Pinniped phylogeny and a new hypothesis for their origin and dispersal

The relationships and the zoogeography of the three extant pinniped families, Otariidae (sea lions and fur seals), Odobenidae (one extant species, the walrus), and Phocidae (true seals), have been contentious. Here, we address these topics in a molecular study that includes all extant species of true seals and sea lions, four fur seals and the walrus. Contrary to prevailing morphological views the analyses conclusively showed monophyletic Pinnipedia with a basal split between Otarioidea (Otariidae+Odobenidae) and Phocidae. The northern fur seal was the sister to all remaining otariids and neither sea lions nor arctocephaline fur seals were recognized as monophyletic entities. The basal Phocidae split between Monachinae (monk seals and southern true seals) and Phocinae (northern true seals) was strongly supported. The phylogeny of the Phocinae suggests that the ancestors of Cystophora (hooded seal) and the Phocini (e.g. harp seal, ringed seal) adapted to Arctic conditions and ice-breeding before 12 MYA (million years ago) as supported by the white natal coat of these lineages. The origin of the endemic Caspian and Baikal seals was dated well before the onset of major Pleistocene glaciations. The current findings, together with recent advances in pinniped paleontology, allow the proposal of a new hypothesis for pinniped origin and early dispersal. The hypothesis posits that pinnipeds originated on the North American continent with early otarioid and otariid divergences taking place in the northeast Pacific and those of the phocids in coastal areas of southeast N America for later dispersal to colder environments in the N Atlantic and the Arctic Basin, and in Antarctic waters.     

Defining and identifying sustainable harvests of resources: Archaeological examples of pinniped harvests in the eastern North Pacific

Archaeologists and resource managers are starting to recognize the value of studying ancient cultures for examples of how resources have, and have not, been sustainably utilized in the past as a way of understanding current trends in environmental degradation. These studies do not provide sweeping generalizations about aboriginal resource use but, rather, identify the range of conditions under which sustainable harvests may be possible. The hypothesis of sustainable harvests must be tested using variables that can be measured equally well in ancient (e.g., archaeological) and modern contexts.These factors are carefully considered in this analysis of pinniped (seal and sea lion) remains from two archaeological sites on the eastern North Pacific (ENP) coast, where pinnipeds have been hunted for millennia. Reconstruction of the age composition, or harvest profile, of Callorhinus ursinus at the Ozette Village Site, Washington, shows that males and females of all ages were harvested, and supports the hypothesis that it was done so sustainably for over 500 years. After this period of apparent stability, C. ursinus abandoned local breeding colonies in the early historic period. In contrast, harvests of this species at the Moss Landing Hill Site, California, primarily targeted young of the year, and sub-adult and adult females. While this harvest is also inferred to have targeted a local breeding colony, C. ursinus appear to have been extirpated nearly 2000 years earlier at Moss Landing than at Ozette.The causes of these extirpations are not known, but the timing does not correspond well with known climatic changes, suggesting that subsistence, and perhaps commercial, hunting may have played a role. These examples underscore the need to recognize that patterns of resource use are highly variable – different cultures have had varying levels of effects on economically important species, and these effects have varied temporally, spatially, and taxonomically.     

Ecological implications of body composition and thermal capabilities in young antarctic fur seals (Arctocephalus gazella)

In comparison with other homeotherms, young recently weaned marine mammals in high latitudes face exceptional energetic demands when foraging and thermoregulating. Lipids are an important source of energy and a major component of insulation that allows them to meet these demands. To examine the role of lipid stores in a high-latitude pinniped, we measured the body composition and thermoregulatory capabilities of Antarctic fur seal (Arctocephalus gazella) pups and yearlings by using flow-through respirometry and hydrogen isotope dilution. From these data, we constructed a model to examine the importance of postweaning fasting capability in free-ranging young fur seals. Resting metabolic rates were different for pups and yearlings measured in 0.6 degrees C water, 10.3 degrees C water, and ambient air; however, mass and percent lipid as covariates accounted for the different metabolic responses in pups and yearlings for all treatments. The estimated lower critical temperature for combined pups and yearlings was 14.4 degrees C, 10 degrees -15 degrees C above water temperatures normally experienced by Antarctic fur seals. Modeling predicted that a weaned fur seal pup would survive at sea from 9.8 to 36.2 d before succumbing to starvation. The most likely maximum travel distance within this time constraint suggests that food resources close to the natal rookery are important to first-year survival for this species.     

Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds

We investigated the impact of foraging location (nearshore vs offshore) and foraging latitude (high vs middle) on the carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope compositions of bone collagen of northern fur seals (Callorhinus ursinus), harbor seals (Phoca vitulina), California sea lions (Zalophus californianus), and northern elephant seals (Mirounga angustirostris). Nearshore-foraging harbor seals from California had δ¹³C values 2.0‰ higher than female northern elephant seals foraging offshore at similar latitudes. Likewise, nearshore-foraging harbor seals from Alaska had values 1.7‰ higher than male northern fur seals, which forage offshore at high latitudes. Middle-latitude pinnipeds foraging in either the nearshore or offshore were ¹³C enriched by ∼1.0‰ over similar populations from high latitudes. Male northern elephant seals migrate between middle and high latitudes, but they had δ¹³C values similar to high-latitude, nearshore foragers. Female northern fur seal δ¹³C values were intermediate between those of high- and middle-latitude offshore foragers, reflecting their migration between high- and middle-latitude waters. The δ¹³C values of California sea lions were intermediate between nearshore- and offshore-foraging pinnipeds at middle latitudes, yet there was no observational support for the suggestion that they use offshore food webs. We suggest that their “intermediate” values reflect migration between highly productive and less-productive, nearshore ecosystems on the Pacific coasts of California and Mexico. The relative uniformity among all of these pinnipeds in δ¹⁵N values, which are strongly sensitive to trophic level, reveals that the carbon isotope patterns result from differences in the δ¹³C of organic carbon at the base of the food web, rather than differences in trophic structure, among these regions. Finally, the magnitude and direction of the observed nearshore-offshore and high-to middle-latitude differences in δ¹³C values suggest that these gradients may chiefly reflect differences in rates and magnitudes of phytoplankton production as well as the δ¹³C value of inorganic carbon available for photosynthesis, rather than the input of ¹³C-enriched macroalgal carbon to nearshore food webs. Received: 8 September 1998 / Accepted: 24 February 1999     

Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification

California sea lions (Zalophus californianus) and northern fur seals (Callorhinus ursinus) are each believed to host distinct hookworm species (Uncinaria spp.). However, a recent morphometric analysis suggested that a single species parasitizes multiple pinniped hosts, and that the observed differences are host-induced. To explore the systematics of these hookworms and test these competing hypotheses, we obtained nucleotide sequences of nuclear ribosomal DNA (D2/D3 28S, D18/D19 28S, and internal transcribed spacer [ITS] regions) from 20 individual hookworms parasitizing California sea lion and northern fur seal pups where their breeding grounds are sympatric. Five individuals from an allopatric population of California sea lions were also sampled for ITS-1 and D18/D19 28S sequences. The 28S D2/D3 sequences showed no diagnostic differences among hookworms sampled from individual sea lions and fur seals, whereas the 28S D18/D19 sequences had one derived (apomorphic) character demarcating hookworms from northern fur seals. ITS sequences were variable for 7 characters, with 4 derived (apomorphic) states in ITS-1 demarcating hookworms from California sea lions. Multivariate analysis of morphometric data also revealed significant differences between nematodes representing these 2 host-associated lineages. These results indicate that these hookworms represent 2 species that are not distributed indiscriminately between these host species, but instead exhibit host fidelity, evolving independently with each respective host species. This evolutionary approach to analyzing sequence data for species delimitation is contrasted with similarity-based methods that have been applied to numerous diagnostic studies of nematode parasites.     

加州Santa Monica海湾鳍足类的生态学

研究了加州Santa Monica海湾鳍足类的生态学.从1997-2007年乘船调查了277次,发现海狮(Zalophus californianus)是最常见的动物(89%,见到的次数为1393次),其次是港海豹(Phoca vitulina richardsi,8%,n=131)和北象海豹(Mirounga angustirostris,1%,n=15).在29%的遇见次数(观察到瓶海豚205次)中,发现海狮(偶尔也发现港海豹)与瓶鼻海豚集群(Tursiops truncatus);短喙真海豚(Delphinus delphis)与长喙真海豚(D.capensis)在53% 的遇见次数(遇见真海豚次数n=155)中,发现短喙真海豚(Delphinus delphis)与长喙真海豚(D.capensis)集群;一般在沿岸水域(离岸边距离<500 m)见到海狮和港海豹,但在整个海湾也能见到,表现出这两个物种对海底峡谷的偏爱.北象海豹仅见于近海,主要在海底峡谷附近. 经常看到海狮、港海豹和北象海豹游动(50%,n=728)、进行热调节(14%,n=205)、以及取食(3.2%,n=47),但几乎见不到有社会性活动(0.21%,n=3).     

