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Spatio-temporal variations in the diet and stable isotope composition of the Argentine hake Merluccius hubbsi Marini, 1933 of the continental shelf of southeastern Brazil

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Abstract

The feeding ecology of Merluccius hubbsi was investigated in 2 regions of SE Brazil. The major food sources for the hakes were fish, crustaceans, and squid. In the upwelling system of Cabo Frio, the diet was very similar in the summers of 2001/2002 and spring 2002; fish were the most important prey followed by crustaceans. In Ubatuba, euphausiids were an important prey during the winter 2001 (100 m), while in the summer 2002, fish and amphipods predominated in the diet in the shallower site (40 m) and squid in the deeper site (100 m). The hakes showed temporal differences in stable isotope signatures in both regions, while C:N ratios varied only in Cabo Frio. δ15N and δ13C (bulk and corrected for lipid content) increased with fish length, which seems to be related to the increasing importance of fish and decreasing importance of euphausiids and amphipods in the diet of larger hakes. The mean trophic level of 3.7 for M. hubbsi was estimated using δ15N of bivalves as baseline and the fractionation of 3.4‰ between trophic levels.

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References

  • Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45(30):601–607

    Article  CAS  Google Scholar 

  • Aidar E, Gaeta SA, Gianesella-Galvão SMF, Kutner MBB, Teixeira C (1993) Ecossistema costeiro subtropical: nutrientes dissolvidos, fitoplâncton e clorofila-a e suas relações com as condições oceanográficas na região de Ubatuba, SP. Publção esp Inst Oceanogr 10:9–43

    Google Scholar 

  • Altabet MA, McCarthy JJ (1985) Temporal and spatial variations in the natural abundance of 15N in PON from a warm-core ring. Deep Sea Res 32:755–772

    Article  CAS  Google Scholar 

  • Badalamenti F, D’Anna G, Pinnegar JK, Polunin NVC (2002) Size-related trophodynamic changes in three target fish species recovering from intensive trawling. Mar Biol 141:561–570

    Article  Google Scholar 

  • Barnes C, Sweeting CJ, Jennings S, Barry JT, Polunun NVC (2007) Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21:356–362

    Article  Google Scholar 

  • Bode A, Alvarez-Ossorio MT (2004) Taxonomic versus trophic structure of mesozooplankton: a seasonal study of species succession and stable carbon and nitrogen isotopes in a coastal upwelling ecosystem. ICES J Mar Sci 61:563–571

    Article  Google Scholar 

  • Castello JP, Habiaga R, Amaral JC, Lima ID Jr (1991) Prospecção hidroacústica e avaliação de biomassa de sardinha e anchoíta na região sudeste do Brasil (outubro/novembro de 1988). Publção esp Inst oceanogr 7(8):15–30

    Google Scholar 

  • Castro Filho BM, de Miranda LB (1998) Physical oceanography of the western atlantic continental shelf located between 4°N and 34°S coastal segment (4, W). In: Robinson AR, Brink KH (eds) The sea: the global coastal ocean: regional studies and syntheses, vol 11. Wiley, New York

  • Cohen DM, Takahashi I, Iwamoto T, Scialabba N (1990) Gadiform fishes of the world (order gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO species catalogue, p 10

  • Corbisier TN (2006) Trofodinâmica do ecossistema bentônico de plataforma continental da costa sudeste do Brasil: uso de isótopos estáveis de carbono e nitrogênio. Dissertation, Universidade de São Paulo

  • Costa PAS, Fernandes FC (1993) Seasonal and spatial changes of cephalopods caught in the Cabo Frio (Brazil) upwelling system. Bull Mar Sci 52(2):751–759

    Google Scholar 

  • Davenport SR, Bax NJ (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can J Fish Aquat Sci 59:514–530

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • DOE 2008. Decreto N° 53.494/2008. Declara as Espécies da Fauna Silvestre Ameaçadas, as Quase Ameaçadas, as Colapsadas, Sobrexplotadas, Ameaçadas de Sobrexplotação e com dados insuficientes para avaliação no Estado de São Paulo e dá providências correlatas. Diário Oficial do Estado de São Paulo, Poder Executivo, Seção I 118(187), São Paulo, 3 de outubro de 2008, pp 2–10

