Skip to main content
Log in

Fitness Evaluation of Ruditapes philippinarum Exposed to Ni

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

In this study, long-term effects of Ni, a widespread heavy metal in the aquatic ecosystems, have been determined on growth and lethality of the clam Ruditapes philippinarum, a known bioindicator of the marine environment. Three/four-month-old bivalves have been exposed to different concentrations of Ni dissolved in synthetic seawater. Growth and lethality as endpoints after 28 days of treatment have been observed. Obtained results are the following: EC25 = 3.97 ± 0.94 and 9.45 ± 1.59 mg/L and NOEC = 1.56 and 6.25 mg/L for growth and mortality, respectively. Moreover, this study can be considered a new tool for the evaluation of fitness of bivalve clam, together with other biological responses following to the biological impacts of metal pollution.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Manfra L, Accornero A (2005) Trace metal concentrations in coastal marine waters of the central Mediterranean. Mar Pollut Bull 50(6):686–692

    Article  CAS  PubMed  Google Scholar 

  2. Torre A, Trischitta F, Faggio C (2013) Effect of CdCl2 on regulatory volume decrease (RVD) in Mytilus galloprovincialis digestive cells. Toxicol in Vitro 27:1260–1266

    Article  CAS  PubMed  Google Scholar 

  3. Soudant P, Paillard C, Choquet G, Lambert C, Reid HI, Marhic A, Donaghy L, Birkbeck TH (2004) Impact of season and rearing site on the physiological and immunological parameters of the Manila clam Venerupis (=Tapes, =Ruditapes) philippinarum. Aquaculture 229(1–4):401–418

    Article  Google Scholar 

  4. Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Polish Journal of Environmental Studies 15(3):375–382

    CAS  Google Scholar 

  5. WHO (1991) Environmental health criteria no 108, chromium. IPCS, World Health Organisation, Geneva

  6. Diagomanolin V, Farhang M, Ghazi-Khansari M, Jafarzadeh N (2004) Heavy metals (Ni, Cr, Cu) in the Karoon waterway river, Iran. Toxicol Lett 151(1):63–68

    Article  CAS  PubMed  Google Scholar 

  7. Gorbi G, Invidia M, Savorelli F, Faraponova O, Giacco E, Cigar M, Buttino I, Leoni T, Prato E, Lacchetti I, Sei S (2012) Standardized methods for acute and semi toxicity tests with the copepod Acartia tonsa. Environ Toxicol Chem 31(9):2023–2028

    Article  CAS  PubMed  Google Scholar 

  8. Mohammed EH, Wang G, Jiang J (2010) The effects of nickel on the reproductive ability of three different marine copepods. Ecotoxicology 19(5):911–916

    Article  CAS  PubMed  Google Scholar 

  9. Sei S, Invidia M, Giannetto M, Gorbi G (2016) Acartia tonsa eggs as a biomonitor to evaluate bioavailability/toxicity of persistent contaminants in anoxic/sulfidic conditions: the case of cadmium and nickel. Ecotoxicol Environ Saf 132:1–8

    Article  CAS  PubMed  Google Scholar 

  10. Hunt JW, Anderson BS, Phillips BM, Tjeerdema RS, Puckett HM, Stephenson M, Tucker WD, Watson D (2002) Acute and toxicity of nickel to marine organisms: implications for water quality criteria. Environ Toxicol Chem 21(11):2423–2430

    Article  CAS  PubMed  Google Scholar 

  11. ASTM E724-98 (2012) Standard guide for conducting static acute toxicity tests starting with embryos of four species of saltwater bivalve molluscs. ASTM International, West Conshohocken, PA, www.astm.org

  12. ASTM E2455-06 (2013) Standard guide for conducting laboratory toxicity tests with freshwater mussels. ASTM International, West Conshohocken, PA, www.astm.org

  13. ISO 17244 (2015) Water quality—determination of the toxicity of water samples on the embryo-larval development of Japanese oyster (Crassostrea gigas) and mussel (Mytilus edulis or Mytilus galloprovincialis). ISO 17244:2015, pp 24

  14. Gagné F, Blaise C, André C, Salazar M (2006) Effects of pharmaceutical products and municipal wastewaters on temperature-dependent mitochondrial electron transport activity in Elliptio complanata mussels. Comp Biochem Physiol 143:388–393