THERMAL FUNCTION OF PHOCID SEAL FUR

In phocid seals, blubber serves as the main thermal insulation instead of fur. The thermal function of fur, at least in adult phocid seals, has therefore been questioned. We measured the relative contribution of fur to the combined thermal resistance (insulation) offered by blubber, skin, and fur in newborn and adult harp ( Pagophilus groenlandicus ) and hooded ( Cystophora cristata ) seals, in air and water, to elucidate the role of fur as insulation in phocid seals. In air the fur contributed 90% of the combined thermal resistance of blubber, skin, and fur in newborn harp seal pups and 29% in adulrs, whereas in hooded seals the fur contributed 73% in newborn pups and 34% in adults. When submerged the thermal resistance of the fur was reduced by 84%-92%, and contributed 65% to the total insulation in newborn harp seal pups and 3% in adults, and 26% in newborn hooded seal pups and 5% in adults. We conclude that in air the fur of phocid seals makes an important contribution to the insulation of pups, and also contributes considerably to the insulation of adult animals. In water, even though the thermal resistance of the fur is dramatically reduced, the fur still contributes substantially to the insulation of pups, but its contribution in adults is negligible.     

Prevalence and characterization of Salmonella spp. among marine animals in the Channel Islands, California

Salmonella enterica is a zoonotic pathogen that has been isolated from free-ranging marine mammals throughout the world, with animals in the Channel Islands of California (USA) showing the highest prevalence. The goal of this study was to determine prevalence, antimicrobial sensitivity and genetic similarity using pulsed-field gel electrophoresis (PFGE) of Salmonella in several non-domestic animal species on San Miguel and San Nicolas Islands. Fecal samples were collected from 90 California sea lion Zalophus californianus pups, 30 northern elephant seal Mirounga angustirostris pups and 87 western gulls Larus occidentalis in the Channel Islands and 59 adult male sea lions in Puget Sound, WA (USA). Salmonella were isolated, identified and serotyped, followed by antimicrobial susceptibility testing and PFGE. Of the California sea lion pups that were sampled on the islands, 21% (n = 19) were positive for Salmonella, whereas no adults males in Puget Sound were positive. Of the northern elephant seal pups sampled, 87% (n = 26) were harboring Salmonella. Only 9% (n = 8) of western gulls were shedding Salmonella, with one of these gulls harboring the only antimicrobial resistant isolate. The serotypes found in these animals were Enteritidis, Montevideo, Newport, Reading, and Saint Paul. The only serotype that showed variation on PFGE was Newport. The pinnipeds of the Channel Islands harbor Salmonella at a higher prevalence than pinnipeds from other geographic areas observed in previous studies. Researchers and veterinarians should exercise increased caution when working with these animals due to the zoonotic potential of Salmonella.     

DARK ADAPTATION AND VISUAL SENSITIVITY IN SHALLOW AND DEEP-DIVING PINNIPEDS1

Pinnipeds forage almost exclusively underwater. Consequently, observing them is difficult and relatively little is known of how they use their senses to locate prey, avoid predators, and navigate while diving. Vision has been presumed to be of primary importance, although previous measurements of visual functioning in pinnipeds have been restricted to just a few shallow-diving species. As diving pinnipeds experience rapid changes in light levels during descent/ascent and low light levels at depth, it has not been clear whether they possess visual capabilities adequate for use while diving, particularly in the case of deep-diving species. To examine this issue, behavioral psychophysics have been used to assess and compare the dark adaptation rates and relative light sensitivities of a deep-diving pinniped (northern elephant seal, Mirounga angustirostris), two shallow-diving species (California sea lion, Zalophus californianus, and harbor seal, Phoca vitulina), and a human subject. In comparison to the human subject, both the California sea lion and the harbor seal dark-adapted relatively quickly and were more light sensitive. These findings suggest that both of these species are well suited for vision in the moderately dim shallow-water environments in which they dive to forage. In contrast, the elephant seal reached complete dark adaptation in less than half the time taken by the other pinnipeds, and it was significantly more light sensitive. Unlike the shallower-diving species, the visual abilities of the elephant seal are commensurate with the extreme conditions experienced while deep diving. Thus, we conclude that elephant seals are sufficiently adapted to rely on vision underwater, even while diving to depths in excess of 1000 meters where bioluminescence may be the sole source of ambient light.     

