Abstract
The feeding ecology of farmed fish escapees has seldom been assessed, although they are one of aquaculture’s main environmental impacts. Here we tested if the diet of Oncorhynchus mykiss rainbow trout escapees was affected by their dispersal from farms in a reservoir in Argentine Patagonia by combining stomach content and stable isotope data, and compared their spatial patterns with those of caged and wild (previously naturalized) conspecifics. Our results reveal a shift in the stomach content and δ13C values of escapees, reflecting a farm (pellets) to wild (mainly Daphnia sp.) diet transition associated to dispersal from farms. The δ13C signal of escapees sampled within the farming area was close to that of caged fish, whereas the δ13C of escapees captured far from it was indistinguishable from that of wild rainbow trout. Furthermore, escapee dispersal from farms was associated with a transition from indiscriminate surface feeding (on indigestible floating items) typical of caged fish to preying heavily on Daphnia sp. In contrast, wild fish diet was homogeneous across all sites. Farm escapees gradually acquiring the feeding behavior of their wild conspecifics as they disperse from the farms may promote competition for food and space, and increase their chances for survival in the wild.
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Abrantes, K. G., J. M. Lyle, P. D. Nichols, J. M. Semmens & M. Trudel, 2011. Do exotic salmonids feed on native fauna after escaping from aquaculture cages in Tasmania, Australia? Canadian Journal of Fisheries and Aquatic Sciences 68: 1539–1551.
Ahlbeck, I., S. Hansson, O. Hjerne & C. W. Ramcharan, 2012. Evaluating fish diet analysis methods by individual-based modelling. Canadian Journal of Fisheries and Aquatic Sciences 69: 1184–1201.
Aigo, J., V. Cussac, S. Peris, S. Ortubay, S. Gómez, H. López, M. Gross, J. Barriga & M. Battini, 2008. Distribution of introduced and native fish in Patagonia (Argentina): patterns and changes in fish assemblages. Reviews in Fish Biology and Fisheries 18: 387–408.
Arechavala-Lopez, P., I. Uglem, D. Fernandez-Jover, J. T. Bayle-Sempere & P. Sanchez-Jerez, 2012. Post-escape dispersion of farmed seabream (Sparus aurata L.) and recaptures by local fisheries in the Western Mediterranean Sea. Fisheries Research 121: 126–135.
Arechavala-Lopez, P., D. Fernandez-Jover, K. D. Black, E. Ladoukakis, J. T. Bayle-Sempere, P. Sanchez-Jerez & T. Dempster, 2013. Differentiating the wild or farmed origin of Mediterranean fish: a review of tools for sea bream and sea bass. Reviews in Aquaculture 5: 137–157.
Arismendi, I., D. Soto, B. Penaluna, C. Jara, C. Leal & J. León-Muñoz, 2009. Aquaculture, non-native salmonid invasions and associated declines of native fishes in Northern Patagonian lakes. Freshwater Biology 54: 1135–1147.
Baffico, G. D. & F. L. Pedrozo, 1996. Growth factors controlling periphyton production in a temperate reservoir in Patagonia used for fish farming. Lakes and Reservoirs: Research and Management 2: 243–249.
Balseiro, E., B. Modenutti, C. Queimaliños & M. Reissig, 2007. Daphnia distribution in Andean Patagonian lakes: effect of low food quality and fish predation. Aquatic Ecology 41: 599–609.
Bell, J., J. Lyle, J. Semmens, C. Awruch, D. Moreno, S. Currie, A. Morash, J. Ross, & N. Barrett, 2016. Movement, habitat utilization and population status of the endangered Maugean skate and implications for fishing and aquaculture operations in Macquarie Harbour. Fisheries Research and Development Corporation Project No. 2013/008. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, January.
Blanchfield, P. J., L. S. Tate & C. L. Podemski, 2009. Survival and behaviour of rainbow trout (Oncorhynchus mykiss) released from an experimental aquaculture operation. Canadian Journal of Fisheries and Aquatic Sciences 66: 1976–1988.