    Google Scholar 

  15. Messina CM, Faggio C, Laudicella AV, Sanfilippo M, Trischitta F, Santulli A (2014) Effect of sodium dodecyl sulfate (SDS) on stress response in the Mediterranean mussel (Mytilus galloprovincialis): regulatory volume decrease (RVD) and modulation of biochemical markers related to oxidative stress. Aquat Toxicol 157:94–100

    Article  CAS  PubMed  Google Scholar 

  16. Pagano M, Capillo G, Sanfilippo M, Palato S, Trischitta F, Manganaro A, Faggio C (2016) Evaluation of functionality and biological responses of Mytilus galloprovincialis after exposure to quaternium-15 (methenamine 3-chloroallylochloride). Molecules 21(2):E144

    Article  PubMed  Google Scholar 

  17. Byrne M (2012) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76:3–15

    Article  CAS  PubMed  Google Scholar 

  18. Stebbing AR, Akesson DB, Calabrese A, Gentile JH, Jensen A, Lloyd R (1980) The role of bioassays in marine pollution monitoring. Rapports et Proces-verbaux des Réunions Conseil International pour l'Éxploration de la Mer 179:322–332

    Google Scholar 

  19. Riba I, DelValls A, Forja JM, Gómez-Parra A (2004) The influence of pH and salinity on the toxicity of heavy metals in sediment to the estuarine clam Ruditapes philippinarum. Environ Toxicol Chem 23(5):1100–1107

    Article  CAS  PubMed  Google Scholar 

  20. Matozzo V, Marin MG (2005) Can 4-nonylphenol induce vitellogenin-like proteins in the clam Tapes philippinarum? Environ Res 97(1):43–49

    Article  CAS  PubMed  Google Scholar 

  21. Casado-Martinez MC, Blasco J, González-Castromil MA, Riba I, DelValls TA (2006) Interlaboratory assessment of marine bioassays to evaluate the environmental quality of coastal sediments in Spain V whole sediment toxicity test using juveniles of the bivalve Ruditapes philippinarum. Ciencias Marinas 32(1B):159–166

    CAS  Google Scholar 

  22. Martín-Díaz ML, Blasco J, Sales D, DelValls A (2007) Biomarkers study for sediment quality assessment in Spanish ports using the crab Carcinus maenas and the clam Ruditapes philippinarum. Arch Environ Contam Toxicol 53(1):66–76

    Article  PubMed  Google Scholar 

  23. Figueira E, Cardoso P, Freitas R (2012) Ruditapes decussatus and Ruditapes philippinarum exposed to cadmium: toxicological effects and bioaccumulation patterns. Comp Biochem Physiol 156:80–86

    CAS  Google Scholar 

  24. Tornambè A, Manfra L, Mariani L, Faraponova O, Onorati F, Savorelli F, Cicero AM, Virno Lamberti C, Magaletti E (2012) Toxicity evaluation of diethylene glycol and its combined effects with produced waters of off-shore gas platforms in the Adriatic Sea (Italy): bioassays with marine/estuarine species. Mar Environ Res 77:141–149

    Article  PubMed  Google Scholar 

  25. Manfra L, Tornambè A, Savorelli F, Rotini A, Canepa S, Mannozzi M, Cicero AM (2015) Ecotoxicity of diethylene glycol and risk assessment for marine environment. J Hazard Mater 284:130–135

    Article  CAS  PubMed  Google Scholar 

  26. Contardo-Jara V, Lorenz C, Pflugmacher S, Nutzmann G, Kloas W, Wiegand C (2011) Exposure to human pharmaceuticals carbamazepine, ibuprofen and bezafibrate causes molecular effects in Dreissena polymorpha. Aquat Toxicol 105:428–437

    Article  CAS  PubMed  Google Scholar 

  27. Matozzo V, Costa Devoti A, Marin MG (2012a) Immunotoxic effects of troclosan in the clam Ruditapes philippinarum. Ecotoxicology 21(1):66–74