The Survival Dynamics of Male Northern Fur Seals (<Emphasis Type="Italic">Callorhinus ursinus</Emphasis>) on Tyulenii Island,Sea of Okhotsk,Based on Long-Term Observations

We discuss and improve the methods proposed previously for estimating the survival rate of male northern fur seals representing different age groups. Estimates of the number of pups and bulls per rookery are given, as well as information on the age structure of animals hunted during the coastal harvest. The data were obtained by researchers from the Pacific Research Fisheries Center over 56 years of observation of the fur seal (Callorhinus ursinus) herd on Tyulenii Island, located in the southwestern part of the Sea of Okhotsk, south of Cape Terpenia, 15 km from Sakhalin Island. Lander’s method and its modifications were used for estimating the juvenile survival rate of male fur seals. This methodology was found to have not been working properly for the past several decades (since the end of the 1980s) due to changes in population harvesting. Satisfactory estimates for all characteristics of the male life cycle were obtained. Structural changes in survival ability were revealed as having occurred at the end of the 1980s, i.e., the survival of subadult and adult males increased slightly. New estimates of survival rates allow us to create a model of the dynamics of bull numbers that is in good agreement with that observed, its mean error of approximation equaling 3.2%.     

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.     

Giardiasis in pinnipeds from eastern Canada

Cysts of Giardia sp. were detected in feces from the rectum of 20 of 74 pinnipeds examined from the eastern coast of Canada in 1997 and 1998 using a monoclonal antibody technique. Infected pinnipeds included 15 adult harp seals (Phoca groenlandica), four adult grey seals (Halichoerus grypus), and one juvenile harbor seal (Phoca vitulina). Cysts were not detected in 15 seal pups <1-yr-old. The highest prevalence (50%) occurred in adult harp seals collected near the Magdalen Islands in the Gulf of St. Lawrence. The overall prevalence of Giardia sp. in grey and harbor seals, excluding pups, from the Gulf and St. Lawrence estuary was 23%. Feces from 11 beluga (Delphinapterus leucas) and one northern bottle-nosed whale (Hyperoodon ampullatus) stranded in the St. Lawrence estuary were negative for Giardia sp. cysts. The significance of Giardia sp. in marine mammals, shown here for the first time in eastern coastal Canada, is unknown.     

Salmonellae in feral pinnipeds off the Southern California coast

Rectal swabs were collected from 90 Northern fur seal (Callorhinus ursinus) and 50 California sea lion (Zalophus californianus) pups on San Miguel Island for Salmonella screening. Three serotypes (newport, heidelberg, and oranienburg) were recovered from 33% of the fur seals and 40% of the sea lions.     

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.     

PERMANENT GENETIC RESOURCES: Ten novel polymorphic dinucleotide microsatellite loci cloned from the Antarctic fur seal Arctocephalus gazella

Ten new dinucleotide microsatellite loci were isolated from the Antarctic fur seal Arctocephalus gazella. These markers should prove useful for studying the reproductive ecology of Antarctic fur seals and other related pinniped species.     

Biased estimates of fur seal pup mass: origins and implications

The mass of fur seal pups weighed in different years can be used to estimate growth rates or compared with one another to make inferences about the relative condition of a population. However, unless appropriate precautions are taken, many factors can bias estimates of pup mass and lead to incorrect conclusions. Using data collected from tagged and untagged northern fur seal pups ( Callorhinus ursinus ) at the Pribilof Islands, Alaska, I assess how milk consumption, the timing of sampling, and the effects of growth and sample size influence the size of pups captured for weighing. Evidence is presented suggesting that pup mass may increase in a sigmoid fashion, with the most rapid rate of growth occurring when about two months old. This phenomenon can confound efforts to compare the masses of pups weighed on different days in different years, particularly if pups are weighed over the period of rapid growth. Variability in pup mass increases with time because growth rates of individuals vary and because the amount of milk pups consume increases with body size. Thus sample sizes must be increased as the pups grow older in order to detect statistically significant differences in mean body mass. There is also evidence that pups of different ages and sizes are not randomly distributed on the breeding beaches and are not randomly selected for weighing. It appears that the first pups captured for weighing are smaller and younger than subsequent captures, possibly because smaller pups are easier to handle and are segregated to the peripheral rookery regions where sampling begins. These hidden biases, related to sampling error and fur seal biology, must be considered and controlled for when weighing fur seal pups.     

