Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-25T21:58:36.569Z Has data issue: false hasContentIssue false
  • English
  • Français

Feeding habits and trophic status of Merluccius hubbsi along the northernmost limit of its distribution in the South-western Atlantic

Published online by Cambridge University Press:  12 April 2019

Paulo A. S. Costa Open the ORCID record for Paulo A. S. Costa [Opens in a new window] ,
Adriana C. Braga ,
Giovanna S. Malavolti ,
Marcos A. L. Franco ,
Pedro V. Gatts ,
Andressa Batista  and
Carlos E. Rezende
Paulo A. S. Costa*
Affiliation:
Departamento de Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, Brazil Programa de Pós-graduação em Dinâmica dos Oceanos e da Terra, Universidade Federal Fluminense, Niterói, RJ, Brazil
Adriana C. Braga
Affiliation:
Departamento de Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, Brazil
Giovanna S. Malavolti
Affiliation:
Departamento de Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, RJ, Brazil
Marcos A. L. Franco
Affiliation:
Departamento de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, RJ, Brazil
Pedro V. Gatts
Affiliation:
Programa de Pós-graduação em Dinâmica dos Oceanos e da Terra, Universidade Federal Fluminense, Niterói, RJ, Brazil Departamento de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, RJ, Brazil
Andressa Batista
Affiliation:
Departamento de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, RJ, Brazil
Carlos E. Rezende
Affiliation:
Departamento de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Campos dos Goytacazes, RJ, Brazil
*
Author for correspondence: Paulo A. S. Costa, E-mail: paulocosta.unirio@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Stomach contents analysis and stable isotope results indicate M. hubbsi is a generalist predator that feeds mainly on demersal fishes, followed by crustaceans and cephalopods. Ontogenetic changes in diet were identified, with fish importance increasing in the diet with hake size. Smaller hake (<250 mm) fed mostly on the sepiolid Semirossia tenera (89.45%IRI) and engraulid fish (89.96%IRI). Mid-sized hake (250–300 mm) fed mainly on benthic fish such as Bellator brachychir (95.63%IRI) and euphausiids (56.46%IRI), while larger hake (>300 mm) fed heavily on Dactylopterus volitans (94.80%IRI) and occasionally on a variety of teleosts. Significant correlations between δ13C (P < 0.05), THg (P < 0.001) and hake size occurred, whereas no relationship was observed between δ15N and hake size or δ15N and total mercury. Signatures were lowest in smaller hake with a tendency of increasing with size. Smaller and larger hake were significantly different in δ13C. Differences regarding isotopic niche width were quantified for each size group; trophic diversity and trophic redundancy among them were negligible, but hake >300 mm possibly have a larger feeding plasticity due to the combination of prey from a wide trophic level range.

Keywords

DietMerluccius hubbsiSouth-western Atlanticstable isotopes
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 6 , September 2019 , pp. 1399 - 1408
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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

Abbey, LD, Glover-Amengor, M, Atikpo, MO and Howell, NK (2017) Proximate and biochemical characterization of burrito (Bachydeuterus auritus) and flying gurnard (Dactylopterus volitans). Food Science & Nutrition 5, 369–373.Google Scholar
Alleman, MM (2013) Estrutura populacional do coió, Dactylopterus volitans (Linnaeus, 1758) (Scorpaeniformes: Dactylopteridae) no Atlântico Sudoeste, Brasil (MSc thesis). Universidade Santa Cecília, São Paulo, Brazil.Google Scholar
Arkhipkin, AI, Laptikhovsky, VV and Barton, AJ (2015) Biology and fishery of common hake (Merluccius hubbsi) and southern hake (Merluccius australis) around the Falkland/Malvinas Islands on the Patagonian shelf of the Southwest Atlantic Ocean. In Arancibia, H (org.), Hakes, Biology and Exploitation. Oxford: Wiley, pp. 154–184.Google Scholar
Bastos, WR, Malm, O, Pfeiffer, WC and Cleary, D (1998) Establishment and analytical quality control of laboratories for Hg determination in biological and geological samples in the Amazon, Brazil. Technical Review. Ciência e Cultura 50, 255–260.Google Scholar
Bearhop, S, Adams, CE, Waldron, S, Fuller, RA and MacLeod, H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73, 1007–1012.Google Scholar
