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Long-term changes in the spiny dogfish (Squalus acanthias) trophic role in the southwestern Atlantic

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Abstract

We used a comprehensive dataset on the diet of Squalus acanthias in the southwestern Atlantic Ocean (35–55°S) to test the hypothesis that fishery has caused a decrease in the trophic level of this species (fishing down process). Of 3,644 stomachs examined between the years 1985 and 2010, 2,214 (60.77%) contained prey items. Generalized linear models were used to evaluate the support in our data for five explanatory variables (sex, predator’s total length, season, region and decade) that may explain the consumption of the given prey. The frequency of fish, mainly Merluccius hubbsi, and benthos in the stomachs decreased through time, whereas the squid Illex argentinus and jellyfishes exhibited positive trends. The trophic level of S. acanthias declined from the 1980s to the 1990s due to the high consumption of prey items at lower trophic levels. On the other hand, the consumption of argentine anchovy, Engraulis anchoita, an underexploited species, did not reveal changes through time.

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References

  • Arai, M. N., 2005. Predation on pelagic coelenterates: a review. Journal of the Marine Biological Association of the United Kingdom 85: 523–536.

    Article  Google Scholar 

  • Aubone, A., S. I. Bezzi, G. Cañete, R. Castrucci, C. Dato, G. Irusta, A. Madirolas, M. Pérez, M. Renzi, B. Santos, M. Simonazzi & M. F. Villarino, 2004. Evaluación y sugerencias de manejo del recurso merluza (Merluccius hubbsi). La situación hasta 1999. In Sánchez, R. P. & S. I. Bezzi (eds), El Mar Argentino y sus recursos pesqueros. Tomo 4. Los peces marinos de interés pesquero. Caracterización biológica y evaluación del estado de explotación, Instituto de Investigación y Desarrollo Pesquero, Mar del Plata: 207–235.

    Google Scholar 

  • Becker, B. H. & S. R. Beissinger, 2006. Centennial decline in the trophic level of an endangered seabird after fisheries declines. Conservation Biology 20: 470–479.

    Article  PubMed  Google Scholar 

  • Bergman, M. J. N. & J. W. van Santbrink, 2000. Mortality in megafaunal benthic populations caused by trawl fisheries on the Dutch continental shelf in the North Sea in 1994. ICES Journal of Marine Science 57: 1321–1331.

    Article  Google Scholar 

  • Bigelow, H. B. & W. C. Schroeder, 1953. Fishes of the Gulf of Maine. Fishery Bulletin of the Fish and Wildlife Service 74: 1–577.

    Google Scholar 

  • Brodeur, R. D., M. B. Decker, L. Ciannelli, J. E. Purcell, N. A. Bond, P. J. Stabeno, E. Acuna & G. L. Hunt Jr., 2008. Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts. Progress in Oceanography 77: 103–111.

    Article  Google Scholar 

  • Brunetti, N. E. & M. L. Ivanovic, 1992. Distribution and abundance of early life stages of squid (Illex argentinus) in the south-west Atlantic. ICES Journal of Marine Science 49: 175–183.

    Article  Google Scholar 

  • Brunetti, N. E., M. Ivanovic, G. Rossi, B. Elena & S. Pineda, 1998. Fishery biology and life history of Illex argentinus. In Okutani, T. (ed.), Contributed Paper to International Symposium on Large Pelagic Squid. Japan Marine Fishery Resources Research Center, Tokyo.

    Google Scholar 

  • Caddy, J. F. & P. G. Rodhouse, 1998. Cephalopod and groundfish landings: evidence for ecological change in global fisheries? Reviews in Fish Biology and Fisheries 8: 431–444.

    Article  Google Scholar 

  • Callaway, R., G. H. Engelhard, J. Dann, J. Cotter & H. Rumohr, 2007. A century of North Sea epibenthos and trawling: comparison between 1902–1912, 1982–1985 and 2000. Marine Ecology Progress Series 346: 27–43.

    Article  Google Scholar 

  • Carranza, A., 2006. Large gastropods by-catch in the hake fishery at the Argentinean–Uruguayan common fishing zone. Comunicaciones de la Sociedad Malacológica del Uruguay 9: 61–67.

