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Comparative study of feeding behaviour of five Mugilidae species juveniles from two estuarine systems in the North Aegean Sea

Published online by Cambridge University Press:  13 September 2016

Ioanna Salvarina*
Affiliation:
NAGREF, Fisheries Research Institute, Nea Peramos, Kavala 64007, Greece Limnological Institute, University of Konstanz, Mainaustrasse 252, 78464, Konstanz, Germany
Emmanuil Koutrakis
Affiliation:
NAGREF, Fisheries Research Institute, Nea Peramos, Kavala 64007, Greece
Ioannis Leonardos
Affiliation:
Biological Applications & Technology Department, University of Ioannina, Ioannina 45110, Greece
*
Correspondence should be addressed to: I. Salvarina Limnological Institute, University of Konstanz, Mainaustr. 252, 78464, Konstanz, Germany email: isalvarina@gmail.com

Abstract

Food is an important factor for the survival of juvenile fish. Knowledge of the diet of co-existing species helps clarify their relationships with each other. A number of Mugilidae species are known to co-exist in estuarine systems, raising the question of whether they compete for food resources. The feeding behaviours of five juvenile Mugilidae species were studied in the estuaries of Strymonikos (North Aegean Sea) using stomach content analysis. It was found that the species Chelon labrosus, Liza saliens and Mugil cephalus presented high feeding activity during summer and autumn and L. ramada and L. aurata during winter and spring. The diet overlap between the species was generally moderate to low and the pair L. saliensM. cephalus exhibited the highest overlap in Richios estuarine system. The species do not appear to compete for common resources, probably because there is not always a spatiotemporal overlap, enough food is available or they exploit different resources. Four out of the five species exhibited similar patterns of feeding strategies with varying levels of specialization at an individual level and a rather generalized pattern at the population level. This more generalized feeding strategy may permit them to co-exist. Only M. cephalus showed a more specialized feeding behaviour, with a strong preference for microalgae. The absence of a general pattern for the trophic levels according to seasons, sizes or locations, also imply the opportunistic character of the species. Both season and fish size influenced the variation in the diet composition.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Albertini-Berhaut, J. (1973) Biologie des stades juvéniles de Télostéens Mugilidae Mugil auratus Risso, 1810, Mugil capito Cuvier, 1829 et Mugil saliens Risso, 1810. I – Régime alimentaire. Aquaculture 2, 251266.CrossRefGoogle Scholar
Albertini-Berhaut, J. (1975) Allométrie chimique et changement de régime alimentaire chez Mugil capito (Téléostéen, Mugilidae). Comptes rendus de l'Académie des Sciences, Paris 280, 297300.Google Scholar
Albertini-Berhaut, J. (1978) Croissance lineaire et ponderale de M. auratus dans le Golfe de Marseille a celle de M. capito . Cybium, 3e serie 4, 5160.Google Scholar
Almeida, P.R. (2003) Feeding ecology of Liza ramada (Risso, 1810) (Pisces, Mugilidae) in a south-western estuary of Portugal. Estuarine, Coastal and Shelf Science 57, 313323.Google Scholar
Almeida, P.R., Moreira, F., Costa, J.L., Assis, C.A. and Costa, M.J. (1993) The feeding strategies of Liza ramada (Risso, 1826) in fresh and brackish water in the River Tagus, Portugal. Journal of Fish Biology 42, 95107.Google Scholar
Amundsen, P.A., Gabler, H.M. and 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, 607614.Google Scholar
Araújo, M.S., Bolnick, D.I., Machado, G., Giaretta, A.A. and dos Reis, S.F. (2007) Using δ 13C stable isotopes to quantify individual-level diet variation. Oecologia 152, 643654.CrossRefGoogle Scholar
