Seal Faeces Research Articles

Diet and Feeding Behavior of the South Polar Skuas Stercorarius maccormicki in the Haswell Islands, East Antarctica

The diet and feeding behavior of South Polar Skuas (Stercorarius maccormicki) are well studied within the species’ breeding range but are poorly understood on the Haswell Islands. The aim of this study was to determine how South Polar Skuas use available resources during the pre-breeding and breeding periods at the Haswell Archipelago (66°31′ S, 93°01′ E, Davis Sea, Southern Ocean) under conditions of prolonged human activity. I studied pellets, spontaneous regurgitation, and stomach contents of feathered birds to study the diet of skuas and used direct observations of their feeding behavior. South Polar Skuas at the Haswell Islands fed primarily on the Emperor Penguin (Aptenodytes forsteri) colony and on terrestrial resources in the Adélie Penguin (Pygoscelis adeliae) and fulmarine petrel colonies. The dominant prey of skuas were breeding Antarctic penguins. Emperor Penguins and Adélie Penguins make up the bulk of the skuas’ diet in the pre-breeding and breeding periods. Surface feeding at sea was observed in the post-breeding period. In recent decades, kitchen waste supported the skua population. Scavenging (placenta and feces of Weddell seals [Leptonychotes weddellii], frozen eggs, chicks and adults of breeding bird species, kitchen refuse) is the dominant strategy for obtaining food. Adélie Penguin eggs and chicks were the main food items of the South Polar Skuas in the Haswell Archipelago. Skua predation could potentially influence the breeding success of Adélie Penguins and fulmarine petrels, but the extent of the impact is unknown. The impact of the South Polar Skua on Emperor Penguins is negligible because skuas feed mainly on frozen chicks and eggs of the species.

Variations in antimicrobial resistance genes present in the rectal faeces of seals in Scottish and Liverpool Bay coastal waters

Antibiotic resistance genes originating from human activity are considered important environmental pollutants. Wildlife species can act as sentinels for coastal environmental contamination and in this study we used qPCR array technology to investigate the variety and abundance of antimicrobial resistance genes (ARGs), mobile genetic elements (MGEs) and integrons circulating within seal populations both near to and far from large human populations located around the Scottish and northwest English coast. Rectal swabs were taken from 50 live grey seals and nine live harbour seals. Nucleic acids were stabilised upon collection, enabling extraction of sufficient quality and quantity DNA for downstream analysis. 78 ARG targets, including genes of clinical significance, four MGE targets and three integron targets were used to monitor genes within 22 sample pools. 30 ARGs were detected, as well as the integrons intl1 and intl2 and tnpA transposase. Four β-lactam, nine tetracycline, two phenicol, one trimethoprim, three aminoglycoside and ten multidrug resistance genes were detected as well as mcr-1 which confers resistance to colistin, an important drug of last resort. No sulphonamide, vancomycin, macrolide, lincosamide or streptogramin B (MLSB) resistance genes were detected. Resistance genes were detected in all sites but the highest number of ARGs (n = 29) was detected in samples derived from grey seals on the Isle of May, Scotland during the breeding season, and these genes also had the highest average abundance in relation to the 16S rRNA gene. This pilot study demonstrates the effectiveness of a culture-independent workflow for global analysis of ARGs within the microbiota of live, free-ranging, wild animals from habitats close to and remote from human habitation, and highlights seals as a valuable indicator species for monitoring the presence, abundance and land-sea transference of resistance genes within and between ecosystems.

A 1500-year record of mercury isotopes in seal feces documents sea ice changes in the Antarctic

Temporal and spatial variations in sea ice coverage at high Northern Hemisphere latitudes have been shown to affect the photodegradation of methylmercury in seawater and the mercury isotope signatures in biological samples, suggesting the potential of mercury isotopes to reconstruct sea ice variability. Here we study the mercury isotopic composition of a 1500-year sediment profile strongly affected by seal activities on the Fildes Peninsula, King George Island, Antarctic Peninsula. The mass independent isotope fractionation of mercury (represented by Δ199Hg) in sediments dominated by seal feces input reflects the Δ199Hg of marine methylmercury before entering the food web, documenting the changes in the degree of photodemethylation. We found much higher Δ199Hg in sediments deposited during a warm period (~700-1000 years ago), suggesting that reduced sea ice promoted greater photodemethylation. Thus, this study demonstrates the modulation of methylmercury photodegradation by sea ice in the Antarctic, and that mercury isotopes can record historical sea ice changes.

