Not to be cited without prior permission from the authors

Not to be cited without prior permission from the authors ICES CM 2005/THEME SESSION R:15 (Marine Mammals: Monitoring Techniques, Abundance Estimation, and Interactions with Fisheries) Harbour porpoise (Phocoena phocoena) feeding ecology in the eastern North Sea M.B. Santos, G.J. Pierce, E.N. Ieno, M. Addink, C. Smeenk, C.C. Kinze & M. Sacau Results are presented on the analyses of harbour porpoise stomach contents from animals stranded and by-caught in Denmark and The Netherlands. A total of 58 non-empty stomach contents were collected and analysed from Denmark between 1985 and 1992, while 90 nonempty stomachs were analysed from The Netherlands between 1986 and 2003. In Denmark cod (Gadidae), viviparous blenny (Zoarcidae) and whiting (Gadidae) made up most of the diet while in the Netherlands whiting was the main prey, making up around ¾ of the total reconstructed prey weight. Variability in the diet was analysed in relation to year, season, cause of death, sex and size and results are compared with those from studies on this species from Scottish waters. Historically, herring was an important component of porpoise diet and we examine whether the recent increase in herring abundance in the North Sea has been reflected in porpoise diets. Preliminary estimates are also made on the amount of fish removed by harbour porpoises in the North Sea. KEYWORDS: harbour porpoise, herring, diet, fisheries M.B. Santos, M. Sacau: Instituto Español de Oceanografía, Centro Oceanográfico de Vigo, P.O. Box 1552, 36200, Vigo, Spain [tel: +34 986 492111, fax: +34 986 492351, e-mail: m.b.santos@vi.ieo.es, mar.sacau@vi.ieo.es]. M.B. Santos, G.J. Pierce, E.N. Ieno: Department of Zoology, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, Aberdeen, UK [tel: +44 1224 272459, fax: +44 1224 272396, e-mail: m.b.santos@abdn.ac.uk, g.j.pierce@abdn.ac.uk, e.n.ieno@abdn.ac.uk]. M. Addink and C. Smeenk: National Museum of Natural History, Darwinweg 22300 RA, Leiden, The Netherlands [tel: +31 71 5687611, smeenk@naturalis.nnm.nl, addink@naturalis.nnm.nl]. C.C.Kinze: CCKonsult Falkoner Alle 35 1th, 2000 Frederiksberg, Denmark [tel: +45 2168 2831, e-mail: CCKonsult@mail.dk]. E.N. Ieno: Highland Statistics Ltd., 6 Laverock road, Newburgh, Aberdeenshire, AB41 6FN, UK [tel: +44 1358 789293, e-mail: highstat@highstat.com]. 1

Introduction The harbour or common porpoise (Phocoena phocoena L.), is one of the most common cetaceans in European waters (Watson, 1985; Hammond et al., 2002). The 1994 survey of Small Cetacean Abundance in the North Sea (SCANS) led to an estimate of around 340,000 porpoises in the North Sea and adjacent waters (Hammond et al., 2002). Harbour porpoise is one of the smallest cetaceans and most of its range is in cold waters. Their life history includes a very short nursing period (usually less than 1 year), sexual maturity is attained at around 3 years of age and there is a very short resting period between pregnancies, so that females are often pregnant and lactating at the same time (Read et al., 1997). Their habitat and life history characteristics thus impose very high energetic demands on harbour porpoises. Their small body size means that they cannot store much energy and makes them more dependant on a year-round proximity to food sources (Brodie, 1995). Strandings data from the Netherlands suggest that porpoise numbers declined in the southern North Sea during the 1960s (Smeenk, 1987). Several hypotheses have been proposed to explain this decline including the well-documented collapse of the North Sea herring (Clupea harengus) stock. Historically, herring was recorded as being among the most important prey of porpoises (e.g. Rae, 1965, 1973). In general, recent dietary studies show that porpoises take both demersal and pelagic fish, as well as invertebrates such as cephalopods, although none indicate that herring dominates the diet. There are differences in diet between areas, although comparisons may be confounded by seasonal and interannual variation in diet. Certain fish species, notably whiting, herring, sandeels and gobies, feature in the diet in several areas. Because of the wide range of prey species found in the diet, it has been proposed that the harbour porpoise is a catholic feeder, not only limited to shallow waters, but able also to feed pelagically on midwater species from deeper habitats (IWC, 1996). However, usually the diet is dominated by a small number of prey species (Santos & Pierce, 2003). Herring is an energy-rich food source compared to gadids such as whiting (Murray & Burt, 1969) and there is evidence from studies on pinnipeds that switching from a clupeid diet to a gadid diet can have adverse physiological effects (e.g. anaemia and reduced leukocyte counts Thompson et al., 1997) and potentially negative consequences for population status (e.g. the decline of Steller s sea lion and the junk food hypothesis Trites & Donnelly, 2003). Dudok van Heel (1962) who observed that captive porpoises fed on young cod lost weight, but this weight loss was halted when the diet was changed to the same amount of herring. Although the North Sea herring fishery has shown marked fluctuations in catches throughout its history, it was the mechanisation of the fishery in the 20 th century that ultimately brought on the stock collapse between the mid-1960s and the mid-1970s. The spawning stock biomass fell from 2 million tonnes to below 50,000 tonnes with recruitment being drastically reduced (ICES 2005). The collapse affected different components of the herring stock in different ways, with the southern components declining before the northern components (Burd, 1985; Cushing, 1992). The fishery was closed from February 1977 to October 1981 (Burd, 1985). The stock was considered to have recovered again by the early 1990s but biomass declined again in the mid-1990s and only strong management measures ensured that the stock did not collapse (Nichols, 2001). Camphuysen (1994) noted that the increase in herring stocks had been followed by a slight increase in sightings of harbour porpoises in the Southeast North Sea since 1992. 2