Belleggia, M, Figueroa, DE, Irusta, G and Bremec, C (2014) Spatio-temporal and ontogenetic changes in the diet of the Argentine hake Merluccius hubbsi. Journal of the Marine Biological Association of the United Kingdom 94, 1701–1710.Google Scholar
Bezerra, MF, Lacerda, LD, Rezende, CE, Franco, MAL, Ameida, MG, Macedo, GR, Pires, TT, Rostán, G and Lopez, GG (2015) Food preferences and Hg distribution in Chelonia mydas assessed by stable isotopes. Environmental Pollution 206, 236–246.Google Scholar
Bisi, TL, Lepoint, G, Azevedo, AF, Dorneles, PR, Flach, L, Das, K, Malm, O and Lailson-Brito, J (2012) Trophic relationships and mercury biomagnifications in Brazilian tropical coastal food webs. Ecological Indicators 18, 291–302.Google Scholar
Bouillon, S, Conolly, RM and Gillian, DP (2011) Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In Polanski, E and McLusky, DS (eds), Treatise on Estuarine and Coastal Science. Waltham, MA: Academic Press, pp. 143–173.Google Scholar
Carpentieri, P, Colloca, F, Cardinale, M, Belluscio, A and Ardizzone, GD (2005) Feeding habits of European hake (Merluccius merluccius) in the central Mediterranean Sea. Fishery Bulletin 103, 411–416.Google Scholar
Cartes, JE, Hidalgo, M, Papiol, V, Massutí, E and Moranta, J (2009) Changes in the diet and feeding of the hake Merluccius merluccius at the shelf-break of the Balearic Islands: influence of the mesopelagic-boundary community. Deep-Sea Research I 56, 344–365.Google Scholar
Chouvelon, T, Caurant, F, Cherel, Y, Simon-Bouhet, B, Spitz, J and Bustamente, P (2014) 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 71, 1073–1087.Google Scholar
Clarke, KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecology 18, 117–143.Google Scholar
Clarke, KR and Warwick, RM (1994) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth: Plymouth Marine Laboratory.Google Scholar
Cohen, DM, Inada, T, Iwamoto, T and Scialabba, N (1990) FAO Species Catalogue. Vol. 10. Gadiform Fishes of the World (Order Gadiformes). An Annotated and Illustrated Catalogue of Cods, Hakes, Grenadiers and other Gadiform Fishes Known to Date. FAO Fisheries Synopsis No. 125. Rome: FAO.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
Cossa, D, Harmelin-Vivien, M, Mellon-Duval, C, Loizeau, V, Averty, B, Crochet, S, Chou, L and Cadiou, J-F (2012) Influences of bioavailability, trophic position, and growth on methylmercury in hakes (Merluccius merluccius) from northwestern Mediterranean and Northeastern Atlantic. Environmental Science & Technology 46, 4885–4893.Google Scholar
Costa, PAS, Mincarone, MM, Braga, AC, Martins, AS, Lavrado, HP, Haimovici, M and Falcão, APC (2015) Megafaunal communities along a depth gradient on the tropical Brazilian continental margin. Marine Biology Research 11, 1053–1064.Google Scholar
Costa, PAS, Braga, AC, Vieira, JMS, Martins, RRM, São-Clemente, RRB and Couto, BR (2018) Age estimation, growth and maturity of the Argentine hake (Merluccius hubbsi Marini, 1933) along the northernmost limit of its distribution in the south-western Atlantic. Marine Biology Research 14, 728–738.Google Scholar
Di Beneditto, APM, Souza, CMM, Kerigh, H and Rezende, CE (2011) Use of multiple tools to assess the feeding preference of coastal dolphins. Marine Biology 158, 2209–2217.Google Scholar
Di Beneditto, APM, Santos, RA, Rosa, KR and Siciliano, S (2014) Magellanic penguins: stomach contents and isotopic profiles to assess the feeding demands of juveniles in a wintering area off Brazil. Journal of the Marine Biological Association of the United Kingdom 95, 423–430.Google Scholar
Eder, EB and Lewis, MN (2005) Proximate composition and energetic value of demersal and pelagic prey species from the SW Atlantic Ocean. Marine Ecology Progress Series 291, 43–52.Google Scholar
Fiperj 2013. Boletim estatístico da pesca marinha no Estado do Rio de Janeiro, anos 2011 e 2012. Available at http://www.fiperj.rj.gov.br/index.php/arquivo/download/70.Google Scholar
Fry, B and Chumchal, MM (2012) Mercury bioaccumulation in estuarine food webs. Ecological Applications 22, 606–623.Google Scholar
Garrison, LP and Link, JS (2000) Diets of five hake species in the northeast United States continental shelf ecosystem. Marine Ecology Progress Series 204, 243–255.Google Scholar
