[en] Top predators are crucial in shaping ecosystem dynamics by regulating key processes such as prey populations, energy transfer, and community structure, particularly in systems where multiple species compete for the same resources. Understanding their trophic niches and interactions is essential for effective conservation. In the southern North Sea, harbor seals, gray seals, and harbor porpoises are top predators with overlapping prey. This multi-method study examined resource partitioning using complementary stomach content analysis, metabarcoding, and carbon, nitrogen, and sulfur stable isotope analysis to refine habitat use, incorporating sulfur isotopes, for the first time in marine mammals of the southern North Sea. Gastrointestinal data from stranded harbor seals (n = 223), gray seals (n = 87), and harbor porpoises (n = 218), alongside 283 scat samples from wild seals, collected between 2014 and 2021, were analyzed. Harbor seal and gray seal showed high prey similarity (Jaccard index 0.71), while porpoises exhibited lower similarity with both seal species (Jaccard index 0.46 and 0.45). Interactions with prey guilds were strongest for demersal roundfish, flatfish, gobies, and sandeels. Bayesian isotope mixing models revealed consistent trophic differences among the three top predators, with seals occupying higher trophic positions than porpoises and showing minimal dietary change over time. Isotopic niche metrics indicated increasing overlap between porpoises and gray seals, particularly in δ34S/δ15N space, suggesting growing trophic similarity, while harbor seals showed a contraction in niche area. Also, stomach content data revealed that high-energy prey in porpoises declined as gray seal abundance increased. These results highlight trophic niche overlap and substantial interspecific interactions, potentially leading to competition under limited resources.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Heße, Eileen; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany ; Wageningen Marine Research, Wageningen University & Research, Den Helder, The Netherlands ; Wageningen Marine Research, Ankerpark 27, 1781 AG, Den Helder, The Netherlands
Boyi, Joy Ometere; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany
Das, Krishna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Lehnert, Kristina; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany
Piette, Mathilde; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany
Pinzone, Marianna
Siebert, Ursula; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany ; Department of Ecoscience, Aarhus University, 8000, Aarhus, Denmark
Gilles, Anita; Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum, Germany. anita.gilles@tiho-hannover.de
Language :
English
Title :
Rising competition among North Sea mammalian top predators: a multi-method perspective on trophic ecology.
Estes JA Heithaus M McCauley DJ Rasher DB Worm B Megafaunal impacts on structure and function of ocean ecosystems Annu. Rev. Environ. Resour. 2016 41 83 116 10.1146/annurev-environ-110615-085622
Ripple WJ et al. Status and ecological effects of the World’s largest carnivores Science 2014 343 1:CAS:528:DC%2BC2cXktVyrsQ%3D%3D 10.1126/science.1241484 24408439 1241484
Allesina S Tang S Stability criteria for complex ecosystems Nature 2012 483 205 208 2012Natur.483.205A 1:CAS:528:DC%2BC38XisVKkt70%3D 10.1038/nature10832 22343894
Raoult V Gaston TF Williamson JE Not all sawsharks are equal: Species of co-existing sawsharks show plasticity in trophic consumption both within and between species Can. J. Fish. Aquat. Sci. 2015 72 1769 1775 10.1139/cjfas-2015-0307
Páez-Rosas D Rodríguez-Pérez M Riofrío-Lazo M Competition influence in the segregation of the trophic niche of otariids: A case study using isotopic bayesian mixing models in Galapagos pinnipeds Rapid Commun. Mass Spectrom. 2014 28 2550 2558 2014RCMS..28.2550P 1:CAS:528:DC%2BC2cXhvVGisrvP 10.1002/rcm.7047 25366402
Sergio F et al. Top predators as conservation tools: Ecological rationale, assumptions, and efficacy Annu. Rev. Ecol. Evol. Syst. 2008 39 1 19 10.1146/annurev.ecolsys.39.110707.173545
DeLong JP Vasseur DA Coexistence via resource partitioning fails to generate an increase in community function PLoS ONE 2012 7 2012PLoSO..730081D 1:CAS:528:DC%2BC38Xht12mu7c%3D 10.1371/journal.pone.0030081 22253888 3254640 e30081
Lev, V. K. & Vyacheslav, L. K. Axiomatic-deductive theory of competition of complete competitors: Coexistence, exclusion and neutrality in one model. bioRxiv, 2020.2007.2022.215533 (2020). https://doi.org/10.1101/2020.07.22.215533
Pianka, E. R. Evolutionary Ecology. (Benjamin Cummings, 2011).
