Species-and size-related patterns in stable isotopes and mercury concentrations in fish help refine marine ecosystem indicators and provide evidence for distinct management units for hake in the Northeast Atlantic

ICES Journal of Marine Science

Volumn 71, Issue 5, 2014, Pages 1073-1087

  Chouvelon, T ^a   Caurant, F ^a   Cherel, Y ^b   Simon Bouhet, B ^a   Spitz, J ^a,c   Bustamante, P ^a  

^a French National Centre for Scientific Research   (France)

^b CNRS   (France)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BAY; CONCENTRATION (COMPOSITION); ENVIRONMENTAL INDICATOR; FISH; FISHERY MANAGEMENT; MERCURY (ELEMENT); SPECIES DIVERSITY; STABLE ISOTOPE; TROPHIC STRUCTURE;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHEAST); BAY OF BISCAY;

EID: 84895873231     PISSN: 10543139     EISSN: 10959289     Source Type: Journal    
DOI: 10.1093/icesjms/fst199     Document Type: Article

References (106)

1. Allain, V., and Lorance, P., 2000. Age estimation and growth of some deep-sea fish from the Northeast Atlantic Ocean. Cybium, 24: 7-16.
2. Amlund, H., Lundebye, A. K., and Berntssen, M. H. G. 2007. Accumulation and elimination of methylmercury in Atlantic cod (Gadus morhua L.) following dietary exposure. Aquatic Toxicology, 83: 323-330.
3. Bacci, E. 1989. Mercury in the Mediterranean. Marine Pollution Bulletin, 20: 59-63.
4. Bearhop, S., Adams, C. E., Waldron, S., Fuller, R. A., and MacLeod, H. 2004. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology, 73: 1007-1012.
5. Bloom, N. S. 1992. On the chemical form of mercury in edible fish and marine invertebrate tissue. Canadian Journal of Fisheries and Aquatic Sciences, 49: 1010-1017.
6. Boening, D. 2000. Ecological effects, transport, and fate of mercury: a general review. Chemosphere, 40: 1335-1351.
7. Borja, A., Galparsoro, I., Irigoien, X., Iriondo, A., Menchaca, I., Muxika, I., Pascual, M., et al. 2011. Implementation of the European Marine Strategy Framework Directive: a methodological approach for the assessment of environmental status, from the Basque Country (Bay of Biscay). Marine Pollution Bulletin, 62: 889-904.
8. Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C., and Caurant, F. 2006. Total and organic Hg concentrations in cephalopods from the North East Atlantic waters: influence of geographical origin and feeding ecology. Science of the Total Environment, 368: 585-596.
9. Cabana, G., and Rasmussen, J. B. 1994. Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature, 372: 255-257.
10. Cabral, H. N., and Murta, A. G. 2002. The diet of blue whiting, hake, horse mackerel and mackerel of Portugal. Journal of Applied Ichthyology, 18: 14-23.
11. Cailliet, G. M., Andrews, A. H., Burton, E. J., Watters, D. L., Kline, D. E., and Ferry-Graham, L. A. 2001. Age determination and validation studies of marine fishes: do deep-dwellers live longer? Experimental Gerontology, 36: 739-764.
12. Castillo, A. G. F., Martinez, J. L., and Garcia-Vasquez, E. 2004. Fine spatial structure of Atlantic hake (Merluccius merluccius) stocks revealed by variation at microsatellite loci. Marine Biotechnology, 6: 299-306.
13. Caurant, F., Chouvelon, T., Lahaye, V., Mendez-Fernandez, P., Rogan, E., Spitz, J., and Ridoux, V. 2009. The useofecological tracers for discriminating populations: the case of the short-beaked common dolphin Delphinus delphis in the European Atlantic waters. International Whaling Commission, SC61/SM/34.
14. 13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology, 46: 443-453.
15. Cherel, Y., Fontaine, C., Richard, P., and Labat, J.P.2010. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnology and Oceanography, 55: 324-332.
16. Cherel, Y., and Hobson, K. A. 2007. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series, 329: 281-287.
17. Chouvelon, T., Spitz, J., Caurant, F., Mèndez-Fernandez, P., Autier, J., Lassus-Débat, A., Chappuis, A., et al. 2012a. Enhanced bioaccumu-lation of mercury in deep-sea fauna from the Bay of Biscay (northeast Atlantic) in relation to trophic positions identified by analysis of carbon and nitrogen stable isotopes. Deep-Sea Research Part I, 65: 113-124.
