Lonneke L. IJsseldijk

Large amounts of marine debris found in sperm whales stranded along the North Sea coast in early 2016

30 sperm whales (Physeter macrocephalus) stranded along the coasts of the North Sea between January and February 2016. The gastro-intestinal tracts of 22 of the carcasses were investigated. Marine debris including netting, ropes, foils, packaging material and a part of a car were found in nine of the 22 individuals. Here we provide details about the findings and consequences for the animals. While none of the items was responsible for the death of the animal, the findings demonstrate the high level of exposure to marine debris and associated risks for large predators, such as the sperm whale.

Exposing the grey seal as a major predator of harbour porpoises

Harbour porpoises (Phocoena phocoena) stranding in large numbers around the southern North Sea with fatal, sharp-edged mutilations have spurred controversy among scientists, the fishing industry and conservationists, whose views about the likely cause differ. The recent detection of grey seal (Halichoerus grypus) DNA in bite marks on three mutilated harbour porpoises, as well as direct observations of grey seal attacks on porpoises, have identified this seal species as a probable cause. Bite mark characteristics were assessed in a retrospective analysis of photographs of dead harbour porpoises that stranded between 2003 and 2013 (n = 1081) on the Dutch coastline. There were 271 animals that were sufficiently fresh to allow macroscopic assessment of grey seal-associated wounds with certainty. In 25% of these, bite and claw marks were identified that were consistent with the marks found on animals that had tested positive for grey seal DNA. Affected animals were mostly healthy juveniles that had a thick blubber layer and had recently fed. We conclude that the majority of the mutilated harbour porpoises were victims of grey seal attacks and that predation by this species is one of the main causes of death in harbour porpoises in The Netherlands. We provide a decision tree that will help in the identification of future cases of grey seal predation on porpoises.

Anisakis spp. induced granulomatous dermatitis in a harbour porpoise Phocoena phocoena and a bottlenose dolphin Tursiops truncatus

Cetaceans are well known definitive hosts of parasitic nematodes of the genus Anisakis (Nematoda: Anisakidae). Anisakid nematodes are also a health hazard for humans, potentially causing gastrointestinal infections or allergic reactions following the consumption of infected fish. In marine mammals, the nematodes develop from third-stage larvae to adults in the stomachs. In the first (or fore-) stomach, these parasites are typically associated with mucosal ulceration; parasites have not been identified in other organs. Two small cetaceans, a bottlenose dolphin Tursiops truncatus and a harbour porpoise Phocoena phocoena, presented marked gastric A. simplex infection, as well as chronic granulomatous and ulcerative dermatitis with intralesional nematodes, bordered by epithelial hyperplasia. Nematodes in the skin of the bottlenose dolphin were morphologically similar to Anisakis spp. Morphology of the parasitic remnants in the skin lesion of the harbour porpoise was indistinct, but molecular identification confirmed the presence of A. simplex. This is the first report of Anisakis spp. infection in the skin of marine mammals.

A novel cetacean adenovirus in stranded harbour porpoises from the North Sea: detection and molecular characterization

Harbour porpoises (Phocoena phocoena) are the most prevalent cetaceans in the North Sea. The fecal viral flora of 21 harbour porpoises stranded along the Dutch coastline was analyzed by a metagenomics approach. Sequences of a novel cetacean mastadenovirus, designated harbour porpoise adenovirus 1 (HpAdV-1), were detected. The sequence of a 23-kbp genomic region, spanning the conserved late region, was determined using primer walking. Phylogenetic analysis indicated that HpAdV-1 is most closely related to bottlenose dolphin adenovirus and clusters with Cetartiodactyla adenoviruses. The prevalence of HpAdV-1 was low (2.6%) based on targeted PCR-screening of the intestinal contents of 151 harbour porpoises stranded between 2010 and 2013.

Plastic ingestion by harbour porpoises Phocoena phocoena in the Netherlands: Establishing a standardised method

Stomach contents of harbour porpoises (Phocoena phocoena) collected in the Netherlands between 2003 and 2013 were inspected for the presence of plastic and other man-made litter. In 654 stomach samples the frequency of occurrence of plastic litter was 7% with less than 0.5% additional presence of non-synthetic man-made litter. However, we show that when a dedicated standard protocol for the detection of litter is followed, a considerably higher percentage (15% of 81 harbour porpoise stomachs from the period 2010–2013) contained plastic litter. Results thus strongly depended on methods used and time period considered. Occurrence of litter in the stomach was correlated to the presence of other non-food remains like stones, shells, bog-wood, etc., suggesting that litter was often ingested accidentally when the animals foraged close to the bottom. Most items were small and were not considered to have had a major health impact. No evident differences in ingestion were found between sexes or age groups, with the exception that neonates contained no litter. Polyethylene and polypropylene were the most common plastic types encountered. Compared to earlier literature on the harbour porpoise and related species, our results suggest higher levels of ingestion of litter. This is largely due to the lack of dedicated protocols to investigate marine litter ingestion in previous studies. Still, the low frequency of ingestion, and minor number and mass of litter items found in harbour porpoises in the relatively polluted southern North Sea indicates that the species is not a strong candidate for annual monitoring of marine litter trends under the EU marine strategy framework directive. However, for longer-term comparisons and regional differences, with proper dedicated protocols applied, the harbour porpoise has specific use in quantifying litter presence in the, for that specific objective, poorly studied benthic marine habitat.