Bartulović, V., Glamuzina, B., Lučić, D., Conides, A., Jasprica, N. and Dulčić, J. (2007) Recruitment and food composition of juvenile thin-lipped grey mullet, Liza ramada (Risso, 1826), in the Neretva River estuary (Eastern Adriatic, Croatia). Acta Adriatica 48, 2537.Google Scholar
Bartulović, V., Matić-Skoko, S., Lučić, D., Conides, A., Jasprica, N., Joksimović, A., Dulčić, J. and Glamuzina, B. (2009) Recruitment and feeding of juvenile leaping grey mullet, Liza saliens (Risso, 1810) in the Neretva River estuary (south-eastern Adriatic, Croatia). Acta Adriatica 50, 91104.Google Scholar
Bounton, W.R. and Zion, H.H. (1981) Importance of juvenile striped bass food habits in the Potomac Estuary. Transactions of the American Fisheries Society 110, 5663.Google Scholar
Bowen, S.H. (1983) Detritivory in neotropical fish communities. Environmental Biology of Fishes 9, 137144.CrossRefGoogle Scholar
Brusle, J. (1981) Food and feeding in grey mullet. In Oren, O.H. (ed.) Aquaculture of grey mullets. Cambridge: Cambridge University, Press p. 507.Google Scholar
Budge, S.M., Iverson, S.J. and Koopman, H.N. (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Marine Mammal Science 22, 759801.Google Scholar
Cabral, H.N. (2000) Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within the nursery areas of the Tagus estuary, Portugal. Journal of Fish Biology 57, 15501562.Google Scholar
Cambrony, M. (1984) Identification et périodicité du recrutement des juveniles de Mugilidae dans les étangs littoraux du Languedoc-Roussillon. Vie et Milieu 34, 221227.Google Scholar
Campo, D., Mostarda, E., Castriota, L., Scarabello, M.P. and Andaloro, F. (2006) Feeding habits of the Atlantic bonito, Sarda sarda (Bloch, 1793) in the southern Tyrrhenian sea. Fisheries Research 81, 169175.Google Scholar
Cardona, L. (1999) Seasonal changes in the food quality, diel feeding rhythm and growth rate of juvenile leaping grey mullet Liza saliens . Aquatic Living Resources 12, 263270.Google Scholar
Cardona, L. (2001) Non-competitive coexistence between Mediterranean grey mullet: evidence from seasonal changes in food availability, niche breadth and trophic overlap. Journal of Fish Biology 59, 729744.Google Scholar
Cardona, L. (2006) Habitat selection by grey mullets (Osteichthyes: Mugilidae) in Mediterranean estuaries: the role of salinity. Scientia Marina 70, 443455.CrossRefGoogle Scholar
Cardona, L. (2016) Food and feeding of Mugilidae. In Crosetti, D. and Blaber, S. (eds) Biology, ecology and culture of grey mullet (Mugilidae). Boca Raton, FL: CRC Press, pp. 165195.Google Scholar
Cardona, L., Hereu, B. and Torras, X. (2008) Juvenile bottlenecks and salinity shape grey mullet assemblages in Mediterranean estuaries. Estuarine, Coastal and Shelf Science 77, 623632.Google Scholar
Castriota, L., Scarabello, M.P., Finoia, M.G., Sinopoli, M. and Andaloro, F. (2005) Food and feeding habits of pearly razorfish, Xyrichtys novacula (Linnaeus, 1758), in the southern Tyrrhenian Sea: variation by sex and size. Environmental Biology of Fishes 72, 123133.CrossRefGoogle Scholar
Christensen, V. and Pauly, D. (1992) ECOPATH-II: a software for balancing steady-state ecosystem models and calculating network characteristics. Ecological Modelling 61, 169185.Google Scholar
Clarke, K.R. and Gorley, R.N. (2001) PRIMER v5: user manual/tutorial. Plymouth: PRIMER-E, 91 pp.Google Scholar
Daly, E.A., Brodeur, R.D. and Weitkamp, L.A. (2009) Ontogenetic shifts in diets of juvenile and subadult Coho and Chinook Salmon in coastal marine waters: important for marine survival? Transactions of the American Fisheries Society 138, 14201438.Google Scholar
De Silva, S.S. (1980) Biology of juvenile grey mullet: a short review. Aquaculture 19, 2136.Google Scholar
Digby, P.G.N. and Kempton, R.A. (1987) Multivariate analysis of ecological communities. London: Chapman and Hall, 206 pp.Google Scholar
Eggold, B.T. and Motta, P.J. (1992) Ontogenetic dietary shifts and morphological correlates in striped mullet, Mugil cephalus . Environmental Biology of Fishes 34, 139158.Google Scholar
