The High Cost of Reproduction in Sea Otters Necessitates Unique Physiological Adaptations

Resting Superimposed on inherently high basal metabolic demands, the additional energetic requirements of reproduction can push female sea otters beyond physiological limits. Indeed, the resulting energy imbalance contributes to disproportionately high rates of mortality at the end of lactation in this species. To examine and quantify metabolic changes associated with reproduction, we measured the resting metabolic rate (RMR) of a female sea otter across gestation, lactation and non-reproductive periods. Concurrently, measurements were made on a non-breeding control female. Our results suggest that RMR declines during gestation. Conversely, RMR increases during lactation, reaches a peak at 3–4 months postpartum, and remains elevated until weaning. Combining these direct measurements with published data, we found the cost of pup rearing to be significantly higher than previously estimated. High baseline energy demands and limited energy reserves, combined with significant lactation and pup rearing costs, appear to necessitate metabolic and thermal lability during key reproductive stages

Comparative Health Assessments of Alaskan Ice Seals

Bearded (Erignathus barbatus), ringed (Pusa hispida), spotted (Phoca largha), and ribbon (Histriophoca fasciata) seals rely on seasonal sea-ice in Arctic and sub-Arctic regions. Many aspects of the biology and physiology of these seals are poorly known, and species-typical health parameters are not available for all species. Such information has proven difficult to obtain due to the challenges of studying Arctic seals in the wild and their minimal historic representation in aquaria. Here, we combine diagnostic information gathered between 2000 and 2017 from free-ranging seals, seals in short-term rehabilitation, and seals living in long-term human care to evaluate and compare key health parameters. For individuals in apparent good health, hematology, and blood chemistry values are reported by the source group for 10 bearded, 13 ringed, 73 spotted, and 81 ribbon seals from Alaskan waters. For a smaller set of individuals handled during veterinary or necropsy procedures, the presence of parasites and pathogens is described, as well as exposure to a variety of infectious diseases known to affect marine mammals and/or humans, with positive titers observed for Brucella, Leptospira, avian influenza, herpesvirus PhHV-1, and morbillivirus. These data provide initial baseline parameters for hematology, serum chemistries, and other species-level indicators of health that can be used to assess the condition of individual seals, inform monitoring and management efforts, and guide directed research efforts for Alaskan populations of ice-associated seals

Comparative and Cumulative Energetic Costs of Odontocete Responses to Anthropogenic Disturbance

Odontocetes respond to vessels and anthropogenic noise by modifying vocal behavior, surface active behaviors, dive patterns, swim speed, direction of travel, and activity budgets. Exposure scenarios and behavioral responses vary across odontocetes. A literature review was conducted to determine relevant sources of disturbance and associated behavioral responses for several odontocete species (bottlenose dolphin, killer whale, harbor porpoise, and beaked whales). The energetic costs of species-specific responses to anthropogenic disturbance were then estimated. The energetic impact varies across species and scenarios as well as by behavioral responses. Overall, the cumulative energetic cost of ephemeral behavioral responses (e.g., performing surface active behaviors, modifying acoustic signals) and modifying swim speeds and activity budgets likely increases daily energy expenditure by ≤4%. In contrast, the reduction in foraging activity in the presence of vessels and/or exposure to sonar has the potential to significantly reduce individuals’ daily energy acquisition. Indeed, across all odontocete species, decreased energy acquisition as a result of reduced foraging undoubtedly has a larger impact on individuals than the increased energy expenditure associated with behavioral modification. This work provides a powerful tool to investigate the biological significance of multiple behavioral responses that are likely to occur in response to anthropogenic disturbance

Energetic Demands of Immature Sea Otters From Birth to Weaning: Implications for Maternal Costs, Reproductive Behavior and Population-Level Trends

Sea otters (Enhydra lutris) have the highest mass-specific metabolic rate of any marine mammal, which is superimposed on the inherently high costs of reproduction and lactation in adult females. These combined energetic demands have been implicated in the poor body condition and increased mortality of female sea otters nearing the end of lactation along the central California coast. However, the cost of lactation is unknown and currently cannot be directly measured for this marine species in the wild. Here, we quantified the energetic demands of immature sea otters across five developmental stages as a means of assessing the underlying energetic challenges associated with pup rearing that may contribute to poor maternal condition. Activity-specific metabolic rates, daily activity budgets and field metabolic rates (FMR) were determined for each developmental stage. Mean FMR of pre-molt pups was 2.29±0.81 MJ day−1 and increased to 6.16±2.46 and 7.41±3.17 MJ day−1 in post-molt pups and dependent immature animals, respectively. Consequently, daily energy demands of adult females increase 17% by 3 weeks postpartum and continue increasing to 96% above pre-pregnancy levels by the average age of weaning. Our results suggest that the energetics of pup rearing superimposed on small body size, marine living and limited on-board energetic reserves conspire to make female sea otters exceptionally vulnerable to energetic shortfalls. By controlling individual fitness, maternal behavior and pup provisioning strategies, this underlying metabolic challenge appears to be a major factor influencing current population trends in southern sea otters (Enhydra lutris nereis)

Exercise at Depth Alters Bradycardia and Incidence of Cardiac Anomalies in Deep-Diving Marine Mammals

Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to 4200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in 473% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic ‘dive reflex’ in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances

Ontogeny Of Energetic Demand And Diving Ability In The Southern Sea Otter (Enhydra Lutris Nereis) And Implications On Diving And Foraging Behavior

