Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-23T09:56:17.065Z Has data issue: false hasContentIssue false

Trophic ecology of an Atlantic kelp forest fish assemblage (NW Spain) targeted by recreational fishers and implications for coastal management

Published online by Cambridge University Press:  07 December 2017

Pablo Pita*
Affiliation:
Department of Applied Economics, Faculty of Economics and Business Administration, University of Santiago de Compostela, Av. Burgo das Nacións s/n, 15782, Santiago de Compostela, Spain
Juan Freire
Affiliation:
Teamlabs, Duque de Alba 15, 28012, Madrid, Spain
*
Correspondence should be addressed to: P. Pita, Department of Applied Economics, Faculty of Economics and Business Administration, University of Santiago de Compostela, Av. Burgo das Nacións s/n, 15782, Santiago de Compostela, Spain email: pablo.pita@usc.es

Abstract

Although necessary for sustainable management of coastal ecosystems the understanding of trophic ecology of kelp fishes remains largely limited in the NE Atlantic. In this paper, stable isotope ratios of carbon (C) and nitrogen (N), complementarily with analyses of stomach contents, were used to investigate the trophic ecology of an Atlantic kelp forest fish assemblage targeted by spear fishers in Galicia (NW Spain). Trophic habits of the fishes were consistent across the species ranges and six trophic niches were identified. Chelon labrosus was the only pelagic omnivore, while Conger conger and Dicentrarchus labrax were the principal predators, preying on benthic osteichthyes. The intermediate carnivorous Diplodus sargus mainly preyed on benthic molluscs, while Labrus bergylta exploited a wider range of prey. Although associated with different trophic niches, the two morphotypes of L. bergylta showed some degree of diet overlap, providing little support to the hypothesis of their separate management. Moreover, L. bergylta can be a keystone species whose adequate management has relevant implications for the sustainable use of the European kelp forest ecosystems.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Airoldi, L., Balata, D. and Beck, M.W. (2008) The Gray Zone: relationships between habitat loss and marine diversity and their applications in conservation. Journal of Experimental Marine Biology and Ecology 366, 815.Google Scholar
Allison, G.W., Lubchenco, J. and Carr, M.H. (1998) Marine reserves are necessary but not sufficient for marine conservation. Ecological Applications 8, S79S92.Google Scholar
Almada, F., Casas, L., Francisco, S.M., Villegas-Ríos, D., Saborido-Rey, F., Irigoien, X. and Robalo, J.I. (2016) On the absence of genetic differentiation between morphotypes of the ballan wrasse Labrus bergylta (Labridae). Marine Biology 163, 16.Google Scholar
Arim, M., Abades, S.R., Laufer, G., Loureiro, M. and Marquet, P.A. (2010) Food web structure and body size: trophic position and resource acquisition. Oikos 119, 147153.Google Scholar
Arlinghaus, R. (2006) Overcoming human obstacles to conservation of recreational fishery resources, with emphasis on central Europe. Environmental Conservation 33, 4659.Google Scholar
Attrill, M.J. and Power, M. (2002) Climatic influence on a marine fish assemblage. Nature 417, 275278.Google Scholar
Bárbara, I., Cremades, J., Calvo, S., López-Rodríguez, M.C. and Dosil, J. (2005) Checklist of the benthic marine and brackish Galician algae (NW Spain). Anales del Jardín Botánico de Madrid 62, 69100.Google Scholar
Bauchot, M.L. and Saldanha, L. (1986) Congridae. In Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J. and Tortonese, E. (eds) Fishes of the Northeastern Atlantic and the Mediterranean. Volume 2. Paris: UNESCO, pp. 567574.Google Scholar
Baudron, A.R., Needle, C.L., Rijnsdorp, A.D. and Tara Marshall, C. (2014) Warming temperatures and smaller body sizes: synchronous changes in growth of North Sea fishes. Global Change Biology 20, 10231031.Google Scholar
