Demographic risk assessment for a harvested species threatened by climate change: polar bears in the Chukchi Sea.

Climate change threatens global biodiversity. Many species vulnerable to climate change are important to humans for nutritional, cultural, and economic reasons. Polar bears Ursus maritimus are threatened by sea-ice loss and represent a subsistence resource for Indigenous people. We applied a novel population modeling-management framework that is based on species life history and accounts for habitat loss to evaluate subsistence harvest for the Chukchi Sea (CS) polar bear subpopulation. Harvest strategies followed a state-dependent approach under which new data were used to update the harvest on a predetermined management interval. We found that a harvest strategy with a starting total harvest rate of 2.7% (˜85 bears/yr at current abundance), a 2:1 male-to-female ratio, and a 10-yr management interval would likely maintain subpopulation abundance above maximum net productivity level for the next 35 yr (approximately three polar bear generations), our primary criterion for sustainability. Plausible bounds on starting total harvest rate were 1.7-3.9%, where the range reflects uncertainty due to sampling variation, environmental variation, model selection, and differing levels of risk tolerance. The risk of undesired demographic outcomes (e.g., overharvest) was positively related to harvest rate, management interval, and projected declines in environmental carrying capacity; and negatively related to precision in population data. Results reflect several lines of evidence that the CS subpopulation has been productive in recent years, although it is uncertain how long this will last as sea-ice loss continues. Our methods provide a template for balancing trade-offs among protection, use, research investment, and other factors. Demographic risk assessment and state-dependent management will become increasingly important for harvested species, like polar bears, that exhibit spatiotemporal variation in their response to climate change.

Using claws to compare reproduction, stress and diet of female bearded and ringed seals in the Bering and Chukchi seas, Alaska, between 1953-1968 and 1998-2014.

Rapid climate warming is decreasing sea ice thickness, extent and duration. Marine mammals such as bearded (Erignathus barbatus) and ringed (Pusa hispida) seals, which use sea ice for pupping, molting and resting, may be negatively affected. Claws from bearded and ringed seals store up to 14 and 12 years of sequential analyte data, respectively. These data can be used to compare reproduction, stress and diet across decades. In this study, we compare progesterone, cortisol and carbon and nitrogen stable isotopes in female bearded and ringed seals during 1953-1968 (pre-1968, a period prior to sea ice decline) to 1998-2014 (post-1998, a period during sea ice decline). When comparing these periods, bearded seals had statistically higher cortisol concentrations post-1998, and for both species δ13C was more negative post-1998, while progesterone and δ15N did not change. There was a positive relationship between progesterone and cortisol Z-scores for both species, except for ringed seals post-1998. There was a negative relationship between cortisol Z-scores and δ13C for bearded seals evident in post-1998 indicating that higher cortisol Z-scores are associated with more negative δ13C in bearded seals in recent years. This negative relationship between cortisol and δ13C in bearded seals suggests a shift to higher prey diversity, possibly due to changes in sea ice in the Pacific Arctic evident post 1998. Progesterone Z-scores corresponded to expected differences among non-pregnant, unimplanted, implanted and post-partum individuals. Using these data, pregnancy history was determined for reproductive years for each individual female sampled, which could allow for yearly pregnancy rates to be calculated given a large enough representative sample of the population. These results combine decades of observational studies with hormones and stable isotopes to infer changes in reproduction, stress and diet, as well as the connection between these life history parameters.

Validation of a novel method to create temporal records of hormone concentrations from the claws of ringed and bearded seals.

Ringed (Pusa hispida) and bearded seals (Erignathus barbatus) inhabit vast and often remote areas in the Arctic, making it difficult to obtain long-term physiological information concerning health and reproduction. These seals are experiencing climate-driven changes in their habitat that could result in physiological stress. Chronic physiological stress can lead to immunosuppression, decreased reproduction and decreased growth. Recently, keratin has become a popular matrix to measure steroid hormones, such as stress-related cortisol and reproduction-related progesterone. We developed and validated methods to extract cortisol and progesterone from the claws of adult female ringed (n = 20) and bearded (n = 3) seals using enzyme immunosorbent assays. As ringed and bearded seal claws grow, a pair of dark- and light-colored bands of keratin is deposited annually providing a guide for sampling. Two processing methods were evaluated, removal of claw material with a grinding bit or grinding followed by mechanical pulverization (102 paired samples from six claws, two each from three seals). Adding the mechanical pulverization step resulted in a 1.5-fold increase in hormone extraction. Progesterone from the proximal claw band was evaluated to biologically validate claw material as a measure of pregnancy in ringed seals (n = 14). Claws from pregnant seals had significantly higher claw progesterone concentrations than from non-pregnant seals. This suggests that the elevated progesterone associated with gestation was reflected in the claws, and that the most proximal claw band was indicative of pregnancy status at time of death. Thus, although the sample size was low and the collection dates unbalanced, this study demonstrates the potential to use claws to examine an extended time series (up to 12 yrs) of cortisol and progesterone concentrations in ringed and bearded seal claws.