  • Fagundes-Netto EB, Gaelzer LR (1991) Associação de peixes bentônicos e demersais na região de Cabo Frio, RJ, Brasil. Nerítica 6(1–2):139–156

    Google Scholar 

  • Ferraton F, Harmelin-Vivien M, Mellon-Duval C, Souplet A (2007) Spatio-temporal variation in diet may affect condition and abundance of juvenile European hake in the Gulf of Lions (NW Mediterranean). Mar Ecol Prog Ser 337:197–208

    Article  Google Scholar 

  • Fry B, Wainright SC (1991) Diatom sources of 13C-rich carbon in marine food webs. Mar Ecol Prog Ser 76:149–157

    Article  Google Scholar 

  • Galván DE, Sweeting CJ, Reid WDK (2010) Power of stable isotope techniques to detect size-based feeding in marine fishes. Mar Ecol Prog Ser 407:271–278

    Article  Google Scholar 

  • Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183

    Article  Google Scholar 

  • Gonzalez-Rodriguez E, Valentin JL, André DL, Jacob SA (1992) Upwelling and downwelling at Cabo Frio (Brazil): comparison of biomass and primary responses. J Plankt Res 14(2):289–306

    Article  Google Scholar 

  • Haimovici M, Martins AS, Teixeira RL (1993) Distribución, alimentación y observaciones sobre la reproducción de la merluza M. hubbsi en el sur de Brasil. Frente Marítimo 14:81–86

    Google Scholar 

  • Haimovici M, Rossi-Wongtschowski CLDB, Bernardes RÁ, Fischer LG, Vooren CM, Santos RA, Rodrigues AR, Santos S (2008) Prospecção Pesqueira de espécies demersais com rede de arrasto-de-fundo na região Sudeste-Sul do Brasil. Série Documentos REVIZEE, Score Sul. São Paulo, Instituto Oceanográfico, Universidade de São Paulo

  • Herzka SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar Coast Shelf Sci 64:58–69

    Article  Google Scholar 

  • Hyslop EJ (1980) Stomach content analysis: a review of methods and their application. J Fish Biol 17(4):411–429

    Article  Google Scholar 

  • Jennings S, Greenstreet SPR, Piet GJ, Pinnegar JK, Warr KJ (2002) Long-term in the trophic structure of the north Sea fish community: evidence from stable-isotopes analysis, size-spectra and community metrics. Mar Biol 141:1085–1097

    Article  Google Scholar 

  • Kampel M (2003) Estimativa da produção primária e biomassa fitoplanctônica através de sensoriamento remoto da cor do oceano e dados in situ na costa sudeste brasileira. Dissertation, Universidade de São Paulo

  • Kanneworff E (1965) Life cycle, food and growth of the amphipod A. macrocephala Liljeborg from the Øresund. Ophelia 2(2):305–318

    Article  Google Scholar 

  • Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing δ13C values from aquatic organisms: with implications for isotope mixing models. J Appl Ecol 43:1213–1222

    Article  CAS  Google Scholar 

  • Kinsey ST, Hopkins TL (1994) Trophic strategies of euphausiids in a low-latitude ecosystem. Mar Biol 118(4):651–661

    Article  Google Scholar 

  • Le Loc’h F, Hily C (2005) Stable carbon and nitrogen isotope analysis of N. norvegicus/M. merluccius fishing grounds in the Bay of Biscay (Northeast Atlantic). Can J Fish Aquat Sci 62:123–132

    Article  Google Scholar 

  • Martins AS (2000) As assembléias e as guildas tróficas de peixes ósseos e cefalópodes demersais da plataforma continental e talude superior do extremo sul do Brasil. Dissertation, Universidade Federal do Rio Grande