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, 10071012.Google Scholar
Beiras, R., Bellas, J., Fernández, N., Lorenzo, J.I. and Cobelo-García, A. (2003) Assessment of coastal marine pollution in Galicia (NW Iberian Peninsula); metal concentrations in seawater, sediments and mussels (Mytilus galloprovincialis) versus embryo-larval bioassays using Paracentrotus lividus and Ciona intestinalis. Marine Environmental Research 56, 531553.Google Scholar
Bellas, J., Fernández, N., Lorenzo, I. and Beiras, R. (2008) Integrative assessment of coastal pollution in a Ría coastal system (Galicia, NW Spain): correspondence between sediment chemistry and toxicity. Chemosphere 72, 826835.Google Scholar
Bode, A., Alvarez-Ossorio, M.T., Cabanas, J.M., Miranda, A. and Varela, M. (2009) Recent trends in plankton and upwelling intensity off Galicia (NW Spain). Progress in Oceanography 83, 342350.Google Scholar
Brodeur, R.D., Smith, B.E., McBride, R.S., Heintz, R. and Farley, E. (2017) New perspectives on the feeding ecology and trophic dynamics of fishes. Environmental Biology of Fishes 100, 293297.Google Scholar
Bucci, J.P., Showers, W.J., Rebach, S., DeMaster, D. and Genna, B. (2007) Stable isotope analyses (15N and 13C) of the trophic relationships of Callinectes sapidus in two North Carolina estuaries. Estuaries and Coasts 30, 10491059.Google Scholar
Byrnes, J., Stachowicz, J.J., Hultgren, K.M., Randall Hughes, A., Olyarnik, S.V. and Thornber, C.S. (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecology Letters 9, 6171.Google Scholar
Carabel, S., Godínez-Domínguez, E., Verísimo, P., Fernández, L. and Freire, J. (2006) An assessment of sample processing methods for stable isotope analyses of marine food webs. Journal of Experimental Marine Biology and Ecology 336, 254261.Google Scholar
Carabel, S., Verísimo, P. and Freire, J. (2009) Effects of preservatives on stable isotope analyses of four marine species. Estuarine, Coastal and Shelf Science 82, 348350.Google Scholar
Coll, J., Linde, M., García-Rubies, A., Riera, F. and Grau, A.M. (2004) Spear fishing in the Balearic Islands (west central Mediterranean): species affected and catch evolution during the period 1975–2001. Fisheries Research 70, 97111.Google Scholar
Connell, S.D. and Russell, B.D. (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proceedings of the Royal Society of London B: Biological Sciences 277, 14091415.Google Scholar
Cooke, S.J. and Cowx, I.G. (2006) Contrasting recreational and commercial fishing: searching for common issues to promote unified conservation of fisheries resources and aquatic environments. Biological Conservation 128, 93108.Google Scholar
Correia, A.T., Barros, F. and Sial, A.N. (2011) Stock discrimination of European conger eel (Conger conger L.) using otolith stable isotope ratios. Fisheries Research 108, 8894.Google Scholar
Costanza, R., dÁrge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., ÓNeill, R.V., Paruelo, J., Raskin, R.G., Sutton, P. and van den Belt, M. (1997) The value of the world's ecosystem services and natural capital. Nature 387, 253260.Google Scholar
Council of the European Union (2008a) Concerning the establishment of a community framework for the collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy. Brussels: Official Journal of the European Union, pp. 112.Google Scholar
Council of the European Union (2008b) On the conservation of natural habitats and of wild fauna and flora. Brussels: Official Journal of the European Union, pp. 166.Google Scholar
Council of the European Union (2015) As regards certain fishing opportunities. Brussels: Official Journal of the European Union, pp. 119.Google Scholar
Cheung, W.W.L., Pitcher, T.J. and Pauly, D. (2005) A fuzzy logic expert system to estimate intrinsic extinction vulnerabilities of marine fishes to fishing. Biological Conservation 124, 97111.Google Scholar
