Skipping reproduction (i.e. non-breeding by individuals that previously bred) is often observed in long-lived organisms [1]. The ‘prudent parent hypothesis’ posits that non-breeding decision should be favoured, when the value of the immediate reproduction is low relative to the value of future reproductive opportunities and survival [2], as it is expected to be in young adults. Moreover, senescent individuals may take advantage of sabbatical years to recover from previous reproductive efforts [3]. Alternatively, non-breeding events, instead of being strategically decided, might be imposed by physiological constraints in low-quality individuals [1]. Age appears to be the keystone of skipped breeding, since this behaviour is markedly observed in the youngest and in the oldest adult birds [4,5]. Thus, some of the needed physiological requirements for successful reproduction may be deficient in young and senescent adults [6].

The study was conducted on Terre Adélie (66°40′ S, 140°01′ E), Antarctica. Snow petrels are very long-lived birds with low fecundity (one egg per year [10]). Many birds were of known age, because chicks have been banded each year since 1964 [10]. Twenty-four males and 17 females, from 11 to 45 years old, were handled during the pre-laying period (i.e. the courtship and mating period), from 11 to 23 November 2008. Only one bird was captured at each nest and birds were observed as breeders in previous years. They were caught by hand and a first blood sample was collected from the alar vein with a syringe immediately after capture (mean ± s.e.: 3 min and 9 ± 5 s) to determine baseline LH levels. Then, birds were immediately (5 min 51 ± 9 s after capture) injected with exactly 0.1 ml of a GnRH solution in the second alar vein ([Gin⁸], Sigma Lot 121H04314). The GnRH was dissolved in a physiological solution to yield a dosage of 0.6 µg (0.1 ml)⁻¹ (about 1.5 µg kg⁻¹ body mass in 1 ml of 0.9% saline solution, as validated for seabirds [11]). Blood samples were collected from alar veins between 10 and 30 min after the GnRH injection to measure LH levels. LH changes from 0 to 10 min post-GnRH injection [(LH_{t =10} − LH_{t =0})/LH_{t =0}] and LH changes from 10 to 30 min post-GnRH injection [(LH_{t =30} − LH_{t =10})/LH_{t =10}] were examined as individual abilities to release LH. Blood samples were centrifuged and plasma was stored at −20°C. LH levels were assayed by radioimmunoassay at the CEBC (Centre d'Etudes Biologiques de Chizé) [11]. The lowest detectable concentration of LH was 0.05 ng ml⁻¹ and the intra-assay coefficient of variation was 6.2 per cent (three duplicates). Following GnRH injections, LH levels (baseline: 8.348 ± 0.534 ng ml⁻¹) significantly increased (10 min: 11.544 ± 0.842 ng ml⁻¹), then decreased (30 min: 9.059 ± 0.838 ng ml⁻¹; generalized linear mixed model (GLMM), time as factor: F_2,76 = 21.540, p < 0.001, time × sex: F_2,76 = 0.244, p = 0.784). The 41 nests were checked every 2 days, until the end of the breeding season, to monitor if birds engaged in breeding (n = 32) or if they skipped breeding (n = 9).

Although young petrels exhibited low baseline LH levels, they showed a substantial increase in LH levels from 0 to 10 min post-injection and reached similar absolute LH levels compared with older petrels at 10 min. LH changes from 0 to 10 min reflect the individual ability to release LH after a GnRH injection, relative to the baseline levels. This indicates that young petrels with previous reproductive experience had functional pituitaries. How, then, is it possible to explain their lower baseline LH levels? Although photoperiod is the primary signal controlling seasonal reproductive activities, social interactions can influence central physiology by modifying GnRH neurosecretory cells, which in turn stimulates the adjustment of reproductive physiology and behaviour [9]. In the monogamous snow petrel, repeated breeding attempts with the same partner could therefore provide important benefits by improving coordination of breeding activities [12]. In this context, low mate stimulations in young and newly paired petrels could explain their lower baseline LH levels. In our study, although sex steroids were not measured owing to small blood samples, we suggest that young females may reduce reproductive costs by delaying oestradiol secretion and ovarian development until establishing long-term pair bond [8]. Contrary to young petrels, old birds showed high baseline LH levels and did not strongly respond to the GnRH challenge. This may suggest that older petrels already secreted LH at their maximum levels, because of strong mate–mate interactions stimulated by long-term partnerships. Alternatively, as the pool of available ova decreases with age, higher LH levels found in old females may have originated from a lower negative feedback at the hypothalamus level, compared with young females [13].