Mediterranean juvenile white seabream rely on phytal fauna as primary food source in coastal nursery areas

Published: Mar 15, 2023
essential fish habitats coastal habitats nursery habitats fish settlement juvenile fish diet macroalgae harpacticoid copepods Diplodus sargus

Nursery areas are essential fish habitats due to their relevance in the survival of early stages of fish populations. They are also considered as of high priority in marine conservation strategies. Here, we investigated the diet of white seabream [Diplodus
sargus (Linnaeus, 1758)] settlers in six nursery areas located in the shallow waters of coves in Minorca Island (Balearic Islands, Spain). Our aim was to characterize the food sources at different stages of juvenile development and their site-related variability in order to discern the importance of trophic links in cove selection during settling. The gut contents of 101 juveniles captured at different coves, three to the north of the island (N), and three in the southern coast (S), revealed a marked preference for feeding on crustaceans and, in particular, on harpacticoid copepods (>90% of gut contents). Copepods represented the main food source (80 ±4.4%; mean ±S.E.) in younger seabream individuals (10 - 15 mm length). A higher diversity in prey items was observed in the larger size-classes (s2: 16 - 23 and S3: 24 - 30 mm, respectively), which incorporated other prey items such as amphipods, isopods, foraminiferans or ostracods. Diet composition did not vary between the two surveyed locations (North vs. South of the island), but it did show significant differences among the six coves (p<0.001). Comparison between cove sediment infaunal composition and gut contents revealed that predation on sediment communities was scarce. Instead, diet was typically of phytal origin. Our results highlight the importance of the algal component of shallow coastal areas as a foraging habitat. In particular, harpacticoid copepods were key for survival during early development phases. The potential use of harpacticoid copepods to track ontogenic shifts in habitat use by juvenile fish is discussed.

Article Details
  • Section
  • Research Article
Download data is not yet available.
Aarnio, K., Bonsdorff, E., Rosenback, N., 1996. Food and feeding habits of juvenile flounder, Platichthys flesus (L.), and turbot, Scophthalmus maximus L., in the Åland archipelago, northern Baltic Sea. Journal of Sea Research, 36, 311- 320.
Abrantes, K., Barnett, A., Baker, R., Sheaves, M., 2015. Habitat- specific food webs and trophic interactions supporting coastal-dependent fishery species: an Australian case study. Reviews in Fish Biology and Fisheries, 25, 337-363.
Afonso, P., Tempera, F., Menezes, G., 2008. Population structure and habitat preferences of red porgy (Pagrus pagrus) in the Azores, central north Atlantic. Fisheries Research, 93, 338-345.
Altin, A., Özen, Ö., Ayyildiz, H., Ayaz, A., 2015. Feeding habits and diet overlap of juveniles of 2 sparids, Diplodus puntazzo (Walbaum, 1792) and Diplodus vulgaris (Geoffrey Saint-Hilaire, 1817), from the North Aegean Sea of Turkey. Turkish Journal of Zoology, 39, 80-87.
Anderson, M.J., 2001. Permutation tests for univariate or multivariate analysis of variance and regression. Canadian Journal of Fisheries and Aquatic Sciences, 58, 626-639.
Anderson, M.J., Millar, R.B. 2004. Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. Journal of Experimental Marine Biology and Ecology, 305, 191-221. Anderson, M.J., Gorley, R. (Eds), 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth, UK.
Arroyo, N.L., Maldonado, M., Perez-Portela, R., Benito, J., 2004. Distribution patterns of meiofauna associated with a sublittoral Laminaria bed in the Cantabrian Sea (northeastern Atlantic). Marine Biology, 144, 231-242.
Arroyo, N.L., Maldonado, M., Walters, K., 2006. Within- and between-plant distribution of harpacticoid copepods in a North Atlantic bed of Laminaria ochroleuca. Journal of the Marine Biological Association of the U.K., 86, 309-316.
Arroyo, N.L., Castejón, I., Domínguez, M., Terrados, J., 2013. Harpacticoid copepod response to epiphyte load variations in Posidonia oceanica (L.) Delile meadows. Marine Ecology, 34, 345-362.