Bridger, C., R. K. Booth, R. S. McKinley & D. A. Scruton, 2001. Site fidelity and dispersal patterns of domestic triploid steelhead trout (Oncorhynchus mykiss Walbaum) released to the wild. ICES Journal of Marine Science 58: 510–516.
Brush, J. M., A. T. Fisk, N. E. Hussey, T. B. Johnson & W. G. Sprules, 2012. Spatial and seasonal variability in the diet of round goby (Neogobius melanostomus): stable isotopes indicate that stomach contents overestimate the importance of dreissenids. Canadian Journal of Fisheries and Aquatic Sciences 69: 573–586.
Buchheister, A. & R. J. Latour, 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67: 445–461.
Bureau, D. P. & K. Hua, 2010. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research 41: 777–792.
Carss, D. N., 1990. Concentrations of wild and escaped fishes immediately adjacent to fish farm cages. Aquaculture 90: 29–40.
Caut, S., E. Angulo & F. Courchamp, 2009. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46: 443–453.
Caut, S., M. J. Jowers, X. Arnan, J. Pearce-Duvet, A. Rodrigo, X. Cerda & R. R. Boulay, 2014. The effects of fire on ant trophic assemblage and sex allocation. Ecology and Evolution 4: 35–49.
Charles, C., P. Blanchfield & D. Gillis, 2017. Site fidelity of escaped rainbow trout to an experimental freshwater aquaculture facility and habitat overlap with native fish fauna. Aquaculture Environment Interactions 9: 415–428.
Ciancio, J. E., M. A. Pascual, F. Botto, E. Frere & O. Iribarne, 2008. Trophic relationships of exotic anadromous salmonids in the southern Patagonian Shelf as inferred from stable isotopes. Limnology and Oceanography 53: 788–798.
Connan, M., C. McQuaid, B. Bonnevie, M. Smale & Y. Cherel, 2014. Combined stomach content, lipid and stable isotope analyses reveal spatial and trophic partitioning among three sympatric albatrosses from the Southern Ocean. Marine Ecology Progress Series 497: 259–272.
Consuegra, S., N. Phillips, G. Gajardo & C. G. de Leaniz, 2011. Winning the invasion roulette: escapes from fish farms increase admixture and facilitate establishment of non-native rainbow trout. Evolutionary applications 4: 660–671.
Correa, C., 2012. Tissue preservation biases in stable isotopes of fishes and molluscs from Patagonian lakes. Journal of Fish Biology 81: 2064–2073.
Cussac, V. E., D. E. Ruzzante, S. J. Walde, P. J. Macchi, V. Ojeda, M. F. Alonso & M. A. Denegri, 1998. Body shape variation of three species of Percichthys in relation to their coexistence in the Limay River, in northern Patagonia. Environmental Biology of Fishes 53: 143–153.
Cussac, V., L. Becker, J. Aigo, C. Conte-Grand, G. Blasetti, P. Cordero, S. Crichigno & D. Nabaes Jodar, 2014. Abundance of native fishes, wild-introduced salmonids and escaped farmed rainbow trout in a Patagonian reservoir. Lakes & Reservoirs: Research & Management 19: 74–85.
Davies, C. L., B. W. J. Surridge & D. C. Gooddy, 2014. Phosphate oxygen isotopes within aquatic ecosystems: global data synthesis and future research priorities. Science of The Total Environment 496: 563–575.
Dempson, J. B. & M. Power, 2004. Use of stable isotopes to distinguish farmed from wild Atlantic salmon, Salmo salar. Ecology of Freshwater Fish 13: 176–184.
Dempster, T., P. Sanchez-Jerez, I. Uglem & P. A. Bjørn, 2010. Species-specific patterns of aggregation of wild fish around fish farms. Estuarine, Coastal and Shelf Science 86: 271–275.