Gasalla, MA, Rodrigues, AR and Postuma, FA (2010) The trophic role of the squid Loligo plei as a keystone species in the South Brazil Bight ecosystem. ICES Journal of Marine Science 67, 1413–1424.Google Scholar
Haimovici, M, Martins, AS and Teixeira, ERL (1993) Distribución, alimentación y observaciones sobre la reprodución de la merluza (Merluccius hubbsi) en el sur de Brasil. Frente Marítimo 14, 33–40.Google Scholar
Harmelin-Vivien, M, Mahé, K, Bodiguel, X and Mellon-Duval, C (2012) Possible link between prey quality, condition and growth of juvenile hake (Merluccius merluccius) in the Gulf of Lions (NW Mediterranean). Cybium 36, 323–328.Google Scholar
Hurlbert, SH and Lombardi, CM (2009) Final collapse of the Neyman-Pearson decision theoretic framework and rise of the neoFisherian. Annales Zoologici Fennici 46, 311–349.Google Scholar
Hyslop, EJ (1980) Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Iitembu, JA, Miller, TW, Ohmori, K, Kanime, A and Wells, S (2012) Comparison of ontogenetic trophic shift in two hake species, Merluccius capensis and Merluccius paradoxus, from the Northern Benguela Current ecosystem (Namibia) using stable isotope analysis. Fisheries Oceanography 21, 215–225.Google Scholar
Irusta, CG, Macchi, GJ, Louge, E, Rodrigues, K, D’Atri, LL, Villarino, MF, Santos, B and Simonazzi, M (2016) Biology and fishery of the Argentine hake (Merluccius hubbsi). Revista de Investigación y Desarrollo Pesquero 28, 9–36.Google Scholar
Jackson, AL, Inger, R, Parnell, AC 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.Google Scholar
Kehrig, HA, Fernandes, KWG, Malm, O, Seixas, TG, Di Beneditto, APM and Souza, CMM (2009) Trophic transference of mercury and selenium in the northern coast of Rio de Janeiro. Química Nova 32, 1822–1828.Google Scholar
Koen-Alonso, M, Crespo, ES, Garcia, NA, Pedraza, SN, Mariotti, PA, Vera, BB and Mora, NJ (2001) Food habits of Dipturus chilensis (Pisces: Rajidae) off Patagonia, Argentina. ICES Journal of Marine Science 58, 288–297.Google Scholar
Layman, CA, Arrington, DA, Montana, CG and Post, DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.Google Scholar
Link, JS and Garrison, LP (2002) Trophic ecology of Atlantic cod Gadus morhua on the northeast US continental shelf. Marine Ecology Progress Series 227, 109–123.Google Scholar
Loizaga de Castro, R, Saporiti, F, Vales, DG, García, NA, Cardona, L and Crespo, EA (2016) What are you eating? A stable isotope insight into the trophic ecology of short-beaked common dolphins in the Southwestern Atlantic Ocean. Mammalian Biology 81, 571–578.Google Scholar
Lopez-Lopez, L, Bartolino, V and Preciado, I (2015) Role of prey abundance and geographical variables in a demersal top predator's feeding habits (Merluccius merluccius). Marine Ecology Progress Series 541, 165–177.Google Scholar
Lorenzo, MI and Defeo, O (2015) The biology and fishery of hake (Merluccius hubbsi) in the Argentinean-Uruguayan common fishing zone of the Southwest Atlantic Ocean. In Arancibia, H (org.), Hakes, Biology and Exploitation. Oxford: Wiley, pp. 185–210.Google Scholar
Mahe, K, Amara, R, Bryckaert, T, Kacher, M and Brylinski, JM (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.Google Scholar
Muñoz, AA and Ojeda, FP (1998) Guild structure of carnivorous intertidal fishes of the Chilean coast: implications of ontogenetic dietary shifts. Oecologia 114, 563–573.Google Scholar
Muto, EY and Soares, LSH (2011) 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. Marine Biology 158, 1619–1630.Google Scholar
Muto, EY, Soares, LSH, Sarkis, JES, Hortellani, MA, Petti, MAV and Corbisier, TN (2014) Biomagnification of mercury through the food web of the Santos continental shelf, subtropical Brazil. Marine Ecology Progress Series 512, 55–69.Google Scholar
Nascimento, MA, Velasco, G, Okey, TA, Christensen, V and Amaral, ACZ (2012) Trophic model of the outer continental shelf and upper slope demersal community of the southern Brazilian Bight. Scientia Marina 76, 763–779.Google Scholar
Ocampo Reinaldo, M, González, R and Romero, MA (2011) Feeding strategy and cannibalism of the Argentine hake Merluccius hubbsi. Journal of Fish Biology 79, 1795–1814.Google Scholar
Okey, TA, Banks, S, Born, AF, Bustamante, RH, Calvopiña, M, Edgar, GJ, Espinoza, E, Fariña, JM, Garske, LE, Reck, GK, Salazar, S, Shepherd, S, Toral-Granda, V and Wallem, P (2004) A trophic model of Galápagos subtidal rocky reef for evaluating fisheries and conservation strategies. Ecological Modelling 172, 383–401.Google Scholar