Beck, M.W., Heck, K.L. Jr., Able, K.W., Childers, D.L., Eggleston, D.B. et al., 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience, 51 (8), 633-641.
Bell, J.D., Pollard, D.A., 1989. Ecology of fish assemblages and fisheries associated with seagrasses. p. 565-609. In: The Biology of Seagrasses: An Australian Perspective. Larkum, A.W.D., McComb, A.J., Shepherd, S.A. (Eds.), Elsevier, Amsterdam.
Biagi, F., Gambaccini, S., Zazzetta, M., 1998. Settlement and recruitment in fishes: The role of coastal areas. Italian Journal of Zoology, 65, 269-274.
Blott, S.J., Pye, K., 2001. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth surface processes and Landforms, 26 (11), 1237-1248.
Bussotti, S., Guidetti, P., 2011. Timing and habitat preferences for settlement of juvenile fishes in the Marine Protected Area of Torre Guaceto (south-eastern Italy, Adriatic Sea). Italian Journal of Zoology, 78, 243-254.
Cheminée, A., Sala, E., Pastor, J., Bodilis, P., Thiriet, P., 2013. Nursery value of Cystoseira forests for Mediterranean rocky reef fishes. Journal of Experimental Marine Biology and Ecology, 442, 70-79.
Cheminée, A., Rider, M., Lenfant, P., Zawadzki, A., Mercière, A. et al., 2017a. Shallow rocky nursery habitat for fish: Spatial variability of juvenile fishes among this poorly protected essential habitat. Marine Pollution Bulletin, 119 (1), 245-254.
Cheminée, A., Pastor, J., Bianchimani, O., Thiriet, P., Sala, E. et al., 2017b. Juvenile fish assemblages in temperate rocky reefs are shaped by the presence of macro-Algae canopy and its three-dimensional structure. Scientific Reports 7, 14638.
Cheminée, A., Le Direach, L., Rouanet, E., Astruch, P., Goujard, A. et al., 2021. All shallow coastal habitats matter as nurseries for Mediterranean juvenile fish. Scientific reports, 11 (1), 1-17.
Christensen, M.S., 1978. Trophic relationships in juveniles of three species of Sparid fishes in the South African marine littoral. Fishery Bulletin, 76 (2), 389-401.
Christie, H., Norderhaug, K.M., Fredriksen, S., 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series, 396, 221-233.
Clarke, K.R., Gorley, R.N., 2006. Primer v6: User Manual/Tutorial – Primer-E Ltd. 190. Coleman, F.C., Williams, S. L., 2002. Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends in Ecology & Evolution, 17 (1), 40-44.
Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F. et al., 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS ONE, 5(8), e11842.
Crain, C.M., Halpern, B.S., Beck, M.W., Kappel, C.V., 2009. Understanding and managing human threats to the coastal marine environment. Annals of the New York Academy of Science, 1162, 39-62.
Cuadros, A., Moranta, J., Cardona, L., Thiriet, P., Pastor, J. et al., 2017. Seascape attributes, at different spatial scales, determine settlement and post-settlement of juvenile fish, Estuarine, Coastal and Shelf Science, 185, 120-129.
Cuadros, A., Basterretxea, G., Cardona, L., Cheminée, A., Hidalgo, M. et al., 2018. Settlement and post-settlement survival rates of the white seabream (Diplodus sargus) in the western Mediterranean Sea. PLoS ONE, 13(1), e0190278.
Daban, I.B., 2022. Comparative study on the feeding ecology of the White Seabream, Diplodus sargus, and the Black Seabream, Spondyliosoma cantharus (Osteichthyes: Sparidae) in the North Aegean Sea. Zoology in the Middle East, 68 (2), 126-134.
Dahlgren, C.P., Eggleston, D.B., 2000. Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology, 81, 2227-2240.
Dahlgren, C.P., Kellison, G.T., Adams, A.J., Gillanders, B.M., Kendall, M.S. et al., 2006. Marine nurseries and effective juvenile habitats: concepts and applications. Marine Ecology Progress Series, 312, 291-295.
