed by captivity eventually ended their spring staging period with reduced body condition. If the elevated corticosterone levels associated with the acute stress of capture persisted for some time [39], it could also have deleterious effects on the reproductive physiology and behaviour [40,41]. For instance, Goutte et al [41] found that elevated levels of baseline corticosterone during the pre-laying period were associated with a higher probability of skipping breeding in female snow petrel (Pagodroma nivea).…”

“…If the elevated corticosterone levels associated with the acute stress of capture persisted for some time [39], it could also have deleterious effects on the reproductive physiology and behaviour [40,41]. For instance, Goutte et al [41] found that elevated levels of baseline corticosterone during the pre-laying period were associated with a higher probability of skipping breeding in female snow petrel (Pagodroma nivea). Our experimental design also manipulated males because they were maintained in captivity for the same length of time as females (though all of them received ad libitum food) to ensure that mates could reunite upon release.…”