18. 15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures-The case of an open ecosystem: the Bay of Biscay (North-East Atlantic). Progress in Oceanography, 101: 92-105.
19. 15N values and Hg and Cd concentrations in cephalopods. Marine Ecology Progress Series, 433: 107-120.
20. Choy, C. A., Popp, B. N., Kaneko, J.J., and Drazen, J. C. 2009. The influence of depth on mercury levels in pelagic fishes and their prey. Proceedings of the National Academy of Sciences of the United States of America, 106: 13865-13869.
21. Cimmaruta, R., Bondanelli, P., and Nascetti, G. 2005. Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Molecular Ecology, 14: 2577-2591.
22. Cohen, J. E., Pimm, S. L., Yodzis, P., and Saldaña, J. 1993. Body sizes of animal predators and animal prey in food webs. Journal of Animal Ecology, 62: 67-78.
23. Cope, J. M, and Punt, A. E. 2009. Drawing the lines: resolving fishery management units with simple fisheries data. Canadian Journal of Fisheries and Aquatic Sciences, 66: 1256-1273.
24. Cossa, D., Harmelin-Vivien, M., Mellon-Duval, C., Loizeau, V., Averty, B., Crochet, S., Chou, L., et al. 2012. Influences of bioavailability, trophic position, and growth on methylmercury in hakes (Merluccius merluccius) from Northwestern Mediterranean and Northeastern Atlantic. Environmental Science and Technology, 46: 4885-4893.
25. Cronin, M., Davies, I. M., Newton, A., Pirie, J. M., Topping, G., and Swan, S. 1998. Trace metal concentrations in deep sea fish from the North Atlantic. Marine Environmental Research, 45: 225-238.
26. Crozier, W.W.1985. Observationsonthe food and feedingoftheangler-fish, Lophius piscatorius L., in the northern Irish Sea. Journal of Fish Biology, 27: 655-665.
27. Cury, P., Shannon, L., and Shin, Y. J. 2003. The functioning of marine ecosystems: a fisheries perspective. In Responsible Fisheries in the Marine Ecosystem, pp. 103-123. Ed. by M. Sinclair, and G. Valdimarsson. CAB International, Walingford.
28. Dang, F., and Wang, W. X. 2012. Why mercury concentration increases withfishsize? Biokinetic explanation. Environmental Pollution, 163: 192-198.
29. De Niro, M.J., and Epstein, S. 1977. Mechanism ofcarbon fractionation associated with lipid synthesis. Science, 197: 261-263.
30. De Niro, M. J., and Epstein, S. 1978. Influenceof dietonthe distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42: 495-506.
31. De Niro, M. J., and Epstein, S. 1981. Influenceof dietonthe distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45: 341-351.
32. De Pontual, H., Groison, A. L., Pineiro, C., and Bertignac, M. 2006. Evidence of underestimation of European hake growth in the Bay of Biscay, and its relationship with bias in the agreed method of age estimation. ICES Journal of Marine Science, 63: 1674-1681.
33. Drouineau, H., Mahévas, S., Bertignac, M., and Duplisea, D. 2010. A length-structured spatially explicit model for estimating hake growth and migration rates. ICES Journal of Marine Science, 67: 1697-1709.
34. Eisler, R. 1987. Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biological Report 85, (1.10).
35. European Commission. 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008, establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union, L 164, pp. 19-40.
36. European Commission. 2010. Commission Decision of 1 September 2010 on criteria and methodological standards on good environmental status of marine waters. Official Journal of the European Union, L 232, pp. 14-24.
37. Fitzgerald, W. F., Lamborg, C. H., and Hammerschmidt, C. R. 2007. Marine biogeochemical cycling of mercury. Chemical Reviews, 107: 641-662.
38. France, R. L. 1995. Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Marine Ecology Progress Series, 124: 307-312.
39. Fritsch, M., Morizur, Y., Lambert, E., Bonhomme, F., and Guinand, B. 2007. Assessment of sea bass (Dicentrarchus labrax, L.) stock delimitation in the Bay of Biscay and the English Channel based on mark-recapture and genetic data. Fisheries Research, 83: 123-132.
40. Gray, J. S. 2002. Biomagnification in marine systems: the perspective of an ecologist. Marine Pollution Bulletin, 45: 46-52.
41. Greenstreet, S. P. R., McMillan, J. A., and Armstrong, E. 1998. Seasonal variation in the importance of pelagic fish in the diet of piscivorous fish in the Moray Firth, NE Scotland: a response to variation in prey abundance? ICES Journal of Marine Science, 55: 121-133.