Di Franco, A., Guidetti, P., 2011. Patterns of variability in early- life traits of fishes depend on spatial scale of analysis. Biology Letters, 7, 454-456.
Di Franco, G. F., Guidetti, A. 2015. Mismatch in early life traits between settlers and recruits in a Mediterranean fish: Clue of the relevance of the settlement tail? Acta Ichthyologica et Piscatoria, 45 (2), 153-159.
Dias, M., Silva, A., Cabral, H.N., Vinagre, C., 2014. Diet of marine fish larvae and juveniles that use rocky intertidal pools at the Portuguese coast. Journal of Applied Ichthyology, 30, 970-977.
Eggersten, L., Ferreira, C., Fontoura, L., Kautsky, N., Gullström, M. et al., 2017. Seaweed beds support more juvenile reef fish than seagrass beds: Carrying capacity in a south-western Atlantic tropical seascape. Estuarine, Coastal and Shelf Science, 196, 97-108.
García-Rubies, A., Macpherson, E., 1995. Substrate use and temporal pattern of recruitment in juvenile fishes of the Mediterranean littoral. Marine Biology, 124, 35-42.
Gee, J.M., 1989. An ecological and economic review of meiofauna as food for fish. Zoological Journal of the Linnean Society, 96, 243-261.
Guidetti, P., 2000. Differences Among Fish Assemblages Associated with Nearshore Posidonia oceanica Seagrass Beds, Rocky-algal Reefs and Unvegetated Sand Habitats in the Adriatic Sea. Estuarine Coastal and Shelf Science, 50, 515- 529.
Harmelin-Vivien, M., Harmelin, J.G., Leboulleux, V., 1995. Microhabitat requirements for settlement of juvenile sparid fishes on Mediterranean rocky shores. Hydrobiologia, 300/301, 309-320.
Heck, K.L.J., Orth, R.J., 1980. Seagrass habitats: the roles of habitat complexity, competition and predation in structuring associated fish and motile macroinvertebrate assemblages. In: Estuarine Perspectives. p. 449-464. Kennedy, V.S. (Ed.). Academic Press, New York.
Hereu, B., Linares, C., Sala, E., 2005. The effects of predator abundance and habitat structural complexity on survival of juvenile sea urchins. Marine Biology, 146 (2), 293-299.
Hicks, G.R.F., Coull, B.C., 1983. The ecology of marine meiobenthic harpacticoid copepods. Oceanography and Marine Biology, 21, 67-175.
Hinz, H., Reñones, O., Gouraguine, A., Johnson, A.F., Moranta, J., 2019. Fish nursery value of algae habitats in temperate coastal reefs. Peer J, 7, 67-97.
Hyndes, G.A., Lavery, P.S., 2005. Does transported seagrass provide an important trophic link in unvegetated, nearshore areas? Estuarine, Coastal and Shelf Science, 63, 633-643.
Jenkins, G.P., Black, K.P., Wheatley, M.J., Hatton, D.N., 1997. Temporal and spatial variability in recruitment of a temperate, seagrass-associated fish is largely determined by physical processes in the pre- and post-settlement phases. Marine Ecology Progress Series, 148, 23- 25.
Jenkins, G.P., Syme, A., Macreadie, P.I., 2011. Feeding ecology of King George whiting Sillaginoides punctatus (Perciformes) recruits in seagrass and unvegetated habitats. Does diet reflect habitat utilization? Journal of Biology, 78, 1561-1573.
Jenkins, G.P., Wheatley, M.J., 1998. The influence of habitat structure on nearshore fish assemblages in a southern Australian embayment: comparison of shallow seagrass, reef-algal and unvegetated sand habitats, with emphasis on their importance to recruitment. Journal of Experimental Marine Biology and Ecology 221, 147-172.
Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as Ecosystem Engineers. Oikos 69 (3), 373 - 386.
Karachle, P.K., Stergiou, K.I., 2017. An update on the feeding habits of fish in the Mediterranean Sea (2002-2015). Mediterranean Marine Science, 18 (1), 43-52.
Kramer M.J., Bellwood, O., Bellwood, D.R., 2013. The trophic importance of algal turfs for coral reef fishes: the crustacean link. Coral Reefs, 32 (2), 575-583.
