Top‐down pressure on a coastal ecosystem by harbor seals

Historic hunting has led to severe reductions of many marine mammal species across the globe. After hunting ceased, some populations have recovered to pre-exploitation levels and may have regained their prominent position as top predator in marine ecosystems. Also, the harbor seal population in the international Wadden Sea grew at an exponential rate following a ban on seal hunting in 1960s, and the current number ~38,000 is close to the historic population size. Here we estimate the impact of the harbor seal predation on the fish community in the Wadden Sea and nearby coastal waters. Fish remains in fecal samples and published estimates on the seal’s daily energy requirement were used to estimate prey selection and the magnitude of seal consumption. Estimates on prey abundance were derived from demersal fish surveys, and fish growth was estimated using a Dynamic Energy Budget model. GPS tracking provided information on where seals most likely caught their prey. Harbor seals hauling-out in the Dutch Wadden Sea fed predominantly on demersal fish, for example, flatfish species (flounder, sole, plaice, dab), but also on sandeel, cod, and whiting. Although harbor seals acquire the majority of prey further offshore in the adjacent North Sea, and only spend 14% of their diving time in the Wadden Sea, seal predation was still estimated to cause an average annual mortality of 43% of the remaining fish in the Wadden Sea and 60% in the nearby shallow coastal waters (<20 m). There were however large sources of uncertainty in the estimated impact of seals on fish, including the migration of fish between the North Sea and Wadden Sea, and catchability estimates of the fish survey sampling gear, particularly for sandeel and other pelagic fish species. Our estimate suggested a considerable top-down pressure by harbor seals on demersal fish. However, predation by seals may also alleviate density-dependent competition between the remaining fish, allowing for increased fish growth, and partly compensating for the reduction in fish numbers. This study shows that recovering coastal marine mammal populations could become an important component in the functioning of shallow coastal ecosystems.

[1]  J. Teilmann,et al.  Population Wide Decline in Somatic Growth in Harbor Seals—Early Signs of Density Dependence , 2018, Front. Ecol. Evol..

[2]  T. Härkönen,et al.  Competition for the fish – fish extraction from the Baltic Sea by humans, aquatic mammals, and birds , 2018 .

[3]  J. Teilmann,et al.  Echoes from the past: Regional variations in recovery within a harbour seal population , 2018, PloS one.

[4]  A. S. Couperus,et al.  Burrow distribution of three sandeel species relates to beam trawl fishing, sediment composition and water velocity, in Dutch coastal waters , 2017 .

[5]  J. Støttrup,et al.  Changes in distributional patterns of plaice Pleuronectes platessa in the central and eastern North Sea; do declining nutrient loadings play a role? , 2017 .

[6]  L. Bolle,et al.  Can guild- or site-specific contrasts in trends or phenology explain the changed role of the Dutch Wadden Sea for fish? , 2017 .

[7]  Sean C. Anderson,et al.  Improving estimates of population status and trend with superensemble models , 2017 .

[8]  S. Wood.  Generalized Additive Models: An Introduction with R, Second Edition , 2017 .

[9]  N. Stenseth,et al.  Interaction between top-down and bottom-up control in marine food webs , 2017, Proceedings of the National Academy of Sciences.

[10]  M. Hufnagl,et al.  Annual brown shrimp (Crangon crangon) biomass production in Northwestern Europe contrasted to annual landings , 2016 .

[11]  M. Heithaus,et al.  Megafaunal Impacts on Structure and Function of Ocean Ecosystems , 2016 .

[12]  U. Siebert,et al.  Seasonal Variation of Harbor Seal's Diet from the Wadden Sea in Relation to Prey Availability , 2016, PloS one.

[13]  J. Witte,et al.  Possible causes for growth variability and summer growth reduction in juvenile plaice Pleuronectes platessa L. in the western Dutch Wadden Sea , 2016 .

[14]  Sascha M. M. Fässler,et al.  Abundance and tidal behaviour of pelagic fish in the gateway to the Wadden Sea , 2016 .