Dempster, T., P. Arechavala-Lopez, L. T. Barrett, I. A. Fleming, P. Sanchez-Jerez & I. Uglem, 2016. Recapturing escaped fish from marine aquaculture is largely unsuccessful: alternatives to reduce the number of escapees in the wild. Reviews in Aquaculture 10: 1–15.
Edwards, P., 2015. Aquaculture environment interactions: past, present and likely future trends. Aquaculture 447: 2–14.
Elsbury, K. E., A. Paytan, N. E. Ostrom, C. Kendall, M. B. Young, K. Mclaughlin, M. E. Rollog & S. Watson, 2009. Using oxygen isotopes of phosphate to trace phosphorus sources and cycling in Lake Erie. Environmental Science & Technology 43: 3108–3114.
Fiske, P., R. A. Lund & L. P. Hansen, 2005. Identifying fish farm escapees. In Cadrin, S. X., K. D. Friedland & J. R. Waldman (eds), Stock Identification Methods: Applications in Fishery Science. Elsevier, Amsterdam: 659–680.
Fiske, P., R. A. Lund & L. P. Hansen, 2006. Relationships between the frequency of farmed Atlantic salmon, Salmo salar L., in wild salmon populations and fish farming activity in Norway, 1989-2004. ICES Journal of Marine Science 63: 1182–1189.
Ford, J. S. & R. A. Myers, 2008. A global assessment of salmon aquaculture impacts on wild salmonids. PLoS Biology 6: e33.
Galloway, A. W., M. E. Eisenlord, M. N. Dethier, G. W. Holtgrieve & M. T. Brett, 2014a. Quantitative estimates of isopod resource utilization using a Bayesian fatty acid mixing model. Marine Ecology Progress Series 507: 219–232.
Galloway, A. W., S. J. Taipale, M. Hiltunen, E. Peltomaa, U. Strandberg, M. T. Brett & P. Kankaala, 2014b. Diet-specific biomarkers show that high-quality phytoplankton fuels herbivorous zooplankton in large boreal lakes. Freshwater Biology 59: 1902–1915.
Galván, D. E., C. J. Sweeting & N. V. C. Polunin, 2012. Methodological uncertainty in resource mixing models for generalist fishes. Oecologia 169: 1083–1093.
Green, D. M., D. J. Penman, H. Migaud, J. E. Bron, J. B. Taggart & B. J. McAndrew, 2012. The impact of escaped farmed Atlantic salmon (Salmo salar L.) on catch statistics in Scotland. PLoS ONE 7: e43560.
Hamoutene, D., D. Cote, K. Marshall, S. Donnet, S. Cross, L. C. Hamilton, S. McDonald, K. D. Clarke & C. Pennell, 2018. Spatial and temporal distribution of farmed Atlantic salmon after experimental release from sea cage sites in Newfoundland (Canada). Aquaculture 492: 147–156.
Hansen, L., 2006. Migration and survival of farmed Atlantic salmon (Salmo salar L.) released from two Norwegian fish farms. ICES Journal of Marine Science 63: 1211–1217.
Hedger, R. D., R. M. Serra-Llinares, P. Arechavala-Lopez, R. Nilsen, P. A. Bjørn & I. Uglem, 2017. Tracking escaped Atlantic cod (Gadus morhua L.) aggregated around Norwegian farms: considerations for management strategies. Fisheries Management and Ecology 24: 265–273.
Herberich, E., J. Sikorski & T. Hothorn, 2010. A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS ONE 5: e9788.
Hothorn, T., F. Bretz & P. Westfall, 2008. Simultaneous inference in general parametric models. Biometrical journal 50: 346–363.
Hyslop, E. J., 1980. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology 1741: 1–429.
