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.     

Microbiome maturation during a unique developmental window

Shortly after birth, mammals are colonized by a multitude of microbes derived from the mother and the environment. Studies in model organisms have demonstrated that the structure and composition of the gut microbiome of offspring steadily mature with increasing diversity during nursing and weaning (Sommer & Bäckhed, 2013). This period of microbiome assembly is critical for young mammals because the gut microbes they acquire will help train their immune system (Lathrop et al., 2011) with potential long‐lasting effects on their health (Cox et al., 2014). In an article in this issue of Molecular Ecology, Stoffel et al. (2020) investigated the gut microbiota of northern elephant seals (Mirounga angustirostris) during a key developmental window. A month after giving birth, elephant seal mothers stop nursing their pups and return to the sea. As a consequence, their pups go from a diet of milk rich in fat to abruptly enter a post weaning fasting period which lasts for about two months while they remain with the colony. This particular life‐history trait therefore offered the authors a unique and exciting opportunity to evaluate intrinsic factors contributing to gut microbiota development in a wild marine mammal.     

Maximum likelihood population size estimation of harbour seals in the Dutch Wadden Sea based on a mark–recapture experiment

1. The harbour seal population Phoca vitulina in the entire Wadden Sea was severely depleted due to a virus-epizootic during 1988. A comprehensive study on the population biology and activity patterns was subsequently initiated to design a management and conservation plan. The main objective of this study was to estimate harbour seal abundance in the different regions of the Wadden Sea.
2. We investigated the potential of a mark–recapture experiment using VHF radio-tags in combination with repeated aerial surveys to estimate the number of harbour seals in the Dutch part of the Wadden Sea. The number of harbour seals hauled-out and the presence of any radio-tagged seals was monitored during seven aerial surveys of all known haul-out sites in the Dutch Wadden Sea over the 1994 breeding season.
3. A maximum likelihood (ML) estimator was developed to infer the rate of tag-loss and the size of the local prepupping population.
4. The ML estimate of the number of harbour seals in the Dutch Wadden Sea was 1536 (95% confidence limits were 1225 and 2200). The corresponding maximum proportion of seals hauled-out was 68%.
5. The use of VHF radio-tags which can be monitored from the air provides a way of correcting aerial survey counts for the proportion of harbour seals hauled-out during the surveys. Since haul-out behaviour may be influenced by local conditions, such as exposure time of sand banks, we recommend this technique be repeated in other areas of the Wadden Sea rather than using the estimates from the current study in other areas.     

Diet differences among age classes of Arctic seals: evidence from stable isotope and mercury biomarkers

A basic understanding of current food web dynamics and baseline data from which to measure future change is necessary to understand species re-distribution and altered competition for food with climate change. We use mercury (Hg) and carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope ratios as biomarkers to understand species diet differences and age class differences among ringed (Phoca hispida), bearded (Erignathus barbatus), and harbour (P. vitulina) seals in a subarctic marine ecosystem. Adult bearded seals had significantly lower δ¹⁵N and muscle Hg than bearded seal pups, whereas the opposite was observed in ringed seals where pups had lower δ¹⁵N than adults, suggesting age specific foraging differences in trophic food level for both species. For harbour seals, δ¹⁵N did not differ significantly among ages while Hg and δ¹³C did. The δ¹³C in muscle supports that bearded seals in this study are benthic feeders and are part of a separate food web from ringed seals and harbour seals. Harbour seals had the highest levels of mercury and δ¹⁵N, indicating they feed at a higher trophic level relative to the other two seal species. Carbon and nitrogen isotopic ratios and Hg levels illustrate how resources are partitioned among three seal species and offer evidence for separation based on life stages within species.     

