EAT AND BE EATEN PORPOISE DIET STUDIES Maarten Frederik Leopold Thesis committee Promotor Prof. dr. ir. P.J.H. Reijnders Professor of Ecology and Management of Marine Mammals Wageningen University Other members Prof. dr. A.D. Rijnsdorp, Wageningen University Prof. dr. U. Siebert, University of Veterinary Medicine, Hannover, Germany Prof. dr. M. Naguib, Wageningen University Mr M.L. Tasker, Joint Nature Conservation Committee, Peterborough, United Kingdom This research was conducted under the auspices of the Netherlands Research School for the Socio-Economic and Natural Sciences of the Environment (SENSE). EAT AND BE EATEN PORPOISE DIET STUDIES Maarten Frederik Leopold Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. ir. A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 20 November 2015 at 4 p.m. in the Aula. Maarten Frederik Leopold Eat or be eaten: porpoise diet studies 239 pages PhD thesis, Wageningen University, Wageningen, NL (2015) With references, with summaries in Dutch and English ISBN 978-94-6257-558-5 There is a crack a crack in everything... that’s how the light gets in Leonard Cohen (1992) Anthem Contents 1. Introduction: Being small, living on the edge 9 2. Not all harbour porpoises are equal: which factors determine 26 what individual animals should, and can eat? 3. Are starving harbour porpoises (Phocoena phocoena) sentenced 56 to eat junk food? 4. Stomach contents analysis as an aid to identify bycatch 88 in stranded harbour porpoises Phocoena phocoena 5. Follow the fish: do harbour porpoises (Phocoena phocoena) 112 respond to better water quality up rivers? 6. Detection of grey seal Halichoerus grypus DNA in attack wounds 136 on stranded harbour porpoises Phocoena phocoena 7. Exposing the grey seal as a major predator of harbour porpoises 151 8. Porpoises: From predators to prey 168 9. Are porpoises opportunistic foragers? What are the constraints 196 for feeding of this supposed top-predator? 10. Addendum 208 Curriculum vitae 211 Summary 213 Nederlandse samenvatting 219 Publications: diet (related) studies 225 Dankwoord / Acknowledgements 232 Names and addresses of authors Geert Aarts1 Guido O. Keijl1,11 Lineke Begeman2,3 Mardik F. Leopold1,12 Judith D. L. van Bleijswijk4 Jaap van der Meer13,14 Sophie M. J. M. Brasseur1 Erik H.W.G Meesters1 Elze Dijkman1 Lara Mielke1,6 Andrea Gröne2 Peter J.H. Reijnders1,12 Jan Haelters5 Tara Schelling1,6 Eileen Heße1,6 Liliane Solé1,15 Jaap van der Hiele7,8 Lizzy van der Steeg1,6 Sjoukje Hiemstra2 Carolien H. Strating1,16 Lonneke L. IJsseldijk2 Dorien Verheyen1 Thierry Jauniaux9,10 Harry J. Witte4 1 Wageningen-IMARES, PO Box 57, 1780 AB Den Helder, The Netherlands 2 Department of Pathology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The Netherlands 3(current address): Viroscience Department, Erasmus MC, Wytemaweg 80, 3015 CN Rotterdam, The Netherlands 4Molecular Biology Laboratory, Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, The Netherlands 5Royal Belgian Institute of Natural Sciences (RBINS), Operational Directorate Natural Environment (OD Nature), 3de en 23ste Linieregimentsplein, B-8400 Oostende, Belgium 6University of Applied Sciences van Hall Larenstein, PO Box 1528, 8901 BV Leeuwarden, The Netherlands 7EHBZ Regio zuidwest, c/o Seal Rehabilitation and Research Centre, Hoofdstraat 94a, 9968 AG Pieterburen, The Netherlands 8Present address: Stichting A Seal for Sea Mammal Rescue, Haringvlietplein 3, 3251 LD Stellendam, The Netherlands 9Department of Pathology, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, B43 Liège University, 4000 Liège, Belgium 10Royal Belgian Institute of Natural Sciences (RBINS), Operational Directorate Natural Environment (OD Nature), Gulledelle 100, 1200 Brussels, Belgium 11Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands 12Department of Aquatic Ecology and Water Quality Management, PO Box 47, 6700 AA Wageningen University, The Netherlands 13Royal Netherlands Institute for Sea Research, PO BOX 59, 1790 AB Den Burg, The Netherlands 14Vrije Universiteit, Faculty of Earth & Life Sciences, Department of Theoretical Biology, de Boelelaan 1085, 1081 HV Amsterdam, The Netherlands 15HZ University of Applied Sciences, Edisonweg 4, 4382 NW Vlissingen, The Netherlands 16CAH Vilentum Applied University, Stadhuisplein 40, 1315 XA Almere, The Netherlands Chapter 1 8 Introduction Introduction: Being small, living on the edge 1 9 Chapter 1 10 Introduction Introduction: Being small, living on the edge 1 The harbour porpoise Phocoena phocoena (Linnaeus, 1758), is one of the smallest cetaceans, in an order that holds less than 100 living species (Rice 