Peterson, BJ and Fry, B (1987) Stable isotopes in ecosystems studies. Annual Review of Ecology and Systematics 18, 293–320.Google Scholar
Pinkas, LM, Oliphant, S and Iverson, ILK (1971) Food habits of albacore, bluefin tuna and bonito in Californian waters. California Fish and Game 125, 1–105.Google Scholar
Post, DM, Layman, CA, Arrington, DA, Takimoto, G, Quattrochi, J and Montaña, J (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.Google Scholar
Prenski, LB and Angelescu, V (1993) Ecología trófica de la merluza común (Merluccius 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, no. 1, 188 pp.Google Scholar
R Development Core Team (2018) R: A Language and Environment for Statistical Computing. Available at http://www.R-project.org/.Google Scholar
Rexstad, EA and Pikitch, EK (1986) Stomach contents and food consumption estimates of Pacific hake, Merluccius productus. Fishery Bulletin 84, 947–956.Google Scholar
Sackett, DK, Cope, WG, Rice, JA and Aday, DD (2013) The influence of fish length on tissue mercury dynamics: implications for natural resource management and human health risk. International Journal of Environmental Research and Public Health 10, 638–659.Google Scholar
Sala, JE, Wilson, RP, Frere, E and Quintana, F (2012) Foraging effort in Magellanic penguins in coastal Patagonia, Argentina. Marine Ecology Progress Series 464, 273–287.Google Scholar
Santos, RA and Haimovici, M (1998) Trophic relationships of the long-finned squid Loligo sanpaulensis on the southern Brazilian shelf. South African Journal of Marine Science 20, 81–91.Google Scholar
Santos, RA and Haimovici, M (2001) Cephalopods in the diet of marine mammals stranded or incidentally caught along southeastern and southern Brazil (21–34oS). Fisheries Research 52, 99–112.Google Scholar
Segadilha, JL, Nascimento, PS, Mauro, FM, Serejo, CS, Ramos, TR, Cardoso, IA, Martins, AS and Costa, PAS (2018) The carcinofauna found in stomach contents of the flying gurnard (Dactylopterus volitans) on the continental shelf of the Campos Basin, Brazil. Journal of Natural History 52, 1–11.Google Scholar
Soares, LSH, Muto, EY, Lopez, JP, Clauzet, GRV and Valiela, I (2014) Seasonal variability of δ13C and δ15N of fish and squid in the Cabo Frio upwelling system of the southwestern Atlantic. Marine Ecology Progress Series 512, 9–21.Google Scholar
Stott, FC (1982) Notes on the biology of the Patagonian hake, Merluccius hubbsi (Marini), the southern blue whiting, Micromesistius australis (Norman) and others in the Falkland Islands shelf area. Journal of Fish Biology 21, 705–714.Google Scholar
Temperoni, B, Viñas, MD and Buratti, CC (2013) Feeding strategy of juvenile (age-0+ year) Argentine hake Merluccius hubbsi in the Patagonian nursery ground. Journal of Fish Biology 83, 1354–1370.Google Scholar
Treiman, DM and Adams, DH (2012) Mercury and sea basses from the Gulf of Mexico: relationships with size, age and feeding ecology. Transactions of the American Fisheries Society 141, 1247–1286.Google Scholar
Vaske, T Jr, Travassos, PR, Hazin, FHV, Tolotti, MT and Barbosa, TC (2012) Forage fauna in the diet of bigeye tuna (Thunnus obesus) in the Western Tropical Atlantic Ocean. Brazilian Journal of Oceanography 60, 89–97.Google Scholar
Vaz-dos-Santos, AM and Schwingel, PR (2015) Biology and fisheries of hake (Merluccius hubbsi) in Brazilian waters, Southwest Atlantic. In Arancibia, H (org.), Hakes, Biology and Exploitation. Oxford: Wiley, pp. 211–233.Google Scholar
Vaz-dos-Santos, AM and Rossi-Wongtschowski, CLDB (2005) Merluccius hubbsi marini, 1933. In Cergole, MC, Ávila-da-Silva, AO and Rossi-Wongtschowski, CLDB (eds), Análise das principais pescarias comerciais da região sudeste-sul do Brasil: dinâmica populacional das espécies em explotação. São Paulo: Instituto Oceanográfico-USP, pp. 88–93.Google Scholar
Vecchione, M, Roper, CFE, Sweeney, MJ and Lu, CC (2001) Distribution, relative abundance and developmental morphology of paralarval cephalopods in the Western North Atlantic Ocean. NOAA Technical Report NMFS 152, 1–58.Google Scholar
Yasue, N, Doiuchi, R and Takasuda, A. (2014) Trophodynamic similarities of three sympatric clupeoid species throughout their life histories in the Kii Channel as revealed by stable isotope approach. ICES Journal of Marine Science 71, 44–55.Google Scholar