, Volume 20, Issue 8, pp 1870–1880 | Cite as

Comparative toxicity of antifouling compounds on the development of sea urchin

  • Fernando Cesar Perina
  • Denis Moledo de Souza Abessa
  • Grasiela Lopes Leães Pinho
  • Gilberto Fillmann


In the present study, embryotoxicity experiments using the sea urchin Lytechinus variegatus were carried out to better clarify the ecotoxicological effects of tributyltin (TBT) and triphenyltin (TPT) (the recently banned antifouling agents), and Irgarol and Diuron (two of the new commonly used booster biocides). Organisms were individually examined to evaluate the intensity and type of effects on embryo-larval development, this procedure has not been commonly used, however it showed to be a potentially suitable approach for toxicity assessment. NOEC and LOEC were similar for compounds of same chemical class, and IC10 values were very close and showed overlapping of confidence intervals between TBT and TPT, and between Diuron and Irgarol. In addition, IC10 were similar to NOEC values. Regardless of this, the observed effects were different. Embryo development was interrupted at the gastrula and blastula stages at 1.25 and 2.5 μg l−1 of TBT, respectively, whereas pluteus stage was reached with the corresponding concentrations of TPT. Furthermore, embryos reached the prism and morula stages at 5 μg l−1 of TPT and TBT, respectively. The effects induced by Irgarol were also more pronounced than those caused by Diuron. Pluteus stage was always reached at any tested Diuron concentration, while embryogenesis was interrupted at blastula/gastrula stages at the highest concentrations of Irgarol. Therefore, this study proposes a complementary approach for interpreting embryo-larval responses that may be employed together with the traditional way of analysis. Consequently, this application leads to a more powerful ecotoxicological assessment tool focused on embryotoxicity.


Antifouling Aquatic pollutant Assessment tool Ecotoxicology Embryo-larval response Embryogenesis 



The authors would like to thank Petrobras S.A. for the infrastructure built (Research grant No. 4600224067) at CONECO Laboratory (FURG-RS), and to colleagues Ítalo Braga de Castro and Luís Alberto Echenique Dominguez for help in the chemical analyses. F. C. Perina (MSc grant No. 134170/2007-5), D. M. S. Abessa (PQ 303620/2008-0) and G. Fillmann (PQ 311459/2006-4 and 314335/2009-9) were sponsored by CNPq (Brazilian National Research Council).


