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Feeding comparisons of four batoids (Elasmobranchii) in coastal waters of southern Brazil

Published online by Cambridge University Press:  02 May 2014

Hugo Bornatowski*
Affiliation:
Universidade Federal do Paraná, Caixa Postal 19020, CEP 81531-980 Curitiba, PR, Brazil GPIc—Grupo de Pesquisas em Ictiofauna, Museu de História Natural Capão da Imbuia, Rua Prof. Benedito Conceição, 407, 82810-080, Curitiba, PR, Brazil
Natascha Wosnick
Affiliation:
Departamento de Fisiologia, Setor de Ciências Biológicas, Centro Politécnico, Universidade Federal do Paraná, Curitiba, Paraná, CEP 81531-990, Brazil
Wanessa P. David do Carmo
Affiliation:
Laboratório de Reprodução e Comunidade de Peixes, Universidade Federal do Paraná, CP 19031, CEP 81531-980, Curitiba, PR, Brazil
Marco Fábio Maia Corrêa
Affiliation:
Universidade Federal do Paraná, Caixa Postal 19020, CEP 81531-980 Curitiba, PR, Brazil GPIc—Grupo de Pesquisas em Ictiofauna, Museu de História Natural Capão da Imbuia, Rua Prof. Benedito Conceição, 407, 82810-080, Curitiba, PR, Brazil
Vinícius Abilhoa
Affiliation:
Universidade Federal do Paraná, Caixa Postal 19020, CEP 81531-980 Curitiba, PR, Brazil GPIc—Grupo de Pesquisas em Ictiofauna, Museu de História Natural Capão da Imbuia, Rua Prof. Benedito Conceição, 407, 82810-080, Curitiba, PR, Brazil
*
Correspondence should be addressed to: H. Bornatowski, Universidade Federal do Paraná, Caixa Postal 19020, CEP 81531-980 Curitiba, PR, Brazil email: anequim.bio@gmail.com

Abstract

Food partitioning between species is a common strategy for avoiding resource competition which allows the coexistence of two or more species in the same place. In order to evaluate the feeding of four species of batoids regularly caught by artisanal fisheries in southern Brazil, the present study aimed to analyse and compare the diet of the four batoid species. The Chola guitarfish, Rhinobatos percellens, had a specialized diet, consisting predominantly of blue crabs Callinectes sp., followed by teleost fish. The Lesser guitarfish Zapteryx brevirostris also had a very specialized diet, consuming mainly on Polychaeta, followed by Caridea shrimp. The Cownose ray, Rhinoptera bonasus, fed mainly on Ophiuroidea, followed by Gastropoda and Bivalvia. Finally, the Rio skate Rioraja agassizi, fed on teleost fish, Gammaridae, Caridea shrimp and Dendrobranchiata shrimp. An analysis of similarity showed significant differences among species in their diet. The trophic levels of the batoids in this study are <4.0, placing them in intermediate trophic levels. The analysis of the diets indicates that feeding differs substantially among the four species, suggesting a partitioning of food resources available in the environment.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Barbini, S.A. and Lucifora, L.O. (2011) Feeding habits of the Rio skate, Rioraja agassizi (Chondrichthyes: Rajidae), from off Uruguay and north Argentina. Journal of the Marine Biological Association of the United Kingdom 91, 11751184.CrossRefGoogle Scholar
Barbini, S.A., Lucifora, L.O. and Hozbor, N.M. (2011) Feeding habits and habitat selectivity of the shortnose guitarfish, Zapteryx brevirostris (Chondrichthyes, Rhinobatidae), off north Argentina and Uruguay. Marine and Biological Research 7, 365377.CrossRefGoogle Scholar
Barausse, A., Baremore, I.E., Murie, D.J. and Carlson, J.K. (2010) Seasonal and size-related differences in diet of the Atlantic angel shark Squatina dumeril in the northeastern Gulf of Mexico. Aquatic Biology 8, 125136.Google Scholar