Monk seal faeces as a non-invasive technique to monitor the incidence of ingested microplastics and potential presence of plastic additives

Anthropogenic debris, including plastics, has recently been identified as a major threat for marine mammals and the Marine Strategy Framework Directive aims to achieve the good environmental status of European waters by addressing among other criteria, the effects of marine litter on biota.This study implemented for the first time a non-invasive technique for collecting monk seal samples to assess microdebris ingestion in combination with identifying plastic additives and porphyrins biomarkers. A total of 12 samples of monk seal faeces were collected from marine caves in Zakynthos Island, Greece.A total of 166 microplastic particles were identified; 75 % of the particles were smaller than 3 mm. Nine phthalates and three porphyrins were detected. A strong correlation was found between the number of microplastics and the concentration of phthalates. The values of both phthalates and porphyrins were found lower than in other marine mammal tissues, suggesting that seals might not be impacted by them yet.

New perspectives on morphological and genetic variability of Corynosoma bullosum [Linstow, 1892] parasitizing southern elephant seals from the Antarctic Peninsula.

Previous descriptions of Corynosoma bullosum (Linstow, 1892) show that specimens vary greatly in the proportions of different body structures, measurements of females and males, number of rows of hooks, and egg measurements, among other features. We redescribe this species from specimens found in southern elephant seal faeces from King George Island. We also provide a molecular characterization, in addition to 5.8S and internal transcribed spacer (ITS) existing sequences. We examined 41 elephant seals, and 30 adult acanthocephalans were found in 15 of them. The specimens were identified as belonging to the genus Corynosoma due to each having a tubular body with an inflated anterior part forming a thorny disk and the posterior part bearing somatic spines on the ventral surface, and genital spines surrounding the genital pore. Individual morphology corresponded to C. bullosum: large size, marked sexual dimorphism, and proboscis with 16-18 rows of spines with 11-15 spines per row. The molecular profile of three specimens of C. bullosum was analysed using 18S rDNA. We inferred phylogenetic relationships of the family Polymorphidae using maximum likelihood and Bayesian inference. We provide an updated morphological redescription for C. bullosum including electron microscopy photographs and molecular data. The 18S gene sequences showed low genetic variation and supported that C. bullosum is a sister to Corynosoma australe.

Trace and rare earth elements in excreta of two species of marine mammals from South Shetland Islands, Antarctica.

Pinnipeds are sentinel species for marine pollution, but their role as vectors of trace elements (TEs) or rare earth elements (REEs) to ecosystems has been poorly studied. The present study tested pinniped feces for 61 elements, including REEs. Feces of adult seals (Mirounga leonina, Hydrurga leptonyx) from Fildes Bay, King George Island, Antarctica, were analyzed by ICP-MS. TEs varied by several orders of magnitude across the suite examined herein, with Fe, Al, Zn, Mn, HgII and Sr as the top six in both species. Of the REEs, Ce, Dy, Er, Eu, Gd, Ho, La, Lu, Nd, Pr, Sc, Sm, Tb, Y and Yb were found consistently in all samples and ranged from 0.935 to 0.006μgg-1 d.w. The results show that both species act as biovector organisms of TEs and REEs through feces in remote environments, whose actual impacts and long-term fate need further exploration.

Faeces of marine birds and mammals as substrates for microbial plankton communities

