On the methodology of feeding ecology in fish

Open access

Abstract

Feeding ecology explains predator’s preference to some preys over others in their habitat and their competitions thereof. The subject, as a functional and applied biology, is highly neglected, and in case of fish, a uniform and consistent methodology is absent. The currently practiced methods are largely centred on mathematical indices and highly erroneous because of non-uniform outcomes. Therefore, it requires a relook into the subject to elucidate functional contributions and to make it more comparable and comprehensive science. In this article, approachable methodological strategies have been forwarded in three hierarchical steps, namely, food occurrence, feeding biology and interpretative ecology. All these steps involve wide ranges of techniques, within the scope of ecology but not limited to, and traverse from narrative to functional evolutionary ecology. The first step is an assumption-observation practice to assess food of fish, followed by feeding biology that links morphological, histological, cytological, bacteriological or enzymological correlations to preferred food in the environment. Interpretative ecology is the higher level of analysis in which the outcomes are tested and discussed against evolutionary theories. A description of possible pedagogics on the methods of feeding ecological studies has also been forwarded.

Adams, M.A., Johnsen, P.B. & Zhou, H.Q. (1988) Chemical enhancement of feeding for the herbivorous fish Tilapia zilli. Aquaculture, 72, 95-107.

Albo-Puigserver, M., Navarro, J., Coll, M., Aguzzi, J., Cardona, L. & Sáez-Liante, R. (2015) Feeding ecology and trophic position of three sympatric demersal chondrichthyans in the northwestern Mediterranean. Marine Ecological progressive Series, 524, 255-268.

Amundsen, P.A., Gabler, H.M. & Staldvik, F.J. (1996) A new approach to graphical analysis of feeding strategy from stomach contents data modification of the Costello (1990) method. Journal of Fish Biology, 48, 607-614.

Anastasopoulou, A., Mytilineou, C., Lefkaditou, E., Kavadas, S., Bekas, P., Smith, C.J., Papadopoulou, K.N. & Christides, G. (2013) The diet and feeding ecology of Conger conger (L. 1758) in the deep waters of the Eastern Ionian Sea. Mediterranean Marine Science, 14(2), 365-368.

Arai, T., Amalina, R. & Bachok, Z. (2015) Diverse feeding ecology and habitat use in coral reef fishes in the Malaysian South China Sea, as revealed by liver fatty acid composition. Oceanological and Hydrobiological Studies, 44(1), 120-126.

Begon, M., Townsend, C.R. & Harper, J.L. (2006) Ecology: From Individuals to Ecosystems, 4th edn. Blackwell Publication, Malden, MA.

Baker, R., Buckland, A. & Sheaves, M. (2014) Fish gut content analysis: robust measures of diet composition analysis. Fish and Fisheries, 15, 170-177.

Behrens, M.D. & Lafferty, K.D. (2007) Temperature and diet effects on omnivorous fish performance: Implications for the latitudinal diversity gradient in herbivorous fishes. Canadian Journal of Fisheries and Aquatic Sciences, 64(6), 867-873.

Boglione, C., Gigantic, M., Selmo, C. & Cataudella, S. (2003) Morphoecology in larval fin-fish: a new candidate species for aquaculture, Diplodus puntazzo (Sparidae). Aquaculture International, 11, 17-41.

Bohórquez-Herrera, J., Cruz-Escalona, V.H., Adams, D.C. & Peterson, M.S. (2015) Feeding ecomorphology of seven demersal marine fish species in the Mexican Pacific Ocean. Environmental Biology of Fishes, 98, 1459-1473.

Bolnick, D.I., Snowberg, L.K., Hirsch, P.E., Lauber, C.L., Knight, R., Caporaso, J.G. & Svanbäck, R. (2014) Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (Threespine stckileback and Eurasian perch). Ecology Letters, 8, 979-987.

Cabana, G. & Rasmussen, J.B. (1994) Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Science of the United States of America, 93, 10844-10847.

Cailliet, G.M., Love, M.S. & Ebeling, A.W. (1996) Fishes: A Field and Laboratory Manual on their Structure, Identification and Natural History, Waveland, Long Grove.

Carreon-Martinez, L., Johnson, T.B., Ludsin, S.A. & Heath, D.D. (2011) Utilization of stomach content DNA to determine diet diversity in piscivorous fishes. Journal of Fish Biology 78(4), 1170-1182.

Carss, D.N. (1995) Foraging behavior and feeding ecology of the otter Lutra lutra: a selective review. Hystrix, 7, 179-194.