    Google Scholar 

  • Carranza, A. & S. Horta, 2008. Megabenthic gastropods in the outer Uruguayan continental shelf: composition, distribution and some effects of trawling. Revista de Biología Marina y Oceanografía 43: 137–142.

    Article  Google Scholar 

  • Cortés, E., 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54: 726–738.

    Google Scholar 

  • Cortés, E., 1999. Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Sciences 56: 707–717.

    Article  Google Scholar 

  • Cousseau, M. B. & R. G. Perrotta, 2004. Peces marinos de Argentina. Biología, distribución, pesca. Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata.

    Google Scholar 

  • Crawley, M. J., 2005. Statistics: An Introduction Using R. Wiley, Chichester.

    Book  Google Scholar 

  • Crespi, A. C. A., E. M. Morsan & P. J. Barón, 2008. Contribution to understanding the population structure and maturation of Illex argentinus (Castellanos, 1960): the case of the inner-shelf spawning groups in San Matias Gulf (Patagonia, Argentina). Journal of Shellfish Research 27: 1225–1231.

    Article  Google Scholar 

  • Ebert, D. A. & J. J. Bizzarro, 2007. Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental Biology of Fishes 80: 221–237.

    Google Scholar 

  • Franklin, A. B., T. M. Shenk, D. R. Anderson & K. P. Burnham, 2001. Statistical model selection: the alternative to null hypothesis testing. In Shenk, T. M. & A. B. Franklin (eds), Modeling in Natural Resource Management: Development, Interpretation, and Application. Island Press, Washington: 75–90.

    Google Scholar 

  • Frid, C. L. J., R. A. Clark & J. A. Hall, 1999. Long-term changes in the benthos on a heavily fished ground off the NE coast of England. Marine Ecology Progress Series 188: 13–20.

    Article  Google Scholar 

  • García de la Rosa, S. B. & F. Sánchez, 1997. Alimentación de Squalus acanthias y predación sobre merluza Merluccius hubbsi en el Mar Argentino entre 34°47′–47°S. Revista de Investigación y Desarrollo Pesquero 11: 119–133.

    Google Scholar 

  • Hansen, J. E., 2004. Anchoíta (Engraulis anchoita). In Sánchez, R. P. & S. I. Bezzi (eds), El Mar Argentino y sus recursos pesqueros. Tomo 4. Los peces marinos de interés pesquero. Caracterización biológica y evaluación del estado de explotación. Instituto de Investigación y Desarrollo Pesquero, Mar del Plata: 101–115.

    Google Scholar 

  • Hyslop, E. J., 1980. Stomach content analysis a review of methods and their application. Journal of Fish Biology 17: 411–429.

    Article  Google Scholar 

  • Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner & R. R. Warner, 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–638.

    Article  PubMed  CAS  Google Scholar 

  • Jennings, S., J. K. Pinnegar, N. V. C. Polunin & K. J. Warr, 2001. Impacts of trawling disturbance on the trophic structure of benthic invertebrate communities. Marine Ecology Progress Series 213: 127–142.

    Article  Google Scholar 

  • Johnson, J. B. & K. S. Omland, 2004. Model selection in ecology and evolution. Trends in Ecology & Evolution 19: 101–108.

    Article  Google Scholar 

  • Kaiser, M. J. & S. J. de Groot, 2000. Effect of Fishing on Non Target Species and Habitats: Biological, Conservation and Socio-Economic Issues. Blackwell Science, Oxford.

    Google Scholar 

  • Koen Alonso, M., E. A. Crespo, N. A. Garcia, S. N. Pedraza, P. A. Mariotti & N. J. Mora, 2002. Fishery and ontogenetic driven changes in the diet of the spiny dogfish, Squalus acanthias, in Patagonian waters, Argentina. Environmental Biology of Fishes 63: 193–202.

    Article  Google Scholar 

  • Koenker, R., 2007. Package ‘quantreg’, Quantile Regression, R package version 4.67 [available on internet at http://cran.r-project.org/web/packages/quantreg/quantreg.pdf]. Accessed 26 April 2011.

  • Laptikhovsky, V. V., A. I. Arkhipkin & A. C. Henderson, 2001. Feeding habits and dietary overlap in spiny dogfish Squalus acanthias (Squalidae) and narrowmouth catshark Sroederichthys bivius (Scyliorhinidae). Journal of the Marine Biological Association of the United Kingdom 81: 1015–1018.

