Thermal limits in young northern fur seals,Callorhinus ursinus

The thermoregulatory abilities of northern fur seals (Callorhinus ursinus) during their first two years in the frigid waters of the North Pacific Ocean may limit their geographic distribution and alter the costs for exploiting different species of prey. We determined the thermoneutral zone of six young northern fur seals by measuring their metabolism in ambient air and controlled water temperatures (0°C–12°C) from ages 8 to 24 mo. We found that the ambient air temperatures within our study (overall 1.5°C–23.9°C) did not affect resting metabolic rates. Calculated lower critical temperatures in water varied between 3.9°C and 8.0°C, while an upper critical temperature in water was only discernible during a single set of trials. These thermal responses provide insight into the possible physiological constraints on foraging ecology in young northern fur seals, as well as the potential energetic consequences of ocean climate change and altered prey distributions.     

Telemetry tags increase the costs of swimming in northern fur seals,Callorhinus ursinus

Animal‐borne instruments have become a standard tool for collecting important data from marine mammals. However, few studies have examined whether placement of these data loggers affects the behavior and energetics of individual animals, potentially leading to biasing data. We measured the effect of two types of relatively small data loggers (<1% of animals’ mass and front profile) on the swimming speeds and energy expenditure of four female northern fur seals (Callorhinus ursinus) while swimming at depth. Swim speeds and rates of oxygen consumption were measured as the trained fur seals repeatedly swam an underwater circuit, with or without the tags. We found the placement of either tested tag significantly affected both the behavior and energetics of the fur seals in our study. Diving metabolic rate increased an average of 8.1%–12.3% (depending on tag type) and swim speed decreased an average of 3.0%–6.0% when wearing the tags. The combined changes in velocities and metabolic rates resulted in a 12.0%–19.0% increase in the total energy required by the fur seals to swim a set distance. The demonstrated effects of tags on behavior and energy expenditure may bias data sets from wild animals and potentially incur longer‐term impacts on the studied animals.     

Foraging habitats based on the diet of female northern fur seals (Callorhinus ursinus) on the Pribilof Islands, Alaska

Scats (fecal samples) collected between 1987 and 2000 on northern fur seal Callorhinus ursinus rookeries of St Paul ( n =2968) and St George Islands ( n =1203), Alaska, were used to examine the relationship between breeding sites and food habits of adult female seals. On the basis of the frequency of occurrence (FO) and per cent minimum number of individual prey (%MNI) in scats, juvenile walleye pollock Theragra chalcogramma and gonatid squid Gonatopsis borealis/Berryteuthis magister and Gonatus madokai/Gonatus middendorffi were the dominant prey species consumed overall. Other primary prey (FO>5%) included Pacific sand lance Ammodytes hexapteus , Pacific herring Clupea pallasi , northern smoothtongue Leuroglossus schmidti , Atka mackerel Pleurogrammus monopterygius , Pacific salmon ( Oncorhynchus spp.) and other squid of the Gonatus genus. We identified five rookery complexes from a cluster analysis of the FO of primary prey in scats. Rookery complexes were separated geographically and each was further defined by characteristic patterns in the representation of prey types typically associated with specific hydrographic domains. Diet differences were observed among rookeries on the north and south side of St George Island and on the east, south and south-west side of St Paul Island. The rookery clusters observed in this study provide evidence of resource partitioning among adult female northern fur seals and have important implications for fur seal conservation and management.     

Enzyme‐linked immunosorbent assay to quantitate serum ferritin in the northern fur seal (Callorhinus ursinus)

Serum ferritin concentration correlates with tissue iron stores in humans, horses, calves, dogs, cats, and pigs. Serum ferritin is considered the best serum analyte to predict total body iron stores in these species, and is more reliable than serum iron or total iron‐binding capacity, both of which may be affected by disorders unrelated to iron adequacy or excess (including hypoproteinemia, chronic infection, hemolytic anemia, hypothyroidism, renal disease, and drug administration). Iron overload has been documented to result in hemochromatosis in captive northern fur seals (Callorhinus ursinus); therefore, we developed an enzyme‐linked immunosorbent assay (ELISA) to measure serum ferritin in this species. The assay uses two murine anti‐canine ferritin monoclonal antibodies in a sandwich arrangement that was originally used in an ELISA to measure serum ferritin in dogs. Ferritin isolated from fur seal liver was used as a standard. Ferritin standards were linear from 0 to 50 ng/ml. Recovery of purified ferritin from fur seal serum varied from 89% to 99%. The within‐assay variability was 6%, and the assay‐to‐assay variability for two different samples was 10% and 16%. Zoo Biol 23:79‐84, 2004.© 2004 Wiley‐Liss, Inc.     