Cheung, W.W.L., Watson, R., Morato, T., Pitcher, T.J. and Pauly, D. (2007) Intrinsic vulnerability in the global fish catch. Marine Ecology Progress Series 333, 112.Google Scholar
Christensen, V., Guénette, S., Heymans, J.J., Walters, C.J., Watson, R., Zeller, D. and Pauly, D. (2003) Hundred-year decline of North Atlantic predatory fishes. Fish and Fisheries 4, 124.Google Scholar
Dayton, P.K. (1985) Ecology of kelp communities. Annual Review of Ecology and Systematics 16, 215245.Google Scholar
Dayton, P.K., Tegner, M.J., Edwards, P.B. and Riser, K.L. (1998) Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecological Applications 8, 309322.Google Scholar
Dipper, F.A., Bridges, C.R. and Menz, A. (1977) Age, growth and feeding in the ballan wrasse Labrus bergylta Ascanius 1767. Journal of Fish Biology 11, 105120.Google Scholar
Doldán-Garcia, X., Chas-Amil, M. and Touza, J. (2011) Estimating the economic impacts of maritime port development: the case of a Coruña, Spain. Ocean and Coastal Management 54, 668677.Google Scholar
Efird, T.P. and Konar, B. (2014) Habitat characteristics can influence fish assemblages in high latitude kelp forests. Environmental Biology of Fishes 97, 12531263.Google Scholar
European Parliament and Council of the European Union (2008) Establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Brussels: Official Journal of the European Union, pp. 1940.Google Scholar
European Parliament and Council of the European Union (2013) The Common Fisheries Policy. 1380/2013. Brussels: Official Journal of the European Union, pp. 2261.Google Scholar
Fantle, M.S., Dittel, A.I., Schwalm, S.M., Epifanio, C.E. and Fogel, M.L. (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120, 416426.Google Scholar
Fernández, C. (2016) Current status and multidecadal biogeographical changes in rocky intertidal algal assemblages: the northern Spanish coast. Estuarine, Coastal and Shelf Science 171, 3540.Google Scholar
Fernández-Vidal, D. and Muiño, R. (2014) Fact or fiction? Assessing governance and co-management of Marine Reserves of Fishing Interest in Cedeira and Lira (NW Spain). Marine Policy 47, 1522.Google Scholar
Figueiredo, M., Morato, T., Barreiros, J.P., Afonso, P. and Santos, R.S. (2005) Feeding ecology of the white seabream, Diplodus sargus, and the ballan wrasse, Labrus bergylta, in the Azores. Fisheries Research 75, 107119.Google Scholar
Fraley, C. and Raftery, A.E. (2002) Model-based clustering, discriminant analysis, and density estimation. Journal of the American Statistical Association 97, 611631.Google Scholar
Fraley, C., Raftery, A.E., Murphy, T.B. and Scrucca, L. (2012) mclust Version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation. Department of Statistics, University of Washington, Technical Report No. 597.Google Scholar
Franco, M.A., Viñas, L., Soriano, J.A., de Armas, D., González, J.J., Beiras, R., Salas, N., Bayona, J.M. and Albaigés, J. (2006) Spatial distribution and ecotoxicity of petroleum hydrocarbons in sediments from the Galicia continental shelf (NW Spain) after the Prestige oil spill. Marine Pollution Bulletin. The Prestige Oil Spill: A Scientific Response 53, 260271.Google Scholar
Franco-Nava, M.A., Blancheton, J.P., Deviller, G. and Le-Gall, J.Y. (2004) Particulate matter dynamics and transformations in a recirculating aquaculture system: application of stable isotope tracers in seabass rearing. Aquacultural Engineering 31, 135155.Google Scholar
Fredriksen, S. (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine Ecology Progress Series 260, 7181.Google Scholar
Freire, J., Carabel, S., Verísimo, P., Bernárdez, C. and Fernández, L. (2009) Patterns of juvenile habitat use by the spider crab Maja brachydactyla as revealed by stable isotope analyses. Scientia Marina 73, 3949.Google Scholar