    Google Scholar 

  • Leonarduzzi, E., D. R. Brown & R. P. Sánchez, 2010. Seasonal variations in the growth of anchovy larvae (Engraulis anchoita) on the Argentine coastal shelf. Scientia Marina 74: 267–274.

    Article  Google Scholar 

  • Link, J. S. & M. D. Ford, 2006. Widespread and persistent increase in Ctenophora in the Northeast U.S. Shelf ecosystem. Marine Ecology Progress Series 320: 153–159.

    Article  Google Scholar 

  • Massa, A. & N. B. Hozbor, 2003. Peces cartilaginosos de la plataforma Argentina: explotación, situación y necesidades para un menejo pesquero adecuado. Frente Marítimo 19: 199–206.

    Google Scholar 

  • Massa, A. M., L. O. Lucifora & N. M. Hozbor, 2004. Condrictios de la región costera bonaerense y uruguaya. In Sánchez, R. P. & S. I. Bezzi (eds), El Mar Argentino y sus recursos pesqueros. Tomo 4. Los peces marinos de interés pesquero. Caracterización biológica y evaluación del estado de explotación. Instituto de Investigación y Desarrollo Pesquero, Mar del Plata: 85–99.

    Google Scholar 

  • Massa, A., N. Marí, A. Giussi & N. B. Hozbor, 2007. Índices de abundancia de Squalus acanthias en la Plataforma Continental Argentina. INIDEP Technical Report 6: 1–17.

  • Mensink, B. P., C. V. Fischer, G. C. Cadée, M. Fonds, C. C. Ten Hallers-Tjabbes & J. P. Boon, 2000. Shell damage and mortality in the common whelk Buccinum undatum caused by beam trawl fishery. Journal of Sea Research 43: 53–64.

    Article  Google Scholar 

  • Mianzan, H. W., N. Marí, L. B. Prenski & F. Sánchez, 1996. Fish predation on neritic ctenophores from the Argentine continental shelf. A neglected food resource? Fisheries Research 27: 69–79.

    Article  Google Scholar 

  • Myers, R. A. & B. Worm, 2003. Rapid worldwide depletion of predatory fish communities. Nature 423: 280–283.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, J. S., 2006. Fishes of the World. Wiley and Sons, New York.

    Google Scholar 

  • Pájaro, M., G. J. Macchi, E. Leonarduzzi & J. E. Hansen, 2009. Spawning biomass of Argentine anchovy (Engraulis anchoita) from 1996 to 2004 using the Daily Egg Production Method. Journal of the Marine Biological Association of the United Kingdom 89: 829–837.

    Article  Google Scholar 

  • PAN, 2009. Plan de Acción Nacional para la conservación y el manejo de Condrictios (Tiburones, Rayas y Quimeras) en la República Argentina. Subsecretaría de Pesca y Acuicultura, Argentina.

    Google Scholar 

  • Pauly, D. & V. Christensen, 2000. Trophic levels of fishes. In Froese, R. & D. Pauly (eds), FishBase 2000: Concepts, Design and Data Sources. ICLARM, Manila: 1–181.

    Google Scholar 

  • Pauly, D., V. Christensen, J. Dalsgaard, R. Froese & F. J. Torres, 1998. Fishing Down Marine Food Webs. Science 279: 860–863.

    Article  PubMed  CAS  Google Scholar 

  • Pauly, D., V. Christensen, S. Guénette, T. J. Pitcher, U. R. Sumaila, C. Walters, R. Watson & D. Zeller, 2002. Towards sustainability in world fisheries. Nature 418: 689–695.

    Article  PubMed  CAS  Google Scholar 

  • Pauly, D., W. Graham, S. Libralato, L. Morissette & M. L. D. Palomares, 2009. Jellyfish in ecosystems, online databases and ecosystem models. Hydrobiologia 616: 67–85.

    Article  Google Scholar 

  • Pinkas, L. M., S. Oliphant & I. L. K. Iverson, 1971. Food habits of albacore, bluefin tuna and bonito in Californian waters. California Fish and Game 152: 1–105.

    Google Scholar 

  • Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms. Journal of the Marine Biological Association of the United Kingdom 85: 461–476.

    Article  Google Scholar 

  • Purcell, J. E., S. Uye & W. T. Lo, 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.