[15]  R. Cook,et al.  The effects of grey seal predation and commercial fishing on the recovery of a depleted cod stock , 2016 .

[16]  M. Cronin,et al.  Effects of seal predation on a modelled marine fish community and consequences for a commercial fishery , 2016 .

[17]  G. Hays,et al.  Disentangling the cause of a catastrophic population decline in a large marine mammal. , 2015, Ecology.

[18]  S. Holmes,et al.  Grey seal predation impairs recovery of an over‐exploited fish stock , 2015 .

[19]  Joe Roman,et al.  Lifting baselines to address the consequences of conservation success. , 2015, Trends in ecology & evolution.

[20]  S. Brasseur,et al.  Rapid recovery of Dutch gray seal colonies fueled by immigration , 2015 .

[21]  M. Hufnagl,et al.  Decreasing predation levels and increasing landings challenge the paradigm of non-management of North Sea brown shrimp (Crangon crangon) , 2015 .

[22]  Adriaan D. Rijnsdorp,et al.  Bio‐energetics underpins the spatial response of North Sea plaice (Pleuronectes platessa L.) and sole (Solea solea L.) to climate change , 2012 .

[23]  D. Pauly,et al.  Marine Mammal Impacts in Exploited Ecosystems: Would Large Scale Culling Benefit Fisheries? , 2012, PloS one.

[24]  S. Bearhop,et al.  A review of spatial and temporal variation in grey and common seal diet in the United Kingdom and Ireland , 2012, Journal of the Marine Biological Association of the United Kingdom.

[25]  G. Breed,et al.  Evaluating the potential for grey seal predation to explain elevated natural mortality in three fish species in the southern Gulf of St. Lawrence , 2011 .

[26]  G. Aarts,et al.  Long-term trends in juvenile flatfish indicate a dramatic reduction in nursery function of the Balgzand intertidal, Dutch Wadden Sea , 2011 .

[27]  J. Link,et al.  The importance of including predation in fish population models: Implications for biological reference points , 2011 .

[28]  S. Kooijman,et al.  Dynamic energy budget theory restores coherence in biology , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[29]  M. Peck,et al.  Temperature tolerance and energetics: a dynamic energy budget-based comparison of North Atlantic marine species , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  M. Cronin,et al.  Diet of the harbour seal (Phoca vitulina vitulina) in the west and south-west of Ireland , 2010, Journal of the Marine Biological Association of the United Kingdom.

[31]  S. Ehrich,et al.  Length–weight relationships of 216 North Sea benthic invertebrates and fish , 2010, Journal of the Marine Biological Association of the United Kingdom.

[32]  M. Peck,et al.  Physiological performance of plaice Pleuronectes platessa (L.): A comparison of static and dynamic energy budgets , 2009 .

[33]  A. Frid,et al.  Predicting ecological consequences of marine top predator declines. , 2008, Trends in ecology & evolution.

[34]  G. Piet,et al.  Taking account of catchability in groundfish survey trawls: implications for estimating demersal fish biomass , 2007 .

[35]  R. Ydenberg,et al.  Ashmole's halo and population regulation in seabirds , 2007 .

[36]  P. Herman,et al.  Impacts of Nutrient Reduction on Coastal Communities , 2007, Ecosystems.

[37]  R. E. Grift,et al.  Changes in the spatial distribution of North Sea plaice ( Pleuronectes platessa) and implications for fisheries management , 2007 .

[38]  W. Bowen,et al.  Continued decline of an Atlantic cod population: how important is gray seal predation? , 2006, Ecological applications : a publication of the Ecological Society of America.

[39]  J. V. D. Meer,et al.  An introduction to Dynamic Energy Budget (DEB) models with special emphasis on parameter estimation , 2006 .

[40]  P. Clapham,et al.  Modelling the past and future of whales and whaling. , 2004, Trends in ecology & evolution.

[41]  A. Rijnsdorp,et al.  Growth changes in plaice, cod, haddock and saithe in the North Sea: a comparison of (post-)medieval and present-day growth rates based on otolith measurements , 2004 .