  • Matsuura K, Amaral JK, Sato G, Tamássia STJ (1985) Ocorrência de peixes pelágicos e estrutura oceanográfica da região entre Cabo de São Tomé (RJ) e Cananéia (SP), em janeiro-fevereiro/1979. Série Documentos Técnicos, PDP/DUDEPE, Brasilia 33:3–70

    Google Scholar 

  • Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener R (eds) Stable isotopes in ecology and environmental science, 1st edn. Blackwell Scient. Publs, Oxford

    Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Muto EY (2004) Variações isotópicas de 13C e 15N de peixes demerso-pelágicos do ecossistema de plataforma ao largo de Cabo Frio (RJ) e Ubatuba (SP). Dissertation, Universidade de São Paulo

  • Muxagata E (1999) Avaliação da biomassa e distribuição zooplanctônica na plataforma continental sudeste brasileira durante o inverno de 1995. Dissertation, Fundação Universidade Federal do Rio Grande do Sul

  • Nakatami K (1982) Estudos sobre os ovos e larvas de E. anchoita (Hubbs and Marini 1935) (Teleostei, Engraulidae) coletados na região entre Cabo Frio (23°S) e Cabo de Santa Marta Grande (29°S). Dissertation, Universidade de São Paulo

  • Natali-Neto JF (1994) Ictiofauna do ecossistema tropical marinho de Ubatuba (23°36′S–24°22′S; 44°33′W–45°08′W), SP, Brasil, entre 50 e 100 m de profundidade: composição, distribuição, abundância e diversidade. Dissertation, Universidade de São Paulo

  • Nyssen F, Brey T, Lepoint G, Bouquegneau JM, De Broyer C, Dauby P (2002) A stable isotope approach to the eastern Weddell Sea trophic web: focus on benthic amphipods. Polar Biol 25:280–287

    Google Scholar 

  • Olive PJW, Pinnegar JK, Polunin NVC, Richards G, Welch R (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608–617

    Article  Google Scholar 

  • Perez JAA, Pezzuto PR (2006) A pesca de arrasto de talude do sudeste e sul do Brasil: tendências da frota nacional entre 2001 e 2003. Bol Inst Pesca 32(2):127–150

    Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Pinkas L, Oliphant MS, Iverson ILK (1971) Food habits of albacore, bluefin tuna and bonito in California waters. Fish Bull 152:1–105

    Google Scholar 

  • Poore AGB (1994) Selective herbivory by amphipods inhabiting the brown algae Z. angustata. Mar Ecol Prog Ser 107:113–123

    Article  Google Scholar 

  • Prenski LB, Angelescu V (1993) Ecología trofica de la merluza comun (M. hubbsi) del mar Argentino. Parte 3. Consumo anual de alimento a nivel poblacional y su relación con la explotación de las pesquerías multiespecificas. INIDEP Documento Científico, Mar del Plata, p 1

  • Rau GH, Mearns AJ, Young DR, Olson RJ, Schafer HA, Kaplan IR (1983) Animal 13C/12C correlates with trophic levels in pelagic food webs. Ecology 64:1314–1318

    Article  Google Scholar 

  • Reñones O, Polunin NVC, Goni R (2002) Size related dietary shifts of E. marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. J Fish Biol 61:122–137

    Article  Google Scholar 

  • Rocha GRA, Rossi-Wongtschowski CLDB, Pires-Vanin AMS, Jarre-Teichmann A (2003) Seasonal budgets of organic matter in the ubatuba shelf system, SE Brazil. I. Planktonic and benthic components. Oceanol Acta 26:487–495

    Article  Google Scholar 

  • Rolff C (2000) Seasonal variation in δ13C and δ15N of size fractionated plankton at a coastal station in the northern Baltic proper. Mar Ecol Prog Ser 203:47–65

    Article  CAS  Google Scholar 

  • Schwingel PR (1998) Feeding ecology of E. anchoita (Hubbs and Marini 1935) in Brazilian waters (22–34°S). Dissertation, University of Hamburg