In the last few years, the North Sea herring stock has recovered and it is now believed to be above 2 million tones (ICES, 2005). Harbour porpoise sightings in Dutch coastal waters have increased dramatically since the mid-1980s, with the sightings rate in 2004 being almost 40 times higher than that in the mid-1980s (Camphuysen, 2005). This increase presumably reflects a shift in distribution rather than increased abundance and may reflect changes in prey distribution and abundance. The most recent published study, for Scottish (UK) waters, indicated that sandeels (Ammodytidae) and whiting (Merlangius merlangus) were the most important prey species during 1992-2003 (Santos et al., 2004). These authors also found evidence that some variation in diet could be related to variation in fish abundance, seasonally and geographically. No similarly detailed analysis has been carried out for other parts of the NE Atlantic. The present study presents new results on porpoise diet from Dutch and Danish waters, identifying the main prey species and analysing sources of variation. In particular, we examine evidence that dietary variation has tracked changes in herring abundance. Material & Methods Collection of samples Denmark: stomach contents and ancillary biological data from harbour porpoises by-caught and stranded in Denmark were collected under the auspices of the Danish Stranding Network run by the Fisheries and Maritime Museum of Esbjerg, the Zoological Museum part of the University of Copenhagen and the Danish Ministry of Environment and Energy. The animals studied were mainly collected between 1985 and 1992, although some specimens from earlier years were also analysed. Ancillary biological data available usually included total length, weight and sex. Netherlands: stomach contents of harbour porpoises stranded in the Netherlands were collected through the national strandings network from 1986 to 2003. An additional sample from 1976 was also available. As for Denmark, data on length, weight, sex and maturity were available for most animals. Ancillary data Age estimates were based on counts of growth layer groups in tooth sections, prepared following standard methodology (e.g. Hohn & Lockyer, 1995). Assessment of maturity was based on examination of gonads, again following standard methodology (Perrin et al., 1984): ovaries were measured and checked for presence of corpora scars; testes were measured and examined histologically. Full details of life history parameters are presented elsewhere. Since age was not available for all animals we also used body length as a proxy for age. Basic statistical analysis of sample composition in terms of region, age, size, sex, season and year was carried out using ANOVA and Chi-squared tests, to identify imbalances in the sampling and possible confounding factors which could affect the interpretation of dietary variability (e.g. did the sex ratio differ between seasons?). Prey identification Methods for prey identification follow those described by Santos et al. (2004). Hard remains 3

of fish and cephalopods were identified using reference material and published guides (Clarke 1986; Härkönen 1986; Watt et al. 1997). The minimum number of individual fish and cephalopods in each stomach was estimated from hard remains (from otoliths and paired skull bones such as jaws, and beaks, respectively). Prey length was estimated from measurements on otoliths and beaks, using published regressions. Prey weight was estimated either from prey length or directly from hard part size, depending on the availability of published regressions (Bedford et al. 1986; Clarke 1986; Härkönen 1986; Coull et al. 1989). Fish size estimates were generally based on otolith length but width was used for otoliths with broken tips and for all otoliths of clupeids and gobies (Härkönen 1986). For cephalopods, measurements were normally made on the lower beak - rostral length for squid and hood length for octopus and sepiolids (Clarke 1986). For stomachs in which one category of fish or cephalopod was represented by >30 otoliths (or beaks), a random sample of 30-60 (from that category) was measured. Estimates of total prey biomass therefore incorporate raising factors, assuming that unmeasured remains represent prey of similar size to those measured. For otoliths identifiable only to a high taxonomic category (e.g. family), regressions were based on combined data from all the species in the taxon which could be present and for which data were available. Each otolith was assumed to represent 0.5 fishes. Complete pairs of cephalopod beaks were rarely present and in all cases size was estimated from either the upper or the lower beak. Few crustacean and polychaete remains were present in the samples and these were usually not identifiable to species, due to the poor state of preservation. Reconstructed prey weights are not corrected for digestive erosion. The option of using only fresh prey remains or only the least digested otoliths to reconstruct diet was not considered viable as few fresh prey remains were recovered. Otolith grading, followed by use of gradespecific correction factors, is theoretically possible but relevant correction factors are not currently available for all prey groups. Most analysis in the present study is therefore based on prey numbers so that size reduction of hard parts is not an issue. Furthermore, comparisons are generally based on single categories of prey to avoid biases due to interspecific variation in recovery rate of otoliths from stomachs (loss of otoliths is normally assumed to be due to complete digestion the frequency of which will depend on otolith robustness). Assessment of the importance of individual prey categories Overall importance of each prey type in the diet of porpoises was assessed using (a) frequency of occurrence, (b) proportion of the total number of prey, and (c) proportion of total prey weight. Although prey weight provides the best proxy for the energetic importance of each prey type to porpoises, not all prey remains could be used to estimate prey size and the weight data are thus slightly less complete than data on prey numbers or presence (see results). To evaluate the effect of this bias on estimated overall diet composition, corrections were made for prey that could be identified (e.g. from bone fragments) but for which size could not be estimated: it is assumed that they had the same size distribution as the prey measured. In several cases bones could be identified to family level but not species. In these cases, for estimation of overall diet composition, such prey remains were assigned pro rata to the species (from that family) already identified. This adjustment was not possible at the individual (porpoise) level. No explicit weighting was applied to individual stomach samples. Thus, when calculating the overall diet, the contribution of each stomach is proportional to the total estimated reconstructed weight of the prey contained therein. 4

We analysed dietary differences related to area, season (quarter), porpoise size, age, sex, maturity and year. Years were grouped into 5-year periods. Three porpoise length classes were defined: 118 cm, 119-140 cm, >140 cm. This division serves to separate first year animals ( 118 cm, Lockyer, 1995). Diets of different groups of porpoises were compared in terms of numbers and average (median) size for each of the main prey types in individual porpoise stomachs. The Dutch and Danish data were initially analysed together and then separately. To examine multivariate patterns in diet and to identify which environmental factors (in this case 5-year period, season, sex and body size) best explained these patterns, we used PRIMER 5 software (Primer-E Ltd). MDS (multidimensional scaling) was used to visualise patterns in the dietary data. For this analysis, prey types present in only one or two individuals were excluded, as were any animals containing only those prey types. Dietary data were square root transformed prior to calculating similarity matrices based on Euclidean distance. The categorical and ordinal environmental variables country, quarter, sex and length class were re-coded into dummy variables, each of which took a value of 0 or 1. The RELATE routine (using Spearman s rank correlation coefficient) was used to test the null hypothesis that there was no multivariate relationship between dietary and environmental data. The BIOENV and BVSTEP routines were used to select the set of environmental variables best explaining patterns the dietary data. Both routines compute rank correlations between dietary and environmental similarity matrices using different permutations of the environmental variables. The former compares different combinations of a specified number of environmental variables; the latter uses a step-wise procedure to identify the best subset of variables. Note that the set of environmental variables selected is not necessarily the set of variables that, individually, correlate most highly with dietary variation. If two environmental variables are strongly correlated with each other, once the first has been selected as a predictor the second will add little to predictive power and is unlikely to be selected. To examine the effects on diet of each factor in more detail, univariate analyses were used. Diets of different groups of porpoises were compared in terms of numbers and average (median) size for each of the main prey types in individual porpoise stomachs. For illustration of prey size spectra we reconstructed the overall size distributions, for each prey category, for each group of porpoises. However, since different individual fish of the same species from a single stomach are not independent samples, for statistical comparisons we used median prey lengths for each prey category for each porpoise. This avoids the problem of pseudoreplication. Because the statistical distributions of dietary parameters were generally non-normal, we relied primarily on non-parametric tests. Where significant variation was detected using Kruskal-Wallis tests, each pair of samples was compared using Mann-Whitney tests to identify groups that differed significantly from others. We also used correlation analysis to quantify the relationship between body size and porpoise diet. Clupeid consumption and fish abundance Total estimated weight of herring consumed by porpoises was divided by the number of stomachs analysed each year in each area to obtain an average figure of fish consumed that year. Correlations between this average and two indices of North Sea herring stock abundance (recruitment and spawning stock biomass) were quantified. Both indices of herring abundance 5