    Article  CAS  PubMed  Google Scholar 

  28. Matozzo V, Formenti A, Donadello G, Marin MG (2012b) A multi-biomarker approach to assess effects of triclosan in the clam Ruditapes philippinarum. Mar Environ Res 74:40–46

    Article  CAS  PubMed  Google Scholar 

  29. Matozzo V, Rova S, Marin MG (2012c) The nonsteroidal anti-inflammatory drug, ibuprofen, affects the immune parameters in the clam Ruditapes philippinarum. Mar Environ Res 79:116–121

    Article  CAS  PubMed  Google Scholar 

  30. Aguirre-Martínez GV, Buratti S, Fabbri E, DelValls AT, Martín-Díaz ML (2013) Using lysosomal membrane stability of haemocytes in Ruditapes philippinarum as a biomarker of cellular stress to assess contamination by caffeine, ibuprofen, carbamazepine and novobiocin. J Environ Sci 25(7):1408–1418

    Article  Google Scholar 

  31. Milan M, Pauletto M, Patarnello T, Bargellonia L, Marin MG, Matozzo V (2013) Gene transcription and biomarker responses in the clam Ruditapes philippinarum after exposure to ibuprofen. Aquat Toxicol 126:17–29

    Article  CAS  PubMed  Google Scholar 

  32. Almeida A, Freitas R, Calisto V, Esteves VI, Schneider RJ, Soares AMVM, Figueira E (2015) Toxicity of the antiepileptic carbamazepine on the clam Ruditapes philippinarum. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 172-173:26–35

    CAS  Google Scholar 

  33. Xu Y, Wang WX (2002) Exposure and potential food chain transfer factor of Cd, Se and Zn in marine fish Lutjanus argentimaculatus. Mar Ecol Prog Ser 238:173–186

    Article  CAS  Google Scholar 

  34. De la Roche JP, Marín B, Freites L, Vélez A (2002) Embryonic development and larval and post-larval growth of the tropical scallop Nodipecten (= Lyropecten) nodosus (L., 1758) (Mollusca: Pectinidae). Aquac Res 33:819–827

    Article  Google Scholar 

  35. Helm MM, Bourne N (2004) Hatchery culture of bivalves. A practical manual FAO, pp 203

  36. Neves R (2004) Propagation of endangered freshwater mussels in North America. Journal of Conchology Special Publication 4:69–80

    Google Scholar 

  37. Wang N, Ingersoll CG, Greer IE, Hardesty DK, Ivey CD, Kunz JL, Brumbaugh WG, Dwyer FJ, Roberts AD, Augspurger T, Kane CM, Neves RJ, Barnhart MC (2007) Toxicity of copper and ammonia to juvenile freshwater mussels (Unionidae). Environ Toxicol Chem 26(10):2048–2056

    Article  CAS  PubMed  Google Scholar 

  38. Wang N, Ingersoll CG, Ivey CD, Hardesty DK, May TW, Augspurger T, Roberts AD, Van Genderen E, Barnhart MC (2010) Sensitivity of early life stages of freshwater mussels (Unionidae) to acute and toxicity of lead, cadmium and zinc in water. Environ Toxicol Chem 29(9):2053–2063

    CAS  PubMed  Google Scholar 

  39. US EPA (1994) Short-term methods for estimating the toxicity of effluents and receiving waters to marine and estuarine organisms EPA-600/4–91/003, Cincinnati, Ohio, USA, pp 483

  40. Centeno MD, Brendoc L, Persoone G (1993) Cyst-based toxicity tests III development and standardization of an acute toxicity test with the freshwater anostracan crustacean Streptocephalus proboscideus In: Soares AMVM, Calow P (eds) Progress in standardization of aquatic toxicity tests, Lewis Publishrs, SETAC Special Publications Series, pp 37–55

  41. Calabrese A, Macinnes JR, Nelson DA, Miller JE (1977) Survival and growth of bivalve larvae under heavy-metal stress. Mar Biol 41:179–184

    Article  CAS  Google Scholar 

  42. Hunt JW, Anderson BS, Phillips BM, Tjeerdema RS, Puckett HM, Stephenson M, Tucker DW, Watson D (2002) Chronic toxicity of nickel to marine organisms: implications for water quality criteria. Environ Toxicol Chem 21:2423–2430