[42]  T. Williams,et al.  Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  K. Lorenzen,et al.  Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  J. Hislop,et al.  Seasonal variations in the energy density of fishes in the North Sea , 2001 .

[45]  R. Arnett,et al.  Comparing the diet of cod (Gadus morhua) and grey seals (Halichoerus grypus): an investigation of secondary ingestion , 2001, Journal of the Marine Biological Association of the United Kingdom.

[46]  Phillip J. Clapham,et al.  Baleen Whales: Conservation Issues and The Status Of The Most Endangered Populations , 1999 .

[47]  M. Leopold,et al.  Diet of cormorants and the impact of cormorant predation on juvenile flatfish in the Dutch Wadden Sea , 1998 .

[48]  D. Rosen,et al.  Correlates of seasonal changes in metabolism in Atlantic harbour seals (Phoca vitulina concolor) , 1998 .

[49]  P. Reijnders,et al.  Maximum likelihood population size estimation of harbour seals in the Dutch Wadden Sea based on a mark–recapture experiment , 1998 .

[50]  Stuart I. Rogers,et al.  Demersal fish populations in the coastal waters of the UK and continental NW Europe from beam trawl survey data collected from 1990 to 1995 , 1998 .

[51]  P. Thompson,et al.  Prey selection by harbour seals, Phoca vitulina, in relation to variations in prey abundance , 1997 .

[52]  A. Rijnsdorp,et al.  Changes in growth of North Sea plaice since 1950 in relation to density, eutrophication, beam-trawl effort, and temperature , 1996 .

[53]  R. Beverton.  Spatial limitation of population size; The concentration hypothesis , 1995 .

[54]  W. Dickson.  Estimation of the capture efficiency of trawl gear. I: Development of a theoretical model , 1993 .

[55]  P. Yodzis,et al.  Body Size and Consumer-Resource Dynamics , 1992, The American Naturalist.

[56]  T. Härkönen,et al.  The harbour seal Phoca vitulina as a predator in the Skagerrak , 1991 .

[57]  M. Ryg,et al.  Energy requirements for maintenance and growth of captive harbour seals, Phoca vitulina , 1990 .

[58]  A. Rijnsdorp,et al.  Monitoring juvenile stocks of flatfish in the Wadden Sea and the coastal areas of the southeastern North Sea , 1989, Helgoländer Meeresuntersuchungen.

[59]  T. Härkönen.  Seasonal and regional variations in the feeding habits of the harbour seal, Phoca vitulina, in the Skagerrak and the Kattegat , 1987 .

[60]  K. Kovacs,et al.  FEEDING RATES OF SEALS AND WHALES , 1987 .

[61]  A. Dawson,et al.  Quantitative seasonal changes in the protein, lipid and energy content of the carcass, ovaries and liver of adult female plaice, Pleuronectes platessa L. , 1980 .

[62]  J. F. D. Veen.  On selective tidal transport in the migration of North Sea Plaice (pleuronectes platessa) and other flatfish species , 1978 .

[63]  B. Kuipers.  On the efficiency of a two-metre beam trawl for juvenile plaice (Pleuronectes Platessa) , 1975 .

[64]  S. Brasseur,et al.  Spatial distribution and habitat preference of harbour seals (Phoca vitulina) in the Dutch North Sea , 2016 .

[65]  Sophie Smout,et al.  Forage fish, their fisheries, and their predators: who drives whom? , 2014 .

[66]  M. Scheidat,et al.  Abundance of harbour porpoises (Phocoena phocoena) on the Dutch Continental Shelf, aerial surveys in July 2010 - March 2011 , 2013 .

[67]  Adriaan D. Rijnsdorp,et al.  Signals from the shallows: in search of common patterns in long-term trends in Dutch estuarine and coastal fish , 2008 .

[68]  S. Ehrich,et al.  Estimating the catching efficiency of a 2-m beam trawl for sampling epifauna by removal experiments , 2006 .

[69]  A. M. Springera,et al.  Sequential megafaunal collapse in the North Pacific Ocean: An ongoing legacy of industrial whaling? , 2003 .