Abstract
A need for environmentally acceptable alternative antifouling (AF) biocides has arisen through restrictions in the use of many common biocides in the European Union through the Biocidal Product Regulation (Regulation EU No. 528/2012). Three such alternatives are triphenylborane pyridine (TPBP), tralopyril and capsaicin. This study aims at extending the available information on the toxicity of these three emerging AF biocides to key marine invertebrates. Here we investigate the toxicity of tralopyril and capsaicin to the early life stages of the mussel Mytilus galloprovincialis and the sea urchin Paracentrotus lividus and also of tralopyril, capsaicin and TPBP to the early life stages of the copepod Tisbe battagliai. The EC50 that causes abnormal development of mussel’s D-veliger larvae and impairs the growth of sea urchin pluteus larvae are respectively 3.1 and 3.0 μg/L for tralopyril and 3,868 and 5,248 μg/L for capsaicin. Regarding the copepod T. battagliai, the LC50 was 0.9 μg/L for tralopyril, 1,252 μg/L for capsaicin and 14 μg/L for TPBP. The results obtained for the three substances are compared to a reference AF biocide, tributyltin (TBT), and their ecological risk evaluated. These compounds pose a lower environmental risk than TBT but still, our results suggest that tralopyril and TPBP may represent a considerable threat to the ecosystems.
Similar content being viewed by others
References
Angarano M-B, McMahon RF, Hawkins DL, Schetz JA (2007) Exploration of structure-antifouling relationships of capsaicin-like compounds that inhibit zebra mussel (Dreissena polymorpha) macrofouling. Biofouling 23:295–305. doi:10.1080/08927010701371439
Barroso CM, Reis-Henriques MA, Ferreira M, Gibbs PE, Moreira MH (2005) Organotin contamination, imposex and androgen/oestrogen ratios in natural populations of Nassarius reticulatus along a ship density gradient. Appl Organomet Chem 19:1141–1148. doi:10.1002/aoc.995
Beiras R, Bellas J (2008) Inhibition of embryo development of the Mytilus galloprovincialis marine mussel by organic pollutants; assessment of risk for its extensive culture in the Galician Rias. Aquaculture 277:208–212. doi:10.1016/j.aquaculture.2008.03.002
Bellas J (2008) Prediction and assessment of mixture toxicity of compounds in antifouling paints using the sea-urchin embryo-larval bioassay. Aquat Toxicol 88:308–315. doi:10.1016/j.aquatox.2008.05.011
Bellas J, Beiras R, Mario-Balsa JC, 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 14:337–353. doi:10.1007/s10646-004-6370-y
Briant N, Bancon-Montigny C, Elbaz-Poulichet F, Freydier R, Delpoux S, Cossa D (2013) Trace elements in the sediments of a large Mediterranean marina (Port Camargue, France): levels and contamination history. Mar Pollut Bull 73:78–85. doi:10.1016/j.marpolbul.2013.05.038
Cope WG, Bartsch MR, Marking LL (1997) Efficacy of candidate chemicals for preventing attachment of zebra mussels (Dreissena polymorpha). Environ Toxicol Chem 16:1930–1934. doi:10.1002/etc.5620160923
EPA—United States Environmental Protection Agency—Office of Prevention, Pesticides and Toxic Substances (1992) Capsaicin: reregistration eligibility decision (RED) fact sheet http://www.epa.gov/oppsrrd1/REDs/factsheets/4018fact.pdf. Accessed 1 Dec 2013
European Commission (2003) European Commission Technical Guidance Document on Risk Assessment in support of Commission Directive 93/67/EEC on Risk Assessment for new notified substances Commission Regulation (EC) No 1488/94 on Risk Assessment for existing substances Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market Part II available online at http://ihcp.jrc.ec.europa.eu/our_activities/public-health/risk_assessment_of_Biocides/doc/tgd/tgdpart2_2ed.pdf. Accessed 23 Mar 2014
European Commission (2012) Regulation (EU) No 528/2012 of the European Parliament and of the council of 22 May 2012 concerning the making available on the market and use of biocidal products. OJ L167, 1–123