Bornatowski, H., Abilhoa, V. and Charvet-Almeida, P. (2009) Elasmobranchs of the Paraná Coast, southern Brazil, south-western Atlantic. Marine Biodiversity Records 2, e158. doi: http://dx.doi.org/10.1017/S1755267209990868.CrossRefGoogle Scholar
Bornatowski, H., Robert, M.C. and Costa, L. (2010) Feeding of guitarfish Rhinobatos percellens (Walbaum, 1972) (Elasmobranchii, Rhinobatidae), the target of artisanal fishery in southern Brazil. Brazilian Journal of Oceanography 58, 4552.CrossRefGoogle Scholar
Bornatowski, H., Heithaus, M.R., Abilhoa, V. and Corrêa, M.F.M. (2012) Feeding of the Brazilian sharpnose shark Rhizoprionodon lalandii (Müller & Henle, 1839) from southern Brazil. Journal of Applied Ichthyology 28, 623627.CrossRefGoogle Scholar
Braga, R.R., Bornatowski, H. and Vitule, J.R.S. (2012) Feeding ecology of fishes: an overview of worldwide publications. Reviews in Fish Biology and Fisheries 22, 915929.CrossRefGoogle Scholar
Bornatowski, H., Navia, A.F., Braga, R.R., Abilhoa, V. and Corrêa, M.F.M. (2014) Ecological importance of sharks and rays in a structural foodweb analysis in southern Brazil. ICES Journal of Marine Science. doi: 10.1093/icesjms/fsu025.CrossRefGoogle Scholar
Brickle, P., Laptikhovsky, V.V., Pompert, J. and Bishop, A. (2003) Ontogenetic changes in the feeding habits and dietary overlap between three abundant rajid species on the Falkland Islands' shelf. Journal of the Marine Biological Association of the United Kingdom 83, 11191125.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual. Plymouth: PRIMER-E.Google Scholar
Collins, A.B., Heupel, M.R. and Motta, P.J. (2007) Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. Journal of Fish Biology 70, 120.Google Scholar
Colwell, R.K. (2005) EstimateS version 7.5: Statistical estimation of species richness and shared species from samples. Available from: http://purl.oclc.org/estimates (accessed 7 April 2014).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, 726738.CrossRefGoogle Scholar
Cortés, E. (1999) Standardized diet composition and trophic levels of sharks. ICES Journal of Marine Science 56, 707717.CrossRefGoogle Scholar
Costa, L. and Chaves, P.T.C. (2006) Elasmobrânquios capturados pela pesca artesanal na costa sul do Paraná e norte de Santa Catarina, Brasil. Biota Neotropica 6, available at: http://www.biotaneotropica.org.br/v6n3/pt/abstract?article+bn02706032006 (accessed 7 April 2014).CrossRefGoogle Scholar
Dean, M.N., Bizzarro, J.J. and Summers, A.P. (2007) The evolution of cranial design, diet, and feeding mechanisms in batoid fishes. Integrative and Comparative Biology 47, 7081.CrossRefGoogle ScholarPubMed
Ebert, D.A. and Bizzarro, J.J. (2007) Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental Biology of Fishes 80, 221237.CrossRefGoogle Scholar
Ellis, J.R., Pawson, M.G. and Shackley, S.E. (1996) The comparative feeding ecology of six species of shark and four species of ray (Elasmobranchii) in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 76, 89106.CrossRefGoogle Scholar
Ferretti, F., Worm, B., Britten, G.L., Heithaus, M.R. and Lotze, H.K. (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13, 10551071.CrossRefGoogle ScholarPubMed
Ferry, L.A. and Caillet, G.M. (1996) Sample size and data analysis: are we characterizing and comparing diet properly? In MacKinlay, D. and Shearer, K. (eds) Feeding ecology and nutrition in fish. Proceedings of the Symposium on the Feeding Ecology and Nutrition in Fish. International Congress on the Biology of Fishes. San Francisco, CA: American Fisheries Society, pp. 71–80.Google Scholar
Goiten, R., Torres, F.S. and Signorini, C.E. (1998) Morphological aspects related to feeding of two marine skates Narcine brasiliensis Olfers and Rhinobatos horkelli Müller & Henle. Acta Scientiarum 20, 165169.Google Scholar