1998; Committee on Taxonomy 2014; Wilson & Mittermeier 2014). The taxonomy of cetaceans is not yet fully resolved, and many “species” may in fact be clusters of very similar, or cryptic species that are not easily distinguished from each other. With the rapidly advancing work on genetics, existing species are increasingly being split into several species (e.g. LeDuc et al. 2008; Jackson et al. 2014). The same may be said about the skills of field observers, who also provide new evidence that known species should probably be split into several new species (e.g. Pitman et al. 2010). The size range within the limited number of cetacean species is rather staggering. The order has the largest animal species that ever lived on Earth at one end of the size spectrum, the blue whale Balaenoptera musculus, and several smaller-than- man sized species at the other end. The largest recorded blue whales measured more than 30 meters and must have weighed over 175 tons (although none were ever weighed, for obvious reasons). Such gigantism has been made possible by the abundant, reliable, and high-quality food resources in the world’s oceans (Sibly & Brown 2007), and the zero-gravity environment that these animals live in (Gaskin 1982). Some species evolved in exactly the opposite direction, however, and became dwarfs, at least among the cetaceans. The harbour porpoise is one of these “dwarfs”, at less than 2 meters long and less than 100 kg, ca 0.05% of the mass of a blue whale. Harbour porpoise taxonomy is still being debated, as the species has many populations, or “subspecies” that effectively live in isolation from each other. One may wonder if distant and diagnosable populations are still joined by a cline, and should thus be treated as subspecies, or not, and should be seen as full species 11 Chapter 1 (see Helbig et al. 2002 for a discussion on speciation). The Committee on Taxonomy (2014) currently recognises four subspecies of Phocoena phocoena: P. p. phocoena, the Atlantic harbour porpoise; P. p. vomerina, the Eastern Pacific harbour porpoise; P. p. relicta, the Black Sea harbour porpoise; and a yet unnamed subspecies (scientifically), the Western Pacific harbour porpoise. Even in the NE Atlantic, where different populations appear to be well-connected, harbour porpoises may be evolving towards forming several new species (Andersen 2003; Fontaine et al. 2007, 2014). The largest population in the Atlantic probably lives in and around the North Sea, and is over 300,000 individuals strong (Hammond et al. 2013). North Sea animals are connected to animals living further south (Biscay and possibly further), east (Baltic), north (Norwegian Sea and Barents Sea), and west (Faroe Islands, Island and possibly still further west). Even though porpoises are small for cetaceans, they are larger than most (remaining) fish in the North Sea, and with their comparatively large numbers and high metabolic rates (see below) they are important predators within the North Sea ecosystem. One might speculate that the removal of most large (>1 m or so) fish from the North Sea should have benefitted the harbour porpoise. Along similar lines, it has been suggested that the large-scale removal of krill-eating whales from the Antarctic would have benefitted other krill-eaters, such as penguins and seals (Gaskin 1982; Fraser et al. 1992), but such correlations are difficult to substantiate as other factors have also had major impact on the population developments of the latter (Croxall et al. 1992). Likewise, it has been suggested that North Sea seabirds have profited at large from the removal of large predatory fish from the system, which significantly released the predation pressure on small fish (Daan et al. 2005), the main prey of small cetaceans and seabirds. However, a critical review of the carry-on effects on seabird populations has shown that again, other factors were probably more influential (Camphuysen & Garthe 2000). Population trajectories of North Sea seabirds (Mitchell et al. 2004) are much better known than those of harbour porpoises, with data from only two recent, North Sea-wide surveys available (Hammond et al. 2002, 2013). Moreover, while seabirds generally may have benefitted from the removal of large fish, some species have certainly benefitted from the vast amounts of discards and offal provided to them by modern fisheries. In contrast, porpoises are not known to take fishery waste and must thus have profited less, if at all. In any case, even though harbour porpoises may have benefitted slightly from fisheries by a relaxation of competition, they have also suffered directly,