The chemical composition of the seawater soluble fraction (WSF) of yellow-legged gulls and harbour seal faeces and their impact on microbial plankton communities from an eutrophic coastal area have been tested. After characterisation of the C:N:P stoichiometry, trace metals content and organic molecular composition of the faeces, significant differences between species have been observed in all parameters. Seagull faeces present about three times larger N content than seal faeces and are also richer in trace elements except for Cu and Zn. Organic nitrogen in seagull faeces is dominated by uric acid, while the proteins are the main N source in seal faeces. It is remarkable that seagull faeces are five times more soluble in seawater than seal faeces and present a much higher N content (48.0 versus 3.5 mg N in the WSF per gram of dry faeces), >85% of which as dissolved organic nitrogen, with C:N molar ratios of 2.4 and 13 for seagull and seal faeces, respectively. Based on this contrasting N content, large differences were expected in their impact on microbial populations. To test this hypothesis, a 3-day microcosm incubation experiment was performed, in which coastal seawater was amended with realistic concentrations of the WSF of seagull or seal faeces. A significant and similar increase in bacterial biomass occurred in response to both treatments. In the case of phytoplankton, the impact of the treatment with seagull faeces was significantly larger that the effect of the treatment with seal faeces. Our data suggest that the distinct competitive abilities of phytoplankton and bacteria largely influence the potential impact of distinct animal faeces on primary productivity in coastal ecosystems. Impacts on the microbial plankton communities do not affect only this trophic level, but the whole trophic chain, contributing to nutrient recycling in coastal areas where large populations of these species are settled.

Coprophagic behaviour of southern giant petrels (Macronectes giganteus) during breeding period

Southern giant petrels (Macronectes giganteus) are opportunistic generalists whose feeding strategies include hunting, scavenging and fishing. While seals are important for southern giant petrels as a source of carrion, we documented that live seals also provide feeding opportunities for southern giant petrels. We tracked breeding southern giant petrels from Harmony Point, Antarctica, during incubation and chick rearing with solar-powered GPS-UHF devices. Tracking results showed that animals often visited confirmed haul-out sites of seals, mainly Weddell seals (Leptonychotes weddellii). Feeding on seal faeces was confirmed by direct observation. Southern giant petrels were more likely to visit haul-out sites during incubation than during chick-rearing. This behaviour suggests that the birds fed on seal faeces mainly when fasting, which could last as long as 15 days. Seal faeces could be a resource consumed to quickly recover from the fast before leaving for a longer trip.

Could biotransport be an important pathway in the transfer of phenol derivatives into the coastal zone and aquatic system of the Southern Baltic?

Bird guano and the faeces of marine mammals appear to be a significant yet undisclosed biotransporter of Endocrine Disrupting Compounds in the marine environment. The authors determined the concentration of bisphenol A (BPA), 4-tert-octylphenol (4-t-OP) and 4-nonylphenol (4-NP) removed from birds and seals in their droppings into the coastal zone of the Gulf of Gdansk (Southern Baltic Sea).The research was carried out on samples of bird guano collected during the breeding season and after in 2016 at nesting sites, as well as on faecal samples from grey seals (Halichoerus grypus grypus) living in the Seal Centre of the Marine Station in Hel between 2014 and 2018. Measurements were carried out using high performance chromatography with fluorescence detector. Results have shown that the presence of seabird habitats and grey seal colonies in the coastal zone of the Gulf of Gdansk can have an impact on the pollution of the seashore (beach sand, bottom sediment and surface seawater) with phenol derivatives. The concentrations of BPA, 4-t-OP and 4-NP ranged from 0.1 to 32.97 ng∙g−1dw in sediment and beach sand, and from 0.23 to over 800 ng dm−3 in seawater. In the cases of bisphenol A and 4-tert-octylphenol safe concentration levels in the waters were exceeded. Bisphenol A concentrations were almost always found to be the highest. This was also noted in bird guano and seal faeces, although it was found to be much higher in the seal faeces - average 10149.79 ng g−1 dw, than in bird guano. An experiment conducted to assess BPA, 4-t-OP, 4-NP leaching from bird guano and seal faeces into seawater, also confirmed the importance of animal excrement in the circulation of these compounds in the marine ecosystem. The highest % of leaching related to BPA was noted at 20 °C and reached 84%. The lowest % of leaching was for 4-nonylphenol (44%).