Freire, J. and García-Allut, A. (2000) Socioeconomic and biological causes of management failures in European artisanal fisheries: the case of Galicia (NW Spain). Marine Policy 24, 375384.Google Scholar
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, 123132.Google Scholar
Frost, W.E. (1943) The natural history of the minnow, Phoxinus phoxinus. Journal of Animal Ecology 12, 139162.Google Scholar
Hall, S.J. and Raffaelli, D.G. (1993) Food webs: theory and reality. Advances in Ecological Research 24, 187239.Google Scholar
Hansson, S., Hobbie, J.E., Elmgren, R., Larsson, U., Fry, B. and Johansson, S. (1997) The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78, 22492257.Google Scholar
Harley, C.D., Anderson, K.M., Demes, K.W., Jorve, J.P., Kordas, R.L., Coyle, T.A. and Graham, M.H. (2012) Effects of climate change on global seaweed communities. Journal of Phycology 48, 10641078.Google Scholar
Harvey, E., Fletcher, D. and Shortis, M. (2001) A comparison of the precision and accuracy of estimates of reef-fish lengths determined visually by divers with estimates produced by a stereo-video system. Fishery Bulletin 99, 6371.Google Scholar
Hilborn, R., Stokes, K., Maguire, J.-J., Smith, T., Botsford, L.W., Mangel, M., Orensanz, J., Parma, A., Rice, J. and Bell, J. (2004) When can marine reserves improve fisheries management? Ocean and Coastal Management 47, 197205.Google Scholar
Hobson, K.A. and Welch, H.E. (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Marine Ecology Progress Series 84, 918.Google Scholar
Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 6570.Google Scholar
Hyslop, E. (1980) Stomach contents analysis-a review of methods and their application. Journal of Fish Biology 17, 411429.Google Scholar
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, 595602.Google Scholar
Jefatura del Estado de España (2002) Ley 15/2002, de 1 de julio, por la que se declara el Parque Nacional marítimo-terrestre de las Islas Atlánticas de Galicia. Volume 157, de 2 de julio de 2002, Madrid: Boletín Oficial del Estado.Google Scholar
Jennings, S., Greenstreet, S., Hill, L., Piet, G., Pinnegar, J. and Warr, K.J. (2002) Long-term trends in the trophic structure of the North Sea fish community: evidence from stable-isotope analysis, size-spectra and community metrics. Marine Biology 141, 10851097.Google Scholar
Jennings, S., Renones, O., Morales-Nin, B., Polunin, N.V.C., Moranta, J. and Coll, J. (1997) Spatial variation in the 15N and 13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Marine Ecology Progress Series 146, 109116.Google Scholar
Jouvenel, J.Y. and Pollard, D.A. (2001) Some effects of marine reserve protection on the population structure of two spearfishing target-fish species, Dicentrarchus labrax (Moronidae) and Sparus aurata (Sparidae), in shallow inshore waters, along a rocky coast in the northwestern Mediterranean Sea. Aquatic Conservation: Marine and Freshwater Ecosystems 11, 19.Google Scholar
Kearney, R.E. (2001) Fisheries property rights and recreational/commercial conflict: implications of policy developments in Australia and New Zealand. Marine Policy 25, 4959.Google Scholar
Kelley, D.F. (2009) Food of bass in UK waters. Journal of the Marine Biological Association of the United Kingdom 67, 275286.Google Scholar
Klarberg, D.P. and Benson, A. (1975) Food habits of Ictalurus nubulosus in acid polluted water of northern West Virginia. Transactions of the American Fisheries Society 104, 541547.Google Scholar
Lee-Thorp, J.A., Sealy, J.C. and van der Merwe, N.J. (1989) Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. Journal of Archaeological Science 16, 585599.Google Scholar
Leitão, F., Santos, M.N. and Monteiro, C.C. (2007) Contribution of artificial reefs to the diet of the white sea bream (Diplodus sargus). ICES Journal of Marine Science 64, 473478.Google Scholar