  1. ABNT (2006) Ecotoxicologia aquática-Toxicidade crônica de curta duração—“Método de ensaio com ouriço-do-mar (Echinodermata: Echinoidea)”. Norma ABNT-NBR:15350:2006, Associação Brasileira de Normas Técnicas, Rio de Janeiro, 14 pGoogle Scholar
  2. Alzieu C (1998) Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast Manag 40(1):23–36CrossRefGoogle Scholar
  3. Alzieu C (2000) Impact of tributyltin on marine invertebrates. Ecotoxicology 9(1–2):71–76CrossRefGoogle Scholar
  4. ASTM (2004) Standard guide for “Conducting static acute toxicity tests with echinoid embryos”. Standard E1563:1995 (2004), ASTM International, West Conshohocken, PA, 20 pGoogle Scholar
  5. Becker Van-Slooten K, Tarradellas J (1994) Accumulation, depuration and growth effects of tributyltin in the freshwater bivalve Dreissena polymorpha under field conditions. Environ Toxicol Chem 13:755–762Google Scholar
  6. Bellas J (2008) Prediction and assessment of mixture toxicity of compounds in antifouling paints using the sea-urchin embryo-larval bioassay. Aquat Toxicol 88(4):308–315CrossRefGoogle Scholar
  7. Bellas J, Beiras R, Marino-Balsa J, Fernandez N (2005) Toxicity of organic compounds to marine invertebrate embryos and larvae: a comparison between the sea urchin embryogenesis bioassay and alternative test species. Ecotoxicology 14(3):337–353CrossRefGoogle Scholar
  8. Bresch H, Arendt U (1977) Influence of different organochlorine pesticides on the development of the sea urchin embryo. Environ Res 13(1):121–128CrossRefGoogle Scholar
  9. CETESB (1999) Água do mar—“Teste de toxicidade crônica de curta duração com Lytechinus variegatus, Lamarck, 1816”. Norma Técnica L5.250:1999, Companhia de Tecnologia e Saneamento Ambiental, São Paulo, 20 pGoogle Scholar
  10. Chambers LD, Stokes KR, Walsh FC, Wood RJK (2006) Modern approaches to marine antifouling coatings. Surf Coat Technol 201(6):3642–3652CrossRefGoogle Scholar
  11. Cima F, Ballarin L, Bressa G, Martinucci G, Burighel P (1996) Toxicity of organotin compounds on embryos of a marine invertebrate (Styela plicata; Tunicata). Ecotoxicol Environ Saf 35(2):174–182CrossRefGoogle Scholar
  12. Cornelis C, Bierkens J, Joris I, Nielsen P, Pensaert S (2006) Quality criteria for re-use of organotin-containing sediments on land. J Soils Sediments 6(3):156–162CrossRefGoogle Scholar
  13. Crane M, Newman MC (2000) What level of effect is a no observed effect? Environ Toxicol Chem 19(2):516–519CrossRefGoogle Scholar
  14. dema-Hannes R, Shenker J (2008) Acute lethal and teratogenic effects of tributyltin chloride and copper chloride on mahi mahi (Coryphaena hippurus) eggs and larvae. Environ Toxicol Chem 27(10):2131–2135CrossRefGoogle Scholar
  15. Dimitriou P, Castritsi-Catharios J, Miliou H (2003) Acute toxicity effects of tributyltin chloride and triphenyltin chloride on gilthead seabream, Sparus aurata L., embryos. Ecotoxicol Environ Saf 54(1):30–35CrossRefGoogle Scholar
  16. Downs C, Downs A (2007) Preliminary examination of short-term cellular toxicological responses of the coral Madracis mirabilis to acute irgarol 1051 exposure. Arch Environ Contam Toxicol 52(1):47–57CrossRefGoogle Scholar
  17. Drifmeyer J (1981) Urchin Lytechinus variegatus grazing on Eelgrass, Zostera marina. Estuar Coasts 4(4):374–375CrossRefGoogle Scholar
  18. Duft M, Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J (2003) Toxicity of triphenyltin and tributyltin to the freshwater mudsnail Potamopyrgus antipodarum in a new sediment biotest. Environ Toxicol Chem 22(1):145–152Google Scholar
  19. Environment Canada (1997) Biological Test Method: “Fertilization assay using echinoids (sea urchin and sand dollars)”. Report EPS1/RM/27:(1992)1997, Ottawa, Ontario, Canada, 97 pGoogle Scholar
  20. Evans SM, Birchenough AC, Brancato MS (2000) The TBT ban: out of the frying pan into the fire? Mar Pollut Bull 40(3):204–211CrossRefGoogle Scholar
  21. Fent K (1996) Ecotoxicology of organotin compounds. Crit Rev Toxicol 26(1):3–117CrossRefGoogle Scholar