Prey selection of subadult male northern fur seals (Callorhinus ursinus) and evidence of dietary niche overlap with adult females during the breeding season

During the breeding season northern fur seals (Callorhinus ursinus) congregate on the Pribilof Islands in large numbers creating the potential for intraspecific competition. Due to the declining trend in the Pribilof Islands population of fur seals, it is important to understand how prey resources are partitioned among the population. Fur seals exhibit a high degree of sexual dimorphism resulting in energetic differences among age and sex classes. Therefore, we hypothesized that subadult male and adult female fur seals would differ in the type and size of prey consumed. We examined the diets of subadult male (age 2–8; mean mass 28–176 kg) and adult female (age ≥ 3 yr; mean mass 13–50 kg) seals on St. Paul Island from 1992 to 2000. Prey remains found in fecal samples were compared using niche overlap indices. There was nearly complete dietary niche overlap between subadult male and adult female fur seals. Walleye pollock (Theragra chalcogramma), Pacific salmon (Oncorhynchus spp.), Pacific herring (Clupeia pallasi), and cephalopods were common prey items found in the diets of both groups. We found differences in the size of pollock consumed and that geographic location of sample collection may be important in determining diet differences. Our results indicate high levels of dietary overlap among subadult male and adult female fur seals.     

Otolith size and location in digestive tracts of northern fur seals (Callorhinus ursinus): Implications for dietary interpretations

Walleye pollock (Theragra chalcogramma) otoliths (n= 2,706) recovered from stomachs, small intestines, and colons of 43 northern fur seals (Callorhinus ursinus) were evaluated for size and wear by location in the digestive tract. Pollock fork length was regressed on otolith length after correction for erosion, and age was estimated from the calculated body size. Age‐1+ pollock otoliths (≥6.3‐mm length) were concentrated in stomachs while age‐0 otoliths (≤6.2‐mm length) were concentrated in colons. Less than 10% of otoliths were found in the small intestines. Pollock age decreased with progression along seal gastrointestinal tracts. Otolith quality increased along gastrointestinal tracts in numbers ≥20, which was typical of age‐0 otoliths recovered from colons. Otolith distribution by age and quality along gastrointestinal tracts suggests that small (≤12 cm) schooling prey are consumed in large volume and passed as a bolus rapidly through the digestive tract before significant erosion of bony remains occurs; while larger prey are eaten in smaller volume and subjected to otolith erosion due to longer retention in the stomach. Our results illustrate the importance of multiple sampling strategies to comprehensively represent prey size in pinniped diet.     

Foraging a new trail with northern fur seals (Callorhinus ursinus): Lactating seals from islands with contrasting population dynamics have different foraging strategies,and forage at scales previously unrecognized by GPS interpolated dive data

We reconstructed the foraging tracks of lactating northern fur seals (Callorhinus ursinus) from two eastern Bering Sea islands (St. Paul Island and Bogoslof Island) using linear interpolation between GPS locations recorded at a maximum of four times per hour and compared it to tri‐axial accelerometer and magnetometer data collected at 16 Hz to reconstruct pseudotracks between the GPS fixes. The high‐resolution data revealed distances swum per foraging trip were much greater than the distances calculated using linearly interpolated GPS tracks (1.5 times further for St. Paul fur seals and 1.9 times further for Bogoslof fur seals). First passage time metrics calculated from the high resolution data revealed that the optimal scale at which the seals searched for prey was 500 m (radius of circle searched) for fur seals from St. Paul Island that went off‐shelf, and 50 m for fur seals from Bogoslof Island and surprisingly, 50 m for fur seals from St. Paul that foraged on‐shelf. These area‐restricted search scales were significantly smaller than those calculated from GPS data alone (12 km for St. Paul and 6 km for Bogoslof) indicating that higher resolution movement data can reveal novel information about foraging behaviors that have important ecological implications.     