Characterizing estrus by trans-abdominal ultrasounds, fecal estrone-3-glucuronide, and vaginal cytology in the Steller sea lion (Eumetopias jubatus).

The ability to monitor the estrus cycle in wild and captive marine species is important for identifying reproductive failures, ensuring a successful breeding program, and monitoring animal welfare. Minimally invasive sampling methods to monitor estrus in captive populations have been developed, but results suggest these tools can be species-specific in their precision and accuracy. Therefore, the minimally invasive sampling methods of trans-abdominal ultrasounds, a fecal steroid analysis (estrone-3-glucuronide, E1G), and vaginal cytology, were evaluated for their efficacy to characterize and monitor estrus in a captive breeding population of Steller sea lions (Eumetopias jubatus). Three adult females were sampled over five breeding seasons, resulting in six estrus profiles characterized by trans-abdominal ultrasounds, five by fecal E1G, and four by vaginal cytology. Animals were trained to allow trans-abdominal ultrasounds, fecal samples, and vaginal swabs to be collected approximately daily. Of the 76 trans-abdominal ultrasound sessions attempted, 8 successfully visualized both ovaries. From these scans, the chronology of ovarian changes during proestrus and estrus was estimated. The time from the detection of developing follicles to the identification of a dominate follicle occurred in 2-5 days and a corpus hemorrhagicum formed approximately 4 days later. However, because visualization of the ovaries was prevented by the gastrointestinal system in 88% of scans, this tool was overall unreliable for monitoring changes associated with estrus. To detect fine scale physiological changes associated with estrus, we analyzed changes in fecal E1G (n = 62) and vaginal cytology (n = 157) 15 days before and after each female's single copulation event (Day = 0). Changes in fecal E1G had the highest accuracy at detecting Day = 0. Fecal E1G increased leading up to estrus, peaked at Day = 0, and then declined. Although we did observe the characteristic increase in superficial cells associated with impending estrus, the type of cell which peaked closest to Day = 0 was intermediate. The uncertainty around the peak in intermediate cells, indicating estrus, was greater than the uncertainty associated with detecting estrus from fecal E1G. Collectively, these results suggest that changes in fecal E1G and vaginal cytology are viable tools to detect estrus in Steller sea lions, but require daily sampling to detect gradual changes, limiting their applicability to studies of wild populations.

Serum estradiol and progesterone profiles during estrus, pseudopregnancy, and active gestation in Steller sea lions.

While the proximate driver behind the decline of the Western stock of Steller sea lions (Eumetopias jubatus, >80% since 1970s) is likely multifactorial, the population reduction may have been powered by a decrease in fecundity. A harvest of Steller sea lions in the 1970s and 80s revealed a 30% reduction in the proportion of pregnant females from early (October-November) to late gestation (April-May). Identification and quantification of these reproductive failures are difficult when we lack species-specific data on endocrinology associated with discrete stages of the reproductive cycle (i.e., estrus, implantation, and gestation). We tracked changes in serum estradiol and progesterone in three adult female Steller sea lions from 2011 to 2015. In all years and most females, a discrete increase in estradiol was observed during the breeding season (June-August), indicative of estrus. Estradiol concentrations from October to May in a pregnant female compared to her corresponding values when non-pregnant did not consistently differ through gestation. An elevation in progesterone was observed in all females and all years beginning approximately in June and lasting through November. This likely results from progesterone production by the corpus luteum in both pregnant and pseudopregnant females. Serum progesterone shows promise as a diagnostic tool to identify pregnancy during months 3-5 (December-February) of the 8-month active gestation following embryonic implantation. This study provides ranges of key hormones during estrus, embryonic diapause/pseudopregnancy, and gestation in pregnant and non-pregnant females for studying reproduction in Steller sea lions.