Trophic niche overlap between sympatric harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) at the southern limit of their European range (Eastern English Channel)

Sympatric harbour (Phoca vitulina) and grey seals (Halichoerus grypus) are increasingly considered potential competitors, especially since recent local declines in harbour seal numbers while grey seal numbers remained stable or increased at their European core distributions. A better understanding of the interactions between these species is critical for conservation efforts. This study aimed to identify the trophic niche overlap between harbour and grey seals at the southern limit of their European range, in the Baie de Somme (BDS, Eastern English Channel, France), where numbers of resident harbour seals and visiting grey seals are increasing exponentially. Dietary overlap was identified from scat contents using hierarchical clustering. Isotopic niche overlap was quantified using δ¹³C and δ¹⁵N isotopic values from whiskers of 18 individuals, by estimating isotopic standard ellipses with a novel hierarchical model developed in a Bayesian framework to consider both intraindividual variability and interindividual variability. Foraging areas of these individuals were identified from telemetry data. The three independent approaches provided converging results, revealing a high trophic niche overlap due to consumption of benthic flatfish. Two diet clusters were dominated by either small or large benthic flatfish; these comprised 85.5% [CI95%: 80.3%–90.2%] of harbour seal scats and 46.8% [35.1%–58.4%] of grey seal scats. The narrower isotopic niche of harbour seals was nested within that of grey seals (58.2% [22.7%–100%] overlap). Grey seals with isotopic values similar to harbour seals foraged in coastal waters close to the BDS alike harbour seals did, suggesting the niche overlap may be due to individual grey seal strategies. Our findings therefore provide the basis for potential competition between both species (foraging on benthic flatfish close to the BDS). We suggest that a continued increase in seal numbers and/or a decrease in flatfish supply in this area could cause/amplify competitive interactions and have deleterious effects on harbour seal colonies.     

An assessment of population size and distribution of harbour seals in the Republic of Ireland during the moult season in August 2003

The status of Ireland's harbour seal Phoca vitulina vitulina population is poorly understood. The most recent national population estimate dates back to the breeding season in 1978 and did not cover the entire coastline. Reliable up-to-date information on the abundance and distribution of harbour seals in Ireland is necessary to assess the conservation status of the species and for the effective identification, management and monitoring of special areas of conservation required for harbour seals under the EU Habitats Directive. To provide comprehensive current information on Ireland's harbour seal population, a geographically extensive survey was conducted along the coastline of the Republic of Ireland during the species' annual moult in August 2003. This complemented a similar survey of Northern Ireland, which was conducted in 2002. Using thermal imaging technology, haul-out groups of harbour seals and grey seals Halichoerus grypus were identified from the air, aerial-counts were obtained and compared with simultaneous ground-count data from selected sites. Harbour seal distribution recorded during the 2003 moult season was concentrated in the south-west, west and north-west of the country. This national survey yielded a minimum population estimate for the Republic of Ireland of 2905 harbour seals, delivering an effective baseline for current and future population research.     

Assessing the potential impact of salmon fisheries management on the conservation status of harbour seals (Phoca vitulina) in north-east Scotland

Conservation efforts are often constrained by uncertainty over the factors driving declines in marine mammal populations. In Scotland, there is concern over the potential impact of unrecorded shooting of seals, particularly where this occurs near Special Areas of Conservation. Here, we show that the abundance of harbour seals Phoca vitulina in the Moray Firth, north-east Scotland, declined by 2–5% per annum between 1993 and 2004. Records from local salmon fisheries and aquaculture sites indicated that 66–327 harbour seals were shot each year between 1994 and 2002. Matrix models and estimates of potential biological removal indicate that this level of shooting is sufficient to explain observed declines. Nevertheless, uncertainty over the number and identity of seals shot means that other factors such as changes in food availability may be contributing. Recent conservation measures markedly reduced the recorded levels of shooting in 2003 and 2004. In 2005, a coordinated management plan was developed to protect salmon fisheries interests while minimizing impacts on local seal populations. Comprehensive monitoring of future population trends and improved regulation of culls are now required to provide more robust assessments of the impact of human persecution on harbour seal populations in the Moray Firth and in other parts of the UK.     

Ice seals as sentinels for algal toxin presence in the Pacific Arctic and subarctic marine ecosystems

Domoic acid (DA) and saxitoxin (STX)-producing algae are present in Alaskan seas, presenting exposure risks to marine mammals that may be increasing due to climate change. To investigate potential increases in exposure risks to four pagophilic ice seal species (Erignathus barbatus, bearded seals; Pusa hispida, ringed seals; Phoca largha, spotted seals; and Histriophoca fasciata, ribbon seals), this study analyzed samples from 998 seals harvested for subsistence purposes in western and northern Alaska during 2005–2019 for DA and STX. Both toxins were detected in bearded, ringed, and spotted seals, though no clinical signs of acute neurotoxicity were reported in harvested seals. Bearded seals had the highest prevalence of each toxin, followed by ringed seals. Bearded seal stomach content samples from the Bering Sea showed a significant increase in DA prevalence with time (logistic regression, p = .004). These findings are consistent with predicted northward expansion of DA-producing algae. A comparison of paired samples taken from the stomachs and colons of 15 seals found that colon content consistently had higher concentrations of both toxins. Collectively, these results suggest that ice seals, particularly bearded seals (benthic foraging specialists), are suitable sentinels for monitoring HAB prevalence in the Pacific Arctic and subarctic.     

