Steroid hormones in Pacific walrus bones collected over three millennia indicate physiological responses to changes in estimated population size and the environment

Abstract

The Pacific walrus (Odobenus rosmarus divergens) is an iconic Arctic marine mammal and an important resource to many Alaska Natives. A decrease in sea ice habitat and unknown population numbers has led to concern of the long-term future health of the walrus population. There is currently no clear understanding of how walrus physiology might be affected by a changing Arctic ecosystem. In this study, steroid hormone concentrations (progesterone, testosterone, cortisol and estradiol) were analysed in walrus bones collected during archaeological [3585–200 calendar years before present (BP)], historical [1880–2006 common era (CE)] and modern (2014–2016 CE) time periods, representing ~ 3651 years, to track changes in reproductive activity and cortisol concentrations (biomarker of stress) over time. Our results show that modern walrus samples have similar cortisol concentrations (median = 43.97 ± standard deviation 904.38 ng/g lipid) to archaeological walruses (38.94 ± 296.17 ng/g lipid, P = 0.75). Cortisol concentrations were weakly correlated with a 15-year average September Chukchi Sea ice cover (P = 0.002, 0.02, r2 = 0.09, 0.04, for females and males, respectively), indicating a possible physiological resiliency to sea ice recession in the Arctic. All steroid hormones had significant negative correlations with mean walrus population estimates from 1960 to 2016 (P < 0.001). Progesterone in females and testosterone in males exhibited significant correlations with average September Chukchi Sea ice cover for years 1880–2016 (P < 0.001 for both, r2 = 0.34, 0.22, respectively). Modern walruses had significantly lower (P = < 0.001) reproductive hormone concentrations compared with historic walruses during times of rapid population increase, indicative of a population possibly at carrying capacity. This is the first study to apply bone as a tool to monitor long-term changes in hormones that may be associated with changes in walrus population size and sea ice cover.

Lifetime hormone profiles for a long-lived teleost: opercula reveal novel estimates of age-specific reproductive parameters and stress trends in yelloweye rockfish (Sebastes ruberrimus)

“…While biologically relevant patterns of trace elements and stable isotopes have been measured in opercula of teleost species (Tzadik et al 2017), no lipophilic steroid hormones measurements, to date, have been reported from these hard parts. However, teleost bones contain considerable amount of lipid (Toppe et al 2007) and lipophilic steroid hormones (progesterone, testosterone, estradiol, and cortisol) have been measured in marine mammal cortical bone buried for thousands of years, lending evidence that bone is a long-term reservoir of biologically relevant steroid hormones (Charapata et al 2018(Charapata et al , 2021. Potentially, lipophilic steroid hormones are deposited in annual growth increments of teleost opercula through time, similar to findings of various mammalian vertebrates (Trumble et al 2013).…”

“…To correct these errors, samples estimated at >100 % lipid were assigned a standardized 90% lipid value, while total error in measurement (negative lipid mass extracted) was assigned the mean percent lipid from all other growth increments for each individual fish. These lipid correction factors (90% and mean percent lipid) were multiplied to individual GI masses to retain a relative individualized lipid mass per sample (Charapata et al 2018(Charapata et al , 2021. Samples were reconstituted with 1.25 mL of methanol, transferred into another 2 mL microvial, and stored at -80 C until steroid hormone could be measured.…”

Female Pacific walruses (Odobenus rosmarus divergens) show greater partitioning of sea ice organic carbon than males: Evidence from ice algae trophic markers

“…The loss of sea ice could impact the females’ ability to successfully reproduce and provide adequate nutrition for their offspring [ 12 , 36 , 86 ]. Stress and reproductive biomarkers analyzed from recent and archaeological Pacific walrus bones suggested potential resilience to declining sea ice [ 91 ], but ongoing monitoring of this species is necessary to track their response to unprecedented change.…”