Skip to main content
SpringerLink
Log in

Heavy metals in five Sabellidae species (Annelida, Polychaeta): ecological implications

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The present work analyzed three hard-bottom and two soft-bottom species of sabellid polychaetes to determine the content of several heavy metals in their branchial crown and body. The highest concentrations of heavy metals were recorded in the hard-bottom species Branchiomma bairdi, a recent Mediterranean introduction. Differences in the metal concentrations were most notable in the high trace metal levels of the branchial crown for all the studied species. Statistical analysis showed that the Mediterranean hard-bottom species were similar each other in their heavy metal content in the body as well as in the branchial crown and appeared separated from all the other species. Arsenic and vanadium hyperaccumulation in the branchial crowns of the considered sabellid species probably acts as a deterrent for predation. The observed differences among the examined species were discussed not only at the light of habitat colonization but also in terms of the phylogeny.

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.

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

    Google Scholar 

  • Anderson M, Braak CT (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comput Sim 73(2):85–113

    Article  Google Scholar 

  • Anderson MJ, Robinson J (2003) Generalised discriminant analysis based on distances. Aust NZ J Stat 45:301–318

    Article  Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Ansari TM, Marr IL, Tariq N (2004) Heavy metals in marine pollution perspective—a mini review. J Appl Sci 4(1):1–20

    Article  Google Scholar 

  • Arias A, Giangrande A, Gambi MC, Anadon N (2013) Biology and new records of the invasive species Branchiomma bairdi (Annelida: Sabellidae) in the Mediterranean Sea. Medit. Mar. Sci. 14(1):162–171

    Article  Google Scholar 

  • Bocchetti R, Fattorini D, Gambi MC, Regoli F (2004) Trace metal concentrations and susceptibility to oxidative stress in the polychaete Sabella spallanzanii (Gmelin) (Sabellidae): potential role of antioxidants in revealing stressful environmental conditions in the Mediterranean. Arch Environ Con Tox 46:353–361

    Article  CAS  Google Scholar 

  • Casado-Martinez MC, Smith BD, DelValls TA, Luoma SN, Rainbow PS (2009) Biodynamic modelling and the prediction of accumulated trace metal concentrations in the polychaete Arenicola marina. Environ Pollut 157(10):2743–2750

    Article  CAS  Google Scholar 

  • Casado-Martinez MC, Smith BD, Luoma SN, Rainbow PS (2010) Metal toxicity in a sediment-dwelling polychaete: threshold body concentrations or overwhelming accumulation rates? Environ. Pollut 158(10):3071–3076

    Article  Google Scholar 

  • Chiarelli R, Roccheri MC (2014) Marine invertebrates as bioindicators of heavy metal pollution. O J Metal 4:93–106. doi:10.4236/ojmetal.2014.44011

    Article  Google Scholar 

  • Christensen M, Andersen O, Banta GT (2002) Metabolism of pyrene by the polychaete Nereis diversicolor and Arenicola marina. Aquat Toxicol 58:15–25

    Article  CAS  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke, K.R., Gorley, R.N., 2006. Primer v6. Primer-E Ltd. INVECE DI Clarke, K.R., Gorley, R.N., 2006. PRIMER V6: User Manual/Tutorial. Plymouth, UK: PRIMER-E.

  • Croteau MN, Luoma SN (2005) Delineating copper accumulation pathways for the freshwater bivalve Corbicula using stable copper isotopes. Environ Toxicol Chem 24:2871–2878

    Article  CAS  Google Scholar 

  • Dean HK (2008) The use of polychaetes (Annelida) as indicator species of marine pollution: a review. Rev Biol Trop 56(4):11–38

    Google Scholar 

  • Deudero S, Box A, March D, Valencia JM, Grau AM, Tintore J, Calvo M, Caixach J (2007) Organic compounds temporal trends at some invertebrate species from the Balearics, Western Mediterranean. Chemosphere 68(9):1650–1659

    Article  CAS  Google Scholar 

  • Driscoll SK, McElroy AE (1996) Bioaccumulation and metabolism of Benzo[a]pyrene in three species of polychaete worms. Environ Toxicol Chem 15:1401–1410

    Article  CAS  Google Scholar 

  • European Commission Regulation (2006) Commission Regulation (EC) No 1881/2006. Setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union L 364/5–24, 20.12.2006.