Lewin, W.C., Arlinghaus, R. and Mehner, T. (2006) Documented and potential biological impacts of recreational fishing: insights for management and conservation. Reviews in Fisheries Science 14, 305367.Google Scholar
Ling, S.D., Johnson, C.R., Frusher, S.D. and Ridgway, K.R. (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proceedings of the National Academy of Sciences USA 106, 2234122345.Google Scholar
Lloret, J., Zaragoza, N., Caballero, D., Font, T., Casadevall, M. and Riera, V. (2008) Spearfishing pressure on fish communities in rocky coastal habitats in a Mediterranean marine protected area. Fisheries Research 94, 8491.Google Scholar
Macho, G., Naya, I., Freire, J., Villasante, S. and Molares, J. (2013) The key role of the Barefoot Fisheries Advisors in the co-managed TURF system of Galicia (NW Spain). Ambio 42, 10571069.Google Scholar
Madin, E.M.P., Gaines, S.D., Madin, J.S. and Warner, R.R. (2010) Fishing indirectly structures macroalgal assemblages by altering herbivore behavior. American Naturalist 176, 785801.Google Scholar
Maxwell, S.M., Hazen, E.L., Bograd, S.J., Halpern, B.S., Breed, G.A., Nickel, B., Teutschel, N.M., Crowder, L.B., Benson, S., Dutton, P.H., Bailey, H., Kappes, M.A., Kuhn, C.E., Weise, M.J., Mate, B., Shaffer, S.A., Hassrick, J.L., Henry, R.W., Irvine, L., McDonald, B.I., Robinson, P.W., Block, B.A. and Costa, D.P. (2013) Cumulative human impacts on marine predators. Nature Communications 4, 2688.Google Scholar
McComish, T.S. (1967) Food habits of bigmouth and smallmouth buffalo in Lewis and Clark Lake and the Missouri River. Transactions of the American Fisheries Society 96, 7074.Google Scholar
Melville, A.J. and Connolly, R.M. (2003) Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136, 499507.Google Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 11351140.Google Scholar
Molloy, P.P., Anticamara, J.A., Rist, J.L. and Vincent, A.C.J. (2010) Frugal conservation: what does it take to detect changes in fish populations? Biological Conservation 143, 25322542.Google Scholar
Montero-Serra, I., Edwards, M. and Genner, M.J. (2015) Warming shelf seas drive the subtropicalization of European pelagic fish communities. Global Change Biology 21, 144153.Google Scholar
Morales-Nin, B., Moranta, J., García, C., Tugores, M.P., Grau, A.M., Riera, F. and Cerdà, M. (2005) The recreational fishery off Majorca Island (western Mediterranean): some implications for coastal resource management. ICES Journal of Marine Science 62, 727739.Google Scholar
Myers, R.A., Baum, J.K., Shepherd, T.D., Powers, S.P. and Peterson, C.H. (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 18461850.Google Scholar
Myers, R.A. and Worm, B. (2003) Rapid worldwide depletion of predatory fish communities. Nature 423, 280283.Google Scholar
Newsome, S.D., Martinez del Rio, C., Bearhop, S. and Phillips, D.L. (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5, 429436.Google Scholar
Norderhaug, K., Christie, H., Fosså, J. and Fredriksen, S. (2005) Fish–macrofauna interactions in a kelp (Laminaria hyperborea) forest. Journal of the Marine Biological Association of the United Kingdom 85, 12791286.Google Scholar
O'Brien, C.M., Fox, C.J., Planque, B. and Casey, J. (2000) Climate variability and North Sea cod. Nature 404, 142.Google Scholar
Orland, C., Queirós, A.M., Spicer, J.I., McNeill, C.L., Higgins, S., Goldworthy, S., Zananiri, T., Archer, L. and Widdicombe, S. (2016) Application of computer-aided tomography techniques to visualize kelp holdfast structure reveals the importance of habitat complexity for supporting marine biodiversity. Journal of Experimental Marine Biology and Ecology 477, 4756.Google Scholar
Pawson, M.G., Glenn, H. and Padda, G. (2008) The definition of marine recreational fishing in Europe. Marine Policy 32, 339350.Google Scholar
Pérez-Camacho, A., González, R. and Fuentes, J. (1991) Mussel culture in Galicia (NW Spain). Aquaculture (Netherlands) 94, 263278.Google Scholar