Chervova, L.S. & Lapshin, D.N. (2005) The threshold sensitivity of external chemoreceptor in carp Cyprinus carpio to amino acids and classical gustatory substances. Journal of Ichthyology, 45, S307-S314.

Chesson, J. (1978) Measuring preference in selective predation. Ecology, 59, 211-215.

Colwell, R.K. & Futuyma, D.J. (1971) On the measurement of niche breadth and overlap. Ecology, 52, 567-576.

Corse, E., Costedoat, C., Chappaz, R., Pech, N., Martin J.F. & Gills, A. (2010) A PCR-based method for diet analysis in freshwater organisms using 18S rDNA barcoding on faeces. Molecular Ecology Resources 10(1), 96-108.

Cortés, E., Papastamatiou, Y.P., Carlson, J., Ferry, L.A. & Wetherbee, B.M. (2008) An overview of the feeding ecology and physiology of elasmobranch fishes. In: Feeding and digestive functions of fishes. (eds J.E.P. Cyrino, D.P. Bureau, B.G. Kapour) Science Publishers, Enfield, New Hampshire, 575pp.

Costello, M.J. (1990) Predator feeding strategy and prey importance: a new graphical analysis. Journal of Fish Biology, 36, 261-263.

Cresson, P., Ruitton, S., Ourgaud, M. & Harmelin-Vivien, M. (2014) Contrasting perception of fish trophic level from stomach content and stable isotope analysis: A Mediterranean artificial reef experience. Journal of Experimental Marine Biology and Ecology, 452, 54-62.

Cummis, K.W. & Klug, M.J. (1979) Feeding ecology of stream invertebrates. Annual Review of Ecology, Evolution, and Systematics, 10, 147-172.

Dantas, D.V., Barletta, M. & Costa, M.F. (2015) Feeding ecology and seasonal diet overlap between Stellifer brasiliensis and Stellifer stellifer in a tropical estuarine ecocline. Journal of Fish Biology, 86, 707-733.

Døving, K.B., Sandvig, K. & Kasumyan, A. (2009) Ligand–specific induction of endocytosis in taste receptor cells. Journal of Experimental Biology, 212, 42-49.

Erzini, K., Goncalves, J.M.S., Bentes, L. & Lino, P.G. (1997) Fish mouth dimensions and size selectivity in a Portuguese longline fishery. Journal of Applied Ichthyology, 13, 41-44.

Ferry, L.A. & Cailliet, G.M. (1996) Sample size sufficiency and data analysis: Are we characterizing and comparing diet properly? In: Feeding ecology and nutrition in fish: proceedings of the symposium on the feeding ecology and nutrition in fish. (eds D. Mackinlay and K. Shearer) International Congress on the Biology of Fishes, San Fransisco, pp. 71-80.

Finger, T.E. (1997) Evolution of taste and solitary chemoreceptor cell system. Brain, Behavior and Evolution, 50, 234-243.

Franchini, P., Fruciano, C., Frickey, T., Jones, J.C. & Meyer, A. (2014) The gut microbial community of Midas Cichlid fish in repeatedly evolved limnetic-benthic species pairs. PLoS ONE, 9(7), e 103923. doi: 10.1371/journal.pone.0103923

Froese, R. & Pauly, D. (2016) FishBase, World Wide Web electronic publication. www.fishbase.org, version 01/2016. (accessed on 10th June 2016)

Gerking, S.D. (1994) Feeding Ecology of Fish. Academic Press, 525 B Street, San Diego, California.

Horn, H.S. (1966) Measurement of overlap in comparative ecological studies. The American Naturalist, 100, 419-424.

Horn, M.H., Gawlicka, A.K., German, D.P., Logothetis, E.A., Cavanagh, J.W. & Boyle, K.S. (2006) Structure and function of the stomachless digestive system in three related species of New World silverside fishes (Atherinopsidae) representing herbivory, omnivory, and carnivory. Marine Biology, 149, 1237-1245.

Hurlbert, S.H. (1978) The measurement of niche overlap and some relatives. Ecology, 59, 67-77.

Hyslop, E.J. (1980) Stomach contents analysis- a review of methods and their application. Journal of Fish Biology, 17, 411-429.

Ivlev, I.S. (1961) Experimental Ecology of the Feeding of Fishes. Yale University Press, New Haven, Connecticut, USA.

Jo, H., Gim. J.-A., Jeong, K.-S., Kim, H.-S. & Joo, G.-J. (2014) Application of DNA barcoding for identification of freshwater carnivorous fish diets: Is number of prey items dependent on size class for Micropterus salmoides? Ecology and Evolution 4(2), 219-229.