El-Ghobashy, A.E. (2009) Natural fish fry food of seven commercial species in the Egyptian Mediterranean Water. World Applied Sciences Journal 7, 320331.Google Scholar
Froese, R. and Pauly, D. (eds) (2010) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org, version (05/2010).Google Scholar
Gabler, H.-M. and Amundsen, P.-A. (2010) Feeding strategies, resource utilisation and potential mechanisms for competitive coexistence of Atlantic salmon and alpine bullhead in a sub-Arctic river. Aquatic Ecology 44, 325336.Google Scholar
Gisbert, E., Cardona, L. and Castelló, F. (1996) Resource partitioning among planktivorous fish larvae and fry in a Mediterranean coastal lagoon. Estuarine, Coastal and Shelf Science 43, 723735.Google Scholar
Gisbert, E., Cardona, L. and Castelló Orvay, F. (1995) Alimentación de los alevines de mugílidos en el delta del Ebro. Miscellania Zoologica 18, 145151.Google Scholar
Hammerschlag, N., Ovando, D. and Serafy, J.E. (2010) Seasonal diet and feeding habits of juvenile fishes foraging along a subtropical marine ecotone. Aquatic Biology 9, 279290.Google Scholar
Herder, F. and Freyhof, J. (2006) Resource partitioning in a tropical stream fish assemblage. Journal of Fish Biology 69, 571589.Google Scholar
Hureau, J.C. (1966) Biologie comparée de quelques poissons antartique (Nototheniidae). Bulletin of the Institute of Oceanography of Monaco 68, 1244.Google Scholar
Hyslop, E.J. (1980) Stomach content analysis – a review of methods and their application. Journal of Fish Biology 17, 411429.Google Scholar
Ingram, B. and De Silva, S. (2007) Diet composition and preference of juvenile Murray cod, Trout cod and Macquarie perch (Percichthyidae) reared in fertilised earthen ponds. Aquaculture 271, 260270.Google Scholar
Jardas, I., Santic, M. and Pallaoro, A. (2004) Diet composition and feeding intensity of horse mackerel, Trachurus trachurus (Osteichthyes: Carangidae) in the eastern Adriatic. Marine Biology 144, 10511056.Google Scholar
Kasimoğlu, C. and Yilmaz, F. (2012) Feeding habits of the thin-lipped grey mullet, Liza ramada, in Gökova Bay in the southern Aegean Sea. Zoology in the Middle East 56, 5561.Google Scholar
Katselis, G., Hotos, G., Minos, G. and Vidalis, K. (2006) Phenotypic affinities on fry of four Mediterranean grey mullet species. Turkish Journal of Fisheries and Aquatic Sciences 6, 4955.Google Scholar
Katselis, G., Koukou, K., Dimitriou, E. and Koutsikopoulos, C. (2007) Short-term seaward fish migration in the Messolonghi-Etoliko lagoons (Western Greek coast) in relation to climatic variables and the lunar cycle. Estuarine, Coastal and Shelf Science 73, 571582.Google Scholar
Koussoroplis, A.-M., Bec, A., Perga, M.-E., Koutrakis, E., Desvilettes, C. and Bourdier, G. (2010) Nutritional importance of minor dietary sources for leaping grey mullet Liza saliens (Mugilidae) during settlement: insights from fatty acid δ13C analysis. Marine Ecology Progress Series 404, 207217.Google Scholar
Koutrakis, E.T. (2004) Temporal occurrence and size distribution of grey mullet juveniles (Pisces, Mugilidae). Journal of Applied Ichthyology 20, 7678.Google Scholar
Koutrakis, E.T. (2011) Reproductive biology of two grey mullet species (Actinopterygii: Mugiliformes: Mugilidae) in a northern Aegean Sea estuarine system. Acta Ichthyologica et Piscatoria 41, 3746.Google Scholar
Koutrakis, E. (2016) Biology and ecology of fry and juveniles of Mugilidae. In Crosetti, D. and Blaber, S. (eds) Biology, ecology and culture of grey mullet (Mugilidae). Boca Raton, FL: CRC Press, pp. 264292.Google Scholar
Koutrakis, E.T., Kallianiotis, A. and Tsikliras, A. (2004) Temporal patterns of larval fish distribution and abundance in a coastal area of Northern Greece. Scientia Marina 68, 585595.Google Scholar