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.     

Variations in heart rate and rhythm of harbor seal pups during rehabilitation

Heart rate and rhythm is regulated by the autonomic nervous system, which matures during the first months of life. Little is known about heart rate and rhythm development and potential arrhythmias in seal pups during rehabilitation in seal centers. Using an iPhone ECG device, 1 min ECGs were obtained from harbor seal pups admitted to a seal rehabilitation facility. ECGs were taken from 55 seals after admission, 53 seals after 14 d, and 52 seals prior to release. From 24 seal pups additional ECGs were taken daily for the first week of rehabilitation. At admission sinus rhythm with a median heart rate of 148 complexes per minute was detected, prior to release sinus bradycardia or sinus arrhythmia with a median heart rate of 104 complexes minute was present. P wave morphology was highly variable and single supra‐ and ventricular premature complexes were recorded in individual animals. The first 14 d were characterized by highly variable heart rates and rhythms, including episodes of sinus tachycardia and 2nd degree atrioventricular blocks. The reduction in heart rates and development of a regular heart rhythm during rehabilitation suggest adaptation to the unfamiliar environment, resolution of disease, and/or maturation of the autonomic nervous system.     

The effects of climate change on harp seals (Pagophilus groenlandicus)

Harp seals (Pagophilus groenlandicus) have evolved life history strategies to exploit seasonal sea ice as a breeding platform. As such, individuals are prepared to deal with fluctuations in the quantity and quality of ice in their breeding areas. It remains unclear, however, how shifts in climate may affect seal populations. The present study assesses the effects of climate change on harp seals through three linked analyses. First, we tested the effects of short-term climate variability on young-of-the year harp seal mortality using a linear regression of sea ice cover in the Gulf of St. Lawrence against stranding rates of dead harp seals in the region during 1992 to 2010. A similar regression of stranding rates and North Atlantic Oscillation (NAO) index values was also conducted. These analyses revealed negative correlations between both ice cover and NAO conditions and seal mortality, indicating that lighter ice cover and lower NAO values result in higher mortality. A retrospective cross-correlation analysis of NAO conditions and sea ice cover from 1978 to 2011 revealed that NAO-related changes in sea ice may have contributed to the depletion of seals on the east coast of Canada during 1950 to 1972, and to their recovery during 1973 to 2000. This historical retrospective also reveals opposite links between neonatal mortality in harp seals in the Northeast Atlantic and NAO phase. Finally, an assessment of the long-term trends in sea ice cover in the breeding regions of harp seals across the entire North Atlantic during 1979 through 2011 using multiple linear regression models and mixed effects linear regression models revealed that sea ice cover in all harp seal breeding regions has been declining by as much as 6 percent per decade over the time series of available satellite data.     

Hydrodynamic trail following in a California sea lion (<Emphasis Type="Italic">Zalophus californianus</Emphasis>)

The mystacial vibrissae of pinnipeds constitute a sensory system for active touch and detection of hydrodynamic events. Harbour seals (Phoca vitulina) and California sea lions (Zalophus californianus) can both detect hydrodynamic stimuli caused by a small sphere vibrating in the water (hydrodynamic dipole stimuli). Hydrodynamic trail following has only been shown in harbour seals. Hydrodynamical and biomechanical studies of single vibrissae of the two species showed that the specialized undulated structure of harbour seal vibrissae, as opposed to the smooth structure of sea lion vibrissae, suppresses self-generated noise in the actively moving animal. Here we tested whether also sea lions were able to perform hydrodynamic trail following in spite of their non-specialized hair structure. Hydrodynamic trails were generated by a remote-controlled miniature submarine. Linear trails could be followed with high accuracy, comparable to the performance of harbour seals, but in contrast, increasing delay resulted in a reduced performance as compared to harbour seals. The results of this study are consistent with the hypothesis that structural differences in the vibrissal hair types of otariid compared to phocid pinnipeds lead to different sensitivity of the vibrissae during forward swimming, but still reveal a good performance even in the species with non-specialized hair type.     

