Abstract

1. Diet studies of marine mammals typically summarise prey composition across all individuals studied. Variation in individual diets is usually ignored, but may be more than just “noise” around an optimal foraging strategy that should be the same across the entire population. Instead, different individuals may have both different needs, and different skills to fulfill their requirements and diets may differ structurally between different groups of individuals within a population. Here we show that diets of harbour porpoises differ with age and nutritional condition of individuals, as well as seasonally. Even though all porpoises should probably strive to feed, at least partially, on energy-rich prey, such as clupeids or sandeels, the diet of juveniles is dominated by small, lean, gobies, and that of adults by larger, but also lean gadoids. Prey with a relatively high energy density was found in only a third of the porpoises with non-empty stomachs, and in about one quarter of all porpoises. In a multivariate assessment of prey composition against factors such as porpoise size, season and porpoise body condition, we found the highest proportion of empty stomachs, the lowest reconstructed prey masses in non-empty stomachs, and the lowest proportion of energy-rich prey in summer. We also found lower reconstructed prey masses in porpoises in poorer condition. Our results show that individual differences matter, in that porpoise diet develops with porpoise size (as a proxy for age) and that this development may be affected by the change of the seasons, and by individual mishap, leading to starvation.

2. The distribution of harbour porpoises Phocoena phocoena in the North Sea has shifted southwards in recent years. Apparently, many animals left areas previously rich in sandeels and moved to a region where much leaner gobies and gadoids are important prey. This shift in range, and presumably in diet, does not seem to have affected the body condition of all porpoises in the South. Body condition varies in stranded specimen found in The Netherlands, from very good to very poor. Emaciation is a common cause of death in this species, indicating that periods of decreased quantity or quality of prey can be detrimental to the species. The question thus arises whether emaciated harbour porpoises could not find sufficient food or whether their food was of insufficient quality. Stomachs of emaciated animals are not necessarily empty but, in fact, often contained food remains. In this study we examine these remains and compare the prey composition of well-nourished porpoises to that of progressively leaner specimens, collected between 2006 and 2014. We hypothesize that porpoises might starve by eating relatively too much prey with a low fat content that has a low energy density. Such food may be referred to as junk food: prey that is too lean for maintaining a good body condition. Results show that there is a significant difference in prey composition between animals in a good body condition and animals in a poor body condition, that starving animals have fewer prey remains in their stomachs, and that these prey, on average, are of lower quality. Healthy harbour porpoises take a mixture of fatty fish and leaner prey: the “big four” in dietary terms are clupeids and sandeels with a relatively high fat content, and gadoids and gobies, which are leaner prey. Our findings show that there is a negative correlation between the loss of body mass and the ingestion of fatty fish. This indicates that the emaciation is likely due to a lack of energy-rich prey, and that harbour porpoises need these prey in their diet to prevent starvation.

3. Fisheries bycatch, particularly in bottom-set nets, is an important cause of death in harbour porpoises Phocoena phocoena. Identifying bycatch from post-mortem studies on stranded porpoise carcasses is often difficult and relies on a combination of features. One characteristic considered consistent with bycatch is a full stomach, as this signals an acute death. Here we show that when porpoises are mostly bycaught in bottom-set nets, prey species composition, rather than the quantity of prey remains in their stomachs is the most informative characteristic to identify bycatch. Certain and highly probable bycatches (i.e., those porpoise carcasses brought in by fishers or with net marks and other evidence of bycatch) had a high proportion of demersal fish prey in their stomachs, usually >94% by mass of all fishes identified. Less certain cases, so-called probable and possible bycatches, included progressively more animals with lower percentages of demersal fish prey mass. The certain and highly probable bycatches also tended to have higher proportions of demersal prey in their stomachs, compared to animals that had died from other causes of death (e.g., emaciation, infectious disease, grey seal predation or unknown causes). This relationship was used to improve the classification of those porpoises classified as probable or possible bycatch. Prey species composition may thus be used as an additional bycatch criterion during post-mortem studies of stranded cetaceans, if the type of fishery responsible for the bycatches is known.

