Skip to main content
SpringerLink
Log in

Food web of a confined and anthropogenically affected coastal basin (the Mar Piccolo of Taranto) revealed by carbon and nitrogen stable isotopes analyses

  • Integrated environmental characterization of the contaminated marine coastal area of Taranto, Ionian Sea (southern Italy) - the RITMARE Project
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Carbon and nitrogen stable isotope analysis was used to examine the food web of the Mar Piccolo of Taranto, a coastal basin experiencing several anthropogenic impacts. Main food sources (algal detritus, seaweeds, particulate organic matter (POM) and sediment organic matter (SOM)) and benthic and pelagic consumers were collected during two contrasting seasons (June and April), at four sites distributed over two inlets, and characterized by different level of confinements, anthropogenic inputs and the presence of mussels farming. δ13C values of organic sources revealed an important contribution of POM to both planktonic and benthic pathways, as well as the influence of terrigenous inputs within both inlets, probably due to high seasonal land runoff. Although δ13C of both sources and consumers varied little between sampling sites and dates, δ15N spatial variability was higher and clearly reflected the organic enrichment in the second inlet as well as the uptake of anthropogenically derived material by benthic consumers. On the other hand, within the first inlet, the isotopic composition of consumers did not change in response to chemical contamination. However, the impact of polluted sediments near the Navy Arsenal in the first inlet was detectable at the level of the macrobenthic trophic structure, showing high dominance of motile, upper level consumers capable to face transient conditions and the reduction of the more resident deposit feeders. We therefore underline the great potential of matching stable isotope analysis with quantitative studies of community structure to assess the effects of multiple anthropogenic stressors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alabiso G, Giacomini M, Milillo M, Ricci P (2005) The Mar Piccolo of Taranto: 8 years of chemical-physical measurements. Biol Mar Med 12(1):369–373

    Google Scholar 

  • Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for PRIMER: a guide to software and statistical methods Primer-e. Plymouth, UK

    Google Scholar 

  • Berto D, Rampazzo F, Noventa S, Cacciatore F, Gabellini M, Aubry FB, Girolimetto A, Brusà RB (2013) Stable carbon and nitrogen isotope ratios as tools to evaluate the nature of particulate organic matter in the Venice lagoon. Estuar Coast Shelf Sci 135:66–76

    Article  CAS  Google Scholar 

  • Bode A, Alvarez-Ossorio MT, Varela M (2006) Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Mar Ecol Prog Ser 318:89–102

    Article  CAS  Google Scholar 

  • Bouillon S, Borges AV, Castañeda-Moya E, Diele K, Dittmar T, Duke NC, Kristensen E, Lee SY, Marchand C, Middelburg JJ, Rivera-Monroy VH, Smith III TJ, Twilley RR (2008) Mangrove production and carbon sinks: a revision of global budget estimates. Global Biogeochemical Cycles 22. doi:10.1029/2007GB003052

  • Cardellicchio N, Buccolieri A, Giandomenico S, Lopez L, Pizzulli F, Spada L (2007) Organic pollutants (PAHs, PCBs) in sediments from the Mar Piccolo in Taranto (Ionian Sea, Southern Italy). Mar Pollut Bull 55(10–12):451–458

    Article  CAS  Google Scholar 

  • Cardellicchio N, Annicchiarico C, Di Leo A, Giandomenico S, Spada L The Mar Piccolo of Taranto: an interesting ecosystem for the study of the environmental problems This issue

  • Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Escoubeyrou K, Desmalades M, Caparros J, Grémare A (2007) A seasonal survey of the food web in the Lapalme Lagoon (northwestern Mediterranean) assessed by carbon and nitrogen stable isotope analysis. Estuar Coast Shelf Sci 73:299–315

    Article  Google Scholar 

  • Cibic T, Bongiorni L, Borfecchia F, Di Leo A, Franzo A, Giandomenico S, Karuza A, Micheli C, Rogelja M, Del Negro P. Ecosystem functioning nearby the largest steelworks in Europe and the main Italian naval base: the study case of the Mar Piccolo of Taranto This issue

  • Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560

    Article  CAS  Google Scholar 

  • Costanza R, d’Arge R, De Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’neill RV, Paruelo J (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cresson P, Ruitton S, Fontaine MF, Harmelin-Vivien ML (2012) Spatio-temporal variation of suspended and sedimentary organic matter quality in the Bay of Marseilles (NW Mediterranean) assessed by biochemical and isotopic analyses. Mar Pollut Bull 64:1112–1121

    Article  CAS  Google Scholar 

  • D’ambra I, Graham WM, Carmichael RH, Malej A, Onofri A (2013) Predation patterns and prey quality of medusae in a semi-enclosed marine lake: implications for food web energy transfer in coastal marine ecosystems. J Plankton Res 35(6):1305–1312

    Article  Google Scholar 

  • De Niro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  Google Scholar 

  • Desrosiers G, Savenkoff C, Olivier M, Stora G, Juniper K, Caron A, Gagne J, Legendre L, Mulsow S, Grant J, Roy S, Grehan A, Scaps P, Silverberg N, Klein B, Tremblay J, Therriault J (2000) Trophic structure of macrobenthos in Gulf of St Lawrence and on the Scotian Shelf. Deep Sea Res II 47:663–697

    Article  Google Scholar 

  • Dolenec T, Lojen S, Lambasa Z, Dolenec M (2006) Effects of fish farm loading on seagrass Posidonia oceanica at Vrgada Island (Central Adriatic): a nitrogen stable isotope study. Isot Environ Health Stud 42:77–85

    Article  CAS  Google Scholar 

  • Franzo A, Auriemma R, Nasi F, Vojvoda J, Pallavicini A, Cibic T, Del Negro P Benthic ecosystem functioning in the severely contaminated Mar Piccolo of Taranto (Ionian Sea, Italy): focus on heterotrophic pathways This issue

  • Fry B (2006) Stable Isotope Ecology. Springer Ed, New York, 324 p

    Book  Google Scholar 

  • Fry B, Wainright SC (1991) Diatom sources of 13C-rich carbon in marine food webs. Mar Ecol Prog Ser 76:149–157

    Article  Google Scholar 

  • Gaston GR, Rakocinski CF, Brown SS, Cleveland CM (1998) Trophic functionin estuaries: response of macrobenthos to natural and contaminant gradients. Mar Freshw Res 49:833–846

    Article  Google Scholar 

  • Grall J, Le Loc’h F, Guyonnett B, Riera P (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J Exp Mar Biol Ecol 338:1–15

    Article  CAS  Google Scholar 

  • Gray C, Baird DJ, Baumgartner S, Jacob U, Jenkins GB, O’Gorman EJ, Lu X, Ma A, Pocock MJO, Schuwirth N (2014) Ecological networks: the missing links in biomonitoring science. J Appl Ecol 51:1444–1449

    Article  Google Scholar 

  • Halpern BS, Waldbridge S, Selkoe KA, Kappel CV, Micheli F et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  CAS  Google Scholar 

  • Harmelin-Vivien M, Loizeau V, Mellon C, Beker B, Arlhac D, Bodiguel X, Ferraton F, Hermand R, Philippon X, Salen-Picard C (2008) Comparison of C and N stable isotope ratios between surface particulate organic matter and microphytoplankton in the Gulf of Lions (NW Mediterranean). Cont Shelf Res 28(15):1911–1919

    Article  Google Scholar 

  • Herry A, Diouris M, Le Pennec M (1989) Chemoautotrophic symbionts and translocation of fixed carbon from bacteria to host tissues in the littoral bivalve Loripes lucinalis (lucinidae). Mar Biol 101(3):305–312

    Article  Google Scholar 

  • Holtmann SE, Groenewold A, Schrader KHM, Asjes J, Craeymeersch JA, Duineveld GCA, van Bostelen AJ, van der Meer J (1996) Atlas of the zoobenthos of the Dutch continental shelf. Ministry of Transport, Public Works and Water Management: Rijswijk, The Netherlands, p 243

  • Iles AC, Rasmussen JB (2005) Indirect effects of metal contamination on energetics of yellow perch (Perca flavescens) resulting from food web simplification. Freshw Biol 50:976–992

    Article  CAS  Google Scholar 

  • Karuza A, Caroppo C, Cerino F, Monti M, Stabili L, Camatti E, Cibic T Planktonic trophic web in Mar Piccolo of Taranto (Ionian Sea, Italy) This issue

  • Katsanevakis S, Stelzenmüller V, South A, Sørensen TK, Jones PJS, Kerr S (2011) Ecosystem-based marine spatial management: review of concepts, policies, tools, and critical issues. Ocean Coast Manag 54:807–820

    Article  Google Scholar 

  • Krumins JA, van Oevelen D, Bezemer TM, De Deyn GB, Hol WHG, van Donk E, de Boer W, de Ruiter PC, Middelburg JJ, Monroy F et al (2013) Soil and freshwater and marine sediment food webs: their structure and function. Bioscience 63:35–42

    Article  Google Scholar 

  • Lassauque J, Lepoint G, Thibaud 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(6):843–851

    Article  CAS  Google Scholar 

  • Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562

    Article  Google Scholar 

  • Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77(4):838–846

    Article  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Science 312:1806–1809

    Article  CAS  Google Scholar 

  • Mancinelli G, Vizzini S (2015) Assessing anthropogenic pressures on coastal marine ecosystems using stable CNS isotopes: state of the art, knowledge gaps, and community-scale perspectives. Est Coast Shelf Sci 156:195–204. doi:10.1016/j.ecss.2014.11.030

  • Mateo MA, Serrano O, Serrano L, Michener RH (2008) Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157:105–115

    Article  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Morri C, Bellan-Santini D, Giaccone G, Bianchi C (2004) Principles of bionomy: definition of assemblages and use of taxonomic descriptors (macrobenthos). Biol Mar Mediterranea 11:573–600

    Google Scholar 

  • Owens NJP (1985) Variations in the natural abundance of 15N in estuarine suspended particulate matter: a specific indicator of biological processing. Estuar Coast Shelf Sci 20:505–510

    Article  CAS  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. Plos ONE 5:e9672

    Article  Google Scholar 

  • Parrott L (2010) Measuring ecological complexity. Ecol Indic 10:1069–1076

    Article  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies Annual Rev Ecol. System 18:293–320

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Pugnetti A, Acri F, Bernardi Aubry F, Camatti E, Cecere E, Facca C, Franzoi P, Keppel E, Lugliè A, Mistri M, Munari C, Padedda BM et al (2013) The Italian Long-Term Ecosystem Research (LTER-Italy) network: results, opportunities, and challenges for coastal transitional ecosystems. Transit Waters Bull 1:43–63

    Google Scholar 

  • Rakocinski CF, Brown SS, Gaston GR, Heard RW, Walker WW, Summers JK (2000) Species-abundance-biomass responses by estuarine macrobenthos to sediment chemical contamination. J Aquat Ecosyst Stress Recover 7:201–214

    Article  CAS  Google Scholar 

  • Rau GH, Teyssie JL, Rassoulzadegan F, Fowler S (1990) 13C/12C and 15N/14N variations among size-fractionated marine particles: implications for their origin and trophic relationships. Mar Ecol Prog Ser 59:33–38

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Rubino F, Cibic T, Belmonte M, Rogelja M Microbenthic community structure and trophic status of sediments in Mar Piccolo of Taranto (Mediterranean, Ionian Sea) This issue

  • Savoye N, Aminot A, Tréguer P, Fontugne M, Naulet M, Kérouel R (2003) Dynamics of particulate organic matter δ15N and δ13C during spring phytoplankton blooms in a macrotidal ecosystem (Bay of Seine, France). Mar Ecol Prog Ser 255:27–41

    Article  CAS  Google Scholar 

  • Spiro B, Greenwood PB, Southward AJ, Dando PR (1986) 13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar Ecol Prog Ser 28:233–240

    Article  CAS  Google Scholar 

  • Strong DR, Frank KT (2010) Human involvement in food webs. Annu Rev Environ Resour 35:1–23

    Article  Google Scholar 

  • Umgiesser G, Scroccaro I, Alabiso G (2007) Mass exchange mechanisms in the Taranto Sea. Transit Waters Bull 2:259–71

    Google Scholar 

  • Vafeiadou AM, Materatski P, Adão H, De Troch M, Moens T (2013) Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Mar Biol 160(9):2517–2523. doi:10.1007/s00227-013-2238-0

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Vermuelen S, Sturaro N, Gobert S, Bouquegneau JM, Lepoint G (2011) Potential early indicators of anthropogenically derived nutrients: a multiscale stable isotope analysis. Mar Ecol Prog Ser 422:9–22

    Article  Google Scholar 

  • Vizzini S, Mazzola A (2003) 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. Mar Biol 142:1009–1018

    CAS  Google Scholar 

  • Vizzini S, Mazzola A (2004) Stable isotope evidence for the environmental impact of a land-based fish farm in the western Mediterranean. Mar Pollut Bull 49:61–70

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vizzini S, Savona B, Caruso M, Savona A, Mazzola A (2005) Analysis of stable carbon and nitrogen isotopes as a tool for assessing the environmental impact of aquaculture: a case study from the western Mediterranean. Aquac Int 13:157–165

    Article  CAS  Google Scholar 

  • Yokoyama H, Tamaki A, Koyama K, Ishihi Y, Shimoda K, Harada K (2005) Isotopic evidence for phytoplankton as a major food source for macrobenthos on an intertidal sandflat in Ariake Sound, Japan. Mar Ecol Prog Ser 296:115–128

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The activities described in this publication were funded by the Project Bandiera RITMARE-La Ricerca Italiana per il Mare coordinated by the National Research Council and funded by the Ministry for Education, University and Research within the National Research Programme 2011–2013. We thank all researchers and technicians of IAMC-CNR (Taranto). In particular, we are grateful to N. Cardellicchio, C. Macripò, F. Rubino and L. Prato for technical suggestions and field assistance. We are indebted to A. Petruccelli for helping us with seagrass identification and to L. Spada for providing us fish samples.

Author information

Authors and Affiliations

  1. Istituto di Scienze Marine - Consiglio Nazionale delle Ricerche (ISMAR - CNR), Arsenale - Tesa 104, Castello 2737/F, 30122, Venezia, Italy

    Lucia Bongiorni, Federica Fiorentino, Fabrizio Bernardi Aubry, Elisa Camatti & Marco Pansera

  2. OGS (Istituto Nazionale di Oceanografia e Geofisica Sperimentale di Oceanografia), Sezione Oceanografia, Via A. Piccard 54, 34151, Trieste, Italy

    Rocco Auriemma & Federica Nasi

  3. Piattaforma Isotopi Stabili e Tracciabilità, Dipartimento Qualità Alimentare e Nutrizione, Fondazione E. Mach - Istituto Agrario di San Michele all’Adige, Via Mach 1, 38010 San Michele all’Adige, Trento, Italy

    Federica Camin & Luca Ziller

  4. Observatoire, Séries Faune-Flore, UMS 3113 CNRS, Institut Universitaire Européen de la Mer, rue Dumont d’Urville, 29280, Plouzané, France

    Jacques Grall

Authors
  1. Lucia Bongiorni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Federica Fiorentino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rocco Auriemma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabrizio Bernardi Aubry
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elisa Camatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Federica Camin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Federica Nasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marco Pansera
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luca Ziller
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jacques Grall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucia Bongiorni.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bongiorni, L., Fiorentino, F., Auriemma, R. et al. Food web of a confined and anthropogenically affected coastal basin (the Mar Piccolo of Taranto) revealed by carbon and nitrogen stable isotopes analyses. Environ Sci Pollut Res 23, 12725–12738 (2016). https://doi.org/10.1007/s11356-015-5380-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5380-z

Keywords

Search

Navigation