were obtained from the latest report of the ICES Advisory Committee on Fishery Management and Advisory Committee on Ecosystems (ICES, 2004). Estimation of food consumption by porpoises Annual consumption of the main prey species (I, tonnes) by harbour porpoises in Danish and Dutch waters was estimated using the following simple equation: Where: I = N * P i * F * T N (porpoise population size) was taken from the SCANS survey estimates for each area (Hammond et al., 2002). We considered survey blocks I- Kattegat, L- Coastal areas south and west of Jutland and Y- Northern Wadden Sea as Danish waters and survey block H- South eastern North Sea as Dutch waters for the purposes of this study (see Figure 1). Population size was assumed to be constant during the study period. P i (proportion by weight of prey species i in the diet was calculated, pooling together all the diet data for porpoises stranded in each area during the study period. Lavigne et al. (1986) and Innes et al. (1987) concluded that there was no fundamental difference in energy requirements of marine and terrestrial mammals. Innes et al. (1987) derived equations relating food intake to body mass for odontocete cetaceans. For adults: 0.66 IE = 0.313 M where IE = biomass ingestion rate (kg d -1 ) M = body mass (kg) For harbour porpoises, with body weights up to around 50 kg, this implies daily food consumption of around 8% of body weight. (For large whales the figure drops below 3%.). However, Yasui & Gaskin (1986) suggested that food requirements of harbour porpoises were around 3.5% of body weight daily. Length (cm) and weight (kg) data were available for 68 of the Dutch porpoises; these animals had an average weight of 32.6 kg. A length-weight relationship was derived from these data: 2.6538 W = 0.00008 L (R 2 = 0.86) Applying this to the animals for which body length data but no weight data were available (N=21) givesa final sample size of 79, for which the average body weight of 32.3 kg. Length and weight data were available from 52 of the Danish porpoises; the average weight of these animals was 39.6 kg. A length-weight relationship was derived from these data: 2.1303 W = 0.001139 L (R 2 = 0.89) Applying this to the animals for which body length data but no weight data were available (N=6) gives a final sample size of 61, for which average body weight was 39.7 kg. F (average weight of food eaten daily per porpoise), was then calculated from the values of 3.5% and 8% of porpoise weight (the two extremes from the literature). Mean values for F were then obtained. These were assumed to be representative of the population as a whole. T (number of days when prey and predator are in contact) was assumed to be 365. 6

This approach ignores seasonal and regional variation in diet and furthermore treats each porpoise as an average porpoise, ignoring population structure. However, the data available do not justify a more detailed approach. 7

Results Composition of the samples The Dutch sample comprised 90 stranded and by-caught animals collected between 1976 and 2003, the majority from 1990-1994. For 6 of the 90 animals by-catch could be clearly determined as the cause of death. There were slightly more females than males, while the three size classes were recorded with similar frequency. Almost 80% of the samples derived from the first and fourth quarters of the year (Table 1). Age data were available for 56 animals, with ages ranging from 0 to 13.5 years and a median of 5. The Danish sample comprised 58 mainly by-caught animals collected between 1985 and 1992, the majority from 1990-1992. The sex ratio was almost 1:1 and the sample included relatively few animals from the smallest size class. More than 80% of the sample is from the second and third quarter of the year (Table 1). Age data were available for 39 animals, with ages ranging from 0 to 16 years and a median age of 4. Overall diet composition: Denmark A total of 7,847 otoliths representing approximately 4,108 fish was recovered from the stomachs together with 47 upper and 38 lower beaks belonging to at least 51 cephalopods. Fourteen fish species and two cephalopod species were identified (Table 2). Crustaceans, polychaetes and non-cephalopod mollusc remains were also found in some stomachs (eleven, fifteen and eleven respectively). Cod, viviparous blenny (Zoarcidae) and whiting made up almost two thirds of the total estimated prey weight. Other species eaten included herring, sandeel and gobies. The estimated lengths of viviparous blenny ranged from 6.5 to 34.4 cm with a clear mode at 18.5 cm. Cod eaten ranged from 8.5 to 42.3 cm length with a mode at 24.5 cm. Whiting eaten ranged from 1.9 cm to 31.0 cm length, with a mode at 3.5 cm. Overall diet composition: Netherlands A total of 24,622 otoliths (plus other remains) representing at least 12427 fish was recovered from the stomachs together with 167 upper and 148 lower beaks (plus other remains) belonging to at least 192 individual cephalopods. At least fourteen fish species and five cephalopod species were present (Table 2). Crustaceans, polychaetes and non-cephalopod mollusc remains were also found. Whiting was the main prey consumed, making up more than ¾ of the total estimated prey weight, although gobies dominated the diet in terms of numbers eaten (88% of the total). Correcting for individual prey identified from unmeasured hard parts (e.g. fragments of pre-opercular bones of dragonets, see Watt et al., 1997) resulted in very minor changes in estimated overall importance. Thus, dragonets increased from 0.04 to 0.11% of the diet; overall importance of clupeids rose from 2.3% to 2.6% while overall importance of gadids fell from 83.0% to 82.9% (revised values not shown in Table 2). The estimated lengths for whiting ranged from 2.5 to 41.5 cm with a mode of 19.5 cm. Gobies eaten ranged from 0.5 to 8.5 cm length with a mode at 4.25 cm. Sandeel eaten ranged from 5.5 cm to 23.9 cm length with a mode at 14.5 cm. 8