Schoener TW Field experiments on interspecific competition Am. Nat. 1983 122 240 285 10.1086/284133
Pianka ER Niche overlap and diffuse competition Proc. Natl. Acad. Sci. U. S. A. 1974 71 2141 2145 1974PNAS..71.2141P 1:STN:280:DyaE2c3lvVCgug%3D%3D 10.1073/pnas.71.5.2141 4525324 388403
Alley TR Competition theory, evolution, and the concept of an ecological niche Acta Biotheor. 1982 31 165 179 1:STN:280:DyaL3s%2FntVejtg%3D%3D 10.1007/BF01857239 6815945
Planque Y et al. Trophic niche overlap between sympatric harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) at the southern limit of their European range (Eastern English Channel) Ecol. Evol. 2021 11 10004 10025 10.1002/ece3.7739 34367555 8328439
Galatius, A. et al. Survey results of harbour seals in the wadden sea in 2023. (Common Wadden Sea Secretariat, Wilhelmshaven, Germany, 2023).
Gilles, A. et al. Estimates of cetacean abundance in European Atlantic waters in summer 2022 from the SCANS-IV aerial and shipboard surveys. 64 (2023).
Schop J et al. Grey seal numbers in the Wadden Sea and on Helgoland in 2022 - 2023 2023 Common Wadden Sea Secretariat
ICES. Definition and rationale for ICES ecoregions. (2023).
Ransijn, J. Marine mammal predator-prey interactions in the North Sea Doctoral thesis, University of St Andrews, (2023).
Burthe SJ Wanless S Newell MA Butler A Daunt F Assessing the vulnerability of the marine bird community in the western North Sea to climate change and other anthropogenic impacts Mar. Ecol. Prog. Ser. 2014 507 277 295 2014MEPS.507.277B 10.3354/meps10849
Gilles A Andreasen H Müller S Siebert U Nahrungsökologie von marinen Säugetieren und Seevögeln für das Management von Natura 2000 Gebieten 2008 Forschungs- und Technologiezentrum Westküste 82
Gilles, A. Characterisation of harbour porpoise (Phocoena phocoena) habitat in German waters, Chapter V, Christian-Albrechts-Universität zu Kiel, (2009).
Damseaux F Siebert U Pomeroy P Lepoint G Das K Habitat and resource segregation of two sympatric seals in the North Sea Sci. Total Environ. 2021 764 1:CAS:528:DC%2BB3cXis1ansL3P 10.1016/j.scitotenv.2020.142842 33342563 142842
Aarts G et al. Top-down pressure on a coastal ecosystem by harbor seals Ecosphere 2019 10 10.1002/ecs2.2538 e02538
Leopold MF Eat and be eaten 2015 Wageningen University
Wilson LJ Hammond PS The diet of harbour and grey seals around Britain: Examining the role of prey as a potential cause of harbour seal declines Aquat. Conserv. Mar. Freshw. Ecosyst. 2019 29 71 85 2019ACMFE.29S.71W 10.1002/aqc.3131
Boyi JO et al. Deciphering Eurasian otter (Lutra lutra L.) and seal (Phoca vitulina L.; Halichoerus grypus F.) diet: Metabarcoding tailored for fresh and saltwater fish species Mol. Ecol. 2022 31 5089 5106 1:CAS:528:DC%2BB38Xit1Wjt7nM 10.1111/mec.16635 35965442
Heße E et al. A multi-method approach reveals long- and short-term dietary differences in individual harbour porpoises Phocoena phocoena in the southern North Sea Mar. Ecol. Prog. Ser. 2025 755 115 132 2025MEPS.755.115H 10.3354/meps14787
Siebert U Wohlsein P Lehnert K Baumgärtner W Pathological findings in harbour seals (Phoca vitulina): 1996–2005 J. Comp. Pathol. 2007 137 47 58 1:STN:280:DC%2BD2svht1Cgtw%3D%3D 10.1016/j.jcpa.2007.04.018 17629967
Siebert U et al. Post-mortem Findings in Harbour Porpoises (Phocoena phocoena) from the German North and Baltic Seas J. Compar. Pathol. 2001 124 102 114 1:STN:280:DC%2BD3M3jsFWqtA%3D%3D 10.1053/jcpa.2000.0436
Siebert U et al. Health assessment of harbour porpoises (Phocoena phocoena) from Baltic area of Denmark, Germany, Poland and Latvia Environ. Int. 2020 143 1:STN:280:DC%2BB38nnsFKktw%3D%3D 10.1016/j.envint.2020.105904 32615352 105904
Landesbetrieb für Küstenschutz, N. u. M. S.-H., Nationalparkverwaltung (LKN.SH). Untersuchung und Auswertung zum Mageninhalt und Analyse stabiler Isotope von Benthos- und Fischarten im Rahmen des FishNet Projektes (AP2). (2023).
