Androgen and glucocorticoid production in the male killer whale (Orcinus orca): influence of age, maturity, and environmental factors

Abstract

SUMMARYCirculating concentrations of testosterone and its precursor androstenedione, as well as dehydroepiandrosterone (DHEA) and the adrenal hormones cortisol and corticosterone were measured at monthly intervals in 14 male killer whales (Orcinus orca) aged 0.8-38 years. Analyses were performed for examination of the relationships of age, sexual maturation status (STATUS), season, and environmental temperature (monthly air ambient temperature, A-TEMP) with hormone production using a mixed effects linear regression model with animal ID as the random variable. Hormone profiles, derived from enzyme immunoassay procedures validated herein, established that simultaneous up-regulation of androstenedione and testosterone production occurs at puberty, when males are aged 8-12 years. Androgen (testosterone and androstenedione) production in pubertal and adult males was influenced by season, with highest (p < 0.01) concentrations observed in spring and summer months. A significant effect of STATUS and season on DHEA production was also documented, with higher (p < 0.05) concentrations in pubertal and adult males compared to juvenile males, and higher (p < 0.05) concentrations in the months of summer than the fall. Among adult males (≥13 years), those classified as aged (≥31 years) had concentrations of testosterone and both glucocorticoids that were lower (p < 0.05), and those of androstenedione that were higher (p < 0.05) than their younger counterparts. The cortisol:corticosterone ratio for adult males was 7 : 1, and both glucocorticoids were affected by STATUS (p < 0.05), but not season or A-TEMP. Results of this research enhance our understanding of reproductive and adrenocortical function in healthy male killer whales and provide baseline profiles of hormone production for use in the species' health assessment and conservation.

Effect of age, sex, and season on the variation in blood analytes of a clinically normal ex situ population of killer whales (Orcinus orca)

“…These exclusions appeared to have eliminated sex biases, thereby supporting that sex differences observed in previous studies could be attributed to pregnancy, pseudopregnancy, and early lactation . Since we did not eliminate females who were experiencing regular estrous cycles or males who had seasonal peaks of serum testosterone, we have also provided evidence that these physiologic events do not result in hematologic and serum biochemical differences between male and female killer whales as has been proposed …”

“…Some of the annual circadian patterns, such as food availability, changes in diving patterns, body condition, and water temperature, to which seasonal variation was attributed in free‐ranging cetaceans, are eliminated in this killer whale population. Instead, the high degree of seasonal variation that we detected with high confidence in the dataset could largely be due to diffuse seasonal cycling patterns and the seasonality of sex hormones in killer whales . Alternatively, photoperiods and subsequent endocrine fluctuations that are not related to reproduction, could be the primary drivers.…”

Chronic stress from fishing gear entanglement is recorded in baleen from a bowhead whale (Balaena mysticetus)

“…, O'Brien et al . ), and the results of the current study indicate a primary role for cortisol in the adrenal response to this chronic entanglement. Serum GCs from a physically debilitated, live‐stranded North Atlantic right whale had much higher concentrations of cortisol compared to corticosterone, suggesting that a cortisol response was also predominant in this highly stressed right whale (Rolland et al .…”

Circulating and Excreted Corticosteroids and Metabolites, Hematological, and Serum Chemistry Parameters in the Killer Whale (Orcinus orca) Before and After a Stress Response

“…A comparison of two GC antibodies and assay systems in fecal extracts of several carnivore species revealed that the cortisol antibody was preferable for some species, while the corticosterone antibody was preferable in others (Young et al, 2004). Both a cortisol and a corticosterone enzyme immunoassay (EIA) have been validated for use with killer whale sera (O'Brien et al, 2017;Robeck et al, 2017) but their suitability for measuring fecal glucocorticoid metabolites (FGCMs) has yet to be determined. Furthermore, antibody cross-reactivity with other hormone metabolites (i.e., lack of antibody specificity) is a potential concern.…”

“…Furthermore, structural similarities of fecal androgen metabolites to FGCMs could affect binding to the GC antibody, resulting in inaccurate GC measurements (Ganswindt et al, 2003). In view of the elevated androgen concentrations documented during late pregnancy in the killer whale (Robeck et al, 2017;Legacki et al, 2019), as well as seasonal and sexual maturity influences on androgens in males (O'Brien et al, 2017), the choice of GC antibody is crucial for understanding stress response dynamics in this species. High performance liquid chromatography (HPLC) allows for the separation and characterization of androgen and GC metabolites, and the assay systems are then used with the HPLC fractions to check for any cross-reactivity with the antibodies.…”