Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird

1. In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic–pituitary–gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited. 2. It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food‐restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin‐releasing hormone‐I (GnRH‐I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin‐inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides. 3. At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH‐I, but the duration of food restriction was inversely related to the size of ir‐GnIH perikarya. Furthermore, the number of ir‐NPY cells was higher in food‐restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen‐sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum‐fed birds. 4. Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.