Fent K (2006) Worldwide occurrence of organotins from antifouling paints and effects in the aquatic environment. In: Konstantinou I (ed) Antifouling paint biocides. Part O, vol 5., The handbook of environmental chemistrySpringer, Berlin, pp 71–100
Fernández N, Beiras R (2001) Combined toxicity of dissolved mercury with copper, lead and cadmium on embryogenesis and early larval growth of the Paracentrotus Lividus sea-urchin. Ecotoxicology 10:263–271. doi:10.1023/A:1016703116830
Gerigk U, Schneider U, Stewen U (1998) The present status of TBT copolymer antifouling paints versus TBT-free technology. ACS Div Environ Chem 38(1):91–94
Goldberg ED (1986) TBT: an environmental dilemma. Environ Sci Policy Sustain Dev 28:17–44. doi:10.1080/00139157.1986.9928814
Hassan AM, Juma HA (1992) Assessment of tributyltin in the marine environment of Bahrain. Mar Pollut Bull 24(8):408–410
Hayes WJ Jr (1991) Dosage and other factors influencing toxicity. In: Hayes WJ Jr, Laws ER Jr (eds) Handbook of pesticide toxicology. General principles, vol 1. Academic Press, San Diego, pp 39–105
Hazardous Substances Data Bank (HSDB) (2006), Capsaicin; U.S. Department of Health and Human Services, National Institutes of Health, National Library of Medicine: Bethesda, MD http://npic.orst.edu/factsheets/Capsaicintech.html. Accessed 10 Dec 2013
His E, Seaman M, Beiras R (1997) A simplification the bivalve embryogenesis and larval development bioassay method for water quality assessment. Water Res 31(2):351–355
IMO (1999) Focus on IMO. Anti-Fouling Systems, IMO London www.imo.org. Accessed 14 Oct 2013
ISO, 14669 (1999) International Organisation for Standardisation. Water quality—determination of acute lethal toxicity to marine copepods (Copepoda, Crustacea). ISO 14669:1999
Kaplan MB, Mooney TA, McCorkle DC, Cohen AL (2013) Adverse effects of ocean acidification on early development of squid (Doryteuthis pealeii). PLos One 8(5):e63714
Kempen T (2011). Efficacy, chemistry and environmental fate of tralopyril, a non-metal antifouling agent. European Coatings Conference “Marine Coatings III”, Berlin, 28 February 2011
Kobayashi N, Okamura H (2002) Effects of new antifouling compounds on the development of sea urchin. Mar Pollut Bull 44:748–751
Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30:235–248. doi:10.1016/s0160-4120(03)00176-4
Macken A, Giltrap M, Foley B, McGovern E, McHugh B, Davoren M (2008) A model compound study: the ecotoxicological evaluation of five organic contaminants employing a battery of marine bioassays. Environ Pollut 153(3):627–637
Macken A, Byrne HJ, Thomas KV (2012) Effects of salinity on the toxicity of ionic silver and Ag-PVP nanoparticles to Tisbe battagliai and Ceramium tenuicorne. Ecotoxicol Environ Safe 86:101–110. doi:10.1016/j.ecoenv.2012.08.025
Mochida K, Onduka T, Amano H, Ito M, Ito K, Tanaka H, Fujii K (2012) Use of species sensitivity distributions to predict no-effect concentrations of an antifouling biocide, pyridine triphenylborane, for marine organisms. Mar Pollut Bull 64:2807–2814. doi:10.1016/j.marpolbul.2012.09.007
Nyberg E, Poikane R, Strand J, Larse MM, Danielsson S, Bignert A (2003) Tributyltin (TBT) and imposex. HELCOM Core expert group for hazardous substances indicators available online at http://helcom.fi/Lists/Publications/BSEP129B.pdf. Accessed 24 Oct 2013
OECD—Environment Directorate Organization for Economic Co-operation and Development (2005) OECD series on Emission Scenario Documents: Emission Scenario Document on Antifouling Products, No. 13, 2005
Okamura H, Mieno H (2006) Present status of antifouling systems in Japan: tributyltin substitutes in Japan. In: Konstantinou I (ed) The handbook of environmental chemistry, vol 5., Antifouling paint biocides. Part OSpringer, Berlin, pp 201–212
Okamura H, Watanabe T, Aoyama I, Hasobe M (2002) Toxicity evaluation of new antifouling compounds using suspension-cultured fish cells. Chemosphere 46(7):945–951