  • Soares LSH, Gasalla MA, Rios MAT, Arrasa MV, Rossi-Wongtschowski CLDB (1993) Grupos tróficos de onze espécies dominantes de peixes demersais da plataforma continental interna de Ubatuba, Brasil. Publção esp Inst oceanogr 10:189–198

    Google Scholar 

  • Sweeting CJ, Jennings S, Polunin NVC (2005) Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Funct Ecol 19(5):777–784

    Article  Google Scholar 

  • Tôha FAL (1981) Sistemática e distribuição geográfica de Euphausiacea (Crustacea) ao largo das costas sul do Brasil (Lat. 22–30°S). Dissertation, Universidade de São Paulo

  • Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (S. salar). Rapid Commun Mass Spectrom 19(22):3239–3247

    Article  CAS  Google Scholar 

  • Valentin JL, Lins da Silva NM, Monteiro-Ribas WM, Mureb MA, Bastos CTBT, Tenebaum DR, André DL, Jacob SA, Pessoti E (1986) Le plancton dans l′upwelling de Cabo Frio (Brèsil): microrépartition spatio-temporelle à une station fixe. Annls Inst océanogr 62(1):117–135

    Google Scholar 

  • Valentin JL, André DL, Jacob SA (1987) Hydrobiology in the Cabo Frio (Brazil) upwelling: 2-D structure and variability during a wind cycle. Cont Shelf Res 7(1):77–88

    Article  Google Scholar 

  • Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158

    Article  Google Scholar 

  • Wada E, Hattori A (1991) Nitrogen in the sea: forms, abundance, and rate processes. CRC Press, Boca Raton, p 208

    Google Scholar 

  • Wu J, Calvert SE, Wong CS (1997) Nitrogen isotope variations in the subarctic northeast Pacific: relationships to nitrate utilization and trophic structure. Deep-Sea Res I 44(2):287–314

    Article  CAS  Google Scholar 

  • Wu JP, Calvert SE, Wong CS (1999) Carbon and nitrogen isotope ratios in sedimenting particulate organic matter at an upwelling site off Vancouver Island. Estuar Coast Shelf Sci 48:193–203

    Article  CAS  Google Scholar 

  • Zembruscki SG (1979) Geomorfologia da margem continental sul-brasileira e das bacias oceânicas adjacentes. In: Chaves HAS (ed) Projeto REMAC. Reconhecimento global da margem continental brasileira: geomorfologia da margem continental brasileira e das áreas oceânicas adjacentes (Relatório final). Rio de Janeiro: PETROBRÁS-CENPES-DINTEP. Série PROJETO REMAC, 7

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Acknowledgments

The authors are grateful to the crew of the RV Professor W. Besnard for helping in collecting the samples. We acknowledge Professor Dr Rubens Lopes (IOUSP), Dr Roberta A. Santos (Ibama-CEPSUL), Kazuko Suzuki, MSc. Meiri de Campos, MSc. Charles Gorri, and Caio Marques for their support in identifying certain prey organisms. This study is part of the PhD thesis of Elizabeti Y. Muto sponsored by The State of São Paulo Research Foundation (FAPESP, n. 99/05454-0). The project DEPROAS was supported by National Council for Scientific and Technological Development (CNPq, PRONEX/Proc. n° 368/96). We thank the anonymous reviewer and Dr Christopher J. Sweeting for their helpful and thoughtful comments that contributed to improving the quality of this manuscript.

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  1. Laboratório de Ecologia Trófica, Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, SP, 05508-120, Brazil

    Elizabeti Yuriko Muto & Lucy Satiko Hashimoto Soares

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  1. Elizabeti Yuriko Muto
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Correspondence to Elizabeti Yuriko Muto.

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Communicated by M. A. Peck.

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Muto, E.Y., Soares, L.S.H. Spatio-temporal variations in the diet and stable isotope composition of the Argentine hake Merluccius hubbsi Marini, 1933 of the continental shelf of southeastern Brazil. Mar Biol 158, 1619–1630 (2011). https://doi.org/10.1007/s00227-011-1674-y

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