Structure of arctic fox (Alopex lagopus beringensis) colonies in the northern extremity of Bering Island

Data on the spatial structure of an Arctic fox (Alopex lagopus beringensis) colony were obtained in July-August 1995, using walk counts and observations near living dens around the Northern rookery of the northern fur seals located on Bering Island (Commander Islands). The home ranges of 31 Arctic fox families (61 adults and 145 pups inhabiting 66 dens) were found over 27 km of the coastline. Sixty individuals (3 adults and 57 pups) were marked by color ear-tags. Among adult foxes, 24 (39.3%) were recognized as females and 12 (19.7%) as males; the sex of 25 (41.0%) foxes was not recognized. Among 57 marked cubs, 26 (45.6%) were females and 31 (54.4%) were males. The best studied families (13) had 3–11 pups (6.7 ± 0.7, on average). The survival of cubs at an age younger than 2.0–2.5 months was 82.5%; 30.8% of the families consisted of more than two adults. The distribution of the Arctic fox dens and home ranges along the coastline has been studied; specific features of the location of dens have been described. In the studied area, Arctic foxes have been foraging on birds (67.6% of dens with food remains), northern fur seals (40.5), other marine mammals (13.5), Pacific salmon (29.7), and reindeer (2.7%), as well as on amphipods and voles. Rich constant food sources (rookeries, marine bird colonies, and spawning places of the blueback salmon) were found in 7 home ranges of the Arctic fox; 6 home ranges included temporary food sources (spawning streams of the humpback salmon); and 18 home ranges were poor in food resources. Arctic foxes whose home ranges lie within 6–7 km around a “food patch” used the concentrated food resources together. Food resources are supposed to become important only after the raised pups turn to self-feeding. Differences in the use of space, foraging and breeding of the two Arctic fox subspecies (A. l. beringensis and A. l. semenovi), and arrangement of colonies around the northern fur seal rookeries are discussed.     

Hematology and serum chemistry comparisons between free-ranging and rehabilitated harbor seal (Phoca vitulina richardsi) pups

The objectives of this study were to compare the hematology and serum chemistry values between free-ranging and stranded harbor seal (Phoca vitulina richardsi) pups and to ascertain how blood values of stranded pups changed during the rehabilitation process. Coincident with these comparisons, reference values were obtained for free-ranging pups. Stranded harbor seal pups (n = 28) recovered from areas between Pebble Beach and Moss Landing, California (USA) were admitted to The Marine Mammal Center, Sausalito, from March to May 1995, 1996, and 1998. Blood samples were collected from harbor seal pups before and after rehabilitation. As a control group, wild harbor seal pups were captured at Pebble Beach and Elkhorn Slough (n = 42) during the 1995, 1996, and 1998 pupping seasons. Mean eosinophil and calcium values of wild pups were significantly greater than those of newly admitted pups, whereas mean bands, aspartate aminotransferase, alanine aminotransferase, total bilirubin, and chloride values were significantly lower (P < or = 0.05). Mean neutrophil, band, lymphocyte, eosinophil, basophil, calcium, phosphorus, blood urea nitrogen, potassium, total protein, and globulin values of rehabilitated pups increased significantly after 2-3 mo in captivity, whereas, mean red blood cell, hemoglobin, hematocrit, cholesterol, and total bilirubin values decreased significantly (P < or = 0.05).     

Lipid composition of blood platelets and erythrocytes of southern elephant seal (Mirounga leonina) and antarctic fur seal (Arctocephalus gazella)

Erythrocyte and blood platelet phospholipid compositions were studied in three elephant seals and two fur seals, two species of marine mammals living in the Subantarctic region feeding on preys rich in (n-3) polyunsaturated fatty acids. Results were compared with those reported for related species and humans. In erythrocytes, the phospholipid (PL) and cholesterol (CHOL) contents were lower in pinnipeds than in humans. Phosphatidylcholine (PC) levels were higher in elephant seals than in fur seals, with a reverse trend for phosphatidylethanolamine (PE) and phosphatidylserine (PS). Both species had lower SM/PC ratios and PE plasmalogen concentrations than human. Erythrocytes were richer in (n-3) fatty acids (FA) in pinnipeds than in humans. In platelets, the PL content was lower and the CHOL content higher in elephant seals than in humans or in other phocid seal species studied to date. The SM/PC ratio was much higher than in other seal species or in man. In both species, the proportion of PE plasmalogens was higher in platelets than in erythrocytes. PL were more saturated in elephant seals than in fur seals. These results suggest that the erythrocytes and platelets of wild marine mammals may prove useful models to study the influence of dietary lipids on the structure and hemostatic function of these cells.