  22. Fernandez-Alba AR, Hernando MD, Piedra L, Chisti Y (2002) Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal Chim Acta 456(2):303–312CrossRefGoogle Scholar
  23. Girard JP, Ferrua C, Pesando D (1997) Effects of tributyltin on Ca2+ homeostasis and mechanisms controlling cell cycling in sea urchin eggs. Aquat Toxicol 38(4):225–239CrossRefGoogle Scholar
  24. Hall LW, Giddings JM, Solomon KR, Balcomb R (1999) An ecological risk assessment for the use of Irgarol 1051 as an algaecide for antifoulant paints. Crit Rev Toxicol 29(4):367–437Google Scholar
  25. Harino H, Langston, WJ (2009) Degradation of alternative biocides in the aquatic environment. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Tokyo,Japan, pp 397–412Google Scholar
  26. Harino H, Fukushima M, Kawai S (1999) Temporal trends of organotin compounds in the aquatic environment of the Port of Osaka, Japan. Environ Pollut 105:1–7CrossRefGoogle Scholar
  27. His E, Heyvang I, Geffard O, De Montaudouin X (1999) A comparison between oyster (Crassostrea gigas) and sea urchin (Paracentrotus lividus) larval bioassays for toxicological studies. Water Res 33(7):1706–1718CrossRefGoogle Scholar
  28. Hoch M (2001) Organotin compounds in the environment—an overview. Appl Geochem 16(7–8):719–743CrossRefGoogle Scholar
  29. IMO (2008) International convention on the control of harmful anti-fouling systems on ships. Accessed 17 September 2008
  30. Isnard P, Flammarion P, Roman G, Babut M, Bastien P, Bintein S, Essermeant L, Ferard JF, Gallotti-Schmitt S, Saouter E, Saroli M, Thiebaud H, Tomassone R, Vindimian E (2001) Statistical analysis of regulatory ecotoxicity tests. Chemosphere 45(4–5):659–669CrossRefGoogle Scholar
  31. Koike I, Mukai H, Nojima S (1987) The role of the sea urchin, Tripneustes gratilla (Linnaeus), in decomposition and nutrient cycling in a tropical seagrass bed. Ecol Res 2(1):19–29CrossRefGoogle Scholar
  32. Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30(2):235–248CrossRefGoogle Scholar
  33. Kotrikla A (2009) Environmental management aspects for TBT antifouling wastes from the shipyards. J Environ Manage 90:S77–S85CrossRefGoogle Scholar
  34. Langston WJ, Harino H, Pope ND (2009) Behaviour of organotins in the coastal environment. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, New York, pp 75–94CrossRefGoogle Scholar
  35. Manzo S, Buono S, Cremisini C (2006) Toxic effects of irgarol and diuron on sea urchin Paracentrotus lividus early development, fertilization, and offspring quality. Arch Environ Con Tox 51(1):61–68CrossRefGoogle Scholar
  36. Marin MG, Moschino V, Cima F, Celli C (2000) Embryotoxicity of butyltin compounds to the sea urchin Paracentrotus lividus. Mar Environ Res 50(1–5):231–235CrossRefGoogle Scholar
  37. Mastroti RR, Sousa ECPM, Abessa DMS (2001) Toxicidade de tensoativos aniônicos sobre embriões de ouriço do mar Lytechinus variegatus. In: Moraes R, Crapez M, Pfeiffer W, Farina M, Bainy A, Teixeira V (eds) Efeitos de poluentes sobre organismos marinhos. Arte & Ciência Villipres, São Paulo, SP, pp 207–216Google Scholar
  38. Michel P, Averety B, Andral B, Chiffoleau J, Galgani F (2001) Tributiltin along the coasts of Corsica (Western Mediterranean): a persistent problem. Mar Pollut Bull 42(11):1128–1132CrossRefGoogle Scholar
  39. Mochida K, Fujii K (2009) Further effects of alternative biocides on aquatic organisms. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo,Japan, pp 383–395CrossRefGoogle Scholar
  40. Moschino V, Marin MG (2002) Spermiotoxicity and embryotoxicity of triphenyltin in the sea urchin Paracentrotus lividus Lmk. Appl Organometal Chem 16(4):175–181CrossRefGoogle Scholar
  41. Nipper MG, Prósperi VA, Zamboni AJ (1993) Toxicity testing with coastal species of southeastern Brazil—echinoderm sperm and embryos. Bull Environ Contam Toxicol 50(5):646–652CrossRefGoogle Scholar
  42. Norberg-King TJ (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (Icp) Approach version 2.0. National Effluent Toxicity Assessment Center, Environmental Research Laboratory, Duluth, MN, Technical Report 63–93 Google Scholar