4. As rivers are being cleaned, life is returning to their estuaries and higher parts. Diadromous fish species are on the increase again in many major rivers discharging into the North Sea. Harbour porpoises (Phocoena phocoena), being predators of fish, have been noted to return to North Sea estuaries and rivers as well. Their mere presence in these rivers, however, is no proof that these small cetaceans actually exploit the returning fish. Diet studies of the porpoises found up-river can shed a light on their prey choice and ecological role in the system. Here we show that a major part of the diet of porpoises found in the river Western Scheldt (2007-2014) comprises diadromous fish, particularly juvenile European smelt (Osmerus eperlanus). Smelt contributed 46% to porpoise diet (% prey mass) in the Western Scheldt, against 14% in the river mouth and 3% in the North Sea at either side of the river mouth. Even though porpoise numbers are increasing in the river, not all is well, however. Animals found dead on the river banks were generally in a poor nutritional condition and had an elevated probability of being found dead with an empty stomach. Animals swimming very far upstream sometimes braved major water works such as sluices, which might have hindered their return to the sea. Relatively many animals were reported dead later, but to date, too few have been collected for stomach content analysis to make a valid comparison between diets in the lower and higher parts of this river system possible.

5. DNA was analysed from external wounds on 3 dead harbour porpoises Phocoena phocoena that were stranded in the Netherlands. Puncture wounds as well as the edges of large open wounds were sampled with sterile cotton swabs. With specific primers that target the mtDNA control region of grey seal Halichoerus grypus, a 196 bp DNA fragment was amplified from 4 puncture wounds. Sequencing of the fragments confirmed the presence of grey seal DNA in the puncture wounds. DNA sequences differed between the cases, implying that 3 individual grey seals were involved. As 8 control swabs from intact skin and the transport bag as well as 6 swabs from open wounds on the same harbour porpoises were all negative, contamination with environmental DNA is considered unlikely. The results provide a link between strandings of mutilated harbour porpoises and recent observations of grey seals attacking harbour porpoises. Ours is the first study to use forensic techniques to identify DNA in bite marks from carcasses recovered from the marine environment. This approach can be extended to identify other marine aggressors, including cases involving persons mutilated at sea.

6. 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.

7. Along the Dutch shores hundreds of harbour porpoises Phocoena phocoena are stranded each year. A recurrent phenomenon in the Netherlands is a surge of strandings in late winter and early spring of severely mutilated porpoises, that are mostly in good nutritional body condition (thick blubber layer). These mutilated porpoises have parts of the skin and blubber, and sometimes of the muscle tissue missing. By reviewing photographs of stranded animals taken at the stranding sites as well as necropsy results we found 273 mutilated animals from 2005 to 2012. Mutilations could be classified into several categories, but wounds had been mostly inflicted to the sides of these animals, in a zigzag fashion, or to the throat/cheek region. The stomach contents of 31 zigzags, 12 throats/cheeks and 31 control animals that were not mutilated, from the same age and blubber thickness categories were compared; all these animals had stranded between December and April, 2006–2012. The diet of individuals with zigzag lesions to their sides consisted for a large part of gobies, while animals that had wounds at the throat/cheek had been feeding predominately on clupeids. In comparison, animals without mutilations had a more varied diet, including gobies and clupeids, but also a large proportion of sandeels and gadoids. The finding that the type of mutilation corresponds to a certain diet suggests that porpoises that were feeding on different prey, or in different micro-habitats, were hit in different ways. Animals feeding at the sea floor (on gobies) apparently run a risk of being hit from the side, while animals supposedly feeding higher in the water column (on schooling clupeids), were predominantly hit from below, in the throat region. The wider variation in the diets of non-mutilated porpoises is suggestive of them using a larger variety of micro-habitats.