Jo, H., Ventura, M., Vidal, N., Gim, J.S., Buchaca, T., Barmuta, L.A., Jeppesen, E. & Joo, G.-J. (2015) Discovering hidden biodiversity: the use of complementary monitoring of fish diet based on DNA barcoding in freshwater ecosystems. Ecology and Evolution 6(1), 219-232.

Kamal, M.Y. (1967) Studies on the food and alimentary canal of the Indian Major Carps. II. Labeo rohita (Ham) and III. Cirrhinus mrigala (Ham). Indian Journal of Fisheries, 14, 24-47.

Kawakami, E. & Vazzoler, G. (1980) Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Boletim do Instituto Oceanografico, 29(2), 205-207.

Keppler, F.W., Lanes, L.E.K., Rolon, A.S., Stenert, C., Lehmann, P., Reichard, M. & Maltchik, L. (2015) The morphology-diet relationship and its role in the co-existence of two species of annual fishes. Ecology of Freshwater Fish, 24, 77-90.

King, R.A., Read, D.S., Traugott, M. & Symondson, O.C. (2008) Molecular analysis of predation: a review of best practices for DNA-based approaches. Molecular Ecology, 17, 947-963.

Kirino, M., Parnes, J., Hansen, A., Kiyohara, S. & Finger, T.E. (2014) Evolutionary origins of taste buds: phylogenetic analysis of purinergic neurotransmission in epithelial chemosensors. Open Biology, 3(3), 130015

Knutsen, G. & Tilseth, S. (1985) Growth, development and feeding success of Atlantic code larvae Gadus morhua related to egg size. Transactions of American Fisheries Society, 114, 507-511.

Luczkovich, J.J., Norton, S.F. & Gilmore, R.G. (1995) The influence of oral anatomy on prey selection during the ontogeny of two percoid fishes, Lagodon rhomboides and Centropomus undecimalis. Environmental Biology of Fish, 44, 79-95.

Lukoschek, V. & Mc Cormick, M.I. (2001) Ontogeny of diet changes in a tropical benthic carnivorous fish, Parupeneus barberinus (Mullidae): relationship between foraging behaviour, habitat use, jaw size, and prey selection. Marine Biology, 138, 1099-1113.

MacArthur, R.H. & Levins, R. (1967) The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist, 101, 377-385.

Manly, B.F.J., Miller, P. & Cook, L.M. (1972) Analysis of a selective predation experiment. The American Naturalist, 106, 719-736.

Meyer, A.A. & Fanta, E. (1998) Morpho-functional study of Chemoreception structures of the Antarctic Fish Trematomus newnesi Boulenger, 1902 used for food detection and selection. Pesquisa Antártica Brasileira, 3, 49-63.

Mittelbach, G. & Persson, L. (1998) The ontogeny of piscivory and its ecological consequences. Canadian Journal of Fisheries and Aquatic Sciences, 55, 1454-1465.

Murray, D.C., Bunce, M., Cannell, B.L., Oliver, R., Houston, J., White, N.E., Barrero, R. A., Bellgard, M.I. & Haile, J. (2011) DNA-based faecal dietary analysis- a comparison of qPCR and high throughput sequencing approaches. PLoS One, 6(10), e25776.

Nandi, S. & Saikia, S.K. (2015) Size selective feeding on phytoplankton by two morpho-groups of the small freshwater fish Amblypharyngodon mola. Journal of Fish Biology, 87, 215-230.

Navia, A.F., Mejía-Fall, M.A. & Giraldo, A. (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology, 7(1)

Northcote, T.G. (1954) Observations on the comparative ecology of two species of fish, Cottus asper and Cottus rhotheus, in British Columbia. Copeia, 1954, 25-28.

Northcote, T.G. & Hammar, J. (2006) Feeding ecology of Coregonus albula and Osmerus eperlanus in the limnetic waters of Lake Mälaren, Sweden. Boreal Environment Research, 11, 229-246.

Oike, H., Nagai, T. Furuyama, A., Okada, S., Aihara, Y., Ishimaru, Y., Marui, T., Matsumoto, I., Misaka, T. & Abe, K. (2007) Characterization of ligands for fish taste receptors. The Journal of Neuroscience, 27(21), 5584-5592.

Oscoz, J., Leunda, P.M., Miranda, R. & Escala, M.C. (2005) Diet of 0+ brown trout (Salmo trutta L., 1758) from the River Erro (Navarra, North Spain). Limnetica 24, 319-326.