Serum indices of body stores of iron in northern fur seals (Callorhinus ursinus) and their relationship to hemochromatosis

Iron storage disease (hemochromatosis) has been reported in many species of both captive and free‐ranging animals. In this study we examined the relationship between this disease and concentrations of iron analytes in aquarium‐held northern fur seals (Callorhinus ursinus). Sera were analyzed for iron, total iron‐binding capacity (TIBC), ferritin, ceruloplasmin, and haptoglobin concentrations in a retrospective study that included samples taken over a 14‐year period. The animals ranged in age from <1 year to an estimated 23 years. Serum ferritin was measured using an enzyme‐linked immunosorbent assay (ELISA) for canine sera. The results from this assay are the first reported for any pinniped. Serum iron concentrations in presumed healthy animals ranged from 37 to 196 µg/dl, and TIBC ranged from 136 to 484 µg/dl. The transferrin saturation percentage differed significantly between male (41%) and female (63%) adult fur seals, as did the ferritin levels (54 ng/ml for males vs. 500 ng/ml for females). There was a trend toward increased serum ferritin and percent transferrin saturation with age, especially in females. The data also showed a relationship between serum iron and transferrin saturation among eight mother–pup pairs, which suggests that pups may develop increased iron levels due to placental transfer of iron and/or transfer of iron through the milk from iron‐overloaded females. Diet was considered as a factor in the development of hemochromatosis in at least three geriatric female northern fur seals, and their diets were analyzed for iron concentrations. On the basis of these results, the diets were altered by replacing a portion of the high‐iron‐content fish (herring) with a lower‐iron‐content item (squid), and discontinuing iron and vitamin C supplementation (via a multivitamin tablet). Sera were analyzed before, and 1 and 4 years after the dietary changes were implemented. Paired t‐tests showed no significant changes in the iron analytes from pre‐ to post‐diet‐change samples, which indicates that it may be too late to affect iron levels by diet alone in older animals with a chronic history of elevated iron levels. Zoo Biol 23:205–218, 2004. © 2004 Wiley‐Liss, Inc.     

Differentiating between Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) scats through analysis of faecal DNA

We describe a method to determine the species of pinniped from faeces collected from sympatric Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) rookeries using newly developed species-specific primers that amplify a 667-669-base pair segment from the mitochondrial DNA (mtDNA) cytochrome B (cytB) gene region. The primers yielded the correct species in 100% of tissue samples from 10 known animals and 100% of faecal samples from 13 known animals. Species could be identified unequivocally for 87.7% of faecal samples from 122 unknown individuals. The ability to differentiate between scats of sympatrically breeding Steller sea lions and northern fur seals will contribute to the range-wide knowledge of the foraging strategies of both species as well as allow researchers to examine the niche partitioning and potential resource competition between the two predators.     

Behavioral responses of Australian fur seals (Arctocephalus pusillus doriferus) to environmental variations

Observing how pinnipeds respond to variations in climatic and oceanographic conditions informs marine managers on factors that could limit their range, foraging ability and breeding success. Here, we examine how Australian fur seals (Arctocephalus pusillus doriferus) at Seal Rocks, Victoria, Australia, responded to normal climatic conditions from August 2009 to January 2010, which included their Austral spring‐summer breeding period, to investigate their tolerances to a range of environmental stimuli. Seal numbers ashore and a range of climatic variables were collected hourly during daylight periods and compared using Generalized Additive Mixed Models (GAMMs). Air temperature was the most consistent predictor of haul‐out behavior, with seal numbers ashore declining as air temperature increased (effect size ?50%, edf 1.00, P < 0.001). Increased wave height (effect size 74%, edf 1.00, P < 0.001) and wind speed (effect size 79%, edf 1.00, P < 0.001) were associated with increased seal numbers ashore. Potentially, higher air temperatures reduce the seals tolerance to remain out of the water, while high wind/wave action increases at‐sea metabolic costs. These results demonstrate how changes in climate could alter a seal's ability to remain ashore, to rest or breed, and its ability to forage effectively, thus driving changes in population status and range.     