Gotelli, N.J. and Graves, G.R. (1996) Null models in ecology. Washington, DC: Smithsonian Institution Press.Google Scholar
Gotelli, N.J. and Entsminger, G.L. (2005) EcoSim: Null models software for ecology, version 7.0. Burlington: Kesey-Bear, Acquired Intelligence.Google Scholar
Heithaus, M.R. (2004) Predator–prey interactions. In Carrier, J.C., Musick, J.A. and Heithaus, M.R. (eds) Biology of sharks and their relatives. Boca Raton, FL: CRC Press, pp. 487521.CrossRefGoogle Scholar
Heithaus, M.R., Frid, A., Wirsing, A.J. and Worm, B. (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology and Evolution 23, 202210.CrossRefGoogle ScholarPubMed
Heithaus, M.R., Frid, A., Vaudo, J.J., Worm, B. and Wirsing, A.J. (2010) Unraveling the ecological importance of elasmobranchs. In Carrier, J.C., Musick, J.A. and Heithaus, M.R. (eds) Biology of sharks and their relatives. Boca Raton, FL: CRC Press, pp. 611637.CrossRefGoogle Scholar
Hyslop, E.J. (1980) Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17, 411429.CrossRefGoogle Scholar
Kraeuter, J.N. and Castagna, M. (1980) Effects of large predators on the field culture of the hard clam Mercenaria mercenaria. Fisheries Bulletin 78, 538540.Google Scholar
Krebs, C.J. (1999) Ecological methodology. Menlo Park, CA: Addison Wesley.Google Scholar
Mabragaña, E. and Gilberto, D.A. (2007) Feeding ecology and abundance of two sympatric skates, the shortfin sand skate Psammobatis normani McEachran and the smallthorn sand skate P. rudis Gunther (Chondrichthyes, Rajidae), in the southwest Atlantic. ICES Journal of Marine Science 64, 10171027.CrossRefGoogle Scholar
Magurran, A.E. (2004) Measuring biological diversity. Oxford: Blackwell Publishing.Google Scholar
Marion, C., Vaske-Junior, T., Gadig, O.B.F. and Martins, I.A. (2011) Feeding habits of the shortnose guitarfish, Zapteryx brevirostris (Müller and Henle, 1841) (Elasmobranchii, Rhinobatidae) in southeastern Brazil. Brazilian Journal of Biology 71, 8389.CrossRefGoogle Scholar
Moyle, P.B. and Cech, J.J. Jr (1982) Fishes: an introduction to ichthyology. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
Muto, E.Y., Soares, L.S.H. and Goitein, R. (2001) Food resource utilization of the skates Rioraja agassizii (Müller & Henle, 1841) and Psammobatis extenta (Garman, 1913) on the continental Shelf off ubatuba, south-eastern Brazil. Revista Brasileira de Biologia 61, 217238.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Myers, R.A. and Worm, B. (2003) Rapid worldwide depletion of predatory fish communities. Nature 423, 280283.CrossRefGoogle ScholarPubMed
Navarro-González, J.A., Bohórquez-Herrera, J., Navia, A.F. and Cruz-Escalona, V.H. (2012) Composición trófica de batoideos en la plataforma continental frente a Nayarit y Sinaloa, México. Ciencias Marinas 38, 347362.CrossRefGoogle Scholar
Navia, A.F., Mejía-Falla, P.A. and Giraldo, A. (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology 7, 8.CrossRefGoogle ScholarPubMed
Navia, A.F., Cortés, E. and Mejía-Falla, P.A. (2010) Topological analysis of the ecological importance of elasmobranch fishes: a food web study on the Gulf of Tortugas, Colombia. Ecological Modelling 221, 29182926.CrossRefGoogle Scholar
Navia, A.F., Torres, A., Mejía-Falla, P.A. and Giraldo, A. (2011) Sexual, ontogenetic, temporal and spatial effects on the diet of Urotrygon rogersi (Elasmobranchii: Myliobatiformes). Journal of Fish Biology 78, 12131224.CrossRefGoogle ScholarPubMed
Orth, R.J. (1975) Destruction of eelgrass, Zostera marina, by the cownose ray, Rhinoptera bonasus, in the Chesapeake Bay. Chesapeake Sciences 16, 205208.CrossRefGoogle Scholar