Breed GA Bowen WD McMillan JI Leonard ML Sexual segregation of seasonal foraging habitats in a non-migratory marine mammal Proc. R. Soc. B Biol. Sci. 2006 273 2319 2326 10.1098/rspb.2006.3581
Schwarz D et al. Large-scale molecular diet analysis in a generalist marine mammal reveals male preference for prey of conservation concern Ecol. Evol. 2018 8 9889 9905 10.1002/ece3.4474 30386584 6202700
Brasseur, S. M. J. M. Seals in motion: how movements drive population development of harbour seals and grey seals in the North Sea, Wageningen University, (2017).
Yasui WY Gaskin DE Energy budget of a small cetacean, the harbour Porpoise, Phocoena phocoena (L.). Ophelia 1986 25 183 197 10.1080/00785326.1986.10429749
Osinga N et al. Patterns of stranding and mortality in Common Seals (Phoca vitulina) and Grey Seals (Halichoerus grypus) in The Netherlands between 1979 and 2008. J. Comp. Pathol. 2012 147 550 565 1:STN:280:DC%2BC38nmtlyjtQ%3D%3D 10.1016/j.jcpa.2012.04.001 22632685
Philipp C Unger B Fischer EK Schnitzler JG Siebert U Handle with care - Microplastic particles in intestine samples of seals from German waters Sustainability 2020 12 2020Sust..1210424P 1:CAS:528:DC%2BB3MXkvVyrtbc%3D 10.3390/su122410424 10424
Masland E Sweezy M Ono K Molecular methods for differentiating grey seal (Halichoerus grypus) and harbour seal (Phoca vitulina) scat Mol. Ecol. Resour. 2010 10 214 217 1:CAS:528:DC%2BC3cXht1antr4%3D 10.1111/j.1755-0998.2009.02741.x 21565013
Pinzone, M. Sourcing and dynamic of mercury in arctic seals perspectives for a changing arctic doctoral degree thesis, University of Liege, (2021).
McConnaughey T McRoy CP Food-web structure and the fractionation of carbon isotopes in the Bering Sea Mar. Biol. 1979 53 257 262 1:CAS:528:DyaL3cXhtV2gtbk%3D 10.1007/BF00952434
Post DM et al. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses Oecologia 2007 152 179 189 2007Oecol.152.179P 10.1007/s00442-006-0630-x 17225157
R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2024).
Bürkner P-C brms: An R package for Bayesian multilevel models using Stan. J. Stat. Softw. 2017 80 1 28 10.18637/jss.v080.i01
Carpenter B et al. Stan: A probabilistic programming language. J. Stat. Softw. 2017 76 1 32 10.18637/jss.v076.i01 36568334 9788645
Keeling CD The Suess effect: 13Carbon-14Carbon interrelations. Environ. Int. 1979 2 229 300 1:CAS:528:DyaL3cXmt1Cqtrc%3D 10.1016/0160-4120(79)90005-9
Clark CT et al. SuessR: Regional corrections for the effects of anthropogenic CO2 on δ13C data from marine organisms. Methods Ecol. Evol. 2021 12 1508 1520 10.1111/2041-210X.13622
Hlina, B. L. TRPS: Bayesian trophic position models using ‘Stan’. (2025).