Izquierdo-Gomez, D., J. T. Bayle-Sempere, F. Arreguán-Sánchez & P. Sánchez-Jerez, 2016. Modeling population dynamics and small-scale fisheries yields of fish farming escapes in Mediterranean coastal areas. Ecological Modelling 331: 56–67.
Jackson, D., A. Drumm, S. McEvoy, Ø. Jensen, D. Mendiola, G. Gabiña, J. A. Borg, N. Papageorgiou, Y. Karakassis & K. D. Black, 2015. A pan-European valuation of the extent, causes and cost of escape events from sea cage fish farming. Aquaculture 436: 21–26.
Jacobsen, J. & L. P. Hansen, 2001. Feeding habits of wild and escaped farmed Atlantic salmon, Salmo salar L., in the Northeast Atlantic. ICES Journal of Marine Science 58: 916–933.
Jensen, Ø., T. Dempster, E. Thorstad, I. Uglem & A. Fredheim, 2010. Escapes of fishes from Norwegian sea-cage aquaculture: causes, consequences and prevention. Aquaculture Environment Interactions 1: 71–83.
Jensen, A. J., S. Karlsson, P. Fiske, L. P. Hansen, K. Hindar & G. M. Østborg, 2013. Escaped farmed Atlantic salmon grow, migrate and disperse throughout the arctic ocean like wild salmon. Aquaculture Environment Interactions 3: 223–229.
Johnston, T. A., M. Keir & M. Power, 2010. Response of native and naturalized fish to salmonid cage culture farms in northern Lake Huron, Canada. Transactions of the American Fisheries Society 139: 660–670.
Johnston, T. A. & C. C. Wilson, 2015. Comparative ecologies of domestic and naturalised rainbow trout in northern Lake Huron. Ecology of Freshwater Fish 24: 338–354.
Lacroix, G. L. & M. J. W. Stokesbury, 2004. Adult return of farmed Atlantic salmon escaped as juveniles into freshwater. Transactions of the American Fisheries Society 133: 484–490.
Leather, S. R., 2005. Insect Sampling in Forest Ecosystems. Blackwell Science Ltd, Oxford.
Lima, L. B., F. J. M. Oliveira, H. C. Giacomini & D. P. Lima-Junior, 2016. Expansion of aquaculture parks and the increasing risk of non-native species invasions in Brazil. Reviews in Aquaculture 10: 111–122.
Macchi, P. J., V. E. Cussac, M. F. Alonso & M. A. Denegri, 1999. Predation relationships between introduced salmonids and the native fish fauna in lakes and reservoirs in northern Patagonia. Ecology of Freshwater Fish 8: 227–236.
McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. Mcgrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 2: 378–390.
McGinnity, P., P. Prodohl, A. Ferguson, R. Hynes, N. Maoileidigh, N. Baker, D. Cotter, B. O’Hea, D. Cooke, G. Rogan, J. Taggart & T. Cross, 2003. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings of the Royal Society B: Biological Sciences 270: 2443–2450.
Mehner, T., J. Ihlau, H. Dörner & F. Hölker, 2005. Can feeding of fish on terrestrial insects subsidize the nutrient pool of lakes? Limnology and Oceanography 50: 2022–2031.
Nabaes Jodar, D. N., L. A. Becker, P. Cordero, G. Blasetti & V. E. Cussac, 2017. Native and exotic fishes in a Patagonian reservoir with rainbow trout cage culture: spatial and trophic resource use. Knowledge & Management of Aquatic Ecosystems 418: 33.
Naylor, R., K. Hindar, I. Fleming, R. Goldburg, S. Williams, J. Volpe, F. Whoriskey, J. Eagle, D. Kelso & M. Mangel, 2005. Fugitive salmon: assessing the risks of escaped fish from net-pen aquaculture. Bioscience 55: 427–437.
Niklitschek, E. J., D. Soto, A. Lafon, C. Molinet & P. Toledo, 2013. Southward expansion of the Chilean salmon industry in the Patagonian Fjords: main environmental challenges. Reviews in Aquaculture 5: 172–195.
