Behavioral effects of environmental enrichment on harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus)

Zoos and aquariums have been incorporating environmental enrichment into their animal care programs for the past 30 years to increase mental stimulation and promote natural behaviors. However, most attempts to document the effects of enrichment on animal behavior have focused on terrestrial mammals. Staff at the National Aquarium in Baltimore conducted an investigation of the behavioral effects of enrichment on the seven harbor seals and two gray seals housed in the aquarium's outdoor seal exhibit. We expected that enrichment would change the amount of time the animals spent engaged in specific behaviors. The behaviors recorded were: resting in water, resting hauled out, maintenance, breeding display, breeding behavior, aggression, pattern swimming, random swimming, exploration, and out of sight. Activity levels (random swimming and exploration) were expected to increase, while stereotypic behaviors (pattern swimming) were expected to decrease. The frequency and duration of behaviors were documented for 90 hr in both the control phase (without enrichment) and the experimental phase (with enrichment). Statistically significant differences (P<0.05) in the time spent in pattern swimming, random swimming, exploration, and out of sight were observed between the two phases. With enrichment, pattern swimming and out of sight decreased, while random swimming and exploration behavior increased. These findings demonstrate that enrichment can promote behaviors (random swimming and exploration) that are likely to be normal for phocids in the wild, and that may contribute to the behavioral complexity of these seals in captivity. Zoo Biol 21:375–387, 2002. © 2002 Wiley‐Liss, Inc.     

Postrelease movement of rehabilitated harbor seal (Phoca vitulina richardii) pups compared with cohort‐matched wild seal pups

Harbor seal (Phoca vitulina richardii) populations in the inland waters of Washington and British Columbia are at or near carrying capacity. Stranded pups often are collected and admitted to rehabilitation centers, and then released when they reach a weight of 22 kg and meet a variety of preestablished health and release conditions. While rehabilitation is common practice, it is unclear if rehabilitated seal pups behave like wild weaned pups. Using satellite transmitters, we compared movement patterns of 10 rehabilitated pups with 10 wild weaned pups. When released, rehabilitated seals were longer and heavier than wild pups, while wild pups had a larger mean axillary girth. No clinically different blood parameters were detected. On average, rehabilitated harbor seal pups traveled nearly twice as far cumulatively, almost three times as far daily, and dispersed over three times as far from the release site compared to wild weaned seals. Additionally, wild harbor seals transmitted nearly twice as long as did rehabilitated seals. These patterns suggest that learned behavior during the brief 3–4 wk nursing period likely enables wild harbor seal pups to move less daily and remain closer to their weaning site than rehabilitated pups.     

Food habits of harbor seals (Phoca vitulina richardii) as an indicator of invasive species in San Francisco Bay,California

The diet of harbor seals (Phoca vitulina richardii) in San Francisco Bay (SFB), California, was determined from July 2007 to July 2008 using prey hard parts recovered from 442 scats collected at five haul‐out sites. Twenty‐two species of fish and one species of crustacean were identified, but harbor seals primarily ate a nonnative invasive species, yellowfin goby (Acanthogobius flavimanus), which increased in dietary importance since the diet was last studied in 1991/1992. Additionally, another nonnative invasive fish species, chameleon goby (Tridentiger trigonocephalus), was found for the first time in the diet of harbor seals in SFB. Harbor seal diet was statistically different between years (1991/1992 and 2007/2008), between the pupping and nonpupping seasons, and between North SFB and South SFB haul‐out locations. The diet of harbor seals was significantly correlated with fish species caught in trawl surveys conducted by the California Department of Fish and Wildlife (CDFW) during the same time periods as this study (2007/2008). Harbor seals currently are influencing the health of the SFB ecosystem in a positive manner by consuming large quantities of nonnative invasive fish species.     