Perez de Oliveira, L. (2013) Fishers as advocates of marine protected areas: a case study from Galicia (NW Spain). Marine Policy 41, 95102.Google Scholar
Peterson, B.J. and Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293320.Google Scholar
Peterson, C.H., Summerson, H.C., Thomson, E., Lenihan, H.S., Grabowski, J., Manning, L., Micheli, F. and Johnson, G. (2000) Synthesis of linkages between benthic and fish communities as a key to protecting essential fish habitat. Bulletin of Marine Science 66, 759774.Google Scholar
Philippart, C.J.M., Anadón, R., Danovaro, R., Dippner, J.W., Drinkwater, K.F., Hawkins, S.J., Oguz, T., O'Sullivan, G. and Reid, P.C. (2011) Impacts of climate change on European marine ecosystems: observations, expectations and indicators. Journal of Experimental Marine Biology and Ecology 400, 5269.Google Scholar
Pillay, T. (1952) A critique of the methods of study of food of fishes. Journal of Zoological Society of India 4, 185200.Google Scholar
Pinnegar, J.K., Jennings, S., O'Brien, C.M. and Polunin, N.V.C. (2002) Long-term changes in the trophic level of the Celtic Sea fish community and fish market price distribution. Ecology 39, 377390.Google Scholar
Pinnegar, J.K. and Polunin, N.V.C. (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122, 399409.Google Scholar
Pita, P., Fernández-Márquez, D. and Freire, J. (2014) Short-term performance of three underwater sampling techniques for assessing differences in the absolute abundances and in the inventories of the coastal fish communities of the Northeast Atlantic Ocean. Marine and Freshwater Research 65, 105113.Google Scholar
Pita, P., Fernández-Vidal, D., García-Galdo, J. and Muíño, R. (2016) The use of the traditional ecological knowledge of fishermen, cost-effective tools and participatory models in artisanal fisheries: towards the co-management of common octopus in Galicia (NW Spain). Fisheries Research 178, 412.Google Scholar
Pita, P. and Freire, J. (2011) Movements of three large coastal predatory fishes in the northeast Atlantic: a preliminary telemetry study. Scientia Marina 75, 759770.Google Scholar
Pita, P. and Freire, J. (2014) The use of spearfishing competition data in fisheries management: evidence for a hidden near collapse of a coastal fish community of Galicia (NE Atlantic Ocean). Fisheries Management and Ecology 21, 454469.Google Scholar
Pita, P. and Freire, J. (2016) Assessing the impact of spear fishing by using competitions records and underwater visual census. Scientia Marina 80, 2738.Google Scholar
Pita, P., Freire, J. and García-Allut, A. (2008) How to assign a catch value to fishing grounds when fisheries statistics are not spatially explicit. Scientia Marina 72, 693699.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703718.Google Scholar
Quintela, M., Danielsen, E.A., Lopez, L., Barreiro, R., Svåsand, T., Knutsen, H., Skiftesvik, A.B. and Glover, K.A. (2016) Is the ballan wrasse, Labrus bergylta, two species? Genetic analysis reveals within-species divergence associated with plain and spotted morphotype frequencies. Integrative Zoology 11, 85173.Google Scholar
R Core Team (2016) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Raikow, D.F. and Hamilton, S.K. (2001) Bivalve diets in a midwestern US stream: a stable isotope enrichment study. Limnology and Oceanography 46, 514522.Google Scholar
Roberge, J.M. and Angelstam, P. (2004) Usefulness of the umbrella species concept as a conservation tool. Conservation Biology 18, 7685.Google Scholar
Roberts, C.M. (2000) Selecting marine reserve locations: optimality versus opportunism. Bulletin of Marine Science 66, 581592.Google Scholar
Roberts, C.M., Hawkins, J.P. and Gell, F.R. (2005) The role of marine reserves in achieving sustainable fisheries. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 123132.Google Scholar