Post DM Using stable isotopes to estimate trophic position: Models, methods, and assumptions Ecology 2002 83 703 718 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Vander Zanden MJ Vadeboncoeur Y Fishes as integrators of benthic and pelagic food webs in lakes Ecology 2002 83 2152 2161 10.2307/3072047
Heuvel CE Zhao Y-M Fisk AT Food web structure across basins in Lake Erie, a large freshwater ecosystem Can. J. Fish. Aquat. Sci. 2025 82 1 16 10.1139/cjfas-2024-0028
Borrell A Abad-Oliva N Gómez-Campos E Giménez J Aguilar A Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans Rapid Commun. Mass Spectrom. 2012 26 1596 1602 2012RCMS..26.1596B 1:CAS:528:DC%2BC38Xos1Wrt7s%3D 10.1002/rcm.6267 22693115
Hobson KA Schell DM Renouf D Noseworthy E Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals Can. J. Fish. Aquat. Sci. 1996 53 528 533 10.1139/f95-209
Christianen MJA et al. Benthic primary producers are key to sustain the Wadden Sea food web: Stable carbon isotope analysis at landscape scale Ecology 2017 98 1498 1512 1:STN:280:DC%2BC1cvjvVOjtw%3D%3D 10.1002/ecy.1837 28369845
Jouta, J. The tell-tale isotopes: Towards indicators of the health of the Wadden Sea ecosystem, University of Groningen, (2019).
Poiesz SSH Witte JIJ van der Meer MTJ van der Veer HW Soetaert KER Trophic structure and resource utilization of the coastal fish community in the western Wadden Sea evidence from stable isotope data analysis Mar. Ecol. Prog. Ser. 2021 677 115 128 2021MEPS.677.115P 1:CAS:528:DC%2BB3MXisFGnt7fO 10.3354/meps13855
Jackson AL Inger R Parnell AC Bearhop S Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R J. Anim. Ecol. 2011 80 595 602 10.1111/j.1365-2656.2011.01806.x 21401589
Layman CA Arrington DA Montaña CG Post DM Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 2007 88 42 48 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2 17489452
Layman CA Allgeier JE Characterizing trophic ecology of generalist consumers: A case study of the invasive lionfish in The Bahamas Mar. Ecol. Prog. Ser. 2012 448 131 141 2012MEPS.448.131L 10.3354/meps09511
Newsome SD Martinez del Rio C Bearhop S Phillips DL A niche for isotopic ecology Front. Ecol. Environ. 2007 5 429 436 10.1890/1540-9295(2007)5[429:ANFIE]2.0.CO;2
Leopold MF et al. Porpoises: From predators to prey J. Sea Res. 2015 97 14 23 10.1016/j.seares.2014.12.005
Andreasen H et al. Diet composition and food consumption rate of harbor porpoises (Phocoena phocoena) in the Western Baltic Sea Mar. Mamm. Sci. 2017 33 1053 1079 10.1111/mms.12421
Härkönen, T. Guide to the Otoliths of the Bony Fishes of the Northeast Atlantic. 256 (Danbiu, 1986).
Leopold, M. F., van Damme, C.J.G., Philippart, C.J.M., & Winter, C.J.N. (ed ETI) (Amsterdam, 2001).
Camphuysen, K. & Henderson, P. A. North sea fish and their remains. 326 (Pisces Conservation Ltd, 2017).
Hyslop EJ Stomach contents analysis—A review of methods and their application J. Fish Biol. 1980 17 411 429 10.1111/j.1095-8649.1980.tb02775.x
Wood SN Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models J. Royal Statist. Soc. (B) 2011 73 3 36 2797734 10.1111/j.1467-9868.2010.00749.x
TSEG. Harbour and Grey Seal Numbers in the Wadden Sea and on Helgoland in 2006. (Common Wadden Sea Secretariat, Wilhelmshaven, Germany, 2006).
Chung NC Miasojedow B Startek M Gambin A Jaccard/Tanimoto similarity test and estimation methods for biological presence-absence data BMC Bioinformatics 2019 20 10.1186/s12859-019-3118-5 31874610 6929325 644
Macarthur R Levins R The limiting similarity, convergence, and divergence of coexisting species Am. Nat. 1967 101 377 385 10.1086/282505
van Neer A Jensen LF Siebert U Grey seal (Halichoerus grypus) predation on harbour seals (Phoca vitulina) on the island of Helgoland, Germany J. Sea Res. 2015 97 1 4 10.1016/j.seares.2014.11.006
Haelters J Kerckhof F Jauniaux T Degraer S The grey seal (Halichoerus grypus) as a predator of harbour porpoises (Phocoena phocoena)? Aquat. Mamm. 2012 38 343 353 10.1578/AM.38.4.2012.343
Creel S Four factors modifying the effect of competition on carnivore population dynamics as illustrated by African Wild Dogs Conserv. Biol. 2001 15 271 274 10.1111/j.1523-1739.2001.99534.x
Stäbler M Kempf A Temming A Assessing the structure and functioning of the southern North Sea ecosystem with a food-web model Ocean Coast. Manage. 2018 165 280 297 10.1016/j.ocecoaman.2018.08.017
Ransijn, J., Booth, C. & Smout, S. A calorific map of harbour porpoise prey in the North Sea. Report No. 633, (JNCC, Peterborough, 2019).