Phocanema decipiens: Pathology in seals

Infective larvae of the anisakine nematode, Phocanema decipiens from cod (Gadus morhua), were fed to harbor seals (Phoca vitulina) and gray seals (Halichoerus grypus). At termination of the experimental infections, 6 of 8 harbor seals were infected with 34(6–64) P. decipiens, while the remaining 2 seals had relatively heavy infections of 250 and 547 nematodes, respectively; 10 of 11 gray seals were infected with 128 (68–229) P. decipiens, but only 2 nematodes were recovered from the 11th seal. Larvae and adults of P. decipiens occurred throughout the gastrointestinal tract, but mainly in the fundic portion of the stomach; the anterior extremities of the nematodes were embedded in mucosa and submucosa. Clusters of adult P. decipiens were associated with ulcerous gastric lesions in harbor seals and raised inflammatory areas in stomachs of gray seals. Singly occurring larvae from challenge transmissions were associated with raised inflammatory areas in the stomachs of both host species. Histological examinations revealed that the lesions and inflammatory areas were eosinophilic granulomata. Anisakis sp. larvae from the viscera of cod were also fed to 1 of the gray seals. Eighty of these larvae were subsequently found in association with a general inflammation in the cardiac area of the stomach in this seal. Natural anisakine infection were surveyed in 16 harbor and 53 gray seals from the Nova Scotia mainland. The natural incidence of P. decipiens was 62(5–177) in harbor seals and 577(11–1694) in gray seals. Clusters of adult P. decipiens were found in association with gastric lesions in 2 juvenile harbor seals; however, in gray seals, the nematodes neither occurred in clusters nor in association with gastric lesions.     

Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals

The gut microbiota of mammals underpins the metabolic capacity and health of the host. Our understanding of what influences the composition of this community has been limited primarily to evidence from captive and terrestrial mammals. Therefore, the gut microbiota of southern elephant seals, Mirounga leonina, and leopard seals, Hydrurga leptonyx, inhabiting Antarctica were compared with captive leopard seals. Each seal exhibited a gut microbiota dominated by four phyla: Firmicutes (41.5 ± 4.0%), Fusobacteria (25.6 ± 3.9%), Proteobacteria (17.0 ± 3.2%) and Bacteroidetes (14.1 ± 1.7%). Species, age, sex and captivity were strong drivers of the composition of the gut microbiota, which can be attributed to differences in diet, gut length and physiology and social interactions. Differences in particular prey items consumed by seal species could contribute to the observed differences in the gut microbiota. The longer gut of the southern elephant seal provides a habitat reduced in available oxygen and more suitable to members of the phyla Bacteroidetes compared with other hosts. Among wild seals, 16 ‘core’ bacterial community members were present in the gut of at least 50% of individuals. As identified between southern elephant seal mother–pup pairs, ‘core’ members are passed on via vertical transmission from a young age and persist through to adulthood. Our study suggests that these hosts have co‐evolved with their gut microbiota and core members may provide some benefit to the host, such as developing the immune system. Further evidence of their strong evolutionary history is provided with the presence of 18 shared ‘core’ members in the gut microbiota of related seals living in the Arctic. The influence of diet and other factors, particularly in captivity, influences the composition of the community considerably. This study suggests that the gut microbiota has co‐evolved with wild mammals as is evident in the shared presence of ‘core’ members.     

Molting phenology of the Pacific harbor seal (Phoca vitulina richardii) on two islands off the Baja California Peninsula,Mexico

We document and compare the annual molt of the Pacific harbor seal (Phoca vitulina richardii) on two islands off the west coast of the Baja California Peninsula that are the northern and southern extremes of its distribution in Mexico. During 2014, observations were made from March to July on Todos Santos Island (northern extreme) and from January to June on San Roque Island (southern extreme). On Todos Santos, the premolt lasted 15 wk (March–June) and the molt 12 wk (April–July). On San Roque, the premolt lasted 22 wk (January–June) and the molt 17 wk (February–June). The proportion of seals undergoing molt peaked on 26 May on Todos Santos and on 7 June on San Roque. Shedding of old hair most commonly initiated on the torso and progressed to the head and flippers (reverse molting pattern). The period when the highest number of harbor seals haul out in Mexico is in late April on the more southerly islands and in early May on the more northerly islands, when a large proportion of seals are in premolt.     

