Effects of ontogeny and oiling on the thermal function of southern sea otter (Enhydra lutris nereis) fur.

During the evolution of most marine mammals, fur as an insulator has been replaced with more buoyant, energy storing and streamlining blubber. By contrast, the sea otter (Enhydra lutris) relies on insulation from its dense, air-trapping pelage, which differs morphologically between natal and adult stages. In this study, we investigated the ontogenetic changes in thermal function of southern sea otter (Enhydra lutris nereis) pelts in air, in water, and when saturated with crude oil. Pelt thermal conductivity, thickness, and thermal resistance were measured for six age classes: neonate (<1 month), small pup (1-2 months), large pup (3-5 months), juvenile (6 months-1 year), subadult (1-3 years), and adult (4-9 years). Thermal conductivity was significantly higher for pelts in air than in water, with oiled pelts exhibiting the highest values (P < 0.001). Oiled pelts had the lowest thermal resistance, which suggests that regardless of age, all sea otters are vulnerable to the effects of oiling (P < 0.001). To scale up our laboratory findings, we used a volume-specific geometric model of conductive heat transfer for a simplified sea otter body, representing all tested age classes and treatments. Neonates, small pups, and large pups are more vulnerable to the effects of oiling compared with older age classes (P < 0.0001) due to a higher surface area-to-volume ratio. These results are consistent with the known thermal conductance values for adult sea otter pelts, yet this is the first time such thermal differences have been demonstrated in young otters. Overall, body size and age play a more important role in the thermal abilities of sea otters than previously thought.

Ontogenetic changes in southern sea otter (Enhydra lutris nereis) fur morphology.

Many animals exhibit morphological changes across ontogeny associated with adaptations to their environment. Sea otters (Enhydra lutris) have the densest fur of any animal, which is composed of guard hairs, intermediate hairs, and underhairs. Sea otters live in cold water environments, and their fur traps a layer of air to remain properly insulated, due to morphological adaptations that allow the hairs to trap air when submerged. When a sea otter is born, it has a natal pelage which it will eventually molt and replace with a pelt resembling the adult pelage. Past studies have investigated the morphology and hair density of adult sea otter fur, but these characteristics have not been measured for other age classes, including for the natal pelage. This study quantified ontogenetic changes in hair morphology of southern sea otter (E. lutris nereis) pelts. We measured guard hair length and circularity, shape of cuticular scales on guard hairs and underhairs, and overall hair density for sea otter pelts across six age classes: neonate (<1 month), small pup (1-2 months), large pup (3-5 months), juvenile (6 months-1 year), subadult (1-3 years), and adult (4-9 years). Neonate and small pup pelts had significantly longer guard hairs than older age classes. Natal pelage guard hairs were similarly shaped but smaller in diameter than adult guard hairs. Hairs of the natal pelage had similar cuticular scale patterns as adult hairs, indicating the importance of this structure for the function of the fur. Natal pelage had a lower hair density than the pelage of older age classes, with the adult pelage exhibiting the highest hair density. Overall, the morphological differences between natal and adult pelage in sea otters suggest functional differences that may make sea otter pups more vulnerable to heat loss.

Maintaining control: metabolism of molting Arctic seals in water and when hauled out.

Seals haul out of water for extended periods during the annual molt, when they shed and regrow their pelage. This behavior is believed to limit heat loss to the environment given increased peripheral blood flow to support tissue regeneration. The degree to which time in water, particularly during the molt, may affect thermoregulatory costs is poorly understood. We measured the resting metabolism of three spotted seals (Phoca largha), one ringed seal (Pusa hispida) and one bearded seal (Erignathus barbatus) during and outside the molting period, while resting in water and when hauled out. Metabolic rates were elevated in spotted and ringed seals during molt, but comparable in water and air for individuals of all species, regardless of molt status. Our data indicate that elevated metabolism during molt primarily reflects the cost of tissue regeneration, while increased haul out behavior is driven by the need to maintain elevated skin temperatures to support tissue regeneration.

Metabolic trade-offs in tropical and subtropical marine mammals: unique maintenance and locomotion costs in West Indian manatees and Hawaiian monk seals.

Unlike the majority of marine mammal species, Hawaiian monk seals (Neomonachus schauinslandi) and West Indian manatees (Trichechus manatus latirostris) reside exclusively in tropical or subtropical waters. Although potentially providing an energetic benefit through reduced maintenance and thermal costs, little is known about the cascading effects that may alter energy expenditure during activity, dive responses and overall energy budgets for these warm-water species. To examine this, we used open-flow respirometry to measure the energy expended during resting and swimming in both species. We found that the average resting metabolic rates (RMRs) for both the adult monk seal (753.8±26.1 kJ h-1, mean±s.e.m.) and manatees (887.7±19.5 kJ h-1) were lower than predicted for cold-water marine mammal species of similar body mass. Despite these relatively low RMRs, both total cost per stroke and total cost of transport (COTTOT) during submerged swimming were similar to predictions for comparably sized marine mammals (adult monk seal: cost per stroke=5.0±0.2 J kg-1 stroke-1, COTTOT=1.7±0.1 J kg-1 m-1; manatees: cost per stroke=2.0±0.4 J kg-1 stroke-1, COTTOT=0.87±0.17 J kg-1 m-1). These lower maintenance costs result in less variability in adjustable metabolic costs that occur during submergence for warm-water species. However, these reduced maintenance costs do not appear to confer an advantage in overall energetic costs during activity, potentially limiting the capacity of warm-water species to respond to anthropogenic or environmental threats that require increased energy expenditure.