Monitoring harbour seal (Phoca vitulina) in the Danish Wadden Sea

Monitoring of harbour seal (Phoca vitulina) has been carried out in the Danis part of the Wadden Sea during the past 8 years by the Fishery and Maritime Museum. In addition to this, field observations over three breeding seasons have been undertaken. The census shows a steady increase of approx. 14% per yeart. The distribution of the seals in the area can be split up into two different types of haulout localities, and a varied pattern of haulouts is observed during the year. The mass die-off in 1988 is discussed within the framework of the knowledge on the population, and it is recommended that more effort be put into monitoring and population studies of the harbour seal in the entire International Wadden Sea. Presented at the VI International Wadden Sea Symposium (Biologische Anstalt Helgoland, Wattenmeerstation Sylt, D-2282 List, 1–4 November 1988)     

Evaluating the function of the male harbour seal, Phoca vitulina, roar through playback experiments

The aim of this study was to evaluate the role of vocalizations produced during the breeding season by the male harbour seal, an aquatically breeding pinniped. During the spring of 1999, playback experiments were conducted at eight locations in Elkhorn Slough, California, U.S.A. Through an underwater speaker, we presented male harbour seals with three acoustic stimuli: a long-duration, low-frequency roar (LL), a short-duration, high-frequency roar (SH) and amplified water noise (control). Male responses to the playback boat were characterized by increased approach rates and aggressive flipper slapping during 62.5% of SH sessions (N=8), 25% of LL sessions (N=8) and 0% of control sessions (N=8). No more than one identifiable seal responded during each playback location. We observed no responses by female harbour seals to playbacks. We conclude from these experiments that territorial male harbour seals use roars given by intruders to locate and challenge intruders.     

Histological,histochemical, and ultrastructural investigations on the gastrointestinal system of antarctic seals: Weddell seal (Leptonychotes weddellii) and crabeater seal (Lobodon carcinophagus)

The morphology of the principal sections of the gastrointestinal system of two Antarctic seals with different dietary habits, namely, the Weddell seal (Leptonychotes weddellii) and the crabeater seal (Lobodon carcinophagus), has been investigated. Histologically examined by light microscopy, the tissue layers of the gastrointestinal tract of both seals are almost identical to those observed in most other mammals and no major differences in principle organization could be found between the two seal species. The ultrastructure of the gastric and intestinal epithelial cells has been examined and is also closely comparable to that of these cells in other mammals; however, Paneth cells have not been found in our material. In general, therefore, adaptations of the gastrointestinal tract to the aquatic environment or the diet are not obvious at the morphological levels of organization studied. Histochemical differences are found between the two closely related species; mucins of the surface epithelium in the stomach of Weddell seals are highly sulfated, while those in the crabeater seal are not. Mucous neck cells in Weddell seals contain acid mucosubstances, while those of crabeater seals contain neutral ones. Goblet cells in the small and large intestine in Weddell seals contain both neutral and acid mucosubstances. Both mucin types are detected in the crabeater seal; however, the mucins of the colon in the crabeater seal are more highly sulfated than those in the Weddell seal. The ratio of globet cells to enterocytes in the large intestine of crabeater seals is higher than that in Weddell seals. © 1995 Wiley-Liss, Inc.     

BODY TEMPERATURE IN THE NEWBORN SOUTHERN ELEPHANT SEAL, MIROUNGA LEONINA, AT MACQUARIE ISLAND

Newborn southern elephant seal pups were reported by Laws (1953) to be "to some extent poikilothermic at birth." Rectal temperatures of known age southern elephant seal pups were recorded during the 1985 pupping season at Macquarie Island. The mean pup rectal temperature was found to be 381°C ± 0.1°C SEM ( n = 131, range = 36.5°-39.1°C). Pups at two hours, six hours, and one day after birth had significantly higher rectal temperatures than pups two, three, or four days of age. Rectal temperatures of neonatal southern elephant seals were within the range observed for other pinnipeds, (but never as low as the 31°C previously observed for southern elephant seals at Signy Island in 1953). A significant though weak positive correlation was found between pup temperature and body weight. However, no correlation between pup temperature and age or any environmental factor was found. These observations demonstrated that southern elephant seal pups at Macquarie Island are homeothermic, rather than heterothermic from birth.     