Okamura H, Kitano S, Toyota S, Harino H, Thomas KV (2009) Ecotoxicity of the degradation products of triphenylborane pyridine (TPBP) antifouling agent. Chemosphere 74:1275–1278. doi:10.1016/j.chemosphere.2008.11.014
Onduka T, Ojima D, Ito M, Ito K, Mochida K, Fujii K (2013) Toxicity of degradation products of the antifouling biocide pyridine triphenylborane to marine organisms. Arch Environ Contam Toxicol. doi:10.1007/s00244-013-9945-x
Rial D, Beiras R, Vázquez JA, Murado MA (2010) Acute toxicity of a shoreline cleaner, cytosol, mixed with oil and ecological risk assessment of its use on the galician coast. Arch Environ Contam Toxicol 58:407–416. doi:10.1007/s00244-010-9492-7
Saco-Alvarez L, Durán I, Ignacio Lorenzo J, Beiras R (2010) Methodological basis for the optimization of a marine sea-urchin embryo test (SET) for the ecological assessment of coastal water quality. Ecotoxicol Environ Safe 73:491–499. doi: 10.1016/j.ecoenv.2010.01.018
Sousa ACA, Pastorinho, Takahashi S, Tanabe S (2014) Organotin compounds: from snails to humans. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Pollutant diseases, remediation and recycling. Environmental chemistry for a sustainable world, vol 4. Springer International Publishing, Zürich. doi:10.1007/978-3-319-02387-8_4
Stewart C, de Mora SJ (1990) A review of the degradation of tri(n-butyl)tin in the marine environment. Environ Technol 1(6):565–570. doi:10.1080/0959333900938489
Thomas KV (2001) The environmental fate and behaviour of antifouling paint booster biocides: a review. Biofouling 17:73–86
Thomas KV, Brooks S (2010) The environmental fate and effects of antifouling paint biocides. Biofouling 26:73–88. doi:10.1080/08927010903216564
Tsunemasa N, Okamura H (2011) Effects of organotin alternative antifoulants on oyster embryo. Arch Environ Contam Toxicol 61:128–134. doi:10.1007/s00244-010-9598-y
Tsunemasa N, Tsuboi A, Okamura H (2013) Effects of Organoboron Antifoulants on Oyster and Sea Urchin Embryo Development. Int J Mol Sci 14:421–433. doi:10.3390/ijms14010421
Van Hattum B, Baart A, Boon J (2006) Emission estimation and chemical fate modeling of antifoulants. In: Konstantinou IK (ed) Handbook of Environmental Chemistry, vol 5/O., Antifouling Paint BiocidesSpringer, Berlin, pp 101–120
Xu Q, Barrios C, Cutright T, Newby B (2005a) Assessment of antifouling effectiveness of two natural product antifoulants by attachment study with freshwater bacteria. Environ Sci Pollut Res 12(5):278–284. doi:10.1065/espr2005.04.244
Xu Q, Barrios CA, Cutright T, Zhang Newby B-M (2005b) Evaluation of toxicity of capsaicin and zosteric acid and their potential application as antifoulants. Environ Toxicol 20(5):467–474. doi: 10.1002/tox.20134
Zhou X, Okamura H, Nagata S (2006) Applicability of luminescent assay using fresh cells of Vibrio fischeri for toxicity evaluation. J Health Sci 52(6):811–816. doi:10.1248/jhs.52.811
Zhou X, Okamura H, Nagata S (2007) Abiotic degradation of triphenylborane pyridine (TPBP) antifouling agent in water. Chemosphere 67(10):1904–1910. doi:10.1016/j.chemosphere.2006.12.00
Acknowledgments
The authors would like to sincerely thank to Tania Tato and Nuria Sampedro, from ECIMAT Marine Station, for the assistance during the mussel and sea urchin bioassays. We would also like to thank to Ailbhe Macken for supplying the Tisbe battagliai and providing assistance in performing the copepod assay. This work was supported through a PhD grant attributed to Isabel Oliveira (SFRH/BD/71271/2010) by the Portuguese Science Foundation (FCT) funded by the POPH - QREN and co-financed by the European Social Fund and by the Portuguese national funds from MEC.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Oliveira, I.B., Beiras, R., Thomas, K.V. et al. Acute toxicity of tralopyril, capsaicin and triphenylborane pyridine to marine invertebrates. Ecotoxicology 23, 1336–1344 (2014). https://doi.org/10.1007/s10646-014-1276-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-014-1276-9