Kraufvelin, P., Pekcan-Hekim, Z., Bergström, U., Florin, A.B., Lehikoinen, A. et al., 2016. Essential fish habitats (EFH). Conclusions from a workshop on the importance, mapping, monitoring, threats and conservation of coastal EFH in the Baltic Sea. TemaNord 2016:539 ISSN 0908-6692.
Krebs, C.J., 1989. Ecological Methodology. Harper Collins, New York.
Lefcheck, J.S., Hughes, B.B., Johnson, A.J., Pfirrmann, B.W., Rasher, D.B. et al., 2019. Are coastal habitats important nurseries? A meta‐analysis. Conservation Letters, 12 (4), e12645.
Leitao, F., Santos, M.N., Monteiro, C.C., 2007. Contribution of artificial reefs to the diet of the white sea bream (Diplodus sargus). ICES Journal of Marine Science, 64 (3), 473-478.
Figueiredo, M., Morato, T., Barreiros, J.P., Afonso, P., Santos R.S., 2005. Feeding ecology of the white seabream, Diplodus sargus, and the ballan wrasse, Labrus bergylta in the Azores. Fisheries Research, 75 (1-3), 107-119.
Lindeman, K., Pugliese, R., 2000. Developmental patterns within a multispecies reef fishery: management applications for essential fish habitats and protected areas. Bulletin of Marine Science, 66 (3), 929-956.
Litvin, S.Y., Weinstein, M.P., Sheaves, M., Nagelkerken, I., 2018. What makes nearshore habitats nurseries for nekton? An emerging view of the nursery role hypothesis. Estuaries and Coasts, 41 (6), 1539-1550.
Macpherson, E., Raventos, N., 2006. Relationship between pelagic larval duration and geographic distribution of Mediterranean littoral fishes. Marine Ecology Progress Series, 327, 257-265.
Macreadie, P.I., Connolly, R.M., Jenkins, G.P., Hindell, J.S., Keough, M.J., 2010a. Edge patterns in aquatic invertebrates explained by predictive models. Marine and Freshwater Research, 61, 214-218.
Macreadie, P.I., Connolly, R.M., Keough, M.J., Jenkins, G.P., Hindell, J.S., 2010b. Short‐term differences in animal assemblages in patches formed by loss and growth of habitat. Austral Ecology, 35, 515-521.
Maidanou, M., Koulouri, P., Karachle, P.K., Arvanitidis, C., Koutsoubas, D. et al., 2021. Trophic Diversity of a Fish Community Associated with a Caulerpa prolifera (Forsskål) meadow in a Shallow Semi-Enclosed Embayment. Journal of Marine Science and Engineering, 9, 165.
Nagelkerken, I., Van der Velde, G., Gorissena, M.W., Meijera, G., J., Van’t Hof, T. et al., 2000. Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuarine Coastal and Shelf Science, 51, 31-44.
Nagelkerken, I., Sheaves, M., Baker, R., Connolly, R.M., 2015. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish and Fisheries, 16, 362-371.
Nordström, M.C., Lindblad, P., Aarnio, K., Bonsdorff, E., 2010. A neighbour is a neighbour? Consumer diversity, trophic function, and spatial variability in benthic food webs. Journal of Experimental Marine Biology and Ecology, 391, 101-111.
Orth, R.J., Heck, K.L., Van Montfrans, J., 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7, 339-350.
Osman, A.M., Mahmoud, H.H., 2009. Feeding biology of Diplodus sargus and Diplodus vulgaris (Teleostei, Sparidae) in Egyptian Mediterranean waters. World Journal of Fish and Marine Sciences, 1 (4), 290-296.
Pyke, G.H., Pulliam, H.R., Charnovet, E.L., 1977. Optimal Foraging: A Selective Review of Theory and Tests. The Quarterly Review of Biology, 52 (2), 137-154.
Reñones, O., Massuti, E., Moranta, J., Coll, J., Moreno, I., 1995. Fish fauna of Posidonia oceanica seagrass meadows in Palma Bay (Balearic Islands). Cybium, 19, 201-206.