Increasing numbers of harbour seals and grey seals in the Solent

Harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) both occur within the UK, but display regional contrasting population trends. While grey seals are typically increasing in number, harbour seals have shown varying trends in recent decades following repeated pandemics. There is a need for monitoring of regional and local populations to understand overall trends. This study utilized a 20‐year dataset of seal counts from two neighboring harbours in the Solent region of south England. Generalized additive models showed a significant increase in the numbers of harbour (mean 5.3–30.5) and grey (mean 0–12.0) seals utilizing Chichester Harbour. Conversely, in Langstone Harbour there has been a slight decrease in the number of harbour seals (mean 5.3–4.0). Accompanying photographic data from 2016 to 18 supports the increase in seal numbers within Chichester Harbour, with a total of 68 harbour and 8 grey seals identified. These data also show evidence of site fidelity of harbour seals in this area, with almost a quarter of animals resighted within the past three years. Overall, this long‐term study indicates an increasing number of both harbour and grey seals within the Solent. However, more research is required to identify the drivers of this trend.     

Killing of Cape fur seal (Arctocephalus pusillus pusillus) pups by brown hyenas (Parahyaena brunnea) at mainland breeding colonies along the coastal Namib Desert

Brown hyenas (Parahyaena brunnea) scavenge and kill seal pups at mainland Cape fur seal (Arctocephalus pusillus pusillus) colonies. The prey encounter interval and interval between kills depended on seal density, and increased density resulted in an increase of the capture rate and increase in hunting efficiency from 14% in November to 47% in January. The time brown hyenas spent at the seal colony decreased with increasing seal density and increasing air temperatures. Nevertheless, they were regularly active during the day when less adult seals were present at the colony, which indicates that the attendance of adult seals might play a role in the choice of foraging time. Brown hyenas killed seal pups throughout the study period. The predation rate was independent of the availability of non-violent mortalities, but the absolute number of kills was positively density-dependent. Mass kill events were recorded throughout the study period and are therefore not unusual occurrences. The overabundance of easy and vulnerable prey may lead to an over stimulus situation that triggers killing independent of the consumption of the prey or the hunger state.     

Brain size in neonatal and adult Weddell seals: Costs and consequences of having a large brain

Little is known about the ontogeny of brain size in pinnipeds despite potential functional implications of brain substrate (glucose, oxygen) requirements for diving, fasting, growth, and lactation strategies. We measured brain mass (brM) and cranial capacity (CC) in newborn and adult Weddell seals. Neonatal Weddell seals had brM that represented ~70% of adult brM. Weddell seals have the largest neonatal brain, proportional to adult brain, reported for any mammal to date, which is remarkable considering the relatively small size of Weddell seal pups at birth (6%–7% of maternal body mass) compared to neonates of other highly precocial mammals. Provision of sufficient glucose to maintain the large, well‐developed brain of the neonatal Weddell seal has a nontrivial metabolic cost to both pup and mother. We therefore hypothesize that this phenomenon must have functional significance, such as allowing pups to acquire complex under‐ice navigation skills during the period of maternal attendance.     

The harbour seal,Phoca vitulina,in the Oosterschelde: decline and possibilities for recovery

Within a timespan of a few decadesm the harbour seal almost completely disappeared from the estuaries in the south-west of the Netherlands. In 1960 a population of around 350 animals still lived in the Oosterschelde and Westerschelde area. About a quarter of this population lived in the Oosterschelde. At present less than 17 animals can be regularly observed in the whole area. Human influences are responsible for the rapid decline of the population. Initially a high hunting pressure and later environmental pollution are the main causes. Loss of habitat and disturbance at the resting places are additional important factors. The Oosterschelde still is a suitable habitat for seals. A short term natural development of a viable population in the area is not to be expected. Only with human help through active management, i.e. reintroduction of rehabilitated seals (preferably originating from that area) and strict conservation of the extant Oosterschelde seal population, accompanied by environmental sanitation of the neighbouring waters, can the current southern Dutch harbour seal population increase.