Fatal Asphyxiation in Two Long-Finned Pilot Whales (Globicephala melas) Caused by Common Soles (Solea solea)

Long-finned pilot whales (Globicephala melas) are rare visitors to the southern North Sea, but recently two individual strandings occurred on the Dutch coast. Both animals shared the same, unusual cause of death: asphyxiation from a common sole (Solea solea) stuck in their nasal cavity. This is a rare cause of death in cetaceans. Whilst asphyxiation has been reported in smaller odontocetes, there are no recent records of this occurring in Globicephala species. Here we report the stranding, necropsy and diet study results as well as discuss the unusual nature of this phenomenon. Flatfish are not a primary prey species for pilot whales and are rarely eaten by other cetaceans, such as harbour porpoises (Phocoena phocoena), in which there are several reports of asphyxiation due to airway obstruction by soles. This risk may be due to the fish’s flexible bodies which can enter small cavities either actively in an attempt to escape or passively due to the whale ‘coughing’ or ‘sneezing’ to rid itself of the blockage of the trachea. It is also possible that the fish enter the airways whilst the whale is re-articulating the larynx after trying to ingest large, oddly shaped prey. It is unlikely that the soles entered the airways after the death of the whales and we believe therefore that they are responsible for the death of these animals.

Identification of a novel gammaherpesvirus associated with (muco)cutaneous lesions in harbour porpoises (Phocoena phocoena)

Herpesviruses infect a wide range of vertebrates, including toothed whales of the order Cetacea. One of the smallest toothed whales is the harbour porpoise (Phocoena phocoena), which is widespread in the coastal waters of the northern hemisphere, including the North Sea. Here, we describe the detection and phylogenetic analysis of a novel gammaherpesvirus associated with mucocutaneous and skin lesions in stranded harbour porpoises along the Dutch coast, tentatively designated phocoenid herpesvirus 1 (PhoHV1). Phylogenetically, PhoHV1 forms a monophyletic clade with all other gammaherpesviruses described in toothed whales (Odontoceti) to date, suggesting a common evolutionary origin.

Inter-individual differences in contamination profiles as tracer of social group association in stranded sperm whales

Ecological and physiological factors lead to different contamination patterns in individual marine mammals. The objective of the present study was to assess whether variations in contamination profiles are indicative of social structures of young male sperm whales as they might reflect a variation in feeding preferences and/or in utilized feeding grounds. We used a total of 61 variables associated with organic compounds and trace element concentrations measured in muscle, liver, kidney and blubber gained from 24 sperm whales that stranded in the North Sea in January and February 2016. Combining contaminant and genetic data, there is evidence for at least two cohorts with different origin among these stranded sperm whales; one from the Canary Island region and one from the northern part of the Atlantic. While genetic data unravel relatedness and kinship, contamination data integrate over areas, where animals occured during their lifetime. Especially in long-lived animals with a large migratory potential, as sperm whales, contamination data may carry highly relevant information about aggregation through time and space.

Toxoplasma gondii in stranded marine mammals from the North Sea and Eastern Atlantic Ocean : findings and diagnostic difficulties

The occurrence of the zoonotic protozoan parasite Toxoplasma gondii in marine mammals remains a poorly understood phenomenon. In this study, samples from 589 marine mammal species and 34 European otters (Lutra lutra), stranded on the coasts of Scotland, Belgium, France, The Netherlands and Germany, were tested for the presence of T. gondii. Brain samples were analysed by polymerase chain reaction (PCR) for detection of parasite DNA. Blood and muscle fluid samples were tested for specific antibodies using a modified agglutination test (MAT), a commercial multi-species enzyme-linked immunosorbent assay (ELISA) and an immunofluorescence assay (IFA). Out of 193 animals tested by PCR, only two harbour porpoise (Phocoena phocoena) cerebrum samples, obtained from animals stranded on the Dutch coast, tested positive. The serological results showed a wide variation depending on the test used. Using a cut-off value of 1/40 dilution in MAT, 141 out of 292 animals (41%) were positive. Using IFA, 30 out of 244 tested samples (12%) were positive at a 1/50 dilution. The commercial ELISA yielded 7% positives with a cut-off of the sample-to-positive (S/P) ratio≥50; and 12% when the cut-off was set at S/P ratio≥20. The high number of positives in MAT may be an overestimation due to the high degree of haemolysis of the samples and/or the presence of lipids. The ELISA results could be an underestimation due to the use of a multispecies conjugate. Our results confirm the presence of T. gondii in marine mammals in The Netherlands and show exposure to the parasite in both the North Sea and the Eastern Atlantic Ocean. We also highlight the limitations of the tests used to diagnose T. gondii in stranded marine mammals.

Beached bachelors: An extensive study on the largest recorded sperm whale Physeter macrocephalus mortality event in the North Sea

Between the 8th January and the 25th February 2016, the largest sperm whale Physeter macrocephalus mortality event ever recorded in the North Sea occurred with 30 sperm whales stranding in five countries within six weeks. All sperm whales were immature males. Groups were stratified by size, with the smaller animals stranding in the Netherlands, and the largest in England. The majority (n = 27) of the stranded animals were necropsied and/or sampled, allowing for an international and comprehensive investigation into this mortality event. The animals were in fair to good nutritional condition and, aside from the pathologies caused by stranding, did not exhibit significant evidence of disease or trauma. Infectious agents were found, including various parasite species, several bacterial and fungal pathogens and a novel alphaherpesvirus. In nine of the sperm whales a variety of marine litter was found. However, none of these findings were considered to have been the primary cause of the stranding event. Potential anthropogenic and environmental factors that may have caused the sperm whales to enter the North Sea were assessed. Once sperm whales enter the North Sea and head south, the water becomes progressively shallower (<40 m), making this region a global hotspot for sperm whale strandings. We conclude that the reasons for sperm whales to enter the southern North Sea are the result of complex interactions of extrinsic environmental factors. As such, these large mortality events seldom have a single ultimate cause and it is only through multidisciplinary, collaborative approaches that potentially multifactorial large-scale stranding events can be effectively investigated.