O'Shea, O.R., Thums, M., van Keulen, M., Kempster, R.M. and Meekan, M.G. (2013) Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82, 18051820.CrossRefGoogle ScholarPubMed
Paine, R.T. (1969) A note on trophic complexity and community stability. American Naturalist 103, 9193.CrossRefGoogle Scholar
Peterson, C.H., Fodrie, F.J., Summerson, H.C. and Powers, S.P. (2001) Site-specific and density-dependent extinction of prey by schooling rays: generation of a population sink in top-quality habitat for bay scallops. Oecologia 129, 349356.CrossRefGoogle ScholarPubMed
Pinkas, L., Oliphant, M.S. and Iverson, I.L.K. (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. California Fish and Game, Fisheries Bulletin 152, 84 p.Google Scholar
Power, M.E. (1997) Estimating impacts of a dominant detritivore in a neotropical stream. Trends in Ecology and Evolution 12, 4748.CrossRefGoogle Scholar
Power, M.E., Tilman, D., Estes, J.A., Menge, B.A., Bond, W.J., Mills, L.S., Daily, G., Castilla, J.C., Lubchenco, J. and Paine, R.T. (1996) Challenges in the quest for keystones. BioScience 46, 609620.CrossRefGoogle Scholar
Ritchie, E.G. and Johnson, C.N. (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters 12, 982998.CrossRefGoogle ScholarPubMed
Schoener, T.W. (1974) Resource partitioning in ecological communities. Science 185, 2739.CrossRefGoogle ScholarPubMed
Smith, J.W. and Merriner, J.V. (1985) Food habits and feeding behaviour of the cownose ray, Rhinoptera bonasus, in lower Chesapeake Bay. Estuaries 8, 305310.CrossRefGoogle Scholar
Smith, J.W. and Merriner, J.V. (1987) Age and growth, movements and distribution of the cownose ray, Rhinoptera bonasus, in Chesapeake Bay. Estuaries 10, 153164.CrossRefGoogle Scholar
Soares, L.S.H., Rossi-Wongtschowski, C.L.D.B., Álvares, L.M.C., Muto, E.Y. and Gasalla, M.L.A. (1992) Grupos tróficos de peixes demersais da plataforma continental interna de Ubatuba, Brasil. I: Chondrichthyes. Boletim do Instituto Oceanográfico 40, 7985.CrossRefGoogle Scholar
Summers, A.P. (2000) Stiffening the stingray skeleton—an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). Journal of Morphology 243, 113126.3.0.CO;2-A>CrossRefGoogle Scholar
Treloar, M.A., Laurenson, LJ.B. and Stevens, J.D. (2007) Dietary comparisons of six skate species (Rajidae) in south-eastern Australian waters. Environmental Biology of Fishes 80, 181196.CrossRefGoogle Scholar
Valls, M., Quetglas, A., Ordines, F. and Moranta, J. (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Scientia Marina 75, 633639.CrossRefGoogle Scholar
Vaudo, J.J. and Heithaus, M.R. (2009) Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia. Marine Biology 156, 25792590.CrossRefGoogle Scholar
Vaudo, J.J. and Heithaus, M.R. (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425, 247 260.CrossRefGoogle Scholar
Vooren, C.M. and Klippel, S. (2005) Ações para a conservação de tubarões e raias no sul do Brasil. Igaré, Porto Alegre, 262 pp.Google Scholar
Wilga, C.D. and Motta, P.J. (1998) Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: modulation of kinematic and motor activity. Journal of Experimental Biology 201, 31673184.CrossRefGoogle ScholarPubMed
Yick, J.L., Barnett, A. and Tracey, S.R. (2011) Niche overlap and trophic resource partitioning of two sympatric batoids co-inhabiting an estuarine system in southeast Australia. Journal of Applied Ichthyology 27, 12721277.CrossRefGoogle Scholar
Zares, T.M. and Rand, A.S. (1971) Competition in tropical stream fishes: support for the competitive exclusion principle. Ecology 52, 336342.Google Scholar