Koutrakis, E.T., Kokkinakis, A.K., Eleftheriadis, A.E. and Argiropoulou, M.D. (2000) Seasonal changes in distribution and abundance of the fish fauna in the two estuarine systems of Strymonikos gulf (Macedonia, Greece). Belgian Journal of Zoology 130, 4148.Google Scholar
Koutrakis, E.T., Sinis, A.I. and Economidis, P.S. (1994) Seasonal occurrence, abundance and size distribution of grey mullet fry (Pisces, Mugilidae) in the Porto-Lagos lagoon and Lake Vistonis (Aegean Sea, Greece). Israeli Journal of Aquaculture – Bamidgeh 46, 182196.Google Scholar
Lebedev, N.V. (1946) Elementary populations of fish. Zoologicheskii Zhurnal 25, 121135. [In Russian]Google Scholar
Lebreton, B., Richard, P., Guillou, G. and Blanchard, G.F. (2013) Trophic shift in young-of-the-year Mugilidae during salt-marsh colonization. Journal of Fish Biology 82, 12971307.Google Scholar
Lebreton, B., Richard, P., Parlier, E.P., Guillou, G. and Blanchard, G.F. (2011) Trophic ecology of mullets during their spring migration in a European saltmarsh: a stable isotope study. Estuarine, Coastal and Shelf Science 91, 502510.Google Scholar
Pauly, D., Froese, R., Sa-a, P., Palomares, M.L., Christensen, V. and Rius, J. (2000) TrophLab manual. Manila: ICLARM.Google Scholar
Pauly, D., Trites, A., Capuli, E. and Christensen, V. (1998) Diet composition and trophic levels of marine mammals. ICES Journal of Marine Science 55, 467481.CrossRefGoogle Scholar
R Development Core Team (2012) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/.Google Scholar
Romo, S., Fernández, F., Ouahid, Y. and Barón-Sola, A. (2012) Assessment of microcystins in lake water and fish (Mugilidae, Liza sp.) in the largest Spanish coastal lake. Environmental Monitoring and Assessment 184, 939949.Google Scholar
Ross, S.T. (1986) Resource partitioning in fish assemblages: a review of field studies. Copeia 2, 352388.Google Scholar
RStudio Team (2015) RStudio: integrated development for R. Boston, MA: RStudio, Inc. Available at http://www.rstudio.com/.Google Scholar
Schoener, T.W. (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51, 408418.Google Scholar
Schoener, T.W. (1971) Theory of feeding strategies. Annual Review of Ecology and Systematics 2, 369404.CrossRefGoogle Scholar
Stamatis, N., Ioannidou, D. and Koutrakis, E. (2001) Monitoring of key eutrophication parameters at three inshore stations of Strymonikos Gulf, north Aegean Sea. Fresenius Environmental Bulletin 10, 706710.Google Scholar
Stergiou, K.I. and Karpouzi, V.S. (2002) Feeding habits and trophic levels of Mediterranean fish. Reviews in Fish Biology and Fisheries 11, 217254.Google Scholar
Vassilopoulou, V. (2006) Dietary habits of the deep-sea flatfish Lepidorhombus boscii in north-eastern Mediterranean waters. Journal of Fish Biology 69, 12011220.Google Scholar
Verdiell-Cubedo, D., Egea-Serrano, A., Oliva-Paterna, F.J. and Torralva, M. (2007a) Biología trófica de los juveniles del género Liza (Pisces: Mugilidae) en la laguna costera del Mar Menor (SE Península Ibérica). Limnetica 26, 6773.Google Scholar
Verdiell-Cubedo, D., Oliva-Paterna, F.J. and Torralva, M. (2007b) The effects of competitors on fitness of marbled goby Pomatoschistus marmoratus (Pisces, Gobiidae) in the Mar Menor coastal lagoon (SE Iberian Peninsula). Italian Journal of Zoology 74, 69177.Google Scholar
Vinagre, C., Salgado, J.P., Mendonça, V., Cabral, H. and Costa, M.J. (2012) Isotopes reveal fluctuation in trophic levels of estuarine organisms, in space and time. Journal of Sea Research 72, 4959.Google Scholar
Wallace, R.K. (1981) An assessment of diet-overlap indexes. Transactions of the American Fisheries Society 110, 7276.Google Scholar
Walters, C., Christensen, V. and Pauly, D. (1997) Structuring dynamic models of exploited ecosystems from trophic mass-balance assessments. Reviews in Fish Biology and Fisheries 7, 139172.Google Scholar
Williams, M.D. and Williams, W.D. (1991) Salinity tolerances of four species of fish from the Murray-Darling river system. Hydrobiologia 210, 145160.Google Scholar