42. Greenstreet, S.P.R., and Rogers, S.I.2006. Indicatorsofthe health ofthe North Seafish community:identifying reference levels foran ecosystem approach to management. ICES Journal of Marine Science, 63: 573-593.
43. Greenstreet, S. P. R., Rogers, S. I., Rice, J. C., Piet, G. J., Guirey, E. J., Fraser, H. M., and Fryer, R.J.2011. Development ofthe EcoQO for the North Sea fish community. ICES Journal of Marine Science, 68: 1-11.
44. Guichet, R. 1995. The diet of European hake (Merluccius merluccius) in the northern part of the Bay of Biscay. ICES Journal of Marine Science, 52: 21-31.
45. Harris, H. H., Pickering, I. J., and George, G. N, 2003. The chemical forms of mercury in fish. Science, 301: 1203.
46. Hislop, J.R. G., Robb, A. P., Bell, M. A., and Armstrong, D. W. 1991. The diet and food consumptionofwhiting (Merlangius merlangus) inthe North Sea. ICES Journal of Marine Science, 48: 139-156.
47. Hobson, K. A. 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia, 120: 314-326.
48. ICES. 2008. Report of the Working Group on the Assessment of Southern Shelf Stocks of Hake, Monk and Megrim (WGHMM). ICES Document CM 2008/ACOM: 07 613 pp.
49. Jackson, A.L., Inger, R., Parnell, A. C., and Bearhop, S.2011. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology, 80: 595-602.
50. Jennings, S., Greenstreet, S. P. R., Hill, L., Piet, G. J., Pinnegar, J. K., and Warr, K. J. 2002. Long-term trends in the trophic structure of the North Seafish community: evidence from stableisotope analysis, size-spectra and community metrics. Marine Biology, 141: 1085-1097.
51. Jennings, S., Pinnegar, J. K., Polunin, N. V. C., and Boon, T. V. 2001. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. Journal of Animal Ecology, 70: 934-944.
52. Kelly, J. F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology, 78: 1-27.
53. Konovalov, Y.D.1994.Areviewofthe bindingofcadmium and mercury in fish by proteins and low molecular thiols. Hydrobiological Journal, 30: 42-51.
54. Lassalle, G., Gascuel, D., Le Loc'h, F., Lobry, J., Pierce, G. J., Ridoux, V., Santos, M. B., et al. 2012. An ecosystem approach for the assessment of fisheries impacts on marine top predators: the Bay of Biscay case study. ICES Journal of Marine Science, 69: 925-938.
55. Lassalle, G., Lobry, J., Le Loc'h, F., Bustamante, P., Certain, G., Delmas, D., Dupuy, C., et al. 2011. Lower trophic levels and detrital biomass control the BayofBiscay continental shelf food web: implications for ecosystem management. Progress in Oceanography, 91: 561-575.
56. Laurenson, C. H., and Priede, I.G. 2005. The diet and trophic ecology of anglerfish Lophius piscatorius at the Shetland Islands, UK. Journal of the Marine Biological Association UK, 85: 419-424.
57. Layman, C. A., Arrington, D. A., Montana, C. G., and Post, D. M. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology, 88: 42-48.
58. Le Loc'h, F. 2004. Structure, fonctionnement, évolution des commu-nautés benthiques des fonds meubles exploités du plateau continental Nord Gascogne. PhD Thesis, Université de Bretagne Occidentale, Brest, France.
59. Le Loc'h, F., and Hily, C. 2005. Stable carbon and nitrogen isotope analysis of Nephrops norvegicus/Merluccius merluccius fishing grounds in the Bay of Biscay (Northeast Atlantic). Canadian Journal of Fisheries and Aquatic Sciences, 62: 123-132.
60. Lindeman, R. L. 1942. The trophic-dynamic aspect of ecology. Ecology, 23: 399-418.
61. Macer, C. T. 1977. Some aspects of the biology of the horse mackerel Trachurus trachurus (L.) in waters around Britain. Journal of Fish Biology, 10: 51-62.
62. Mahe, K., Amara, R., Bryckaert, T., Kacher, M., andBrylinski, J.M.2007. Ontogenetic and spatial variation in the diet of hake (Merluccius merluccius) in the Bay of Biscay and the Celtic Sea. ICES Journal of Marine Science, 64: 1210-1219.
