Stress and the timing of breeding: Glucocorticoid-luteinizing hormones relationships in an arctic seabird Aurélie Goutte a, * , Frédéric Angelier a,b , Céline Clément Chastel a , Colette Trouvé a , Børge Moe c , Claus Bech d , Geir W. Gabrielsen e , Olivier Chastel a a Centre d’Etudes Biologiques de Chizé, CNRS, F-79360, France b Department of Neurobiology, Physiology and Behavior, University of California, One Shields Avenue, Davis, CA 95616, USA c Norwegian Institute for Nature Research (NINA), Arctic Ecology Department, NO-9296 Tromsø, Norway d Department of Biology, Norwegian University of Science and Technology (NTNU), NO-7491 Trondheim, Norway e Norwegian Polar Research Institute, NO-9296 Tromsø, Norway article info Article history: Received 25 May 2010 Revised 28 July 2010 Accepted 28 July 2010 Available online 3 August 2010 Keywords: Corticosterone HPG axis LHRH challenge LH Testosterone Breeding decision Laying date Long-lived bird Black-legged kittiwake Rissa tridactyla abstract In birds, stressful environmental conditions delay the timing of breeding but the underlying mechanisms are poorly understood. The stress hormone corticosterone appears to be a good candidate for mediating the decision to breed and when to start egg-laying, via a possible inhibition of luteinizing hormone (LH) and sex-steroids production. We used luteinizing hormone releasing hormone (LHRH) challenge in pre- laying male and female Black-legged kittiwakes (Rissa tridactyla) to test whether LH and testosterone secretion were depressed by elevated corticosterone levels. Females bearing high baseline corticosterone levels showed reduced baseline LH levels and a low ability to release LH, following LHRH challenge. Fur- ther, females bearing low baseline LH levels and elevated baseline corticosterone levels were more likely to skip breeding. However, non-breeding females were physiologically primed for breeding, since they mounted high LHRH-induced LH release. Egg-laying date was advanced in good body condition females but was unaffected by hormones secretion. In males, corticosterone levels had no effect on LH and/or tes- tosterone secretion and did not affect their decision to breed. Interestingly, males with high LHRH- induced testosterone release bred early. Our study highlights clear sex-differences in the HPG sensitivity to stress hormones in pre-laying kittiwakes. Because females have to store body reserves and to build up the clutch, they would be more sensitive to stress than males. Moreover, intrasexual competition could force male kittiwakes to acquire reproductive readiness earlier in the season than females and to better resist environmental perturbations. We suggest that high testosterone releasing ability would mediate behavioural adjustments such as courtship feeding, which would stimulate early egg-laying in females. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction Breeding at the right time is a key-component of fitness, as successful reproduction requires a good overlap between energy- demanding needs and the peak of available resources (match-mis- match hypothesis, Cushing, 1990; Visser et al., 1998; Stenseth and Mysterud, 2002; Durant et al., 2007; review in Visser, 2008). Hence, as adaptive responses to environmental variations, free-living organisms must exhibit considerable behavioural and physiological flexibilities in the timing of their seasonal activities (review in Wingfield, 2008). To do so, they integrated photoperiod, as a fixed cue (Wingfield and Kenagy, 1991; Dawson et al., 2001) and variable cues, such as ambient temperature, food supply, nest sites avail- ability, and/or stimulatory social interactions (Wingfield, 1980; Wingfield and Kenagy, 1991; Ball, 1993; Visser et al., 1998; Wing- field et al., 2003; Schoech et al., 2004; Ball and Ketterson, 2008; Both et al., 2009). At the endocrine level, the onset of breeding involves the activation of the hypothalamic-pituitary-gonadal axis (hereafter HPG axis): increasing day length activates the expression of a neuro- hormone, the Gonadotropin Releasing Hormone (GnRH) that trig- gers the release of two pituitary gonadotrophins: the luteinizing hormone and the follicle-stimulating hormone (LH and FSH, re- viewed in Dawson et al., 2001). In turn, gonadotrophins activate the gonadal development and the release of sex steroids such as estradiol and testosterone. A wide range of sex steroid hormone- dependent behaviours is then expressed (Ball, 1993), such as nest building, courtship, and mating. However, this hormonal cascade is not only driven by photoperiod, but could also be regulated by additional non-photoperiodic cues. Specifically, pre-laying ener- getic constraints, such as food shortage and/or environmental cues that enable individuals to anticipate food availability (see Shultz 0016-6480/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2010.07.016 * Corresponding author. E-mail address: goutte@cebc.cnrs.fr (A. Goutte). General and Comparative Endocrinology 169 (2010) 108–116 Contents lists available at ScienceDirect General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen