Abstract
Stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers were investigated seasonally throughout 1999, in order to describe the food web in a western Mediterranean coastal lagoon (Lake of Sabaudia, central Italy). Particulate organic matter and algal material (seagrass epiphytes and macroalgae) seem to constitute the main food sources for primary consumers (zooplankton and small benthic invertebrates, respectively) throughout the sampling year, while the seagrass Cymodocea nodosa appears to play a negligible trophic role. As regards the ichthyofauna, carbon stable isotopes differentiated between planktivore and benthivore fish species. However, a benthic–pelagic coupling seems to occur, with some fish of higher trophic levels feeding both on benthic and pelagic materials. Analysis of variance showed that the interaction between the three main factors (species×size×season) significantly affects the isotopic composition of fish, suggesting the presence of intra- and inter-specific resource partitioning. Wide seasonal variations in the isotopic composition were observed in organic matter sources, invertebrates and fish, with a general trend towards depleted values in winter and enriched values in summer. The winter depletion of organic matter sources may be due to several environmental factors and seems to be mirrored in the upper trophic levels. Primary producers and invertebrates are known to have shorter time-integrated isotopic signatures than vertebrates, yet fish also exhibited seasonal isotopic differences. We concluded that the examined fish species can assume a new muscle isotopic signature relatively quickly in response to changes in the isotopic composition of their diet and/or diet shifts.
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References
Alongi DM (ed) (1998) Coastal ecosystem processes. CRC, Boca Raton, Fla.
Badalamenti F, D'Anna G, Lopiano L, Scilipoti D, Mazzola A (1995) Feeding habits of young-of-the-year greater amberjack Seriola dumerili (Risso, 1810) along the N/W Sicilian coast. Sci Mar 59:317–323
Barnes RSK (1980) Coastal lagoons. The natural history of a neglected habitat. Cambridge University Press, London
Bell JD, Harmelin-Vivien ML (1983) Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. 2. feeding habits. Tethys 11:1–14
Bengtson DA (1984) Resource partitioning by Menidia menidia and Menidia beryllina (Osteichthyes: Atherinidae). Mar Ecol Prog Ser 18:21–30
Bosley KL, Wainright SC (1999) Effects of preservatives and acidification on the stable isotope ratios (15N:14N, 13C:12C) of two species of marine animals. Can J Fish Aquat Sci 56:2181–2185
Bunn SE, Loneragan NR, Kempster MA (1995) Effects of acid washing on stable isotope ratios of C and N in penaeid shrimp and seagrass: implications for food-web studies using multiple stable isotopes. Limnol Oceanogr 40:622–625
Buskey EJ, Dunton KH, Parker PL (1999) Variations in stable carbon isotope ratio of the copepod Acartia tonsa during the onset of the Texas brown tide. Estuaries 22:995–1003
Castel J, Cassifour P, Labourg PJ (1977) Croissance et modifications du régime alimentaire d'un téléostéen mugiliforme: Atherina boyeri Risso, 1810 dans les étangs saumâtres du bassin d' Arcachon. Vie Milieu 27:385–410
Cebrián J, Duarte C, Marbà N, Enriquez S (1997) Magnitude and fate of the production of four co-occurring western Mediterranean seagrass species. Mar Ecol Prog Ser 155:29–44
Chanton JP Lewis FG (1999) Plankton and dissolved inorganic carbon isotopic composition in a river-dominated estuary: Apalachicola Bay, Florida. Estuaries 22:575–583
Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Natural Environment Research Council, Swindon, UK
Cooper LW, De Niro MJ (1989) Stable carbon isotope variability in the seagrass Posidonia oceanica: evidence for light intensity effects. Mar Ecol Prog Ser 50:225–229
Costa C, Minervini R, Lombardi F, Bianchini ML (1985) Indagine sulla fauna planctonica, bentonica e sulla vallicoltura del Lago di Sabaudia. Quad Ist Idrobiol Acquacolt "G Brunelli" 5/6:3–33
Currin CA, Newell SY, Paerl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotopes. Mar Ecol Prog Ser 121:99–116
Dauby P, Poulicek M (1995) Methods for removing epiphytes from seagrasses: SEM observations on treated leaves. Aquat Bot 52:217–228
