[en] Increasing human pressure along Mediterranean coastlines raises the need to define
sensitive bioindicators that provide an early response to nutrient enrichment. We performed multiscale carbon and nitrogen stable isotope analyses on the limpet Patella caerulea, the snail Monodonta turbinata, epilithic biofilms, and the macroalga Rissoella verruculosa inhabiting the rocky midlittoral zone. Samples were seasonally collected in 2006 from 5 sites exposed to a range of anthropogenic discharges in the Revellata Bay area and in Marseille harbour (France). All bioindicators exhibited strongly elevated δ15N values at impacted sites compared to pristine ones, which revealed the biological availability of anthropogenically derived nutrients. Only epilithic biofilms tended to show both the occurrence of nutrient pulses during the tourist season and a δ13C response at impacted sites. In contrast to macroalgae, which exhibited a somewhat equivocal signal, gastropods and especially M. turbinata provided the best time-integrated picture of the graduated exposure of the 5 sites to anthropogenic impact. Results also showed first evidence of large isotopic variability at a scale of tens of metres, close to that found at the kilometre scale. The intra- and interspecific isotopic variability in gastropods may be explained by the patchiness of resources and specific morphological and behavioural features, but these factors do not greatly hamper their potential as early bioindicators of wastewater disturbances.
Research Center/Unit :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Vermeulen, Simon ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Sturaro, Nicolas ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Gobert, Sylvie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Bouquegneau, Jean-Marie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Lepoint, Gilles ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Language :
English
Title :
Potential early indicators of anthropogenically derived nutrients : a multiscale stable isotope analysis
Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601-607 (Pubitemid 30247470)
Armitage AR, Fourqurean JW (2009) Stable isotopes reveal complex changes in trophic relationships following nutrient addition in a coastal marine ecosystem. Estuar Coasts 32:1152-1164
Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: A novel approach using stable isotope analysis. J Anim Ecol 73:1007-1012 (Pubitemid 39123240)
Bishop MJ, Underwood AJ, Archambault P (2002) Sewage and environmental impacts on rocky shores: Necessity of identifying relevant spatial scales. Mar Ecol Prog Ser 236: 121-128 (Pubitemid 34780686)
Brutemark A, Lindehoff E, Granéli E, Granéli W (2009) Carbon isotope signature variability among cultured microalgae: Influence of species, nutrients and growth. J Exp Mar Biol Ecol 372:98-105
Burns A, Ryder DS (2001) Potential for biofilms as biological indicators in Australian riverine systems. Ecol Manag Restor 2:53-64
Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844-10847 (Pubitemid 26333077)
Camus PA, Daroch K, Opazo LF (2008) Potential for omnivory and apparent intraguild predation in rocky intertidal herbivore assemblages from northern Chile. Mar Ecol Prog Ser 361:35-45 (Pubitemid 351975497)
Camus PA, Cid YY, Cisterna L, Cáceres CW (2009) Consumption and digestion of animal food by rocky intertidal herbivores: An evaluation of digestive flexibility and omnivory in three grazing species. Lat Am J Aquat Res 37:191-197
Carballo JL, Naranjo SA, García-Gómez JC (1996) Use of sponges as stress indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula). Mar Ecol Prog Ser 135:109-122
Carlier A, Riera P, Amouroux JM, Bodiou JY, Desmalades M, Grémare A (2008) Food web structure of two Mediterranean lagoons under varying degree of eutrophication. J Sea Res 60:264-275
Clarke KR, Gorley RN (2006) PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth
Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210: 223-253 (Pubitemid 32164184)
Costanzo SD, O'Donohue MJ, Dennison WC, Loneragan NR, Thomas M (2001) A new approach for detecting and mapping sewage impacts. Mar Pollut Bull 42:149-156 (Pubitemid 32178231)
Crothers JH (1994) Student investigations on the population structure of the common topshell, Monodonta lineata, on The Gore, Somerset. Field Stud 8:337-355 (Pubitemid 26448816)
Della-Santina P, Sonni C, Sartoni G, Chelazzi G (1993) Food availability and diet composition of three coexisting Mediterranean limpets (Patella spp.). Mar Biol 116:87-95 (Pubitemid 24412487)
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495-506
Dytham C (2003) Choosing and using statistics: A biologist's guide. Blackwell, Berlin
Fry B, Sherr E (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13-47
Gil M, Armitage AR, Fourqurean JW (2006) Nutrient impacts on epifaunal density and species composition in a subtropical seagrass bed. Hydrobiologia 569:437-447 (Pubitemid 44167590)
Guest MA, Connolly RM, Loneragan NR (2004) Carbon movement and assimilation by invertebrates in estuarine habitats at a scale of metres. Mar Ecol Prog Ser 278:27-34 (Pubitemid 39379418)
Hawkins SJ, Hartnoll RG (1983) Grazing of intertidal algae by marine invertebrates. Oceanogr Mar Biol Annu Rev 21: 195-282
Hedges JI, Stern JH (1984) Carbon and nitrogen determinations of carbonate-containing solids. Limnol Oceanogr 29: 657-663
Hill AS, Hawkins S (1991) Seasonal and spatial variation of epilithic microalgal distribution and abundance and its ingestion by Patella vulgata on a moderately exposed rocky shore. J Mar Biol Assoc UK 71:403-423
Hill WR, Middleton RG (2006) Changes in carbon stable isotope ratios during periphyton development. Limnol Oceanogr 51:2360-2369 (Pubitemid 44520928)
Hutchinson N, Davies MS, Ng JSS, Williams GA (2007) Trail following behaviour in relation to pedal mucus production in the intertidal gastropod Monodonta labio (Linnaeus). J Exp Mar Biol Ecol 349:313-322 (Pubitemid 47198639)
Ifremer (Institut français de recherche pour l'exploitation de la mer) (2007) Synthèse de l'état de la contamination chimique du golfe de Marseille. Report No. R.INT.DOP/ LER-PAC/07-05. Ifremer, Paris
Johnson MP, Hanley ME, Frost NJ, Mosley MWJ, Hawkins SJ (2008) The persistent spatial patchiness of limpet grazing. J Exp Mar Biol Ecol 365:136-141
Krom MD, Herut B, Mantoura RFC (2004) Nutrient budget for the eastern Mediterranean: Implications for phosphorus limitation. Limnol Oceanogr 49:1582-1592 (Pubitemid 39333103)
Kurata K, Minami H, Kikuchi E (2001) Stable isotope analysis of food sources for salt marsh snails. Mar Ecol Prog Ser 223:167-177 (Pubitemid 34067274)
Lancaster J, Waldron S (2001) Stable isotope values of lotic invertebrates: Sources of variation, experimental design, and statistical interpretation. Limnol Oceanogr 46:723-730 (Pubitemid 32434672)
Lassauque J, Lepoint G, Thibaut T, Francour P, Meinesz A (2010) Tracing sewage and natural freshwater input in a northwest Mediterranean bay: Evidence obtained from isotopic ratios in marine organisms. Mar Pollut Bull 60: 843-851
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 136:513-518 (Pubitemid 30300890)
Lorrain A, Paulet YM, Chauvaud L, Savoye N, Donval A, Saout C (2002) Differential δ13C and δ15N signatures among scallop tissues: Implications for ecology and physiology. J Exp Mar Biol Ecol 275:47-61 (Pubitemid 34839102)
MacLeod NA, Barton DR (1998) Effects of light intensity, water velocity, and species composition on carbon and nitrogen stable isotope ratios in periphyton. Can J Fish Aquat Sci 55:1919-1925 (Pubitemid 28554018)
McClelland JW, Valiela I, Michener RH (1997) Nitrogenstable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42:930-937 (Pubitemid 28278270)
McIntyre PB, Flecker AS (2006) Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148:12-21
McKinney RA, Nelson WG, Charpentier MA, Wigand C (2001) Ribbed mussel nitrogen isotope signatures reflect nitrogen sources in coastal salt marshes. Ecol Appl 11: 203-214 (Pubitemid 32113861)
McKinney RA, Lake JL, Charpentier MA, Ryba S (2002) Using mussel isotope ratios to assess anthropogenic nitrogen inputs to freshwater ecosystems. Environ Monit Assess 74:167-192 (Pubitemid 34134161)
Munda IM (1993) Changes and degradation of seaweed stands in the northern Adriatic. Hydrobiologia 260-261: 239-253 (Pubitemid 24415191)
Nixon SW (1995) Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia 41:199-219
Oakes JM, Revill AT, Connolly RM, Blackburn SI (2005) Measuring carbon isotope ratios of microphytobenthos using compound-specific stable isotope analysis of phytol. Limnol Oceanogr Methods 3:511-519 (Pubitemid 43723640)
Oehlmann J, Schulte-Oehlmann U (2003) Molluscs as bioindicators. In: Market BA, Breure AM, Zechmeister G (eds) Bioindicators and biomonitors. Elsevier Science Publishers, New York, NY, p 577-635
Orton JH, Southward AJ, Dodd JM (1956) Studies on the biology of limpets, II. the breeding of Patella vulgata L. in Britain. J Mar Biol Assoc UK 35:149-176
Peduzzi P, Herndl GJ (1991) Mucus trails in the rocky intertidal: A highly active microenvironment. Mar Ecol Prog Ser 75:267-274
Pérès JM, Picard J (1964) Nouveau manuel de bionomie benthique de la mer Méditerranée. Recl Trav Stn Mar Endoume 31:5-137
Pinedo S, García M, Satta MP, De Torres M, Ballesteros E (2007) Rocky-shore communities as indicators of water quality: A case study in the northwestern Mediterranean. Mar Pollut Bull 55:126-135 (Pubitemid 44794510)
Riera P, Stal LJ, Nieuwenhuize J (2000) Heavy δ15N in intertidal benthic algae and invertebrates in the Scheldt estuary (the Netherlands): Effect of river nitrogen inputs. Estuar Coast Shelf Sci 51:365-372
Segar DA, Phillips DJH, Stamnan E (1987) Strategies for longterm pollution monitoring of the coastal oceans. In: Boyle TP (ed) New approaches to monitoring aquatic ecosystems. American Society for Testing and Materials. Philadelphia, PA, p 12-27
Skliris N, Elkalay K, Goffart A, Frangoulis C, Hecq JH (2001) One-dimensional modelling of the plankton ecosystem of the north-western Corsican coastal area in relation to meteorological constraints. J Mar Syst 27:337-362 (Pubitemid 32111119)
Soltan D, Verlaque M, Boudouresque CF, Francour P (2001) Changes in macroalgal communities in the vicinity of a Mediterranean sewage outfall after the setting up of a treatment plant. Mar Pollut Bull 42:59-70 (Pubitemid 32107041)
Staal M, Thar R, Kühl M, Van Loosdrecht MCM, Wolf G, De Brouwer JFC, Rijstenbil JW (2007) Different carbon isotope fractionation patterns during the development of phototrophic freshwater and marine biofilms. Biogeosciences 4:613-626 (Pubitemid 47245246)
Steneck RS, Watling L (1982) Feeding capabilities and limitation of herbivorous molluscs: A functional group approach. Mar Biol 68:299-319
Sturaro N, Caut S, Gobert S, Bouquegneau JM, Lepoint G (2010) Trophic diversity of idoteids (Crustacea, Isopoda) inhabiting the Posidonia oceanica litter. Mar Biol 157:237-247
Sweeting CJ, Jennings S, Polunin NVC (2005) Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Funct Ecol 19:777-784 (Pubitemid 44933501)
Tewfik A, Rasmussen JB, McCann KS (2005) Anthropogenic enrichment alters a marine benthic food web. Ecology 86:2726-2736 (Pubitemid 41408068)
UNEP/FAO/WHO (1996) Assessment of the state of eutrophication in the Mediterranean sea. MAP Technical Series No. 10. United Nations Environment Programme (UNEP), Athens
Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup HH, Christoffersen K, LodgeDM(2003) From Greenland to green lakes: Cultural eutrophication and the loss of benthic energy pathways in lakes. Limnol Oceanogr 48: 1408-1418 (Pubitemid 36964761)
Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395-1404 (Pubitemid 29279940)
Velimirov B, Walenta-Simon M (1992) Seasonal changes in specific growth rates, production and biomass of a bacterial community in the water column above a Mediterranean seagrass system. Mar Ecol Prog Ser 80:237-248 (Pubitemid 23398429)
Vermeulen S (2006) Utilisation des isotopes stables du C et du N dans l'évaluation du potentiel de bioindicateur d'eutrophisation de deux gastéropodes herbivores de la zone médio-littorale en Baie de Calvi (Corse). MSc dissertation, University of Liège
Vizzini S, Mazzola A (2006) The effects of anthropogenic organic matter inputs on stable carbon and nitrogen isotopes in organisms from different trophic levels in a southern Mediterranean coastal area. Sci Total Environ 368: 723-731 (Pubitemid 44148777)
Vizzini S, Savona B, Chi TD, Mazzola A (2005) Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon. Hydrobiologia 550:73-82 (Pubitemid 41361330)
Vuorio K, Meili M, Sarvala J (2006) Taxon-specific variation in the stable isotopic signatures (δ13C and δ15N) of lake phytoplankton. Freshw Biol 51:807-822
Waldron S, Tatner P, Jack I, Arnott C (2001) The impact of sewage discharge in a marine embayment: A stable isotope reconnaissance. Estuar Coast Shelf Sci 52:111-115 (Pubitemid 32205579)
Wilmotte A, Demoulin V (1988) Studies of marine epiphytic algae, Calvi, Corsica. II. Seasonal variations in the populations of epiphytic blue-green algae in three harbours with different pollution loads. Br Phycol J 23:259-266