Prey numbers: combined dataset Although the MDS plot (not shown) suggested no clear separation between data from the two countries, there was a significant relationship between dietary and environmental data sets (r s = 0.066, p=0.027). The environmental variable most closely related to dietary data was country (r s = 0.145). Kruskal-Wallis analysis of numbers for individual prey species in stomachs revealed betweencountry differences in eight prey categories, with more clupeids, viviparous blenny, eel, polychaete and non-cephalopod mollusc remains in Danish samples (P values: 0.002, 0.000, 0.032, 0.045, 0.045 respectively) and more Trisopterus, gobies and sepiolids in Dutch samples (P values: 0.025, 0.041, 0.004 respectively) (Tables 3 and 4). Prey numbers: Netherlands Multivariate analysis of prey number data using PRIMER revealed no relationship between dietary variation and the environmental factors (r s = -0.001, P = 0.471). Univariate analyses on numbers of prey in stomachs revealed significant interannual, seasonal, ontogenetic and sexual variation in diet, involving 7 different prey categories (Table 3). The strongest trend (P<0.001) relates to the higher number of gobies in the stomachs of the smallest porpoises. Whiting was more important in the diet of largest porpoises while a bigger number of individual prey (all species together) was found in the diet of the smallest porpoises. Sprat was more important in the diet of male than female porpoises. In quarter 4, porpoises took more unidentified gadids than in quarter 1 and Loligo were present only in quarter 4. Porpoises took more cod in quarter 3 than in quarter 1 and the species was absent from the diet in quarter 2. Three prey species showed interannual variation in dietary importance, with more herring consumed in the periods 1985-89 and 1995-99 than in 1990-94. More whiting was taken in 1985-89 than in 1990-94 or 1995-99 and more whiting was taken in 2000-03 than in 1995-99. Finally, more unidentified gadids were taken in 1990-94 than in 1995-99 or 2000-03 and more were taken in 1985-89 than in 2000-03 (Table 3). Prey numbers: Denmark Multivariate analysis of prey number data using PRIMER revealed no relationship between dietary variation and the environmental factors (r s = -0.025, P = 0.666). Univariate analyses revealed significant variation in numbers of prey for five prey categories (Table 4). Clupeids were least important in the diet of the smallest porpoises, while pleuronectids were found only in the small (N=3) sample from quarter 4, in which there was also a higher incidence of noncephalopod mollusc remains. Three prey categories (Zoarcidae, eels and Pleuronectidae) were more important in 1986-89 than in 1990-94. Prey length: Netherlands Median length values for the most frequently occurring prey categories (gobies, whiting, sandeels and sepiolids) were unrelated to quarter, length class, 5-year period or sex. Only median sepiolid length was correlated with porpoise body length (r = 0.486, N= 18, P = 0.041). 9

Prey length: Denmark Kruskal-Wallis tests for the three most frequently occurring prey categories (whiting, cod, Zoarcidae) revealed no relationships between median prey length and any of the variables: sex, length class, 5-year period, quarter. However, median whiting length was significantly positively correlated with porpoise length (r = 0.393, N = 26, P = 0.047). Clupeid consumption and fish abundance Correlation analysis did not show any significant relationships between the average weight of herring consumed each year by porpoises and herring abundance (either recruitment or pawning stock biomass) for either Dutch or Danish samples. However, sample sizes for most years were small and it was not possible to factor out effects of other sources of variation. The highest figures for amount of herring consumed were in 1987 and 2003, the former corresponding with rising abundance and the latter corresponding to the highest recorded herring stock biomass in recent years. However, this is based on four and two individual porpoises respectively. Food consumption by harbour porpoises The mean body weight of the harbour porpoises analysed in this study was 39.7 kg (standard deviation 12.8 kg), for animals by-caught off Denmark and 32.3 kg (standard deviation 13.2 kg), for animals stranded in the Netherlands. Estimated average weight of food eaten daily per harbour porpoise (calculated as 3.5% and 8% of porpoise weight) was 1.4 kg (standard deviation 0.5 kg) and 3.2 kg (standard deviation 1.0 kg) for Danish porpoises. For Dutch porpoises, estimated average weight of food eaten daily per harbour porpoise was 1.1 kg (standard deviation 0.5 kg) and 2.6 kg (standard deviation 1.1 kg) Calculations of annual prey consumption of harbour porpoises showed that, off the Danish coast (SCANS blocks I, L and Y), harbour porpoises could be eating from 3,031 to 6,927 tons of herring, 7,508 to 17,161 tons of cod and 7,017 to 16,038 tons of viviparous blenny, while off the Dutch coast (SCANS block H) porpoises could be consuming from 1,315 to 3,005 tons of whiting, 66 to 151 tons of cod and 73 to 167 tons of sandeel. Values for these and other prey species are shown in Table 5. 10