Development of the aerobic dive limit and muscular efficiency in northern fur seals (Callorhinus ursinus)

Northern fur seal (Callorhinus ursinus; NFS) populations have been declining, perhaps due to limited foraging ability of pups. Because a marine mammal’s proficiency at exploiting underwater prey resources is based on the ability to store large amounts of oxygen (O₂) and to utilize these reserves efficiently, this study was designed to determine if NFS pups had lower blood, muscle, and total body O₂ stores than adults. Pups (<1-month old) had a calculated aerobic dive limit only ~40% of adult females due to lower blood and, to a much greater extent, muscle O₂ stores. Development of the Pectoralis (Pec) and Longissimus dorsi (LD) skeletal muscles was further examined by determining their myosin heavy chain (MHC) composition and enzyme activities. In all animals, the slow MHC I and fast-twitch IIA proteins typical of oxidative fiber types were dominant, but adult muscles contained more (Pec ~50%; LD ~250% higher) fast-twitch MHC IID/X protein characteristic of glycolytic muscle fibers, than pup muscles. This suggests that adults have greater ability to generate muscle power rapidly and/or under anaerobic conditions. Pup muscles also had lower aerobic and anaerobic ATP production potential, as indicated by lower metabolically scaled citrate synthase, β-hydroxyacyl CoA dehydrogenase, and lactate dehydrogenase activities (all P values ≤0.001). In combination, these findings indicate that pups are biochemically and physiologically limited in their diving capabilities relative to adults. This may contribute to lower NFS first year survival.     

Inter-island variation in the diet of female northern fur seals (Callorhinus ursinus) in the Bering Sea

The diet of adult female northern fur seals ( Callorhinus ursinus ) is examined through the analysis of faecal material collected during the summer breeding season at three breeding locations in the Bering Sea: St. Paul Island (1988, 1990) and St. George Island (1988, 1990) of the Pribilof Islands Group (USA), and Medny Island (1990) of the Commander Islands Group (Russia). Prey consumption varies annually and accordingly with the physical and biological environment surrounding each island. Juvenile walleye pollock ( Theragra chalcogramma ) is the most common prey of northern fur seals from St. Paul Island; the island is surrounded by a broad neritic environment with widely separated frontal zones and is the greatest distance from the continental shelf-edge. Gonatid squid ( Gonatopsis borealis/Berryteuthis magister and Gonatus madokail Gonatus middendorffi ) were the most common prey of northern fur seals from Medny Island; the island is surrounded by a compressed neritic environment and is adjacent to the continental shelf-edge and the oceanic marine environment. A combination of walleye pollock and gonatid squid is consumed by northern fur seals from St. George Island; the island has a surrounding oceanographic environment intermediate between the other two islands.
Variability in predation on walleye pollock is consistent with fishery information concerning the relative abundance and availability of walleye pollock around St. George and St. Paul Islands. The abundance and availability of these prey resources during the summer breeding season are key factors which influence the health and growth of the northern fur seal populations in the Bering Sea.     

Activity‐specific metabolic rates for diving,transiting, and resting at sea can be estimated from time–activity budgets in free‐ranging marine mammals

Time and energy are the two most important currencies in animal bioenergetics. How much time animals spend engaged in different activities with specific energetic costs ultimately defines their likelihood of surviving and successfully reproducing. However, it is extremely difficult to determine the energetic costs of independent activities for free‐ranging animals. In this study, we developed a new method to calculate activity‐specific metabolic rates, and applied it to female fur seals. We attached biologgers (that recorded GPS locations, depth profiles, and triaxial acceleration) to 12 northern (Callorhinus ursinus) and 13 Antarctic fur seals (Arctocephalus gazella), and used a hierarchical decision tree algorithm to determine time allocation between diving, transiting, resting, and performing slow movements at the surface (grooming, etc.). We concomitantly measured the total energy expenditure using the doubly‐labelled water method. We used a general least‐square model to establish the relationship between time–activity budgets and the total energy spent by each individual during their foraging trip to predict activity‐specific metabolic rates. Results show that both species allocated similar time to diving (~29%), transiting to and from their foraging grounds (~26–30%), and resting (~8–11%). However, Antarctic fur seals spent significantly more time grooming and moving slowly at the surface than northern fur seals (36% vs. 29%). Diving was the most expensive activity (~30 MJ/day if done non‐stop for 24 hr), followed by transiting at the surface (~21 MJ/day). Interestingly, metabolic rates were similar between species while on land or while slowly moving at the surface (~13 MJ/day). Overall, the average field metabolic rate was ~20 MJ/day (for all activities combined). The method we developed to calculate activity‐specific metabolic rates can be applied to terrestrial and marine species to determine the energetic costs of daily activities, as well as to predict the energetic consequences for animals forced to change their time allocations in response to environmental shifts.     