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.

In vivo measurement of lung volume in ringed seals: insights from biomedical imaging.

Marine mammals rely on oxygen stored in blood, muscle and lungs to support breath-hold diving and foraging at sea. Here, we used biomedical imaging to examine lung oxygen stores and other key respiratory parameters in living ringed seals (Pusa hispida). Three-dimensional models created from computed tomography (CT) images were used to quantify total lung capacity (TLC), respiratory dead space, minimum air volume and total body volume to improve assessment of lung oxygen storage capacity, scaling relationships and buoyant force estimates. The results suggest that lung oxygen stores determined in vivo are smaller than those derived from postmortem measurements. We also demonstrate that, whereas established allometric relationships hold well for most pinnipeds, these relationships consistently overestimate TLC for the smallest phocid seal. Finally, measures of total body volume reveal differences in body density and net vertical forces in the water column that influence costs associated with diving and foraging in free-ranging seals.

In Vivo Measurements of Lung Volumes in Ringed Seals: Insights from Biomedical Imaging.

Marine mammals rely on oxygen stored in blood, muscle, and lungs to support breath-hold diving and foraging at sea. Here, we used biomedical imaging to examine lung oxygen stores and other key respiratory parameters in living ringed seals (Pusa hispida). Three-dimensional models created from computed tomography (CT) images were used to quantify total lung capacity (TLC), respiratory dead space, minimum air volume, and total body volume to improve assessments of lung oxygen storage capacity, scaling relationships, and buoyant force estimates. Results suggest that lung oxygen stores determined in vivo are smaller than those derived from postmortem measurements. We also demonstrate that-while established allometric relationships hold well for most pinnipeds-these relationships consistently overestimate TLC for the smallest phocid seal. Finally, measures of total body volume reveal differences in body density and net vertical forces in the water column that influence costs associated with diving and foraging in free-ranging seals.

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 physiology of vocal musculature in two odontocetes, the bottlenose dolphin (Tursiops truncatus) and the harbor porpoise (Phocoena phocoena).

The mechanism by which odontocetes produce sound is unique among mammals. To gain insight into the physiological properties that support sound production in toothed whales, we examined myoglobin content ([Mb]), non-bicarbonate buffering capacity (ß), fiber-type profiles, and myosin heavy chain expression of vocal musculature in two odontocetes: the bottlenose dolphin (Tursiops truncatus; n = 4) and the harbor porpoise (Phocoena phocoena; n = 5). Both species use the same anatomical structures to produce sound, but differ markedly in their vocal repertoires. Tursiops produce both broadband clicks and tonal whistles, while Phocoena only produce higher frequency clicks. Specific muscles examined in this study included: (1) the nasal musculature around the phonic lips on the right (RNM) and left (LNM) sides of the head, (2) the palatopharyngeal sphincter (PPS), which surrounds the larynx and aids in pressurizing cranial air spaces, and (3) the genioglossus complex (GGC), a group of muscles positioned ventrally within the head. Overall, vocal muscles had significantly lower [Mb] and ß than locomotor muscles from the same species. The PPS was predominately composed of small diameter slow-twitch fibers. Fiber-type and myosin heavy chain analyses revealed that the GGC was comprised largely of fast-twitch fibers (Tursiops: 88.6%, Phocoena: 79.7%) and had the highest ß of all vocal muscles. Notably, there was a significant difference in [Mb] between the RNM and LNM in Tursiops, but not Phocoena. Our results reveal shared physiological characteristics of individual vocal muscles across species that enhance our understanding of key functional roles, as well as species-specific differences which appear to reflect differences in vocal capacities.

The high cost of reproduction in sea otters necessitates unique physiological adaptations.

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.

Ontogeny of Oxygen Storage Capacity and Diving Ability in the Southern Sea Otter (Enhydra lutris nereis): Costs and Benefits of Large Lungs.

Small body size, large lungs, and dense pelage contribute to the unique challenges faced by diving sea otters (Enhydra lutris) when compared to other marine mammals. Here we determine the consequences of large lungs on the development of diving ability in southern sea otters (Enhydra lutris nereis) by examining the ontogeny of blood, muscle, and lung oxygen stores and calculating aerobic dive limits (cADL) for immature and mature age classes. Total oxygen storage capacity matures rapidly in sea otters, reaching adult levels by 2 mo postpartum. But this result is driven by exceptional lung capacity at birth, followed by a decrease in mass-specific lung volume with age. Blood and muscle oxygen stores remain well below adult values before weaning, with large pups exhibiting 74% and 54% of adult values, respectively. Slow muscle development limits the capacity of immature sea otters to dive against high positive buoyancy due to comparatively large lungs. Immature sea otters diving with total lung capacity (TLC) experience up to twice the mass-specific positive buoyancy as adults diving with TLC but can reduce these forces to comparable adult levels by using a smaller diving lung volume (DLV). The cADL of a juvenile with DLV is 3.62 min, while the cADL of an adult with TLC is 4.82 min. We find that the magnitude of positive buoyancy experienced by sea otters changes markedly with age and strongly influences the ontogeny of diving ability in this species.