    Article  Google Scholar 

  • R Development Core Team, 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Rabaut, M., U. Braeckman, F. Hendrickx, M. Vincx & S. Degraer, 2008. Experimental beam-trawling in Lanice conchilega reefs: impact on the associated fauna. Fisheries Research 90: 209–216.

    Article  Google Scholar 

  • Richardson, A. J., A. Bakun, G. C. Hays & M. J. Gibbons, 2009. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends in Ecology & Evolution 24: 312–322.

    Article  Google Scholar 

  • Sacau, M., G. J. Pierce, J. Wang, A. I. Arkhipkin, J. Portela, P. Brickle, M. B. Santos, A. F. Zuur & X. Cardoso, 2005. The spatio-temporal pattern of Argentine shortfin squid Illex argentinus abundance in the southwest Atlantic. Aquatic Living Resources 18: 361–372.

    Article  Google Scholar 

  • Sánchez, R. P. & J. D. Ciechomski, 1995. Spawning and nursery grounds of pelagic fish species in the sea shelf off Argentina and adjacent areas. Scientia Marina 59: 455–478.

    Google Scholar 

  • Sánchez, F. & L. B. Prenski, 1996. Ecología trófica de peces demersales en el Golfo San Jorge. Revista de Investigación y Desarrollo Pesquero 10: 57–71.

    Google Scholar 

  • Sea Around Us, 2011. A global database on marine fisheries and ecosystems. http://www.seaaroundus.org. Accessed April 2011.

  • Seco Pon, J. P. & P. A. Gandini, 2007. Bycatch of the piked dogfish Squalus acanthias Linné, 1758 (Chondrichthyes, Squalidae) in semi-pelagic longline fisheries at the Patagonian Shelf. Investigaciones Marinas 35: 85–88.

    Article  Google Scholar 

  • Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S-Plus. Springer, New York.

    Google Scholar 

  • Vögler, R., A. C. Milessi & L. O. Duarte, 2009. Changes in trophic level of Squatina guggenheim with increasing body length: relationships with type, size and trophic level of its prey. Environmental Biology of Fishes 84: 41–52.

    Google Scholar 

  • Vooren, C. M. & S. Klippel, 2005. Diretrizes para conservação de espécies ameaçadas de elasmobrânquios. In Vooren, C. M. & S. Klippel (eds), Ações para a conservação de tubarões e raias na Plataforma Sul. Igaré, Porto Alegre: 229–246.

    Google Scholar 

  • Watling, L., 2005. The global destruction of bottom habitats by mobile fishing gear. In Norse, E. A. & L. B. Crowder (eds), Marine Conservation Biology: The Science of Maintaining the Sea’s Biodiversity. Island Press, Washington, DC: 198–210.

    Google Scholar 

  • Wetherbee, B. M. & E. Cortés, 2004. Food consumption and feeding habits. In Musick, J. A., J. C. Carrier & M. Heithaus (eds), Biology of Sharks and Their Relatives. CRC Press, Boca Raton: 224–246.

    Google Scholar 

  • Zhang, B., Q. Tang & X. Jin, 2007. Decadal-scale variations of trophic levels at high trophic levels in the Yellow sea and the Bohai sea ecosystem. Journal of Marine Systems 67: 304–311.

    Article  Google Scholar 

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Acknowledgments

We thank the Trophic Ecology Group of the Instituto Nacional de Investigacion y Desarrollo Pesquero (INIDEP) for the historical dataset and the specimens collected from the research cruises. We would like to thank Gaby Silvoni and Guilla Cosulich (librarians of INIDEP) who provided most helpful documentation. We are also grateful to J. Collonelo and C. Buratti (Celtas), Fede Cortés, Noe Marí and Pelado Casagrande for their help during sample collection. Earlier versions of the manuscript benefited from comments by the editor and two anonymous reviewers. Belleggia Mauro was supported by a scholarship of CONICET. This research was partially supported by PICT 2007/02200 of CONICET. This is INIDEP contribution No. 1683.

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Correspondence to Mauro Belleggia.

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Belleggia, M., Figueroa, D.E., Sánchez, F. et al. Long-term changes in the spiny dogfish (Squalus acanthias) trophic role in the southwestern Atlantic. Hydrobiologia 684, 57–67 (2012). https://doi.org/10.1007/s10750-011-0967-y

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