Low reproductive success in territorial male Antarctic fur seals (Arctocephalus gazella) suggests the existence of alternative mating strategies

Microsatellites were used to conduct an analysis of paternity of Antarctic fur seals (Arctocephalus gazella) from Bird Island, South Georgia. At most, only 28% of pups at our study site could be assigned a father, even though the majority (approximately 90%) of candidate males within this colony were sampled. The behavioural and genetic evidence from this study suggests that a number of alternative mating strategies may exist within this fur seal population. Holding a land-based territory conferred an advantage to male reproductive success. However, this advantage was much smaller than expected from behavioural observations. At least 70% of fur seal pups born at our study site in a given year are not fathered by males who held a territory or were observed copulating with females in the previous year, implying that there exists a pool of males that seldom venture ashore at this site. To explain this discrepancy we suggest that female choice is an integral component of the Antarctic fur seal mating system and that aquatic mating may play a much larger role in the Antarctic fur seal than previously thought.     

Status,population trend and genetic structure of South American fur seals,Arctocephalus australis,in southwestern Atlantic waters

The South American fur seal (SAFS), Arctocephalus australis, was severely depleted during the 18th century. This work updates information on distribution, abundance, seasonal movements, and genetic structure along the southwestern South Atlantic. Its distribution in Argentine waters includes nineteen rookeries on the Patagonian coast, Isla de los Estados, and islets of the Beagle Channel. Censuses were carried out in rookeries from Isla Escondida to Isla de los Estados from 1996 to 2014. The largest concentrations are found in Chubut, (4,500–15,500 seals) and Isla de los Estados (4,500). Pups were recorded on Isla Escondida, Rasa, and Isla de los Estados. An increasing number of SAFS were recorded in northern Patagonia, including seals marked in Uruguay. Skin samples were taken from southern Brazil to Tierra del Fuego in order to evaluate population structure and demographic trends. Genetic results indicated no population subdivisions (Φ_st = ?0.0292, F_st = ?0.00716, P > 0.05). Bayesian skyline plots constructed for the entire data set indicated evidence of rapid population expansion discernible in Nef between the last 20,000 and 17,000 yr. Genetics results and observation data from marked fur seals support the hypothesis of ancient gene flow and a single Atlantic population. Therefore, SAFS should be managed under international and integrated conservation policies.     

Energetic costs and thermoregulation in northern fur seal (Callorhinus ursinus) pups: the importance of behavioral strategies for thermal balance in furred marine mammals

Behavioral thermoregulation represents an important strategy for reducing energetic costs in thermally challenging environments, particularly among terrestrial vertebrates. Because of the cryptic lifestyle of aquatic species, the energetic benefits of such behaviors in marine endotherms have been much more difficult to demonstrate. In this study, I examined the importance of behavioral thermoregulation in the northern fur seal (Callorhinus ursinus) pup, a small-bodied endotherm that spends prolonged periods at sea. The thermal neutral zones of three weaned male northern fur seal pups (body mass range = 11.8-12.8 kg) were determined by measuring resting metabolic rate using open-flow respirometry at water temperatures ranging from 2.5° to 25.0°C. Metabolic rate averaged 10.03 ± 2.26 mL O?kg?1 min?1 for pups resting within their thermal neutral zone; lower critical temperature was 8.3° ± 2.5°C , approximately 8°C higher than the coldest sea surface temperatures encountered in northern Pacific waters. To determine whether behavioral strategies could mitigate this potential thermal limitation, I measured metabolic rate during grooming activities and the unique jughandling behavior of fur seals. Both sedentary grooming and active grooming resulted in significant increases in metabolic rate relative to rest (P = 0.001), and percent time spent grooming increased significantly at colder water temperatures (P < 0.001). Jughandling metabolic rate (12.71 ± 2.73 mL O?kg?1 min ?1) was significantly greater than resting rates at water temperatures within the thermal neutral zone (P < 0.05) but less than resting metabolism at colder water temperatures. These data indicate that behavioral strategies may help to mitigate thermal challenges faced by northern fur seal pups while resting at sea.