Detecting spiny dogfish in grey seal diets

Grey seal (Halichoerus grypus) populations declined dramatically in U.S. waters during the nineteenth and twentieth centuries, but have rebounded in recent decades as a result of legal protection. In the Gulf of Maine, increasing grey seal populations have the potential to impact commercially important groundfish species such as cod and haddock, but the potential also exists for more complex ecological interactions to occur given the recent increase of spiny dogfish (Squalus acanthias), another potential groundfish predator. Specifically, seal predation on dogfish could free groundfish species from additional predation pressure. Little quantitative data exists on intraguild predation rates by grey seals on spiny dogfish, in part because of the limitations of current methods of food habits analysis for grey seals. We report the development, validation, and field testing of a non-invasive genetic method for the detection of spiny dogfish in grey seal diets using DNA collected from seal feces. Our method amplified spiny dogfish DNA from 10 of 10 positive control scats from a captive seal with a known diet, and amplified spiny dogfish DNA from 0 of 10 negative control scats. We field tested the method on 20 scats from wild seals and detected spiny dogfish in two of the samples. All positive amplifications were sequenced to verify the species identify, and all were spiny dogfish. Our method has the potential to provide valuable information about changing predator prey dynamics in the Gulf of Maine and elsewhere.

Molecular Detection of Circovirus and Adenovirus in Feces of Fur Seals (Arctocephalus spp.).

In some regions, little is known about exposure to viruses in coastal marine mammals. The present study aimed to detect viral RNA or DNA in 23 free-ranging fur seals on the northern coastline of Rio Grande do Sul State, Brazil. Polymerase chain reaction was used to detect nucleic acids of circoviruses, adenoviruses, morbilliviruses, vesiviruses, and coronaviruses in the feces from twenty-one South American fur seals (Arctocephalus australis) and two Subantarctic fur seals (A. tropicalis). Adenovirus DNA fragments were detected in two South American fur seals; nucleotide sequences of these fragments revealed a high degree of similarity to human adenovirus type C. Circovirus DNA fragments were detected in six animals of the same species. Two were phylogenetically similar to the Circovirus genus, whereas the other four nucleotide fragments showed no similarity to any of the known genera within the family Circoviridae. RNA fragments indicating the presence of coronavirus, vesivirus, and morbillivirus were not detected. These findings suggest that adenoviruses and circoviruses are circulating in fur seal populations found along the coast of Rio Grande do Sul State, Brazil.

Erratum to: Identifying prey items from New Zealand fur seal (Arctocephalus forsteri) faeces using massive parallel sequencing

The New Zealand fur seal (Arctocephalus forsteri) is one of many pinniped species that has shown a remarkable recovery from the brink of extinction after cessation of commercial sealing during the eighteenth and nineteenth centuries. It is commonly believed that this species competes with recreational and commercial fisheries. We identified prey items using massive parallel sequencing from New Zealand fur seal faecal samples that were collected throughout the species distribution. The data support generalist feeding behaviour for this species. The diet composition showed significant geographical and inter-seasonal variation. As many as 46 species of fish and 18 species of cephalopod were identified from a single colony. The data suggest cartilaginous species (sharks, rays, and skates) constitute an important part of the New Zealand fur seal diet. Approximately 10 % of the species identified in the seal diet were of significant commercial value, which indicates some qualitative food competition between New Zealand fur seals and commercial fisheries in exploiting marine species.

Identifying prey items from New Zealand fur seal (Arctocephalus forsteri) faeces using massive parallel sequencing

Identifying prey items from New Zealand fur seal (Arctocephalus forsteri) faeces using massive parallel sequencing

Metagenomic Survey of Viral Diversity Obtained from Feces of Subantarctic and South American Fur Seals.

The Brazilian South coast seasonally hosts numerous marine species, observed particularly during winter months. Some animals, including fur seals, are found dead or debilitated along the shore and may harbor potential pathogens within their microbiota. In the present study, a metagenomic approach was performed to evaluate the viral diversity in feces of fur seals found deceased along the coast of the state of Rio Grande do Sul. The fecal virome of two fur seal species was characterized: the South American fur seal (Arctocephalus australis) and the Subantarctic fur seal (Arctocephalus tropicalis). Fecal samples from 10 specimens (A. australis, n = 5; A. tropicalis, n = 5) were collected and viral particles were purified, extracted and amplified with a random PCR. The products were sequenced through Ion Torrent and Illumina platforms and assembled reads were submitted to BLASTx searches. Both viromes were dominated by bacteriophages and included a number of potentially novel virus genomes. Sequences of picobirnaviruses, picornaviruses and a hepevirus-like were identified in A. australis. A rotavirus related to group C, a novel member of the Sakobuvirus and a sapovirus very similar to California sea lion sapovirus 1 were found in A. tropicalis. Additionally, sequences of members of the Anelloviridae and Parvoviridae families were detected in both fur seal species. This is the first metagenomic study to screen the fecal virome of fur seals, contributing to a better understanding of the complexity of the viral community present in the intestinal microbiota of these animals.