Postrelease dive ability in rehabilitated harbor seals

The efficacy of seal rehabilitation is examined in a postrelease study of dive ability in harbor seal pups (Phoca vitulina) in the Wash, United Kingdom. Six rehabilitated seals were fitted with Sea Mammal Research Unit (SMRU) Argos Satellite Relay Data Logger tags and their individual dive behavior was monitored for an average of 122 d. The upper 90 percentile edge of dive behavior (dive duration [DD₉₀] and percentage of time at‐sea spent in a dive [PD₉₀]), in 7 d bins, was used as a proxy for physiological dive ability. The results are compared with data from five wild adult harbor seals. There was no statistically significant difference between (1) the mean track duration of rehabilitated seals (126.20 ± 27.48 [SD] d) and adult seals (150.2 ± 24.62 d) (P= 0.108), indicating no evidence that short‐term survival was less in the rehabilitated group; (2) the mean mass‐scaled DD₉₀ of rehabilitated seals (3.95 ± 0.37 min) and adult seals (4.09 ± 0.55 min) (P= 0.632); and (3) the mean PD₉₀ of rehabilitated seals (81.62 ± 1.21%) and adult seals (81.48 ± 3.93%) (P= 0.943). These three results all suggest the success of the rehabilitation program in terms of short‐term survival and dive ability.     

Making it through the first year: Ontogeny of movement and diving behavior in harbor seals from Svalbard,Norway

Phocid seal pups must learn successful survival strategies, largely independently, following their abrupt weaning at a relatively young age. To explore the ontogeny of aquatic skills, space use and first‐year habitat choices made by harbor seals, pups (n = 30) were instrumented with satellite relay data loggers (SRDLs) in Svalbard, Norway in 2009 and 2010. Initially, the pups had small home ranges and showed rapid changes in their activity budgets and diving capabilities, displaying steep linear increases in diving depth and duration and in the amount of time spent diving. Most pups underwent an abrupt shift in movement patterns at ca. 50 d of age, which likely marked the end of the postweaning fast. Around this same time, the steep progression in diving performance slowed, though longer, deeper dives gradually became the norm. However, bottom time, ascent and descent rates, and postdive recovery times remained stable after the postweaning fast, suggesting that most aquatic skill acquisition was completed during the first months of life. Few clear effects of environmental variables such as upwelling phenomenon, which are known to influence the diving behavior of adults from the same population, were detected in the diving patterns of pups.     

Survival probabilities and movements of harbor seals in central California

Harbor seal numbers and population trajectories differ by location in central California. Within San Francisco Bay (SFB) counts have been relatively stable since the 1972 Marine Mammal Protection Act, but in coastal areas like Tomales Bay (TB), counts increased before stabilizing in the 1990s. Emigration, poor survival, and environmental effects have been hypothesized as contributors to differences between trajectories; however, basic demographic data were not available to evaluate these hypotheses. We monitored 32 radio‐tagged adult females (SFB n = 17, TB n = 15) for 20 mo (2011–2013), and estimated survival, resight, and movement probabilities using mark‐resight analyses and multistate mark‐resight models. Annual survival probability for both sites was 0.90 (95% CI = 0.18–0.99). Six seals were observed moving between locations resulting in an estimated probability of 0.042 (95% CI = 0.023–0.076) per month equal movement between sites. Resight probability was less in SFB relative to TB, likely due to differential haul‐out access, area surveyed, visibility, and resight effort. Because of wide confidence intervals and low precision of these first estimates of adult female harbor seal survival in California, this demographic must be further examined to dismiss its contribution to differing population trajectories. Using aerial survey data, we estimated 950 harbor seals in SFB (95% CI = 715–1,184) confirming numbers are still stable.     