    Article  CAS  PubMed  Google Scholar 

  43. Parametrix (2007) Toxicity test report submitted to Nickel Producers Environmental Research Association, Durham, NC, USA Corvallis, OR: Parametrix Inc

  44. Lussier SM, Gentile JH, Walker J (1985) Acute and chronic effects of heavy metals and cyanide on Mysidopsis bahia (Crustacea: Mysidacea). Aquat Toxicol 7:25–35

    Article  CAS  Google Scholar 

  45. Pesch CE, Hansen DJ, Boothman WS (1995) The role of acid-volatile sulfide and interstitial water metal concentrations in determining bioavailability of cadmium and nickel from contaminated sediments to the marine polychaete Neanthes arenaceodentata. Environ Toxicol Chem 14:129–141

    Article  CAS  Google Scholar 

  46. Howe PL, Reichelt-Brushett AJ, Clark MW (2014) Effects of Cd, Co, Cu, Ni and Zn on asexual reproduction and early development of the tropical sea anemone Aiptasia pulchella. Ecotox 23(9):1593–1606

    Article  CAS  Google Scholar 

  47. Golder Associates Ltd (2007) Laboratory report on: toxicity of nickel to giant kelp (Macrocysts pyrifera) and sheepshead minnow (Cyprinodon vareigatas). Testing laboratory: Golder Associated Ltd Report no: 06–1424-008

  48. Nordberg GF, Fowler BA (2014) Handbook on the toxicology of metals. Monica Nordberg Academic Press, Fourth Edition, p 1542

  49. Tamzin A, Blewett D, Scott Smith C, Wood M, Glover CN (2016) Mechanisms of nickel toxicity in the highly sensitive embryos of the sea urchin Evechinus chloroticus, and the modifying effects of natural organic matter. Environmental Science Technology 50(3):1595–1603

    Article  Google Scholar 

  50. Won EJ, Kim KT, Choi JY, Kim ES, Ra K (2016) Target organs of the Manila clam Ruditapes philippinarum for studying metal accumulation and biomarkers in pollution monitoring: laboratory and in-situ transplantation experiments. Environ Monit Assess 188(8):478. doi:10.1007/s10661-016-5485-y

    Article  PubMed  Google Scholar 

  51. Figueira E, Freitas R (2013) Consumption of Ruditapes philippinarum and Ruditapes decussatus: comparison of element accumulation and health risk. Environ Sci Pollut Res 20(8):5682–5691

    Article  CAS  Google Scholar 

  52. Bressan M, Chinellato A, Munari M, Matozzo V, Manci A, Marceta T, Finos L, Moro I, Pastore P, Badocco D, Marin MG (2014) Does seawater acidification affect survival, growth and shell integrity in bivalve juveniles? Mar Environ Res 99:136–148

    Article  CAS  PubMed  Google Scholar 

  53. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284

    Article  CAS  Google Scholar 

  54. Viganò L (1996) Metodo per la valutazione della tossicità acuta con Mysidopsis bahia. Notiziario dei Metodi Analitici IRSA, IRSA-CNR: 19–31

  55. Manfra L, Savorelli F, Pisapia M, Magaletti E, Cicero AM (2012) Long-term lethal toxicity test with the crustacean Artemia franciscana. Journal Visualized Experiments 62:2182–2185

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank Renato Palazzi (Experimental Ichthyic Center Pellestrina, Rovigo, Italy) and Edoardo Turolla (Research Centre on Molluscs, Ferrara, Italy) for their technical assistance. The authors would also like to thank Laura Bigoni and Michela De Martino for the English revision of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Manfra.

Ethics declarations

Funding

This study was funded by the Institute for Environmental Protection and Research (ISPRA, Roma, Italy) financial resources.

Conflict of Interest

The authors declare that they have no conflict of interest.

Informed Consent

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

This article does not contain any studies with human participants performed by any of the authors.

Additional information

F. S. and L. M. share equal contribution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Savorelli, F., Manfra, L., Croppo, M. et al. Fitness Evaluation of Ruditapes philippinarum Exposed to Ni. Biol Trace Elem Res 177, 384–393 (2017). https://doi.org/10.1007/s12011-016-0885-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-016-0885-y

Keywords