Mercury Stable Isotopes in Ornithogenic Deposits As Tracers of Historical Cycling of Mercury in Ross Sea, Antarctica.

Production of methylmercury (MeHg) in ocean waters and its bioaccumulation in marine organisms are critical processes controlling the fate and toxicity of mercury (Hg). However, these processes are not well understood in the Antarctic, where high levels of MeHg are observed in the subsurface ocean (100-1000 m). We explored the use of Hg stable isotope compositions in historical and modern biological deposits as a new approach for discerning Hg sources and tracing MeHg cycling in the ocean and bioaccumulation in marine biota. We found similar mass independent isotope fractionation (MIF) of Hg between a sediment profile containing historical penguin and seal feces deposits from coastal Antarctica and modern penguin and seal feces, suggesting that penguin and seal feces were the dominant sources of Hg to the sediments at different time periods. Furthermore, sediments dominated by seal feces displayed a significantly lower MIF slope (Δ(199)Hg/Δ(201)Hg) than those dominated by penguin feces despite similar extents of MIF. Since seals forage at greater depths (>400 m) than penguins (<100 m), the high MIF values and lower Δ(199)Hg/Δ(201)Hg in seal feces suggest that a significant fraction of MeHg accumulated by seals was produced in situ in the subsurface ocean from residual inorganic Hg(II) that sank from the euphotic zone after partial photoreduction. Our results suggest that in situ Hg methylation can be an important source of MeHg for marine biota, and Hg isotope compositions in biological archives can be valuable tracers of MeHg cycling.

Surveillance for zoonotic and selected pathogens in harbor seals Phoca vitulina from central California.

The infection status of harbor seals Phoca vitulina in central California, USA, was evaluated through broad surveillance for pathogens in stranded and wild-caught animals from 2001 to 2008, with most samples collected in 2007 and 2008. Stranded animals from Mendocino County to San Luis Obispo County were sampled at a rehabilitation facility: The Marine Mammal Center (TMMC, n = 175); wild-caught animals were sampled at 2 locations: San Francisco Bay (SF, n = 78) and Tomales Bay (TB, n = 97), that differed in degree of urbanization. Low prevalences of Salmonella, Campylobacter, Giardia, and Cryptosporidium were detected in the feces of stranded and wild-caught seals. Clostridium perfringens and Escherichia coli were more prevalent in the feces of stranded (58% [78 out of 135] and 76% [102 out of 135]) than wild-caught (42% [45 out of 106] and 66% [68 out of 106]) seals, whereas Vibrio spp. were 16 times more likely to be cultured from the feces of seals from SF than TB or TMMC (p < 0.005). Brucella DNA was detected in 3.4% of dead stranded harbor seals (2 out of 58). Type A influenza was isolated from feces of 1 out of 96 wild-caught seals. Exposure to Toxoplasma gondii, Sarcocystis neurona, and type A influenza was only detected in the wild-caught harbor seals (post-weaning age classes), whereas antibody titers to Leptospira spp. were detected in stranded and wild-caught seals. No stranded (n = 109) or wild-caught (n = 217) harbor seals had antibodies to phocine distemper virus, although a single low titer to canine distemper virus was detected. These results highlight the role of harbor seals as sentinel species for zoonotic and terrestrial pathogens in the marine environment.