Olsen, R. E. & O. T. Skilbrei, 2010. Feeding preference of recaptured Atlantic salmon Salmo salar following simulated escape from fish pens during autumn. Aquaculture Environment Interactions 1: 167–174.
Olson, R. J., B. N. Popp, B. S. Graham, G. A. López-Ibarra, F. Galván-Magaña, C. E. Lennert-Cody, N. Bocanegra-Castillo, N. J. Wallsgrove, E. Gier, V. Alatorre-Ramírez, L. T. Ballance & B. Fry, 2010. Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progress in Oceanography 86: 124–138.
Osmundsen, T. C., P. Almklov & R. Tveterås, 2017. Fish farmers and regulators coping with the wickedness of aquaculture. Aquaculture Economics & Management 21: 163–183.
Pascual, M. A., V. Cussac, B. Dyer, D. Soto, P. Vigliano, S. Ortubay & P. Macchi, 2007. Freshwater fishes of Patagonia in the 21st century after a hundred years of human settlement, species introductions, and environmental change. Aquatic Ecosystem Health & Management 10: 212–227.
Patterson, K. & P. Blanchfield, 2013. Oncorhynchus mykiss escaped from commercial freshwater aquaculture pens in Lake Huron, Canada. Aquaculture Environment Interactions 4: 53–65.
Pinnegar, J. K. & N. V. C. Polunin, 1999. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13: 225–231.
Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi & C. G. Montaña, 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.
Rikardsen, A. H. & S. Sandring, 2006. Diet and size-selective feeding by escaped hatchery rainbow trout Oncorhynchus mykiss (Walbaum). ICES Journal of Marine Science 63: 460–465.
Rounick, J. S. & B. J. Hicks, 1985. The stable carbon isotope ratios of fish and their invertebrate prey in four New Zealand rivers. Freshwater Biology 15: 207–214.
Šegvić-Bubić, T., P. Arechavala-Lopez, I. Vučić, I. Talijančić, L. Grubišić, I. Žužul & Ž. Kovač, 2018. Site fidelity of farmed gilthead seabream Sparus aurata escapees in a coastal environment of the Adriatic Sea. Aquaculture Environment Interactions 10: 21–34.
Sepúlveda, M., I. Arismendi, D. Soto, F. Jara & F. Farias, 2013. Escaped farmed salmon and trout in Chile: incidence, impacts, and the need for an ecosystem view. Aquaculture Environment Interactions 4: 273–283.
Skilbrei, O. T., J. C. Holst, L. Asplin & M. Holm, 2009. Vertical movements of “escaped” farmed Atlantic salmon (Salmo salar L.)—a simulation study in a western Norwegian fjord. ICES Journal of Marine Science 66: 278–288.
Skilbrei, O. T., 2010. Reduced migratory performance of farmed Atlantic salmon post-smolts from a simulated escape during autumn. Aquaculture Environment Interactions 1: 117–125.
Skilbrei, O. T., 2012. The importance of escaped farmed rainbow trout (Oncorhynchus mykiss) as a vector for the salmon louse (Lepeophtheirus salmonis) depends on the hydrological conditions in the fjord. Hydrobiologia 686: 287–297.
Skilbrei, O. T., M. Heino & T. Svåsand, 2015. Using simulated escape events to assess the annual numbers and destinies of escaped farmed Atlantic salmon of different life stages from farm sites in Norway. ICES Journal of Marine Science 72: 670–685.
Soto, D., F. Jara & C. Moreno, 2001. Escaped salmon in the inner seas, southern Chile: facing ecological and social conflicts. Ecological Applications 11: 1750–1762.
Stock, B. C. & B. X. Semmens, 2016a. Unifying error structures in commonly used biotracer mixing models. Ecology 97: 2562–2569.