Discussion Stomach contents from stranded animals have long been used to try to extract information on the feeding habits of porpoises and other marine mammal species. The problems arising from the use of stranded specimens in dietary analysis are well known (see, for example, Pierce & Boyle, 1991; Pierce et al., 2004). Sampling errors and biases associated with use of strandings include the likely overrepresentation of sick animals that may not have been feeding normally. There is also the general principle that the sample set will be representative of the mortality pattern in the population rather than the age structure of the living population. In contrast, fishery by-catches provide samples of healthy animals (Kuiken et al., 1994). However, the findings on diet from such animals could be biased towards the target species of the fishery and associated species (Waring et al., 1990). Furthermore, some components of the population, notably juveniles, appear to be more vulnerable to by-catch mortality than others (Gaskin & Blair, 1977; Clausen & Andersen, 1988; IWC, 1994; Kinze, 1994; Kock & Benke, 1996). Nevertheless, stomach content analysis still remains a valuable tool and is cheaper, quicker and, above all, more easily interpreted than fatty acid and stable isotope analysis. The major prey species eaten by harbour porpoise in this study in both Danish and Dutch waters included whiting, cod and viviparous blenny with both whiting and cod being species of considerable economic importance. Whiting is a demersal species living in shallow waters, usually from 39-200 m over sandy or muddy grounds. It can reach up to 70 cm standard length, although normally the size is 30-40 cm (Whitehead et al., 1989). Its distribution extends from Northern Norway towards Iceland to the east and towards the northern coasts of Portugal to the south. It is also present in the Mediterranean, Aegean, Adriatic and Baltic Seas (Hislop, 1972). Whiting matures at around 2 years of age and at a modal length (for females) of 26 cm. During the first year of life, whiting is found in shallow waters, concentrating in the central and southern North Sea and in Scottish coastal waters. Most of the whiting consumed by both Dutch and Danish porpoises corresponded to immature fish (i.e. less than 26 cm): more than 70% of whiting and more than 99% for Dutch and Danish porpoises respectively. Cod lives in continental shelf waters from the shoreline to 600 m depth, although it is usually found between 150-200 m, over the bottom or in a water layer between 30-80 m off the bottom (Whitehead et al., 1989). It can reach up to 190 cm standard length although usually it measures 50-80 cm. Its distribution comprises the North Atlantic and adjacent seas, from the Bay of Biscay to Greenland and Spitzbergen. It is also found in the Baltic and White Seas, the Western North Atlantic and both sides of the North Pacific (Whitehead et al., 1989). Cod matures at around 4 years of age and at a modal length for females of 70 cm. Spawning takes place from February to March in waters less than 100 m depth (Hislop, 1984). All the cod eaten by both Dutch and Danish porpoises corresponded to immature fish (less than 70 cm). More recent samples (n=72 by-caught porpoises) from Danish waters were analysed by Iversen & Lockyer (2004) who found that the most important prey were gadoids, including cod, Norway pout (Trisopterus esmarkii) and whiting. Geographic variation in diet The geographical differences found by both the multivariate and univariate analyses could have a number of explanations apart from geographical location. The samples analysed in this study covered different (albeit overlapping) ranges of years for Denmark and the Netherlands. 11