  • Fattorini D, Notti A, Halt MN, Gambi MC, Regoli F (2005) Levels and chemical speciation of arsenic in polychaetes: a review. Mar Ecol 26:255–264

    Article  CAS  Google Scholar 

  • Fattorini D, Notti A, Nigro M, Regoli F (2010) Hyperaccumulation of vanadium in the Antarctic polychaete Perkinsiana littoralis as a natural chemical defense against predation. Environ Science Pollut R 17(1):220–228

    Article  CAS  Google Scholar 

  • Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spallanzanii. Environ Toxicol Chem 23:1881–1887

    Article  CAS  Google Scholar 

  • Fitzhugh K (1989) A systematic revision of the Sabellidae-Caobangiidae-Sabellongidae complex (Annelida: Polychaeta). Bull Am Mus Nat Hist 192:1–104

    Google Scholar 

  • Forbes VE, Andreassen MSH, Christensen L (2001) Metabolism of the polycyclic aromatic hydrocarbon fluoranthene by the polychaete Capitella capitata species I. Environ Toxicol Chem 20:1012–1021

    Article  CAS  Google Scholar 

  • Giangrande A, Licciano M, Musco L (2005) Polychaetes as environmental indicators revisited. Mar Pollut Bull 50(11):1153–1162

    Article  CAS  Google Scholar 

  • Giangrande A, Licciano M, Schirosi R, Musco L, Stabili L (2014) Chemical and structural defensive external strategies in six sabellid worms (Annelida). Mar Ecol-Evol Persp 35:36–45

    Article  Google Scholar 

  • Graeme KA, Pollack CV (1998) Heavy metal toxicity, part I: arsenic and mercury. J Emerg Med 16:45–56

    Article  CAS  Google Scholar 

  • Ishii T, Otake T, Okoshi K, Nakahara M, Nakamura R (1994) Intracellular localization of vanadium in the fan worm Pseudopotamilla occelata. Mar Biol 121(1):143–151

    Article  CAS  Google Scholar 

  • Islam MS, Tanaka M (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar Pollut Bull 48(7):624–649

    Article  CAS  Google Scholar 

  • Kicklighter CE, Hay ME (2006) Integrating prey defensive traits: contrast of marine worms from temperate and tropical habitats. Ecol Monogr 76:195–215

    Article  Google Scholar 

  • Kicklighter CE, Hay ME (2007) To avoid or deter: interactions among defensive and escape strategies in sabellid worms. Oecologia 151:161–173

    Article  Google Scholar 

  • Licciano M, Giangrande A, Gambi MC (2002) Reproduction and simultaneous hermaphroditism in Branchiomma luctuosum (Polychaeta: Sabellidae) from Mediterranean Sea. Invert Biol 121(1):55–65

    Article  Google Scholar 

  • Licciano M, Stabili L, Giangrande A, Cavallo RA (2007) Bacterial accumulation by Branchiomma luctuosum (Annelida: Polychaeta): a tool for biomonitoring marine systems and restoring polluted waters. Mar Environ Res 63:291–302

    Article  CAS  Google Scholar 

  • Lichtenegger HC, Schöberl T, Bartl MH, Waite H, Stucky GD (2002) High abrasion resistance with sparse mineralization: copper biomineral in worm jaws. Science 298(5592):389–392

    Article  CAS  Google Scholar 

  • Linke-Gamenick I, Forbes VE, Mendez N (2000) Effects of chronic fluoranthene exposure on sibling species of Capitella with different development modes. Mar Ecol Prog Ser 203:191–203

    Article  CAS  Google Scholar 

  • Mayer-Pinto M, Junqueira AOR (2003) Effects of organic pollution on the initial development of fouling communities in a tropical bay. Brazil Mar Pollut Bull 46(11):1495–1503

    Article  CAS  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 

  • McElroy AE, Means JH (1988) Uptake, metabolism and depuration of PCBs by the polychaete Nereis virens. Aquat Toxicol 11:416–427

    Article  Google Scholar 

  • McElroy AE (1990) Polycyclic aromatic hydrocarbon metabolism in thpolychaete Nereis virens. Aquat Toxicol 18:35–50

    Article  CAS  Google Scholar 

  • Mishra VK, Tripathi BD (2009) Accumulation of chromium and zinc from aqueous solutions using water hyacinth (Eichhornia crassipes). J Hazard Mater 164(2):1059–1063

    Article  CAS  Google Scholar 

  • Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16(5):917–927

    CAS  Google Scholar 

  • Neff JM (2002) Arsenic in the ocean. In: Neff JM (ed) Bioaccumulation in marine organisms. Effect of contaminants from oil well produced water. Elsevier, Amsterdam, pp. 57–78

    Chapter  Google Scholar 

  • Nejmeddine A, Dhainaut-Courtois N, Baert JL, Sautiere P, Fournet B, Boulenguer P (1988) Purification and characterization of a cadmium-binding protein from Nereis diversicolor (Annelida, Polychaeta). Comp. Biochem. Phys. C 89(2):321–326

    Article  Google Scholar 

  • Notti A, Fattorini D, Razzetti EM, Regoli F (2007) Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii experimental observations. Environ Toxicol Chem 26(6):1186–1191

    Article  CAS  Google Scholar 

  • Pereira ME, Lillebø AI, Pato P, Válega M, Coelho JP, Lopes CB, Duarte AC (2009) Mercury pollution in Ria de Aveiro (Portugal): a review of the system assessment. Environ Monit Assess 155:39–49

    Article  CAS  Google Scholar 

  • Popham JD, d’Auria JM (1982) A new sentinel organism for vanadium and titanium. Mar Pollut Bull 13(1):25–27

    Article  CAS  Google Scholar 

  • Rainbow PS, Phillips DJH (1993) Cosmopolitan biomonitors of trace metals. Mar Pollut Bull 26:593–601

    Article  CAS  Google Scholar 

  • Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507

    Article  CAS  Google Scholar 

  • Rainbow PS (2007) Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ Int 33:576–582

    Article  CAS  Google Scholar 

  • Rainbow PS, Smith BD, Casado-Martinez MC (2011) Biodynamic modelling of the bioaccumulation of arsenic by the polychaete Nereis diversicolor. Environ Chem 8(1):1–8

    Article  CAS  Google Scholar 

  • Reidel GF, Abbe GR, Sanders JG (1995) Silver and copper accumulation in two estuarine bivalves, the eastern oyster (Crassostrea virginica) and the hooked mussel (Ischadium recurvum) in the Patuxent River estuary, Maryland. Estuaries 18(3):445–455

    Article  Google Scholar 

  • Reish DJ, LeMay JA (1991) Toxicity and bioconcentration of metals and organic compounds by polychaetes. Ophelia:653–660

  • Ricevuto E, Lanzoni I, Fattorini D, Regoli F, Gambi MC (2016) Arsenic speciation and susceptibility to oxidative stress in the fanworm Sabella spallanzanii (Gmelin) (Annelida, Sabellidae) under naturally acidified conditions: an in situ transplant experiment in a Mediterranean CO2 vent system. Sci Total Environ 544:765–773

    Article  CAS  Google Scholar 

  • Rowley AF (1983) Preliminary investigations on the possible antimicrobial properties of tunicate blood cell vanadium. J Exp Zool 227(2):319–322

    Article  CAS  Google Scholar 

  • Sandrini JZ, Regoli F, Fattorini D, Notti A, Inácio AF, Linde-Arias AR, Monserrat JM (2006) Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (Polychaeta, Nereididae): subcellular distribution and oxidative stress generation. Environ Toxicol Chem 25(5):1337–1344

    Article  CAS  Google Scholar 

  • Santovito G, Boldrin F, Irato P (2015) Metal and metallothionein distribution in different tissues of the Mediterranean clam Venerupis philippinarum during copper treatment and detoxification. Comp. Biochem. Phys. C 174:46–53

    Google Scholar 

  • Selck H, Decho AW, Forbes VE (1999) Effects of chronic metal exposure and sediment organic matter on digestive absorption efficiency of cadmium by the deposit-feeding polychaete Capitella species I. Environ Toxicol Chem 18:1289–1297

    Article  CAS  Google Scholar 

  • Spada L, Annicchiarico C, Cardellicchio N, Giandomenico S, Di Leo A (2013) Heavy metals monitoring in mussels Mytilus galloprovincialis from the Apulian coasts (Southern Italy). Medit Mar Sci 14(1):99–108

    Article  Google Scholar 

  • Stabili L, Licciano M, Lezzi M, Giangrande A (2014) Microbiological accumulation by the Mediterranean invasive alien species Branchiomma bairdi (Annelida, Sabellidae): potential tool for bioremediation. Mar Pollut Bull 86:325–331

    Article  CAS  Google Scholar 

  • Stankovic S, Jovic M (2012) Health risks of heavy metals in the mediterranean mussels as seafood. Environ Chem Lett 10(2):119–130

    Article  CAS  Google Scholar 

  • Thompson J, Bannigan J (2008) Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 25(3):304–315

    Article  CAS  Google Scholar 

  • UNEP, 1996. State of the Marine and Coastal Environment in the Mediterranean Region. MAP Technical Report Series No. 100. UNEP, Athens

  • Vandermeersch G, Lourenço H, Alvarez-Mu∼noz D, Cunha S, Diogène J, Cano-Sancho G, Sloth JJ, Kwadijk C, Barcel_O D, Allegaert W, Bekaert K, Fernandes JO, Marques A, Robbens J (2015) Environmental contaminants of emerging concern in seafood—European database on contaminant levels. Environ Res 143:29–45

    Article  CAS  Google Scholar 

  • Varol M, Şen B (2012) Assessment of nutrient and heavy metal contamination in surface water and sediments of the upper Tigris River, Turkey. Catena 92:1–10

    Article  CAS  Google Scholar 

  • Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Phys C 104(3):355–372

    Article  Google Scholar 

  • Webb DA (1939) Observations on the blood of certain ascidians, with special reference to the biochemistry of vanadium. J Exp Biol 16(4):499–523

    CAS  Google Scholar 

  • WHO (2010) Preventing disease through healthy environments - action is needed on Chemicals of Major Public Health Concern. World Health Organization, Geneva

    Google Scholar 

  • Zenetos A, Gofas S, Verlaque M, Çinar ME, Garcia Raso JE, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokoul I, Violanti D, Sfriso A, San Martin G, Giangrande A, Kataan T, Ballesteros E, Ramos Esplá A, Mastrototaro F, Ocana O, Zingone A, Gambi MC, Streftaris N (2011) Alien species in the Mediterranean Sea by 2010: a contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterranean Mar Sci 11(2):381–493

    Google Scholar 

Download references

Acknowledgements

We thank the anonymous reviewers for the time-consuming in the revision process as well as for their constructive comments which proved to be particularly useful to improve the manuscript. Thanks are due to Dr. Cataldo Pierri for the help in the field.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali (Di. S. Te. B.A.), Università del Salento, CoNISMa unit of Lecce, Via Prov. Lecce-Monteroni, 73100, Lecce, Italy

    Adriana Giangrande, Margherita Licciano, Michela del Pasqua, Francesco Paolo Fanizzi, Danilo Migoni & Loredana Stabili

  2. Istituto per l’Ambiente Marino Costiero—Sezione di Taranto—CNR, Via Roma 3, 74100, Taranto, Italy

    Loredana Stabili

Authors
  1. Adriana Giangrande
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margherita Licciano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michela del Pasqua
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesco Paolo Fanizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Danilo Migoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Loredana Stabili
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Loredana Stabili.

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

Giangrande, A., Licciano, M., del Pasqua, M. et al. Heavy metals in five Sabellidae species (Annelida, Polychaeta): ecological implications. Environ Sci Pollut Res 24, 3759–3768 (2017). https://doi.org/10.1007/s11356-016-8089-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-8089-8

Keywords

Search

Navigation