Roles and Mechanistic Bases of Glucocorticoid Regulation of Avian Reproduction.

To maximize fitness, organisms must invest energetic and nutritional resources into developing, activating, and maintaining reproductive physiology and behavior. Corticosterone (CORT), the primary avian glucocorticoid, regulates energetic reserves to meet metabolic demands. At low (baseline) plasma levels, CORT activates avian mineralocorticoid receptors and may stimulate lipid mobilization, foraging activity, and feeding behavior. During stress in birds, elevated plasma CORT also stimulates glucocorticoid receptors and may promote glycemia, lipolysis, and proteolysis. Furthermore, CORT orchestrates physiological and behavioral adjustments to perceived threats. While many avian studies demonstrate effects of CORT on reproduction, few studies have elucidated the mechanisms, including receptor activation and site(s) of action, which underlie these effects. Even fewer studies have investigated how low and elevated plasma CORT regulates energetic reserves to meet the metabolic demands of reproduction. Here, we propose several hypotheses to clarify the direct and indirect effects of CORT on avian reproductive physiology and behavior. In addition, we emphasize the need for new manipulative studies involving alterations of endogenous plasma CORT levels and/or food availability to elucidate how CORT regulates the energetic demands of reproduction.

The seasonal glucocorticoid response of male Rufous-winged Sparrows to acute stress correlates with changes in plasma uric acid, but neither glucose nor testosterone.

We sought to clarify functional relationships between baseline and acute stress-induced changes in plasma levels of the stress hormone corticosterone (CORT) and the reproductive hormone testosterone (T), and those of two main metabolites, uric acid (UA) and glucose (GLU). Acute stress in vertebrates generally stimulates the secretion of glucocorticoids, which in birds is primarily CORT. This stimulation is thought to promote behavioral and metabolic changes, including increased glycemia. However, limited information in free-ranging birds supports the view that acutely elevated plasma CORT stimulates glycemia. Acute stress also often decreases the secretion of reproductive hormones (e.g., T in males), but the role of CORT in this decrease and the contribution of T to the regulation of plasma GLU remain poorly understood. We measured initial (pre-stress) and acute stress-induced plasma CORT and T as well as GLU in adult male Rufous-winged Sparrows, Peucaea carpalis, sampled during the pre-breeding, breeding, post-breeding molt, and non-breeding stages. Stress increased plasma CORT and the magnitude of this increase did not differ across life history stages. The stress-induced elevation of plasma CORT was consistently associated with decreased plasma UA, suggesting a role for CORT in the regulation of plasma UA during stress. During stress plasma GLU either increased (pre-breeding), did not change (breeding), or decreased (molt and non-breeding), and plasma T either decreased (pre-breeding and breeding) or did not change (molt and non-breeding). These data provide only partial support to the hypothesis that CORT secretion during acute stress exerts a hyperglycemic action or is responsible for the observed decrease in plasma T taking place at certain life history stages. They also do not support the hypothesis that rapid changes in plasma T influence glycemia.

Endocrine, metabolic, and behavioral effects of and recovery from acute stress in a free-ranging bird.

Acute stress in vertebrates generally stimulates the hypothalamo-pituitary-adrenal axis and is often associated with multiple metabolic changes, such as increased gluconeogenesis, and with behavioral alterations. Little information is available, especially in free-ranging organisms, on the duration of these reversible effects once animals are no longer exposed to the stressor. To investigate this question, we exposed free-ranging adult male Rufous-winged Sparrows, Peucaea carpalis, in breeding condition to a standard protocol consisting of a social challenge (conspecific song playback) followed with capture and restraint for 30min, after which birds were released on site. Capture and restraint increased plasma corticosterone (CORT) and decreased plasma testosterone (T), glucose (GLU), and uric acid (UA). In birds that we recaptured the next day after exposure to conspecific song playback, plasma CORT and UA levels no longer differed from levels immediately after capture the preceding day. However, plasma T was similar to that measured after stress exposure the preceding day, and plasma GLU was markedly elevated. Thus, exposure to social challenge and acute stress resulted in persistent (⩾24h) parameter-specific effects. In recaptured sparrows, the territorial aggressive response to conspecific song playback, as measured by song rate and the number of flights over the song-broadcasting speakers, did not, however, differ between the first capture and the recapture, suggesting no proximate functional association between plasma T and conspecific territorial aggression. The study is the first in free-ranging birds to report the endocrine, metabolic, and behavioral recovery from the effects of combined social challenge and acute stress.

Negative energy balance in a male songbird, the Abert's towhee, constrains the testicular endocrine response to luteinizing hormone stimulation.

Energy deficiency can suppress reproductive function in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary-gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none have investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone responsiveness of the HPG axis. Wild-caught birds were either ad libitum fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma testosterone response to GnRH challenge. Energy deficiency did, however, decrease the plasma testosterone responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting of a decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity.

Negative energy balance in a male songbird, the Abert's Towhee, constrains the testicular endocrine response to luteinizing hormone stimulation.

Energy deficiency can suppress reproductive functions in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary-gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none has investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's Towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone (T) responsiveness of the HPG axis. Wild-caught birds were either ad libitum-fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma T response to GnRH challenge. Energy deficiency did, however, decrease the plasma T responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting in decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity.