Variation in Faecal Testosterone Levels in Male Gray Whales on a Foraging Ground Relative to Maturity and Timing

Overview

Journal Conserv Physiol

Date 2025 Jan 21

PMID 39834348

Authors

A Fernandez Ajo

C L Buck

K E Hunt

E Pirotta

L New

D Dillon

K C Bierlich

L Hildebrand

C N Bird

L G Torres

Affiliations

Soon will be listed here.

Abstract

Understanding wildlife reproductive seasonality is crucial for effective management and long-term monitoring of species. This study investigates the seasonal variability of testosterone in male Pacific Coast Feeding Group (PCFG) gray whales, using an eight-year dataset (2016-2023) of individual sightings, drone-based photogrammetry and endocrine analysis of faecal samples. We analyzed the relationship between faecal testosterone levels and total body length (TL), body condition (body area index, BAI), sexual maturity and day of the year using generalized additive mixed models. Our findings reveal a significant increase in faecal testosterone levels in mature males (MM) towards the end of the foraging season. This increase was not observed in JM, highlighting age-dependent development of sexual characteristics. No significant relationship was found between testosterone levels and TL. Additionally, BAI was not significantly associated with testosterone levels. Our results suggest that the increasing testosterone levels in MM gray whales may indicate preparation for mating before the southbound migration. These findings provide valuable insights into the reproductive biology of PCFG gray whales and underscore the importance of non-invasive faecal sampling for studying reproductive seasonality in large whales. Our approach not only provides further insights into the seasonality of male reproduction for the PCFG gray whales but also offers tools to enhance the understanding of male reproduction in baleen whales broadly with non-invasive approaches.

References

Madliger C, Love O, Hultine K, Cooke S . The conservation physiology toolbox: status and opportunities. Conserv Physiol. 2018; 6(1):coy029. PMC: 6007632. DOI: 10.1093/conphys/coy029. View

Hunt K, Rolland R, Kraus S, Wasser S . Analysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis). Gen Comp Endocrinol. 2006; 148(2):260-72. DOI: 10.1016/j.ygcen.2006.03.012. View

Corkeron P, Rolland R, Hunt K, Kraus S . A right whale pootree: classification trees of faecal hormones identify reproductive states in North Atlantic right whales (). Conserv Physiol. 2017; 5(1):cox006. PMC: 5570057. DOI: 10.1093/conphys/cox006. View

Stewart J, Durban J, Knowlton A, Lynn M, Fearnbach H, Barbaro J . Decreasing body lengths in North Atlantic right whales. Curr Biol. 2021; 31(14):3174-3179.e3. DOI: 10.1016/j.cub.2021.04.067. View

Carone E, Pardo M, Atkinson S, Mashburn K, Perez-Puig H, Enriquez-Paredes L . Sex steroid hormones and behavior reveal seasonal reproduction in a resident fin whale population. Conserv Physiol. 2019; 7(1):coz059. PMC: 6822541. DOI: 10.1093/conphys/coz059. View

Fernandez Ajo A, Pirotta E, Bierlich K, Hildebrand L, Bird C, Hunt K . Assessment of a non-invasive approach to pregnancy diagnosis in gray whales through drone-based photogrammetry and faecal hormone analysis. R Soc Open Sci. 2023; 10(7):230452. PMC: 10354484. DOI: 10.1098/rsos.230452. View

Palme R, Rettenbacher S, Touma C, El-Bahr S, Mostl E . Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Ann N Y Acad Sci. 2005; 1040:162-71. DOI: 10.1196/annals.1327.021. View

Richter M, Barnes B, OReilly K, Fenn A, Buck C . The influence of androgens on hibernation phenology of free-living male arctic ground squirrels. Horm Behav. 2016; 89:92-97. PMC: 5359051. DOI: 10.1016/j.yhbeh.2016.12.007. View

Cates K, Atkinson S, Gabriele C, Pack A, Straley J, Yin S . Testosterone trends within and across seasons in male humpback whales (Megaptera novaeangliae) from Hawaii and Alaska. Gen Comp Endocrinol. 2019; 279:164-173. DOI: 10.1016/j.ygcen.2019.03.013. View

10.

Palme R . Non-invasive measurement of glucocorticoids: Advances and problems. Physiol Behav. 2018; 199:229-243. DOI: 10.1016/j.physbeh.2018.11.021. View

11.

Melica V, Atkinson S, Calambokidis J, Lang A, Scordino J, Mueter F . Application of endocrine biomarkers to update information on reproductive physiology in gray whale (Eschrichtius robustus). PLoS One. 2021; 16(8):e0255368. PMC: 8330940. DOI: 10.1371/journal.pone.0255368. View

12.

Funasaka N, Yoshioka M, Ishibashi T, Tatsukawa T, Shindo H, Takada K . Seasonal changes in circulating gonadal steroid levels and physiological evidence for the presence of intrinsic circannual reproductive cycles in captive finless porpoises Neophocaena asiaeorientalis from the western Inland Sea, Japan. J Reprod Dev. 2018; 64(2):145-152. PMC: 5902902. DOI: 10.1262/jrd.2017-087. View

13.

Hunt K, Robbins J, Buck C, Berube M, Rolland R . Evaluation of fecal hormones for noninvasive research on reproduction and stress in humpback whales (Megaptera novaeangliae). Gen Comp Endocrinol. 2019; 280:24-34. DOI: 10.1016/j.ygcen.2019.04.004. View

14.

Hunt K, Buck C, Ferguson S, Fernandez Ajo A, Heide-Jorgensen M, Matthews C . Male Bowhead Whale Reproductive Histories Inferred from Baleen Testosterone and Stable Isotopes. Integr Org Biol. 2022; 4(1):obac014. PMC: 9125798. DOI: 10.1093/iob/obac014. View

15.

Richard J, Robeck T, Osborn S, Naples L, McDermott A, Laforge R . Testosterone and progesterone concentrations in blow samples are biologically relevant in belugas (Delphinapterus leucas). Gen Comp Endocrinol. 2016; 246:183-193. DOI: 10.1016/j.ygcen.2016.12.006. View

16.

Beehner J, Gesquiere L, Seyfarth R, Cheney D, Alberts S, Altmann J . Testosterone related to age and life-history stages in male baboons and geladas. Horm Behav. 2009; 56(4):472-80. PMC: 3630238. DOI: 10.1016/j.yhbeh.2009.08.005. View

17.

Pirotta E, Fernandez Ajo A, Bierlich K, Bird C, Buck C, Haver S . Assessing variation in faecal glucocorticoid concentrations in gray whales exposed to anthropogenic stressors. Conserv Physiol. 2023; 11(1):coad082. PMC: 10660368. DOI: 10.1093/conphys/coad082. View

18.

Husak J, Fuxjager M, Johnson M, Vitousek M, Donald J, Francis C . Life history and environment predict variation in testosterone across vertebrates. Evolution. 2021; 75(5):1003-1010. DOI: 10.1111/evo.14216. View

19.

Hunt K, Lysiak N, Matthews C, Lowe C, Fernandez Ajo A, Dillon D . Multi-year patterns in testosterone, cortisol and corticosterone in baleen from adult males of three whale species. Conserv Physiol. 2018; 6(1):coy049. PMC: 6148970. DOI: 10.1093/conphys/coy049. View

20.

Fernandez Ajo A, Hunt K, Dillon D, Uhart M, Sironi M, Rowntree V . Optimizing hormone extraction protocols for whale baleen: Tackling questions of solvent:sample ratio and variation. Gen Comp Endocrinol. 2021; 315:113828. DOI: 10.1016/j.ygcen.2021.113828. View