Also stranded harbour porpoises represented the majority of samples in the Netherlands whereas most of the Danish harbour porpoises analysed came from by-catches. Most of the Danish animals were collected in the Skagerrak, Kattegat and Belt seas (ICES divisions IIIa, IIIb and IIIc). Only 20% of the Danish porpoises came from the North Sea. The Skagerrak-Kattegat and Belt region constitutes a transition area between the North Sea and the Baltic in terms of hydrography, topography and fish stocks in the area. Sandeel landings from the Skagerrak-Kattegat region show a different composition of species (a smaller proportion of A. marinus) from that in the North Sea. Although the results of the present work are not conclusive, other studies on porpoise diets in the Northeast Atlantic have shown geographical variation in the main prey consumed. Martin (1996) examined prey remains from the stomachs of 100 porpoises stranded and by-caught on the British coast from 1989 to 1994. He found significant differences in the most common species in stomachs of porpoises between different areas of the British coast. Sandeels were found to be taken in bigger numbers on the east coast, while Norway pout was taken by more than half of the porpoises from Shetland, but was not eaten elsewhere. Santos et al. (2004) analysed regional variation in the diet of 188 porpoises stranded and by-caught on the Scottish coast between 1992 and 2003. The authors found that sandeels were more important in the diet on the east coast while gadids were more important in the diet in Shetland. Aarefjord et al. (1995) found cod, whiting, sandeels and gobies were frequently eaten by harbour porpoises from the Danish North Sea and the Baltic, while saithe, blue whiting and capelin were more frequent in porpoises from Norwegian waters. Berggren (1996) found herring and sprat to be the main food of harbour porpoises stranded and by-caught from 1988-1993 in the Swedish Skagerrak and Kattegat Seas. In porpoises from the North Sea from 1991-1993 sandeel represented 39% of the prey weight and common sole 29%. In the Baltic Sea, 53% of the total prey weight was made up of gobies, while 23% was herring and 15% was cod (Benke & Siebert, 1996). In Ireland, harbour porpoises were found to have taken mainly Trisopterus spp. (Rogan & Berrow, 1996) while in Polish waters herring, sprat and gobies were the most frequent prey found in a sample of 19 by-caught animals from 1986 to 1997 (Malinga et al., 1997). Diet of males and females With respect to the other possible sources of variation, the only difference between the diet of male and females porpoises was found for the Dutch sample set with males taking more sprat than females. This could be explained if there is some sort of resource portioning, by which females feed in different areas than males, perhaps restricted by the presence of calves. Segregation of harbour porpoises in groups of different sex and/or age has been proposed by several authors to explain differences in by-catch figures between groups. Tomilin (1957) explained the presence of more mature males in the catch in the Baltic Sea as the consequence of adult males forming separate groups and being more mobile than groups formed by juveniles of both sexes and females with calves. In offshore Canadian waters, Gaskin & Blair (1977) proposed that subadult males would segregate from other groups and that this would explain why they were being caught in nets in big numbers. In contrast, females accompanied by calves tend to be associated with more shallow waters (Kinze, 1994). If this segregation takes place, females with calves would not only have a different distribution from males but they could also be restricted in their search for food, e.g. not being able to dive very deep or search long distances. Smith & Read (1992) found no milk in the stomachs of six calves bycaught with their mothers in gill nets in the Bay of Fundy. The authors suggested that the lack 12

of milk could be due to the inability of the calves to nurse while their mothers are actively foraging. Comparing the results of the present study with other studies in the Northeast Atlantic, Aarefjord et al. (1995) found no significant differences in diet between 7 adult females and 48 adult males, although the authors noted that the number of females was very low. On the other hand, significant differences in the number of prey were found between male and female porpoises of one year old or less, with males eating more fish than females. Börjesson & Berggren (1996) found seasonal differences in the prey composition of adult female harbour porpoises in a sample of 119 porpoises by-caught in the Swedish Kattegat and Skagerrak fisheries. The authors noted that this variation could be the result of habitat preferences dictated by their association with young calves. Malinga et al. (1997) found that only males had eaten viviparous blennies but no other differences were found in the diet between the sexes in a sample of 19 by-caught porpoises from Polish waters. Iverson & Lockyer (2004) found that females ate a greater variety of prey than males in a sample of 72 by-caught harbour porpoises from Danish waters. Diet and body size Some significant differences were found in the prey composition between small, medium and large porpoises in both studied areas. Large Dutch porpoises took more whiting than did smaller porpoises, which took more gobies and a bigger number of individual prey than medium or large porpoises. In Denmark, small porpoises took fewer clupeids than medium or large porpoises. An ontogenetic shift from eating gobies to taking whiting might be expected in that bigger porpoises are able to eat bigger prey and exploit more offshore waters than small porpoises. Lick (1991a, b) also found differences in the diet of young (less than 120 cm total length) and adult porpoises in a sample of 78 stomachs from porpoises stranded and by-caught in Germany. Young porpoises showed a preference for gobies, as found in the present study, while adult porpoises took more flatfish and gadoids and had a bigger variety of prey species in the stomach. Similar results were found in a sample of 61 porpoises by-caught and stranded in Germany from 1991-1993 (Benke & Siebert, 1996). Börjesson & Berggren (1996) also noted that gobies were important in the diet of calves (< 1 year old) from porpoises by-caught off Swedish waters. The authors concluded that the small size of gobies could make them a suitable prey for calves. Aarefjord et al. (1995) did not find significant differences in the diet between calves (< 113 cm total length) and adult porpoises in Scandinavian waters, but the authors noted that gobies were the most frequent prey in the stomach of 0 and 1 year old porpoises. Martin (1996) found no significant differences in the diet between juvenile and adult porpoises in a sample of animals stranded and by-caught in the UK. Seasonal variation in diet Seasonal differences in the diet were found in both datasets. For Denmark, it should be noted than sample sizes for both quarter 1 and 4 were very small (7 and 3 porpoises respectively). For the Netherlands, quarter 3 was the only quarter poorly represented, with only 3 porpoises with stomach contents analysed for this period. Seasonal variation in harbour porpoise distribution is well documented, consisting of a general inshore movement in summer and offshore movement in winter, although east-west and north-south migrations have also been proposed (e.g. Tomilin, 1957; Gaskin et al., 1974; Gaskin, 1977; Gaskin, 1984; Taylor & 13