The integration of physiological and behavioral studies can yield valuable information important to the conservation and management of imperiled species. In the following chapters, I examine a suite of physiological characteristics and behavioral attributes of southern sea otters (Enhydra lutris nereis) across a variety of life stages and discuss resulting population level consequences in this threatened species. In my first data chapter (Chapter 2), I use open-flow respirometry to determine age- and activity- specific metabolic rates of immature southern sea otters throughout ontogeny. These data are then combined with activity budgets of wild sea otters to determine the energetic cost of pup rearing for adult females. In Chapter 3, I determine age-specific oxygen storage capacity and diving abilities of sea otters from birth through adulthood. Finally, in Chapter 4, I examine the foraging behavior of sea otters off the coast of central California. I found that sea otter pups have elevated mass-specific metabolic rates in comparison to adult conspecifics, which are highest for molting pups and begin to approach adult levels around the average age of weaning (6 mo.). In addition, immature sea otters have limited blood and muscle oxygen stores throughout dependency, which result in a limited capacity for diving and high dependence on adult females throughout lactation. The high energetic demands of pups result in elevated field metabolic rates (FMR) for lactating females. Female FMR is increased 17% by three weeks postpartum and continues to increase throughout lactation. By the average age of weaning female FMR is increased 96% above pre-pregnancy levels. These heightened energetic demands are reflected in the foraging behavior of wild sea otters. Adult females appear behaviorally constrained by dependent young during an already energetically costly life stage. Both physiological and behavioral data suggest that it takes sea otters approximately two years to develop comparable diving abilities to adults; however, individuals at this stage are likely inefficient foragers when compared to adults. Together these data indicate that late-lactation and the first years post-weaning are the most physiologically challenging life stages for sea otters and that these groups are likely the most sensitive to disturbance and resource limitation. The high energetic demands of dependent pups influence body condition, parental provisioning strategies, and life history decisions in adult females. In addition, high energy demands, physiological limitations, and behavioral naïveté make maintaining positive energy balance difficult for juvenile and sub-adult sea otters. Ultimately, these chapters provide novel information regarding age-specific energy demands, physiological abilities, and foraging behavior of southern sea otters across a variety of life stages, and elucidate mechanisms underlying current population level trends

Comparative Health Assessments of Alaskan Ice Seals

Bearded (Erignathus barbatus), ringed (Pusa hispida), spotted (Phoca largha), and ribbon (Histriophoca fasciata) seals rely on seasonal sea-ice in Arctic and sub-Arctic regions. Many aspects of the biology and physiology of these seals are poorly known, and species-typical health parameters are not available for all species. Such information has proven difficult to obtain due to the challenges of studying Arctic seals in the wild and their minimal historic representation in aquaria. Here, we combine diagnostic information gathered between 2000 and 2017 from free-ranging seals, seals in short-term rehabilitation, and seals living in long-term human care to evaluate and compare key health parameters. For individuals in apparent good health, hematology, and blood chemistry values are reported by the source group for 10 bearded, 13 ringed, 73 spotted, and 81 ribbon seals from Alaskan waters. For a smaller set of individuals handled during veterinary or necropsy procedures, the presence of parasites and pathogens is described, as well as exposure to a variety of infectious diseases known to affect marine mammals and/or humans, with positive titers observed for Brucella, Leptospira, avian influenza, herpesvirus PhHV-1, and morbillivirus. These data provide initial baseline parameters for hematology, serum chemistries, and other species-level indicators of health that can be used to assess the condition of individual seals, inform monitoring and management efforts, and guide directed research efforts for Alaskan populations of ice-associated seals

Molting strategies of Arctic seals drive annual patterns in metabolism

Arctic seals, including spotted (Phoca largha), ringed (Pusa hispida) and bearded (Erignathus barbatus) seals, are directly affected by sea ice loss. These species use sea ice as a haul-out substrate for various critical functions, including their annual molt. Continued environmental warming will inevitably alter the routine behavior and overall energy budgets of Arctic seals, but it is difficult to quantify these impacts as their metabolic requirements are not well known-due in part to the difficulty of studying wild individuals. Thus, data pertaining to species-specific energy demands are urgently needed to better understand the physiological consequences of rapid environmental change. We used open-flow respirometry over a four-year period to track fine-scale, longitudinal changes in the resting metabolic rate (RMR) of four spotted seals, three ringed seals and one bearded seal trained to participate in research. Simultaneously, we collected complementary physiological and environmental data. Species-specific metabolic demands followed expected patterns based on body size, with the largest species, the bearded seal, exhibiting the highest absolute RMR (0.48 ± 0.04 L O2 min-1) and the lowest mass-specific RMR (4.10 ± 0.47 ml O2 min-1 kg-1), followed by spotted (absolute: 0.33 ± 0.07 L O2 min-1; mass-specific: 6.13 ± 0.73 ml O2 min-1 kg-1) and ringed (absolute: 0.20 ± 0.04 L O2 min-1; mass-specific: 7.01 ± 1.38 ml O2 min-1 kg-1) seals. Further, we observed clear and consistent annual patterns in RMR that related to the distinct molting strategies of each species. For species that molted over relatively short intervals-spotted (33 ± 4 days) and ringed (28 ± 6 days) seals-metabolic demands increased markedly in association with molt. In contrast, the bearded seal exhibited a prolonged molting strategy (119 ± 2 days), which appeared to limit the overall cost of molting as indicated by a relatively stable annual RMR. These findings highlight energetic trade-offs associated with different molting strategies and provide quantitative data that can be used to assess species-specific vulnerabilities to changing conditions