Stock, B. C. & B. X. Semmens, 2016b. MixSIAR GUI user manual. Version 3: 1. https://doi.org/10.5281/zenodo.1209993.
Stock, B. C., A. L. Jackson, E. J. Ward, A. C. Parnell, D. L. Phillips & B. X. Semmens, 2018. Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6: e5096.
Sweeting, C. J., J. Barry, C. Barnes, N. V. C. Polunin & S. Jennings, 2007a. Effects of body size and environment on diet-tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340: 1–10.
Sweeting, C. J., J. T. Barry, N. V. C. Polunin & S. Jennings, 2007b. Effects of body size and environment on diet-tissue δ13C fractionation in fishes. Journal of Experimental Marine Biology and Ecology 352: 165–176.
Tabor, R., C. Luecke & W. Wurtsbaugh, 1996. Effects of Daphnia availability on growth and food consumption of rainbow trout in two Utah reservoirs. North American Journal of Fisheries Management 16: 591–599.
Temporetti, P. F., M. F. Alonso, G. Baffico, M. M. Diaz, W. Lopez, F. L. Pedrozo & P. H. Vigliano, 2001. Trophic state, fish community and intensive production of salmonids in Alicura Reservoir (Patagonia, Argentina). Lakes and Reservoirs: Research and Management 6: 259–267.
Thorstad, E. B., I. A. Fleming, P. McGinnity, D. Soto, V. Wennevik & F. Whoriskey, 2008. Incidence and impacts of escaped farmed Atlantic salmon Salmo salar in nature. NINA Special Report 36: 1–110.
Troell, M., R. L. Naylor, M. Metian, M. Beveridge, P. H. Tyedmers, C. Folke, K. J. Arrow, S. Barrett, A. S. Crépin, P. R. Ehrlich, Å. Gren, N. Kautsky, S. A. Levin, K. Nyborg, H. Österblom, S. Polasky, M. Scheffer, B. H. Walker, T. Xepapadeas & A. de Zeeuw, 2014. Does aquaculture add resilience to the global food system? Proceedings of the National Academy of Sciences 111: 13257–13263.
Waite R., M. Beveridge, R. Brummett, S. Castine, N. Chaiyawannakarn, S. Kaushik, R. Mungkung, S. Nawapakpilai & M. Phillips, 2014. Improving productivity and environmental performance of aquaculture. Working Paper, Instalment 5 of Creating a Sustainable Food Future. Washington, DC: World Resources Institute.
Wallace, R. K., 1981. An assessment of diet-overlap indexes. Transactions of the American Fisheries Society 110: 72–76.
Warton, D. I. & F. K. C. Hui, 2011. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92: 3–10.
Wellman, S., K. A. Kidd, C. L. Podemski, P. J. Blanchfield & M. J. Paterson, 2017. Incorporation of wastes by native species during and after an experimental aquaculture operation. Freshwater Science 36: 387–401.
Zeileis, A., 2004. Econometric Computing with HC and HAC Covariance Matrix Estimators. Journal of Statistical Software 11: 1–17.
Zeller, N., C. D. Avila & P. Núñez, 2009. Acuicultura. Documento sectorial integral, Ministerio de Desarrollo Territorial, Provincia del Neuquén, Argentina.
Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York.
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This work was supported by Universidad Nacional del Comahue (Grant Nos. 04B181 and B204), Consejo Nacional de Investigaciones Científicas y Técnicas (Grqant No. PIP 11220120100063CO), and Agencia Nacional de Promoción Científica y Tecnológica (Grant No. PICT-2013-2640) of Argentina.
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Nabaes Jodar, D.N., Cussac, V.E. & Becker, L.A. Into the wild: escaped farmed rainbow trout show a dispersal-associated diet shift towards natural prey. Hydrobiologia 847, 105–120 (2020). https://doi.org/10.1007/s10750-019-04075-2
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DOI: https://doi.org/10.1007/s10750-019-04075-2