Lateralized swim positions are conserved across environments for beluga (Delphinapterus leucas) mother-calf pairs.

Research with wild belugas has indicated that, during mother-calf swims, calves spend more time on their mothers' right side, which enables the calves to maintain visual contact with their mothers using their left eye. This bias may facilitate processing of social information by the right hemisphere, much like human and non-human primates and other animals. The current study explored the social laterality of the Cook Inlet, AK beluga population in comparison to a beluga population in managed care. As expected, the results indicated that the calves spent more time on the mothers' right side than the left for both populations. We also examined the developmental trend for the belugas in managed care and found that the calves generally preferred to swim on their mother's right side across most months, although there was an inversion during the third quarter when a left-side preference appeared. Individual differences were present. The results corroborate previous research conducted with two wild beluga populations from the White Sea and from the Sea of Okhotsk in which a left-eye bias was displayed by calves when swimming with their mothers. In conclusion, a preference for a lateralized swim position appears to be conserved across wild and managed care settings, and this lateralized swim position may facilitate the processing of social information or familiar stimuli for the calves.

The diving paradox: new insights into the role of the dive response in air-breathing vertebrates.

When aquatic reptiles, birds and mammals submerge, they typically exhibit a dive response in which breathing ceases, heart rate slows, and blood flow to peripheral tissues is reduced. The profound dive response that occurs during forced submergence sequesters blood oxygen for the brain and heart while allowing peripheral tissues to become anaerobic, thus protecting the animal from immediate asphyxiation. However, the decrease in peripheral blood flow is in direct conflict with the exercise response necessary for supporting muscle metabolism during submerged swimming. In free diving animals, a dive response still occurs, but it is less intense than during forced submergence, and whole-body metabolism remains aerobic. If blood oxygen is not sequestered for brain and heart metabolism during normal diving, then what is the purpose of the dive response? Here, we show that its primary role may be to regulate the degree of hypoxia in skeletal muscle so that blood and muscle oxygen stores can be efficiently used. Paradoxically, the muscles of diving vertebrates must become hypoxic to maximize aerobic dive duration. At the same time, morphological and enzymatic adaptations enhance intracellular oxygen diffusion at low partial pressures of oxygen. Optimizing the use of blood and muscle oxygen stores allows aquatic, air-breathing vertebrates to exercise for prolonged periods while holding their breath.

Adaptations to diving hypoxia in the heart, kidneys and splanchnic organs of harbor seals (Phoca vitulina).

Pinnipeds (seals and sea lions) have an elevated mitochondrial volume density [VV(mt)] and elevated citrate synthase (CS) and beta-hydroxyacyl-CoA dehydrogenase (HOAD) activities in their swimming muscles to maintain an aerobic, fat-based metabolism during diving. The goal of this study was to determine whether the heart, kidneys and splanchnic organs have an elevated VV(mt) and CS and HOAD activities as parallel adaptations for sustaining aerobic metabolism and normal function during hypoxia in harbor seals (Phoca vitulina). Samples of heart, liver, kidney, stomach and small intestine were taken from 10 freshly killed harbor seals and fixed in glutaraldehyde for transmission electron microscopy or frozen in liquid nitrogen for enzymatic analysis. Samples from dogs and rats were used for comparison. Within the harbor seal, the liver and stomach had the highest VV(mt). The liver also had the highest CS activity. The kidneys and heart had the highest HOAD activities, and the liver and heart had the highest lactate dehydrogenase (LDH) activities. Mitochondrial volume densities scaled to tissue-specific resting metabolic rate [VV(mt)/RMR] in the heart, liver, kidneys, stomach and small intestine of harbor seals were elevated (range 1.2-6.6x) when compared with those in the dog and/or rat. In addition, HOAD activity scaled to tissue-specific RMR in the heart and liver of harbor seals was elevated compared with that in the dog and rat (3.2x and 6.2x in the heart and 8.5x and 5.5x in the liver, respectively). These data suggest that organs such as the liver, kidneys and stomach possess a heightened ability for aerobic, fat-based metabolism during hypoxia associated with routine diving. However, a heightened LDH activity in the heart and liver indicates an adaptation for the anaerobic production of ATP on dives that exceed the animal's aerobic dive limit. Hence, the heart, liver, kidneys and gastrointestinal organs of harbor seals exhibit adaptations that promote an aerobic, fat-based metabolism under hypoxic conditions but can provide ATP anaerobically if required.