Natural selection on marine carnivores elaborated a diverse family of classical MHC class I genes exhibiting haplotypic gene content variation and allelic polymorphism

Pinnipeds, marine carnivores, diverged from terrestrial carnivores ~45 million years ago, before their adaptation to marine environments. This lifestyle change exposed pinnipeds to different microbiota and pathogens, with probable impact on their MHC class I genes. Investigating this question, genomic sequences were determined for 71 MHC class I variants: 27 from harbor seal and 44 from gray seal. These variants form three MHC class I gene lineages, one comprising a pseudogene. The second, a candidate nonclassical MHC class I gene, comprises a nonpolymorphic transcribed gene related to dog DLA-79 and giant panda Aime-1906. The third is the diversity lineage, which includes 62 of the 71 seal MHC class I variants. All are transcribed, and they minimally represent six harbor and 12 gray seal MHC class I genes. Besides species-specific differences in gene number, seal MHC class I haplotypes exhibit gene content variation and allelic polymorphism. Patterns of sequence variation, and of positions for positively selected sites, indicate the diversity lineage genes are the seals’ classical MHC class I genes. Evidence that expansion of diversity lineage genes began before gray and harbor seals diverged is the presence in both species of two distinctive sublineages of diversity lineage genes. Pointing to further expansion following the divergence are the presence of species-specific genes and greater MHC class I diversity in gray seals than harbor seals. The elaboration of a complex variable family of classical MHC class I genes in pinnipeds contrasts with the single, highly polymorphic classical MHC class I gene of dog and giant panda, terrestrial carnivores.     

Examination of relationships between stable isotopes and cortisol concentrations along the length of phocid whiskers

Alaskan seals are found in remote and sometimes inaccessible locations, making it difficult to collect time‐series information. This study explores a novel method to examine temporal changes in diet and physiological status of ringed (Pusa hispida), spotted (Phoca largha), and harbor (Phoca vitulina) seals using cortisol concentrations and δ¹⁵N and δ¹³C stable isotopes (SIs) measured in serial sections of whiskers. As whiskers grow, whisker tissue is deposited sequentially making these measurements temporally aligned. Whisker cortisol presented in a distinct pattern with elevated concentrations at the root section followed by a curvilinear decline moving toward the tip of most whiskers. Comparing SIs at the root to the rest of the whiskers, δ¹³C values were slightly lower in ringed and harbor seal whiskers and δ¹⁵N values were slightly higher in harbor seal whiskers. The data were modeled controlling for the observed trends in cortisol concentrations and further associations between cortisol concentrations and SIs were detected in spotted and harbor seal whiskers. Additional research examining the source and stability of whisker cortisol is warranted. However, the methods presented here demonstrate that whiskers could prove valuable to gather long‐term and naturally aligned dietary and physiological information.     

DISPERSAL and BYCATCH MORTALITY IN GRAY, HALICHOERUS GRYPUS, AND HARBOR, PHOCA VITULINA, SEALS TAGGED AT THE NORWEGIAN COAST

Between 1975 and 1998, 3,571 gray and 630 harbor seal pups were tagged along the Norwegian coast, and 259 (7%) gray and 80 (13%) harbor seal tags were returned. Incidental mortality, mainly in bottom-set nets, accounted for the majority of deaths (79% in gray and 48% in harbor seals, respectively). Seals were most vulnerable to incidental mortality in fishing gear during the first three months after birth, but high incidental mortality prevailed during the first 8–10 mo. Gray seals dispersed more widely (mean distance: 120 km) than harbor seals (mean distance: 69 km). Both species dispersed most widely during the two first months after tagging. The maximum distance moved was 739 km for gray and 463 km for harbor seals. Strong fidelity for their place of birth was observed in adult gray seals during breeding season. No significant difference in incidental mortality was detected between the areas of tagging. However, for 37 harbor seals tagged in a 724 km nature reserve no returns were reported.     