  43. Pinsino A, Matranga V, Trinchella F, Roccheri MC (2010) Sea urchin embryos as an in vivo model for the assessment of manganese toxicity: developmental and stress response effects. Ecotoxicology 19(3):555–562CrossRefGoogle Scholar
  44. Piver WT (1973) Organotin compounds: industrial applications and biological investigation. Environ Health Persp 4:61–79CrossRefGoogle Scholar
  45. Raffray M, Mccarthy D, Snowden RT, Cohen GM (1993) Apoptosis as a mechanism of tributyltin cytotoxicity to thymocytes: relationship of apoptotic markers to biochemical and cellular effects. Toxicol Appl Pharm 119(1):122–130CrossRefGoogle Scholar
  46. Ranke J, Jastorff B (2000) Multidimensional risk analysis of antifouling biocides. Environ Sci Pollut Res 7(2):105–114CrossRefGoogle Scholar
  47. Ranke J, Jastorff B (2002) Risk comparison of antifouling biocides. Fresen Environ Bull 11(10A):769–772Google Scholar
  48. Reader S, Moutardier V, Denizeau F (1999) Tributyltin triggers apoptosis in trout hepatocytes: the role of Ca2+, protein kinase C and proteases. Biochim Biophys Acta (BBA)—Mol Cell Res 1448(3):473–485CrossRefGoogle Scholar
  49. Ringwood AH (1992) Comparative sensitivity of gametes and early developmental stages of a sea-urchin species (Echinometra mathaei) and a bivalve species (Isognomon californicum) during metal exposures. Arch Environ Con Toxcol 22(3):288–295Google Scholar
  50. Rüdel H (2003) Case study: bioavailability of tin and tin compounds. Ecotoxicol Environ Saf 56(1):180–189CrossRefGoogle Scholar
  51. Serafy DK (1973) Variation in the polytypic sea urchin Lytechinus Variegatus (Lamarck, 1816) in the Western Atlantic (Echinodermata; Echinoidea). Bull Mar Sci 23:525–534Google Scholar
  52. Takeuchi I, Takahashi S, Tanabe S, Miyazaki N (2004) Butyltin concentrations along the Japanese coast from 1997 to 1999 monitored by Caprella spp. (Crustacea: Amphipoda). Mar Environ Res 57(5):397–414CrossRefGoogle Scholar
  53. Thomas KV, Fileman TW, Readman JW, Waldock MJ (2001) Antifouling paint booster biocides in the UK coastal environment and potential risks of biological effects. Mar Pollut Bull 42(8):677–688CrossRefGoogle Scholar
  54. USEPA (2002) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to marine and estuarine organisms. EPA-821-R-02-014, 3rd edition, U.S. Environmental Protection Agency, Office of Water, Washington, DC, p 464Google Scholar
  55. Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD, Orth RJ, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, The Netherlands, pp 463–501CrossRefGoogle Scholar
  56. Valentine JF, Heck KL (1991) The role of sea urchin grazing in regulating subtropical seagrass meadows: evidence from field manipulations in the northern Gulf of Mexico. J Exp Mar Biol Ecol 154(2):215–230CrossRefGoogle Scholar
  57. Van der Hoeven N (2004) Current issues in statistics and models for ecotoxicological risk assessment. Acta Biotheor 52(3):201–217CrossRefGoogle Scholar
  58. Voulvoulis N, Scrimshaw MD, Lester JN (1999) Alternative antifouling biocides. Appl Organomet Chem 13(3):135–143CrossRefGoogle Scholar
  59. Watts SA, McClintock JB, Lawrence JM (2001) The ecology of Lytechinus variegatus. In: John ML (ed) Developments in aquaculture and fisheries science edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 375–393CrossRefGoogle Scholar
  60. Zhang ZB, Hu JY, Zhen HJ, Wu XQ, Huang C (2008) Reproductive inhibition and transgenerational toxicity of triphenyltin on medaka (Oryzias latipes) at environmentally relevant tip levels. Environ Sci & Technol 42(21):8133–8139CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Fernando Cesar Perina
    • 1
    • 2
  • Denis Moledo de Souza Abessa
    • 2
  • Grasiela Lopes Leães Pinho
    • 1
  • Gilberto Fillmann
    • 1
  1. 1.Laboratório de Microcontaminantes Orgânicos e Ecotoxicologia Aquática (CONECO), Instituto de OceanografiaUniversidade Federal do Rio Grande (FURG)Rio GrandeBrazil
  2. 2.Núcleo de Estudos em Poluição e Ecotoxicologia Aquática (NEPEA)Universidade Estadual Paulista (UNESP), Campus do Litoral PaulistaSão VicenteBrazil

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