Richards, W.J., Lindeman, K.C., 1987. Recruitment dynamics of reef fishes: planktonic processes, settlement and demersal ecologies, and fishery analysis. Bulletin of Marine Science, 41 (2), 392-410.
Rishworth, G.M., Strydom, N.A., Potts, W.M., 2015. The nursery role of a sheltered surf-zone in warm temperate southern Africa. African Zoology, 50, 11-16.
Rodriguez-Ruiz, S., Sánchez-Lizaso, J., Ramos-Esplá, A.A., 2002. Feeding of Diplodus annularis in Posidonia oceanica Meadows: ontogenetic, diel, and habitat related dietary shifts. Bulletin of Marine Science, 71 (3), 1353-1360.
Sala, E., Ballesteros, E., 1997. Partitioning of space and food resources by three fish of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Marine Ecology Progress Series, 152, 273-283.
Sale, P.F., Douglas, W.A., Doherty, P.J., 1984a. Choice of microhabitats by coral reef fishes at settlement. Coral Reefs (3), 91-99.
Sale, P.F, Doherty, P.J., Eckert, G.J., Douglas, W.A., Ferrell, D.J., 1984b. Large scale spatial and temporal variation in recruitment to fish populations on coral reefs. Oecologia (64), 191-198.
Sanuy, J.R., Díaz, C.L., 2002. El Naixement d’una illa, Menorca. Institut Menorquí d’Estudis. Sánchez-Velasco, L., Norbis, W., 1997. Comparative diets and feeding habits of Boops boops and Diplodus sargus larvae, two sparid fishes co-occurring in the northwestern Mediterranean (May 1992). Bulletin of Marine Science, 61 (3), 821-835.
Scharf, F.S., 2000. Patterns in Abundance, Growth, and Mortality of Juvenile Red Drum across Estuaries on the Texas Coast with Implications for Recruitment and Stock Enhancement. Transactions of the American Fisheries Society, 129, 1207-1222.
Schükel, S., Sell, A.F., Kihara, T.C., Koeppen, A., Kröncke, I. et al., 2012. Meiofauna as food source for small-sized demersal fish in the southern North Sea. Helgoland Marine Research, 67, 203-218.
Sogard, S., 1984. Utilization of meiofauna as a food source by a grassbed fish, the spotted dragonet Callionymus pauciradiatus. Marine Ecology Progress Series, 17, 183-191.
Ståhl, J., Pihl, L., Wennhage, H., 2007. Food utilisation by coastal fish assemblages in rocky and soft bottoms on the Swedish West Coast: Inference for identification of Essential Fish Habitats. Estuarine, Coastal and Shelf Science, 71 (3-4), 593-607.
Stergiou, K.I., Karpouzi, V.S., 2002. Feeding habits and trophic levels of Mediterranean fish. Reviews in fish biology and fisheries, 11 (3), 217-254.
Sundblad, G., Bergström, U., Sandström, A., Eklöv, P., 2013. Nursery habitat availability limits adult stock sizes of predatory coastal fish. ICES Journal of Marine Science, 71 (3), 672-680.
Tano, A.D., Eggertsen, M.A, Wikström, S.A., Berkström, C., Buriyo, A.S. et al., 2017. Tropical seaweed beds as important habitats for juvenile fish. Marine and Freshwater Research, 68 (10), 1921-1934.
Tipton, K., Bell, S.S., 1988. Foraging patterns of two sygnathid fishes: importance of harpacticoid copepods. Marine Ecology Progress Series, 47, 31-43.
Tugores, M.P., Ordines, F., Guijarro, B., García-Ruiz, C., Esteban. A. et al., 2019. Essential fish habitats and hotspots of nekto‐benthic diversity and density in the western Mediterranean. Aquatic Conservation: Marine and Freshwater Ecosystems, 29 (3), 461-471.
Vigliola, L., Harmelin-Vivien, M.L., Biagi, F., Galzin, R., García-Rubies, A. et al., 1998. Spatial and temporal patterns of settlement among sparid fishes of the genus Diplodus in the northwestern Mediterranean. Marine Ecology Progress Series, 168, 45-56.
Most read articles by the same author(s)