Abstract
Stable isotope analyses were employed to explore feeding and foraging habitats and trophic levels of littoral fishes in a western Mediterranean Marine Protected Area (Egadi Islands, Sicily, Italy). Carbon and nitrogen stable isotope ratios were measured in primary producers, invertebrates and fishes collected in December 2001 and January 2002. Fishes of the littoral region of the Egadi Islands had isotopic signatures that fell into a wider range for δ 13C (about 6‰) than for δ 15N (about 3‰). Carbon isotope ratios were consistent with a food web based on mixed sources and two trophic pathways leading to different fish species. Differences in the isotopic composition between islands were higher for benthivorous than for planktivorous fishes. The overall picture gained from this study is of a isotopic distinction between planktivorous and benthivorous fishes, resource partitioning facilitating the coexistence of similar species within the same ecosystem, and spatial variability in the isotopic signatures and trophic level of fishes. Asymmetrical analysis of variance showed that estimated trophic levels were lower in the area with the highest level of protection (Zone A) for only two out of the nine fishes analysed. As a consequence, overall spatial differences do not seem to be a consequence of protection, since in most cases trophic levels did not change significantly between zone A and zones C where professional fishing (trawling apart) is permitted, but of natural sources of variation (e.g. variability in food availability and site-specific food preferences of fishes). However, the results of this study suggest a different response at the species compared to the community level.
Similar content being viewed by others
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46 doi:10.1046/j.1442-9993.2001.01070.x
Anderson MJ (2005) DistLM v.5: A FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, New Zealand
Arculeo M, Pipitone C, Riggio S (1989) Aspetti del regime alimentare di Mullus surmuletus L. (Pisces, Mullidae) nel Gofo di Palermo. Oebalia (Taranto) 15:67–77
Arculeo M, Froglia C, Riggio S (1993) Food partitioning between Serranus scriba and Scorpaena porcus (Perciformes) on the infralittoral ground of the south Tyrrhenian Sea. Cybium 17:251–258
Badalamenti F, D’Anna G, Fazio G, Gristina M, Lipari L (1993) Relazioni trofiche tra quattro specie ittiche catturate su differenti substrati nel Golfo di Castellammare (Sicilia N/O). Biol Mar Medit 1:145–150
Bell JD, Harmelin-Vivien ML (1983) Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. 2. Feeding habits. Tethys 11:1–14
Bode A, Carrera P, Lens S (2003) The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: natural abundance of stable carbon and nitrogen isotopes. ICES J Mar Sci 60:11–22 doi:10.1006/jmsc.2002.1326
Chiappone M, Sluka R, Sealey KS (2000) Groupers (Pisces: Serranidae) in fished and protected areas of the Florida Keys, Bahamas and northern Caribbean. Mar Ecol Prog Ser 198:261–272 doi:10.3354/meps198261
Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth
Connolly RM, Gorman D, Guest MA (2005) Movement of carbon among estuarine habitats and its assimilation by invertebrates. Oecologia 144:684–691 doi:10.1007/s00442-005-0167-4
Dahl TM, Falk-Petersen S, Gabrielsen GW, Sargent JR, Hop H, Millar RM (2003) Lipids and stable isotopes in common eider, black-legged kittiwake and northern fulmar: a trophic study from an Arctic fjord. Mar Ecol Prog Ser 256:257–269 doi:10.3354/meps256257
Dayton PK, Tegner MJ, Edwards PB, Riser KL (1998) Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecol Appl 8:309–322 doi:10.1890/1051-0761(1998)008[0309:SBGARE]2.0.CO;2
Dayton PK, Sala E, Tegner MJ, Thrush SF (2000) Marine protected areas: parks, baselines, and fishery enhancement. Bull Mar Sci 66:617–634