Isolation of human pathogen Escherichia albertii from faeces of seals (Leptonychotes weddelli) in James Ross Island, Antarctica

A set of nine gram-negative fermenting rods biochemically identified as Escherichia coli was isolated from faeces of seals. These bacteria were characterized by phenotypic classification, 16S rDNA sequence analyses, automated ribotyping, study of whole-cell protein profiles by SDS-PAGE and finally by bacteriocin production. The results of our polyphasic taxonomic study supported the recognition of P4652, P4653 and P4740 isolates as true members of Escherichia albertii species – probably a major enteric human pathogen. To our best knowledge, this is the first evidence showing that E. albertii produces bacteriocin, colicin D. Obtained data unambiguously showed incon-venience of commercial identification systems to distinguish both Escherichia species due to missing data of E. albertii in the commercial databases. The results of Escherichia isolates taxonomy suggest seals as a novel source of human and animal pathogen,E. albertii in the Antarctic region.

Organic geochemical characterization on a seal excrement sediment core from Fildes Peninsula, Western Antarctica

Organic geochemical analysis was performed on a sediment core HN1 from Fildes Peninsula on King George Island,Western Antarctica. Short-chain n -alkanes were the main components of the aliphatic hydrocarbons present, and they were likelyto be from algae and bacteria; n -C 23 was likely derived from moss. Fecal sterols and phytol dominated the alcohol composition,and may have come from seal feces and vegetation, respectively. The fluctuations in their concentrations generally haveresponded to historical changes in the ecosystems near the region. The even-carbon fatty acids, such as n -C 16 , n -C 18 and n -C 24 ,dominated the alkenoic acid composition, which mainly originated from bacteria, moss and zooplankton. The low concentrationsof unsaturated fatty acids showed a predominance of C 16:1 and C 18:1 unsaturated acids, and demonstrated that the sediment waswell preserved and had a simple and stable source of organic materials.

Diet, individual specialisation and breeding of brown skuas (Catharacta antarctica lonnbergi): an investigation using stable isotopes

The diet of brown skuas (Catharacta antarctica lonnbergi) on Bird Island, South Georgia was assessed using a combination of stable isotope analysis (SIA) and mixing model techniques. We found evidence that individual specialisation in diet of adult brown skuas was related to timing of breeding, which may reflect differences in intrinsic quality. Adults with more enriched 13C values hatched chicks earlier than those with depleted 13C values. Individuals with enriched 13C fed predominantly on Antarctic fur seal (Arctocephalus gazella) carrion and placenta while those with lower ratios appeared to rely more on burrowing petrels (e.g. Antarctic prions Pachyptila desolata). Individual foraging differences clearly influenced timing of breeding and potentially the reproductive output of breeding pairs. We confirmed that the main components of the diet of brown skuas during incubation are, in decreasing order of importance, Antarctic fur seal placenta, burrowing petrels and fur seal muscle. In addition, we identified fur seal faeces in the diet during this stage, which had not been detected previously by traditional sampling methods. Finally we identified a correlation in δ13C values between pair members, attributable to the influence of courtship feeding of females by males, or assortative mating according to foraging preference or intrinsic quality.

Risk factors for infection with pathogenic and antimicrobial-resistant fecal bacteria in northern elephant seals in California.

The goal of this study was to identify potential environmental and demographic factors associated with Campylobacter jejuni (C. jejuni), Salmonella enterica (Salmonella spp.), and antimicrobial-resistant Escherichia coli (E. coli) infection in northern elephant seals stranded along the California coastline. E. coli, Salmonella spp., and C. jejuni were isolated from rectal swabs from 196 juvenile northern elephant seals, which were found stranded and alive along the California coast and brought to The Marine Mammal Center in Sausalito, California, for rehabilitation. Gender, weight, county where the animal stranded, month stranded, coastal human population density, exposure to sewage outfall or freshwater outflow (river or stream), and cumulative precipitation in the previous 24 hours, seven days, 30 days, 90 days, and 180 days were analyzed as potential risk factors for infection. The odds of C. jejuni and antimicrobial-resistant E. coli were higher in feces of seals stranded at sites with higher levels of freshwater outflow compared with lower levels of freshwater outflow. The odds of Salmonella spp. in feces were 5.4 times greater in seals stranded in locations with lower levels of 30-day cumulative precipitation, along with substantially lower odds of Salmonella shedding for seals stranded in Monterey or Santa Cruz county compared with seals stranded in regions further north or south of this central California location. Juvenile northern elephant seals that have entered the water are being colonized by antimicrobial-resistant and pathogenic fecal bacteria that may be acquired from terrestrial sources transmitted via river and surface waters.