Interannual differences in postrelease movements of rehabilitated harbor seal pups (Phoca vitulina richardii) in the Salish Sea

Despite the large number of harbor seals (Phoca vitulina richardii) rehabilitated worldwide, few studies have been conducted on postrelease movement and behavior of rehabilitated harbor seal pups. We compared interannual differences in movements and survival of 24 rehabilitated seal pups released in the Salish Sea in 2010 (n = 10), 2012 (n = 5), 2013 (n = 5), and 2014 (n = 4). We also compared the postrelease movement of these seals to the movement of 10 wild seal pups tracked in the same ecosystem in 2010. Transmission duration, total cumulative distance, and average daily distance varied annually. Maximum linear distance traveled from the release site was similar for the rehabilitated seal groups. Compared to wild seals (n = 10), and consistent with prior studies, rehabilitated pups (n = 24) traveled significantly farther daily and cumulatively than wild weaned pups. Unlike in a prior study in this ecosystem, we found no significant difference between transmission duration in wild and rehabilitated pups.     

Broad thermal capacity facilitates the primarily pelagic existence of northern fur seals (Callorhinus ursinus)

Thermoregulatory capacity may constrain the distribution of marine mammals despite having anatomical and physiological adaptations to compensate for the thermal challenges of an aquatic lifestyle. We tested whether subadult female northern fur seals (Callorhinus ursinus) experience increased thermoregulatory costs in water temperatures potentially encountered during their annual migration in the Bering Sea and North Pacific Ocean. Metabolic rates were measured seasonally in 6 captive female northern fur seals (2.75–3.5 yr old) in ambient air and controlled water temperatures of 2°C, 10°C, and 18°C. Rates of oxygen consumption in ambient air (1°C–18°C) were not related to environmental temperature except below 2.5°C (winter only). However, metabolism was significantly higher during the fall seasonal trials (September–October) compared to other times of year, perhaps due to the costs of molting. The fur seals appeared thermally neutral in all seasons for all water temperatures tested (2°C–18°C) except during the summer when metabolic rates were higher in the 2°C water. Comparing this broad thermal neutral zone to the average sea surface temperatures potentially encountered during annual migrations indicates wild fur seals can likely exploit a large geographic area without added thermal metabolic costs.     

Some anatomical aspects of the cardiovascular system of antarctic seals and their possible functional significance in diving

The hearts and ascending aortae of 11 Weddell seals, Leptonychotes weddelli, three adult Crabeater seals, Lobodon carcinophagus, two adult Ross seals, Ommatophoca rossi, and one adult Leopard seal, Hydrurga leptonyx, were examined for comparison with terrestrial forms. The Weddell seal specimens were from animals ranging in age from midterm in fetal development to mature adults. All specimens were collected in 1971, 1972, and 1973, from McMurdo Sound and the Ross Sea, Antarctica. The phocid hearts were characteristically broader and flatter than those of other carnivore families and they tended toward bifid apices. The heart form indices (height/circumference) averaged 31.5 compared to 39.0 for felids. The right ventricular chambers of the Antarctic seals were found to average longer in Weddells and narrower in all, than those reported for four other carnivore families. An elastic enlargement was present in the ascending aortae of all seals. The largest diameter of the aortic bulb averaged 25.5 mm more than the base of the aorta in the adult Weddell seals which represented an increase of 72.5% over the base. It is suggested that the general heart form, and especially the ascending aortae, are anatomical adaptations to diving. The compressed heart makes possible unimpaired function when the chest is compressed during deep dives. The aortic bulb maintains mean arterial blood pressure and perfusion of the brain and cardiac tissue during diving bradycardia.     

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.     

An apparent population decrease,or change in distribution,of Weddell seals along the Victoria Land coast

Ground counts during 1959–1968 compared with counts using high resolution (0.6 m²) satellite imagery during 2008–2012 indicated many fewer Weddell seals (Leptonychotes weddellii) at two major molting areas in the western Ross Sea: Edisto Inlet‐Moubray Bay, northern Victoria Land, and McMurdo Sound, southern Victoria Land. Breeding seals have largely disappeared from Edisto‐Moubray, though the breeding population in McMurdo Sound appears to have recovered from harvest in the 1960s. The timing of decline, or perhaps spreading (lower numbers of seals in more places), is unknown but appears unrelated to changes in sea ice conditions. We analyzed both historic and satellite‐derived ice data confirming a large expansion of pack ice mostly offshore of the Ross Sea, and not over the continental shelf (main Weddell seal habitat), and a thinning of fast ice along Victoria Land (conceivably beneficial to seals). Timing of fast ice presence and extent in coves and bays along Victoria Land, remains the same. The reduction in numbers is consistent with an altered food web, the reasons for which are complex. In the context of a recent industrial fishery targeting a seal prey species, a large‐scale seal monitoring program is required to increase understanding of seal population changes.     