Park, P.J., Aguirre, W.E., Spikes, D.A. & Myyazaki, J.M. (2013) Landmark-based geometric morphometrics- What fish shapes can tell us about fish evolution. Proceedings of Association of Biological Laboratory Education, 34, 361-371.

Pearre, S. jr. (1986) Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and size-efficient hypothesis. Marine Ecology and Progress Series, 27, 299-314.

Pelicice, F.M. & Agostinho, A.A. (2006) Feeding ecology of fishes associated with Egeria spp. patches in a tropical reservoir, Brazil. Ecology of Freshwater Fish, 15, 10-19.

Pelicice, F.M., Agostinho, A.A. & Thomaz, S.M. (2005) Fish assemblages associated with Egeria in a tropical reservoir: investigating the effects of plant biomass and diel period. Acta Oecologia, 27, 9-16.

Peterson, B.J. & Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18, 293-320.

Pianka, E.R. (1973) The structure of lizard communities. Annual Review of Ecology and Systematics, 4, 53-74.

Pinkas, L., Olipahnt, M.S. & Iverson, I.L.K. (1971) Food habits of albacore, Bluefin tuna, and Bonito in California waters. Fishery Bulletin, 152, 1-105.

Ponton, D. & Mṻller, R. (1990) Size of prey ingested by whitefish, Coregonus sp., larvae. Are Coregonus larvae with gape-limited predators? Journal of Fish Biology, 36, 67-72.

Pothoven, S.A. & Nalepa, T.F. (2006) Feeding ecology of Lake Whitefish in Lake Huron. Journal of Great Lakes Research, 32, 489-501.

Renkonen, O. (1938) Statisch-ökologische Untersuchungen über die terrestrische Käferwelt der finnischen Bruchmoore. Annals of Zoologici Societatis Zoolicæ-Botanicæ Fenniae, 6, 1-231.

Reutter, K. (1986) Chemoreceptor. In: Biology of the Integument (eds J. Bereiter-Hahn, A.G. Matoltsky, K.S. Ricjards), Vol. Vertebrates. Springer Verlag, Heidelberg. pp. 586-604.

Reutter, K., Breipohl, W. and Bijvank, G.J. (1974) Taste bud types in fishes. Cell and Tissue Research, 153, 151-165.

Ricklefs, R.E. & Lau, M. (1980) Bias and dispersion of overlap indices: results of some Monte Carlo simulations. Ecology, 61, 1019-1024.

Rønnestad, I., Yúfera, M., Ueberschär, B., Ribeiro, L., Sæle, Ø. & Boglione, C. (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Reviews in Aquaculture, 5, 559-598.

Roy, T., Mondal, S. & Ray, A.K. (2009) Phytase producing bacteria in the digestive tracts of some freshwater fish. Aquaculture Research, 40, 344-353.

Rybczynski, S.M., Walters, D.M., Fritz, K.M. & Johnson, B.R. (2008) Comparing trophic position of stream fishes using stable isotope and gut contents analysis. Ecology of Freshwater Fish, 17, 199-206.

Saikia, S.K. (2012) Proposal of a new and simple descriptive measure of diet breadth. Ecologia, 2(3), 85-92.

Saikia, S.K. & Das, .D.N. (2009) Feeding ecology of Common carp (Cyprinus carpio L.) in a rice-fish culture system of Apatani plateau (Arunachal Pradesh, India). Aquatic Ecology, 43, 559-568.

Saikia, S.K., Majumder, S., Nandi, S. & Saha, S.K. (2013) Feeding ecology of the freshwater fish Rohu Labeo rohita (Hamilton 1822): A case of intelligent feeding in a periphyton-based environment. Zoology and Ecology, 23(4), 266-274.

Sánchez-Herrnández, J. & Cobo, F. (2011) Summer food resource partitioning between four sympatric fish species in Central Spain (River Tormes). Folia Zoologica, 60 (3), 189-202.

Scharnweber, K., Watanabe, K., Syväranta, J., Wanke, T., Monaghan, M.T. & Mehner, T. (2013) Effects of predation pressure and resource use on morphological divergence in omnivorous prey fish. BMC Evolutionary Biology, 13, 132.

Schoener, T.W. (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49, 704-726.

Schoener, T.W. (1970) Non-synchronous spatial overlap of lizards in patchy habitat. Ecology, 51, 408-418.