Barquete V Strauss V Ryan PG Stable isotope turnover in blood and claws: A case study in captive African Penguins J. Exp. Mar. Biol. Ecol. 2013 448 121 127 1:CAS:528:DC%2BC3sXhsVyltbzN 10.1016/j.jembe.2013.06.021
Pierce GJ et al. Seasonal variation in the diet of common seals (Phoca vitulina) in the Moray Firth area of Scotland J. Zool. 1991 223 641 652 10.1111/j.1469-7998.1991.tb04393.x
Thompson PM Pierce GJ Hislop JRG Miller D Diack JSW Winter foraging by common seals (Phoca vitulina) in relation to food availability in the inner Moray Firth, N.E. Scotland J. Animal Ecol. 1991 60 283 294 10.2307/5460
Tucker S Bowen WD Iverson SJ Dimensions of diet segregation in grey seals Halichoerus grypus revealed through stable isotopes of carbon (δ13C) and nitrogen (δ15N) Mar. Ecol. Prog. Ser. 2007 339 271 282 2007MEPS.339.271T 1:CAS:528:DC%2BD2sXosVKmsr8%3D 10.3354/meps339271
Gosch M Hernandez-Milian G Rogan E Jessopp M Cronin M Grey seal diet analysis in Ireland highlights the importance of using multiple diagnostic features Aquat. Biol. 2014 20 155 167 10.3354/ab00553
McConnell BJ Fedak MA Lovell P Hammond PS Movements and foraging areas of grey seals in the North Sea J. Appl. Ecol. 1999 36 573 590 10.1046/j.1365-2664.1999.00429.x
Dye, B., Peck, M. A., van de Wolfshaar, K. & van Leeuwen, A. Disentangling the effects of resource level and temperature-dependence on the performance of fish in different guilds. Submitted (2025).
Rademaker M Peck MA van Leeuwen A Local reflects global: Life stage-dependent changes in the phenology of coastal habitat use by North Sea herring Global Change Biol. 2024 30 e17285 2024GCBio.30E7285R 1:CAS:528:DC%2BB2cXpvFSqtr0%3D 10.1111/gcb.17285
Audzijonyte A et al. Fish body sizes change with temperature but not all species shrink with warming Nat. Ecol. Evol. 2020 4 809 814 10.1038/s41559-020-1171-0 32251381
ICES. International Bottom Trawl Survey Working Group (IBTSWG). 204 (2023).
Daan, N., Gislason, H., G. Pope, J. & C. Rice, J. Changes in the North Sea fish community: evidence of indirect effects of fishing ICES J. Marine Sci.62, 177–188. https://doi.org/10.1016/j.icesjms.2004.08.020 (2005).
Blasco GD Ferraro DM Cottrell RS Halpern BS Froehlich HE Substantial gaps in the current fisheries data landscape Front. Marine Sci. 2020 10.3389/fmars.2020.612831
Bowen DW Ellis SL Iverson SJ Boness DJ Maternal and newborn life-history traits during periods of contrasting population trends: implications for explaining the decline of harbour seals (Phoca vitulina), on Sable Island J. Zool. 2003 261 155 163 10.1017/S0952836903004047
Thompson D Duck CD Morris CD Russell DJF The status of harbour seals (Phoca vitulina) in the UK Aquatic Conser. Marine Freshwater Ecosys. 2019 29 40 60 2019ACMFE.29S.40T 10.1002/aqc.3110
Reijnders PJH et al. Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic J. Sea Res. 1997 38 161 168 10.1016/S1385-1101(97)00031-2
Galatius A et al. Aerial surveys of Harbour seals in the Wadden sea in 2018 2018 Common Wadden Sea Secretariat
Galatius A et al. Survey results of Harbour seals in the Wadden sea in 2024 2024 Common Wadden Sea Secretariat
Mclean, M. Functional responses of fish communities to environmental gradients in the North Sea, Eastern English Channel, and Bay of Somme, Université du Littoral Cote d’Opale, (2019).