The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions

Respiratory, metabolic, and cardiovascular responses to swimming were examined in two species of pinniped, the harbor seal (Phoca vitulina) and the California sea lion (Zalophus californianus). 1. Harbor seals remained submerged for 82-92% of the time at swimming speeds below 1.2 m.s-1. At higher speeds, including simulated speeds above 1.4 m.s-1, the percentage of time spent submerged decreased, and was inversely related to body weight. In contrast, the percentage of time spent submerged did not change with speed for sea lions swimming from 0.5 m.s-1 to 4.0 m.s-1. 2. During swimming, harbor seals showed a distinct breathhold bradycardia and ventilatory tachycardia that were independent of swimming speed. Average heart rate was 137 beats.min-1 when swimming on the water surface and 50 beats.min-1 when submerged. A bimodal pattern of heart rate also occurred in sea lions, but was not as pronounced as in the seals. 3. The weighted average heart rate (WAHR), calculated from measured heart rate and the percentage time spent on the water surface or submerged, increased linearly with swimming speed for both species. The graded increase in heart rate with exercise load is similar to the response observed for terrestrial mammals. 4. The rate of oxygen consumption increased exponentially with swimming speed in both seals and sea lions. The minimum cost of transport calculated from these rates ranged from 2.3 to 3.6 J.m-1.kg-1, and was 2.5-4.0 times the level predicted for similarly-sized salmonids. Despite different modes of propulsion and physiological responses to swimming, these pinnipeds demonstrate similar transport costs.     

基于卫星信标跟踪的斑海豹放流效果研究

利用卫星标记跟踪方法对斑海豹的野外释放效果进行了研究。2010 年和2011 年6 月分别释放了4 头和3头人工繁殖的2 龄未成年斑海豹,2011 年同时释放了3 头野外出生的救助个体。标记斑海豹在释放后,7 头人工繁殖斑海豹中的5 头信标信号持续时间较长,在信号消失前,1 头斑海豹一直在渤海海域活动,另4 头沿辽宁沿岸、朝鲜西海岸到达辽东湾斑海豹的主要度夏海域韩国白翎岛附近。研究期间,1 头人工繁殖的斑海豹在59 d内运动的距离超过1 250 km。救助斑海豹中,2 头个体的信标信号持续较长,并分别在山东半岛沿海和黄渤海活动。研究结果表明,人工繁殖的斑海豹在经过野化训练后,放归自然海域后可以正常生活洄游。     

Phocanema decipiens: Molting in seals

Infective larvae of the anisakine nematode Phocanema decipiens from the muscle of Atlantic cod (Gadus morhua) were fed to harbor seals (Phoca vitulina) and gray seals (Halichoerus grypus). During maturation in the stomach of seal hosts, P. decipiens molted twice; these molts are the third and fourth of its life cycle. The third molt occurred between the second and fifth days of infection. The third stage, i.e., infective larva entering the third molt, had a cuticular tooth ventral to the mouth; the fourth stage larva emerging from the third molt had three bilobed lips with dentigerous ridges. The fourth molt occurred between the 5th and 15th days in seals. A female nematode emerging from the fourth molt possesses a vulva and a vagina; a male possesses caudal alae, pre- and postanal papillae. Significant morphometric changes in nematodes were associated with both molts. Females and males of P. decipiens reached maturity after 15 to 25 days in seals. Ova were detected in the feces of the seal hosts as early as the 16th day.