Shiffman, D. S., Frazier, B.S., Kucklick, J.R., Brandes, J. & Sancho, G. (2014) Feeding ecology the Sandhar Shark in South Carolina Estuaries revealed through δ13C and δ15N stable isotope analysis. Marine and Coastal Fisheries: Dynamics, management and Ecosystem Sciences, 6, 156-169.

Smith, E.P. (1982) Niche breadth, Resource availability and inference. Ecology, 63, 1675-1681.

Smith, E.P. & Zaret, T.M. (1982) Bias in estimating niche overlap. Ecology, 63, 1248-1253.

Smyly, W.J.P. (1952) Observations of the food of fry of perch (Perca fluviatilis Linn.) in Windermere. Proceedings of Zoological Society of London, 122, 407-416.

Sousa, L.L., Raquel, X., Costa, V., Humphries, N.E., Trueman, C., Rosa, R., Sims, D.W. & Queiroz, N. (2016) DNA barcoding identifies a cosmopolitan diet in the ocean sunfish. Scientific Reports 6.

Sullam, K.E., Essinger, S.D., Lozupone, C.A., O’Connor, M.P., Rosen, G.L., Knight, R., Kilham, S.S. & Russell, J.A. (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta analysis. Molecular Ecology, 21(13), 3363-3378.

Taguchi, T., Miura, Y., Krueger, D. & Sugiura, S. (2014) Utilizing stomach content and faecal DNA analysis techniques to assess the feeding behaviour of largemouth bass Micropterus salmoides and bluegill Lepomis macrochirus. Journal of Fish Biology, 84, 1721-1288.

Tokeshi, M. (1991) Graphical analysis of predator feeding strategy and prey importance. Freshwater Forum, 1, 179-183.

Trauemper, H.A. & Lauer, T.E. (2005) Gape limitation and piscine prey size selection by yellow perch in the extreme southern area of Lake Michigan, with emphasis on two exotic prey items. Journal of Fish Biology, 66, 135-149.

Vander Zanden M.J. & Rasmussen, J. (2001) Variation in δ15N and δ153C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography, 46, 2061-2066.

Voss, R., Dickmann, M. & Schmidt, J.O. (2009) Feeding ecology of sprat (Sprattus sprattus L.) and sardine (Sardina pilchardus W.) larvae in the German Bight, North Sea. Oceanologia, 51(1), 117-138.

Wainwright, P.C. (1988) Morphology and Ecology: Functional basis of feeding constraints in Caribbean labrid fishes. Ecology, 69, 635-645.

Wainwright, P.C. & Richard, B.A. (1995) Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fish, 44, 97-113.

Wainwright, P.C. (1996) Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology, 77, 1336-1343.

Wells, R.J.D. & Rooker, J.R. (2009) Feeding ecology of pelagic fish larvae and juveniles is slope waters of the Gulf of Mexico. Journal of Fish Biology, 75, 1719-1732.

Whitear, M. (1971) Cell specialization and sensory function in fish epidermis. Journal of Zoology, 163, 237-264.

Wilkens, M.A., Wettring, B., Wagner, E., Wojtenek, W. & Russell, D. (2001) Prey detection in selective plankton feeding by the paddle fish: is the electric sense sufficient? Journal of Experimental Biology, 204, 1381-1389.

Windell, J.T. (1971) Food analysis and rate of digestion. In. Methods for assessment of fish production in fresh waters. 2nd ed. (ed. W.E. Ricker), Blackwell Scientific Publications, Oxford and Edinburgh, UK, pp. 215-226.

Wotton, R.J. (1998) Ecology of Teleost Fishes, Kluwer Academic Publisher, Dordrecht.

Xue, M. & Cui, Y. (2001) Effect of several feeding stimulants on diet preference by juvenile gibel carp (Carassius auratus gibelio), fed diets with or without partial replacement of fish meal by meat and bone meal. Aquaculture, 198, 281-292.

Yashpal, M., Kumari, U., Mittal, S. & Mittal, A.K. (2009) Morphological specialization of the buccal cavity in relation to the food and feeding habit of a carp Cirrhinus mrigala: a scanning electron microscopic investigation. Journal of Morphology, 270 (6), 714-728.

Yúfera, M. & Darias, M.J. (2007a) The onset of feeding in marine fish larvae. Aquaculture, 268, 53-63.

Yúfera, M. & Darias, M.J. (2007b). Changes in the gastrointestinal pH from larvae to adult in Senegal sole (Solea senegalensis). Aquaculture, 267, 94-99.

Journal Information

CiteScore 2018: 0.84

Source Normalized Impact per Paper (SNIP) 2018: 0.365

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 1022 721 49
PDF Downloads 681 543 36