63. Martínez del Rio, C., Wolf, N., Carleton, S. A., and Gannes, L. Z. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews of the Cambridge Philosophical Society, 84: 91-111.
64. McClelland, J.M., Valiela, I., and Michener, R.H., 1997. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing ur-banizationin coastal watersheds. Limnology and Oceanography, 42: 930-937.
65. Meissner, A. M., MacLeod, C. D., Richard, P., Ridoux, V., and Pierce, G. 2012. Feeding ecology of striped dolphins, Stenella coeruleoalba, in the north-western Mediterranean Sea based on stable isotope analyses. Journal of the Marine Biological Association UK, 92: 1677-1687.
66. Michener, R.H., and Kaufman, L.2007. Stable isotope ratiosastracers in marine food webs: an update. In Stable Isotopes in Ecology and Environmental Science, pp. 238-282. Ed. by R. Michener, and K. Lajtha. Blackwell Publishing Ltd, 566 pp.
67. Monteiro, L. R., Costa, V., Furness, R. W., and Santos, R. S. 1996. Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Marine Ecology Progress Series, 141: 21-25.
68. Monteiro, L. R., and Lopes, H. D. 1990. Mercury content of swordfish, Xiphias gladius, in relation to length, weight, age, and sex. Marine Pollution Bulletin, 21: 293-296.
69. 15N in marine planktonic ecosystems. In Stable Isotopes in Ecology and Environmental Science, pp. 76-201. Ed. by R. Michener, and K. Lajtha. Blackwell Publishing Ltd, 566 pp.
70. Moore, J. W., and Moore, I. A. 1976. The basis of food selection in some estuarinefishes:eels, Anguillaanguilla (L.), whiting, Merlangius mer-langus (L.), sprat, Sprattus sprattus (L.) and stickleback, Gasterosteus aculeatus (L.). Journal of Fish Biology, 9: 375-390.
71. Morizur, Y., Berrow, S. D., Tregenza, N. J. S., Couperus, A. S., and Pouvraud, S. 1999. Incidental catches of marine mammals in pelagic trawl fisheries of the northeast Atlantic. Fisheries Research, 41: 297-307
72. Murua, H.2010. The biology and fisheriesof European hake, Merluccius merluccius, in the north-east Atlantic. Advances in Marine Biology, 58: 97-154.
73. Navarro, J., Coll, M., Louzao, M., Palomera, I., Delgado, A., and Forero, M. G. 2011. Comparison of ecosystem modelling and isotopic approach as ecological tools to investigate food webs in the NW Mediterranean Sea. Journal of Experimental Marine Biology and Ecology, 401: 97-104.
74. Nerot, C., Lorrain, A., Grall, J., Gillikin, D. P., Munaron, J. M., Le Bris, H., and Paulet, Y. M. 2012. Stable isotope variations in benthic sus-pensionfeeders acrossalargedepthgradientonthecontinentalshelf. Estuarine, Coastal and Shelf Science, 96: 228-235.
75. Newsome, S. D., Martínez del Rio, C., Bearhop, S., and Phillips, D. L. 2007. A niche for isotopic ecology. Frontiers in Ecology and Environment, 5: 429-436.
76. Nicholson, M. D., and Jennings, S. 2004. Testing candidate indicators to support ecosystem-based management: the power of monitoring surveys to detect temporal trends in fish community metrics. ICES Journal of Marine Science, 61: 35-42.
77. Nøttestad, L., Giske, J., Holst, J. C., and Huse, G. 1999. A length-based hypothesis for feeding migrations in pelagic fish. Canadian Journal of Fisheries and Aquatic Sciences, 56: 26-34.
78. Odum, E. P. 1969. The strategyof ecosystem development. Science, 164: 262-270.
79. Olaso, I., Cenderero, O., and Abaunza, P. 1999. The diet of horse mackerel, Trachurus trachurus (Linneaus, 1758), in the Cantabrian Sea (north Spain). Journal of Applied Ichthyology, 15: 193-198.
80. Palomares, M. D., and Pauly, D. (Eds) 2010. SeaLifeBase, World Wide Web electronic publication, Version (12/2010). www.sealifebase.org (last accessed 25 November 2013).
81. Palsbøll, P. J., Bérubé, M., and Allendorf, F. W. 2007. Identification of management units using population genetic data. Trends in Ecology and Evolution, 22: 11-16.