Rooney, N. and McCann, K.S. (2012) Integrating food web diversity, structure and stability. Trends in Ecology and Evolution 27, 4046.Google Scholar
Russell, B.D., Thompson, J.A.I., Falkenberg, L.J. and Connell, S.D. (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Global Change Biology 15, 21532162.Google Scholar
Sala, E. and Ballesteros, E. (1997) Partitioning of space and food resources by three fish of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Marine Ecology Progress Series 152, 273283.Google Scholar
Schiel, D.R. and Foster, M.S. (2015) The biology and ecology of giant kelp forests. Oakland, CA: University of California Press.Google Scholar
Schroeder, D.M. and Love, M.S. (2002) Recreational fishing and marine fish populations in California. California Cooperative Oceanic Fisheries Investigations, 43, 9.Google Scholar
Simberloff, D. (1998) Flagships, umbrellas, and keystones: is single-species management passé in the landscape era? Biological Conservation 83, 247257.Google Scholar
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, 452461.Google Scholar
Steneck, R.S., Graham, M.H., Bourque, B.J., Corbett, D., Erlandson, J.M., Estes, J.A. and Tegner, M.J. (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29, 436459.Google Scholar
Tieszen, L.L., Boutton, T.W., Tesdahl, K.G. and Slade, N.A. (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for D13C analysis of diet. Oecologia 57, 3237.Google Scholar
Travis, J. and Dytham, C. (2004) A method for simulating patterns of habitat availability at static and dynamic range margins. Oikos 104, 410416.Google Scholar
Velando, A. and Munilla, I. (2011) Disturbance to a foraging seabird by sea-based tourism: implications for reserve management in marine protected areas. Biological Conservation 144, 11671174.Google Scholar
Villasante, S. (2012) The management of the blue whiting fishery as complex social-ecological system: the Galician case. Marine Policy 36, 13011308.Google Scholar
Villegas-Ríos, D., Alonso-Fernández, A., Fabeiro, M., Bañón, R. and Saborido-Rey, F. (2013) Demographic variation between colour patterns in a temperate protogynous hermaphrodite, the ballan wrasse Labrus bergylta. PLoS ONE 8, e71591.Google Scholar
Weidman, C.R. and Millner, R. (2000) High-resolution stable isotope records from North Atlantic cod. Fisheries Research 46, 327342.Google Scholar
Wernberg, T., Bennett, S., Babcock, R.C., de Bettignies, T., Cure, K., Depczynski, M., Dufois, F., Fromont, J., Fulton, C.J., Hovey, R.K., Harvey, E.S., Holmes, T.H., Kendrick, G.A., Radford, B., Santana-Garcon, J., Saunders, B.J., Smale, D.A., Thomsen, M.S., Tuckett, C.A., Tuya, F., Vanderklift, M.A. and Wilson, S. (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169172.Google Scholar
Wernberg, T., Russell, B.D., Moore, P.J., Ling, S.D., Smale, D.A., Campbell, A., Coleman, M.A., Steinberg, P.D., Kendrick, G.A. and Connell, S.D. (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. Journal of Experimental Marine Biology and Ecology 400, 716.Google Scholar
Wernberg, T., Thomsen, M.S., Tuya, F., Kendrick, G.A., Staehr, P.A. and Toohey, B.D. (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecology Letters 13, 685694.Google Scholar
Willis, T.J., Millar, R.B., Babcock, R.C. and Tolimieri, N. (2003) Burdens of evidence and the benefits of marine reserves: putting Descartes before des horse? Environmental Conservation 30, 97103.Google Scholar
Xunta de Galicia (2007) Decreto 87/2007, do 12 de abril, polo que se crea a reserva mariña de interese pesqueiro Os Miñarzos. Diario Oficial de Galicia. Volume 87/2007, Santiago de Compostela, pp. 73147318.Google Scholar
Xunta de Galicia (2009) Decreto 28/2009, do 29 de xaneiro, polo que se crea a reserva mariña de interese pesqueiro Ría de Cedeira. Diario Oficial de Galicia. Santiago de Compostela, pp. 31983203.Google Scholar