Dawson, 1984; Gaskin & Watson, 1985; Northridge et al., 1995). Seasonal movements are believed to be related to prey availability or to breeding habitat (Gaskin, 1977; Northridge et al., 1995). It is not clear whether the increase in the importance of unidentified gadoids in the diet of Dutch porpoises in quarter 4 is a reflection of increased abundance in offshore waters at this time of the year or the decrease in availability of other species. Loligo was only found to be present in the diet only in quarter 4 but, since this group makes up less than 2 % in the diet (by estimated weight), the difference may be of little biological importance. Of the other studies on feeding ecology of harbour porpoises, Santos et al. (2004) found seasonal variation in the diet of Scottish porpoises with sandeels being important in the summer months while gadids were more important in the winter. Börjesson & Berggren (1996) found also seasonal variation in the diet in a sample of harbour porpoises by-caught off Swedish waters. While herring was the main prey all year-round, the contribution of sprat and whiting varied seasonally. Iverson & Lockyer (2004) found also seasonal variation in the diet in Danish waters. Gadoids were mainly taken in winter while sandeel was more important in the summer diet and gobies were mainly taken at the end of the year. Outside the Northeast Atlantic, only Palka et al. (1996) investigated seasonal differences in the diet of harbour porpoises off Atlantic Canadian and United States waters. The authors found a higher prey diversity in winter than in summer, with porpoises eating mainly herring, silver hake and pearlsides (Maurolicus weitzmani) in the fall. Interannual variation in diet Differences in the overall diet between years were found for both datasets. In Denmark, the analysis showed that Zoarcidae, eels and Pleuronectidae were more important in 1986-89 than in 1990-94. In Holland, significant annual variation was found for herring, whiting and unidentified gadoids. Interannual variation in the diet might be expected to follow variation in abundance and/or availability of prey. At present there are no accurate abundance estimates available for viviparous blennies, flatfish or eels. Food consumption by harbour porpoises and interactions with fisheries The North Sea and adjacent areas (waters west of Scotland and the Skattegat/Kattegat area) have a long history of fishery exploitation. The types of fishery include pelagic and demersal fisheries for human consumption, and industrial fisheries (where the catch is used for reduction purposes). The pelagic fishery mainly targets species such as herring, mackerel and horse mackerel, while the demersal fisheries usually catch a mixture of roundfish species (e.g. cod, haddock, whiting) and/or a mixture of flatfish species (plaice and sole) with a by-catch of roundfish. The industrial fishery mainly takes sandeel, Norway pout and sprat, although catches also include herring, haddock and whiting. Fish stocks have shown considerable variation in abundance and distribution in the past, some of which has been the result of over exploitation. Well known cases include the collapse of the North Sea herring stocks in the late 1960s (Burd, 1978, Corten, 1990) and the massive decrease of North Sea mackerel population in the early 1970s (Cushing, 1980). Not only pelagic species have shown large fluctuations in abundance: landings from the Shetland sandeel fishery fell during the 1980s and a parallel decline in seabird breeding success followed (Monaghan et al., 1989). A similar decline in sandeel abundance and associated breeding failure in seabirds occurred off the west of Scotland in 2005. 14

Harbour porpoises in the Northeast Atlantic may already have switched prey species following the decline in herring stocks to a diet based on whiting, sandeel and other gadoid species. The studies by Rae (1965, 1973) on harbour porpoise diets in Scotland between 1959 to 1971 showed clupeids (herring and sprat) to be the most frequent prey. Gadoids (mainly whiting) were found to be second in importance in the diet, while sandeels represented a minor proportion. Santos et al. (2004) noted than herring and other clupeids formed a minor component of the diet of Scottish porpoises in the 1990s and that the recovery of the North Sea herring stock was not yet reflected in the diet of porpoises from Scotland. In the present analysis, no relationship was found between herring abundance and average herring consumed by porpoises both in Danish and Dutch waters. However, at present the sample size for the most recent years is too small to provide a rigorous test. Therefore we plan to continue to add data from new strandings to provide a bigger sample size. 15

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