82. Pawson, M. G., Pickett, G. D., Leballeur, J., Brown, M., and Fritsch, M. 2007. Migrations, fishery interactions, and management units of sea bass (Dicentrarchus labrax) in Northwest Europe. ICES Journal of Marine Science, 64, 332-345.
83. Pedersen, J. 1999. Diet comparison between pelagic and demersal whiting in the North Sea. Journal of Fish Biology, 55: 1096-1113.
84. Peterson, B. J., and Fry, B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18: 293-320.
85. Piñeiro, C., and Saínza, M. 2003. Age estimation, growth and maturity of the European hake (Merluccius merluccius (Linnaeus, 1758)) from Iberian Atlantic waters. ICES Journal of Marine Science, 60: 1086-1102.
86. Pope, J.G., Shepherd, J.G., Webb, J., Stebbing, A.R. D., and Mangel, M. 1994. Successful surf-riding on size spectra: the secret of survival in the sea. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 343: 41-49.
87. Post, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology, 83: 703-718.
88. Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J., and Montaña, C. G. 2007. Getting to the fat of the matter: models, methods, and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152: 179-189.
89. Quéro, J.C. 2003. Guide des Poissons de l'Atlantique Européen. Les guides du naturaliste. Ed. by Delachaux and Niestlé, Paris, France.
90. Ramos, R., Ramírez, F., and Jover, L. 2013. Trophodynamicsofinorgan-ic pollutants in a wide-range feeder: the relevance of dietary inputs and biomagnification in the Yellow-legged gull (Larus michahellis). Environmental Pollution, 172: 235-242.
91. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, www.R-project.org (last accessed 25 November 2013).
92. Roldan, M. I., Marin, J. L. G., Utter, F. M., and Pla, C. 1998. Population genetic structure of European hake, Merluccius merluccius. Heredity, 81: 327-334.
93. Rombouts, I., Beaugrand, G., Fizzala, X., Gaill, F., Greenstreet, S. P. R., Lamare, S., Le Loc'h, F., et al. 2013. Food web indicators under the Marine Strategy Framework Directive: from complexity to simplicity? Ecological Indicators, 29: 246-254.
94. Shin, Y. J., Rochet, M. J., Jennings, S., Field, J.G., and Gislason, H. 2005. Using size-based indicators to evaluate the ecosystem effects of fishing. ICES Journal of Marine Science, 62: 384-396.
95. Smedes, F.1999. Determinationoftotal lipid using non-chlorinated solvents. The Analyst, 124: 1711-1718.
96. Spitz, J., Chouvelon, T., Cardinaud, M., Kostecki, C., and Lorance, P. 2013. Prey preferences of adult sea bass Dicentrarchus labrax in the northeastern Atlantic: implications for bycatch of common dolphin Delphinus delphis. ICES Journal of Marine Science, 70: 452-461.
97. Taylor, B.L., and Dizon, A.E.1999. First policy then science: whyaman-agement unit basedsolelyongenetic criteria cannot work. Molecular Ecology, 8: S11-S16.
98. Thompson, D. R., Furness, R. W., and Monteiro, L. R. 1998. Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains. Science of the Total Environment, 213: 299-305
99. Trenkel, V. M., Berthelé, O., Lorance, P., Bertrand, J., Brind'Amour, A., Cochard, M.L., Coppin, F., et al. 2009. Atlas des grands invertébrés et poissons observés par les campagnes scientifiques. Bilan 2008. Ifremer, Nantes, EMH: 09-003, 100 pp.
100. 15N enrichment: a meta-analysis. Oecologia, 136: 169-182.
101. 15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences, 54: 1142-1158.
102. Velasco, F., and Olaso, I. 1998. European hake Merluccius merluccius (L., 1758) feeding in the Catabrian Sea: seasonal, bathymetric and length variations. Fisheries Research, 38: 33-44.
103. Velasco, F., Olaso, I., and Sánchez, F. 2001. The role of cephalopods as forage for the demersal fish community in the southern Bay of Biscay. Fisheries Research, 52: 65-77.
104. Vizzini, S., and Mazzola, A., 2006. The effects of anthropogenic organic matter inputs on stable carbon and nitrogen isotopes in organisms from different trophic levels in a southern Mediterranean coastal area. Science of the Total Environment, 368: 723-731.
105. Zuur, A. F., Ieno, E. N., and Smith, G. M. 2007. Analysing Ecological Data. Springer, New York (USA).
106. Zuur, A.F.2012.Abeginner's guidetoGeneralized AdditiveModels with R. Highland Statistics Ltd, Newburgh (UK).