Dauby P, Mosora F, Vertez M (1990) A yearly study of 13C/12C isotopic ratio variations in the Calvi's Bay plankton. Rapp Comm Int Explor Sci Mer Mediterr 32:201–202
Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47
Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87–112
Durako MJ, Hall MO (1992) Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 86:99–101
Ferrari I, Chieregato AR (1981) Feeding habits of juvenile stages of Sparus auratus L., Dicentrarchus labrax L. and Mugilidae in a brackish embayment of the Po river delta. Aquaculture 25:243–257
Fischer W, Schneider M, Bauchot ML (eds) (1987) Fiches FAO d'identification des espèces pour les besoins de la pêche. Mediterranee et Mer Noire. Zone de pêche 37, vol II. Vertébrés. FAO, Rome
Franzoi P, Maccagnani R, Rossi R, Ceccherelli VU (1993) Life cycles and feeding habits of Syngnathus taenionotus and S. abaster (Pisces, Syngnathidae) in a brackish bay of the Po river delta (Adriatic Sea). Mar Ecol Prog Ser 97:71–81
Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47
Fry B, Macko SA, Zieman JC (1987) Review of stable isotopic investigation of food webs in seagrass meadows. Fla Mar Res Publ 42:189–209
Gearing JN, Gearing PJ, Rudnick DT, Requejo AJ, Hutchins MJ (1984) Isotopic variability of organic carbon in a phytoplankton-based temperature estuary. Geochim Cosmochim Acta 48:1089–1098
Gerking SD (1994) Feeding ecology of fish. Academic, San Diego
Gisbert E, Cardona L, Castellò F (1996) Resource partitioning among planktivorous fish larvae and fry in a Mediterranean coastal lagoon. Estuar Coast Shelf Sci 43:737–746
Goering J, Alexander V, Haubenstock N (1990) Seasonal variability of stable and carbon isotope ratios of organisms in a North Pacific bay. Estuar Coast Shelf Sci 30:239–260
Grice AM, Loneragan NR, Dennison WC (1996) Light intensity and the interactions between physiology, morphology and stable isotope ratios in five species of seagrass. J Exp Mar Biol Ecol 195:91–110
Grossman GD (1980) Ecological aspects of ontogenetic shifts in prey size utilization in the bay goby (Pisces: Gobiidae). Oecologia 47:233–238
Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298
Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus onus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076
Hsieh HL, Kao WY, Po C, Liu PJ (2000) Detrital flow through the feeding pathway of the oyster (Crassostrea gigas) in a tropical shallow lagoon: δ13C signals. Mar Biol 136:677–684
Jennings S, Reñones O, Morales-Nin B, Polunin NVC, Moranta J, Coll J (1997) Spatial variation in the 15N and 13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Mar Ecol Prog Ser 146:109–116
Kaehler S, Pakhomov EA, McQuaid CD (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20
Kang CK, Sauriau PG, Richard P, Blanchard GF (1999) Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron Bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar Ecol Prog Ser 187:147–158
Knoppers B (1994) Aquatic primary production in coastal lagoons. In: Kjerfve B (ed) Coastal lagoon processes. Elsevier, Amsterdam
Koranteng KA, Ofori-Danson PK, Entsua-Mensah M (2002) Fish and fisheries of the Muni lagoon in Ghana, West Africa. Biodiversity Conserv 9:487–499
Loneragan NR, Potter IC, Lenanton RCJ (1989) Influence of site, season and year on contributions made by marine, estuarine, diadromous and freshwater species to the fish fauna of temperate Australian estuary. Mar Biol 103:461–479
Marguillier S, Van der Velde G, Dehairs F, Hemminga MA, Rajagopal S (1997) Trophic relationships in an interlinked mangrove–seagrass ecosystem as traced by δ13C and δ15N. Mar Ecol Prog Ser 151:115–121
Maruyama A, Yamada Y, Rusuwa B, Yuma M (2001) Change in stable nitrogen isotope ratio in the muscle tissue of a migratory goby, Rhinogobius sp., in a natural setting. Can J Fish Aquat Sci 58:2125–2128
Mazzola A, Sarà G, Venezia F, Caruso M, Catalano D, Hauser S (1999) Origin and distribution of suspended organic matter as inferred from carbon isotope composition in a Mediterranean semi-enclosed marine system. Chem Ecol 16:215–238
McClelland JW, Valiela I (1998) Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar Ecol Prog Ser 168:259–271
Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental sciences. Blackwell, Oxford, pp 138–157
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Perdicaro R (1984) Condizioni chimico-fisiche del Lago di Sabaudia o di Paola dal 1933 al 1984. Quad Ist Idrobiol Acquacolt "G Brunelli" 4:71–139
Perdicaro R (1985) Effetti della riduzione del carico eutrofizzante sulle condizioni chimico-fisiche del Lago di Sabaudia. (Campagna di rilevamenti del 1984). Nova Thalassia 7:343–348
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231
Pinnegar JK, Polunin NVC (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718
Quignard JP (1984) Les caractéristiques biologiques et environnementales des lagunes en tant que base biologique de l'aménagement des pêcheries. GFCM Stud Rev 61:3–38
Riera P, Richard P (1997) Temporal variation of δ13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oléron Bay (France): effect of freshwater. Mar Ecol Prog Ser 147:105–115
Riera R, Montagna PA, Kalke RD, Richard P (2000) Utilization of estuarine organic matter during growth and migration by juvenile brown shrimp Penaeus aztecus in a south Texas estuary. Mar Ecol Prog Ser 199:205–216
Ross ST (1986) Resource partitioning in fish assemblages: a review of field studies. Copeia 2:352–388
Sandheinrich MB, Hubert WA (1984) Intraspecific resource partitioning by yellow perch (Perca flavescens) in a stratified lake. Can J Fish Aquat Sci 41:1745–1752
Sarà G, Vizzini S, Mazzola A (2002)The effect of temporal changes and environmental trophic condition on the isotopic composition (δ13C and δ15N) of Atherina boyeri (Risso, 1810) and Gobius niger (L., 1758) in a Mediterranean coastal lagoon (Lake of Sabaudia): implications for food web structure. Mar Ecol 23:352–360
Simenstad CA, Wissmar RC (1985) δ13C evidence of the origins and fates of organic carbon in estuarine and nearshore food webs. Mar Ecol Prog Ser 22:141–152
Tallman RF, Gee JH (1982) Intraspecific resource partitioning in a headwaters stream fish, the pearl dace Semotilus margarita (Cyprinidae). Environ Biol Fishes 7:243–249
Trabelsi M, Kartas F, Quignard JP (1994) Comparaison du régime alimentaire d'une population marine et d'une population lagunaire d'Atherina boyeri des côtes tunisiennes. Vie Milieu 44:117–123
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
Vaas KF, Vlasblom G, De Koeijer P (1975) Studies on the black goby (Gobius niger, Gobiidae, Pisces) in the Veerse Meer, SW Netherlands. Neth J Sea Res 9:56–58
Vander Zanden MJV, Hulshof M, Ridgway MS, Rasmussen JB (1998) Application of stable isotope techniques to trophic studies of age-0 smallmouth bass. Trans Am Fish Soc 127:729–739
Vesey G, Langford TE (1985) The biology of the black goby, Gobius niger L. in an English south-coast bay. J Fish Biol 27:417–429
Vizzini S, Mazzola A (2002) Stable carbon and nitrogen ratios in the sand smelt from a Mediterranean coastal area: feeding habits and effect of season and size on feeding strategy. J Fish Biol 60:1498–1510
Vizzini S, Sarà G, Michener RH, Mazzola A (2002) The role and contribution of Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecol 23:277–285
Wada E, Kadonaga T, Matsuo S (1975) 15N abundance in nitrogen of naturally occurring substances and global assessment of denitrification from isotopic viewpoint. Geochem J 9:139–148
Whitfield AK (1990) Life-history styles of fishes in South African estuaries. Environ Biol Fishes 28:295–308
Acknowledgements
The authors wish to thank Dr. M. Campolmi for her support during field work and Dr. A. Savona for laboratory assistance. Stable isotope analysis was carried out by R.H. Michener at the Boston University Stable Isotope Laboratory. This work was funded by the Ministero Politiche Agricole e Forestali (MiPAF, Italy) and Ministero dell'Istruzione, dell'Università e della Ricerca (MIUR, Italy).
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Communicated by R. Cattaneo-Vietti, Genova
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Vizzini, S., Mazzola, A. Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Marine Biology 142, 1009–1018 (2003). https://doi.org/10.1007/s00227-003-1027-6
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DOI: https://doi.org/10.1007/s00227-003-1027-6