De Pirro M, Marchetti GM, Chelazzi G (1999) Foraging interactions among three benthic fish in a Posidonia oceanica reef lagoon along the Tyrrhenian coast. J Fish Biol 54:1300–1309 doi:10.1006/jfbi.1999.0958
Deudero S, Pinnegar JK, Polunin NVC, Morey G, Morales-Nin B (2004) Spatial variation and ontogenic shifts in the isotopic composition of Mediterranean littoral fishes. Mar Biol (Berl) 145:971–981 doi:10.1007/s00227-004-1374-y
Dittel AI, Epifanio CE, Schwalm SM, Fantle MS, Fogel ML (2000) Carbon and nitrogen sources for juvenile blue crabs Callinectes sapidus in coastal wetlands. Mar Ecol Prog Ser 194:103–112 doi:10.3354/meps194103
Francour P (1994) Pluriannual analysis of the reserve effect on ichthyofauna in the Scandola natural reserve (Corsica, North-western Mediterranean). Oceanol Acta 17:309–317
Fraschetti S, Terlizzi A, Micheli F, Benedetti-Cecchi L, Boero F (2002) Marine protected areas in the Mediterranean Sea: objectives, effectiveness and monitoring. Mar Ecol (Berl) 23:190–200 doi:10.1111/j.1439-0485.2002.tb00018.x
Gannes LZ, O’Brien DM, Martinez Del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276
García-Charton JA, Pérez-Ruzafa A (1999) Ecological heterogeneity and the evaluation of the effects of marine reserves. Fish Res 42:1–20 doi:10.1016/S0165-7836(99)00043-0
García-Charton JA, Pérez-Ruzafa Á, Sánchez-Jerez P, Bayle-Sempere JT, Reňones O, Moreno D (2004) Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on Western Mediterranean rocky reef fish assemblages. Mar Biol (Berl) 144:161–182 doi:10.1007/s00227-003-1170-0
Glasby TM (1997) Analysing data from post-impact studies using asymmetrical analyses of variance: a case study of epibiota on marinas. Aust J Ecol 22:448–459 doi:10.1111/j.1442-9993.1997.tb00696.x
Halpern BJ (2003) The impact of marine reserves: do reserves work and does reserve size matter. Ecol Appl 13:S117–S137 doi:10.1890/1051-0761(2003)013[0117:TIOMRD]2.0.CO;2
Harmelin JG, Bachet F, Garcia F (1995) Mediterranean marine reserves: fish indices as tests for protection efficiency. Mar Ecol (Berl) 16:233–250 doi:10.1111/j.1439-0485.1995.tb00408.x
Hobson KA, Ambrose WG, Renaud PE (1995) Sources of primary production, benthic–pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Mar Ecol Prog Ser 128:1–10 doi:10.3354/meps128001
Iken K, Bluhm BA, Gradinger R (2005) Food web structure in the high Arctic Canada Basin: evidence from δ13C and δ15N analysis. Polar Biol 28:238–249 doi:10.1007/s00300-004-0669-2
Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems. Adv Mar Biol 34:201–352 doi:10.1016/S0065-2881(08)60212-6
Jennings S, Reňones 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 doi:10.3354/meps146109
Khoury C (1984) Ethologies alimentaires de quelques espèces de poisons de l’herbier de Posidonies du Parc National de Port-Cros. In: Boudouresque CF, Jeudy de Grissac A, Olivier J (eds) International workshop Posidonia oceanica beds, vol 1. GIS Posidonie, France, pp 335–347
Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50:324–340 doi:10.1111/j.1095-8649.1997.tb01361.x
Labropoulou M, Machias A, Tsimenides N, Eleftheriou A (1997) Feeding habits and ontogenetic shift of the striped red mullet, Mullus surmuletus Linnaeus, 1758. Fish Res 31:257–267 doi:10.1016/S0165-7836(97)00017-9
Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol (Berl) 136:513–518 doi:10.1007/s002270050711
Lubchenco J, Palumbi SR, Gaines SD, Andelman S (2003) Plugging a hole in the ocean: the emerging science of marine reserves. Ecol Appl 13:S3–S7 doi:10.1890/1051-0761(2003)013[0003:PAHITO]2.0.CO;2
McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulphur. Oikos 102:378–390 doi:10.1034/j.1600-0706.2003.12098.x
Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analysis. Mar Ecol Prog Ser 215:93–106 doi:10.3354/meps215093
Olive PJW, Pinnegar JK, Polunin NVC, Richards G, Welch R (2003) Isotope trophic-step fractionation: a dynamic equilibrium model. J Anim Ecol 72:608–617 doi:10.1046/j.1365-2656.2003.00730.x
Owens NJP (1987) Natural variation in 15N in the marine environment. Adv Mar Biol 24:389–451
Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F (1998) Fishing down marine food webs. Science 279:860–863 doi:10.1126/science.279.5352.860
Pauly D, Palomares MA, Froese R, Sa-a P, Vakily M, Preikshot D et al (2001) Fishing down Canadian aquatic food webs. Can J Fish Aquat Sci 58:51–62 doi:10.1139/cjfas-58-1-51
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320 doi:10.1146/annurev.es.18.110187.001453
Pinnegar JK, Polunin NVC (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409 doi:10.1007/s004420050046
Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML et al (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200 doi:10.1017/S0376892900000205
Pinnegar JK, Jennings S, O’Brien CM, Polunin NCV (2002) Long-term changes in the trophic level of the Celtic Sea fish community and fish market price distribution. J Appl Ecol 39:377–390 doi:10.1046/j.1365-2664.2002.00723.x
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718
Russ GR (2002) Yet another review of marine reserves as reef fisheries management tools. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic, San Diego
Russ GR, Stockwell B, Alcala AC (2005) Inferring versus measuring rates of recovery in no-take marine reserves. Mar Ecol Prog Ser 292:1–12 doi:10.3354/meps292001
Sala E, Boudouresque CF, Harmelin-Vivien M (1998) Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 82:425–439 doi:10.2307/3546364
Shears NT, Babcock RC (2003) Continuing trophic cascade effects after 25 years of no-take marine reserve protection. Mar Ecol Prog Ser 246:1–16 doi:10.3354/meps246001
Steneck RS (1998) Human influences on coastal ecosystems: does overfishing create trophic cascades. Trends Ecol Evol 13:429–430 doi:10.1016/S0169-5347(98)01494-3
Stergiou KI, Karpouzi VS (2002) Feeding habits and trophic levels of Mediterranean fish. Rev Fish Biol Fish 11:217–254 doi:10.1023/A:1020556722822
Tamelander T, Renaud PE, Hop H, Carroll ML, Ambrose WG Jr, Hobson KA (2006) Trophic relationships and pelagic–benthic coupling during summer in the Barents Sea Marginal Ice Zone, revealed by stable carbon and nitrogen isotope measurements. Mar Ecol Prog Ser 310:33–46 doi:10.3354/meps310033
Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci 57:579–589 doi:10.1006/jmsc.2000.0715
Underwood AJ (1993) The mechanisms of spatially replicated sampling programmes to detect environmental impacts in a variable world. Aust J Ecol 18:99–116 doi:10.1111/j.1442-9993.1993.tb00437.x
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182 doi:10.1007/s00442-003-1270-z
Warwick RM, Clarke KR (1993) Increased variability as a symptom of stress in marine communities. J Exp Mar Biol Ecol 172:215–226 doi:10.1016/0022-0981(93)90098-9
Willis TJ, Millar RB, Babcock RC (2000) Detection of spatial variability in relative density of fishes: comparison of visual census, angling, and baited underwater video. Mar Ecol Prog Ser 198:249–260 doi:10.3354/meps198249
Acknowledgements
We wish to thank A. Savona and M. Caruso for assistance with sampling and F. Colombo and L. Camarda for laboratory assistance. This research was funded by Ministero delle Politiche Agricole e Forestali (MiPAF), Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR) and Ministero dell’Ambiente e della Tutela del Territorio (MATT).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vizzini, S., Mazzola, A. Stable isotopes and trophic positions of littoral fishes from a Mediterranean marine protected area. Environ Biol Fish 84, 13–25 (2009). https://doi.org/10.1007/s10641-008-9381-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-008-9381-3