Skip to main content
SpringerLink
Log in

Effects of exposure to ED contaminants (TPT-Cl and Fenarimol) on crinoid echinoderms: comparative analysis of regenerative development and correlated steroid levels

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Regenerative phenomena reproduce developmental processes in adult organisms and are regulated by neuro-endocrine mechanisms. They can therefore provide sensitive tests for monitoring the effects of exposure to endocrine disrupter contaminants (EDs) which can be bioaccumulated by the organisms causing dysfunctions in steroid hormone metabolism and activities and affecting reproduction and development. Echinoderms are prime candidates for this new ecotoxicological approach, since (1) they offer unique models to study physiological regenerative processes and (2) in echinoderms vertebrate-type steroids can be synthesized and used as terminal hormones along the neuro-endocrine cascades regulating reproductive, growth and developmental processes. We are currently exploring the effects on the regenerative potential of echinoderms of different classes of compounds that are well known to have ED activity. The present paper focuses on the possible effects of well-known compounds with suspected androgenic activity such as TPT-Cl (Triphenyltin-chloride) and Fenarimol [(±)-2,4-dichloro-α-(pyrimidin-5-yl) benzhydryl alcohol]. The selected test-species is the crinoid Antedon mediterranea, a tractable and sensitive benthic filter-feeding species which represents a valuable experimental model for investigation on the regenerative process from the macroscopic to the molecular level. The present investigation employs an integrated approach which combines exposure experiments and biological analysis utilizing microscopy, immunocytochemistry and biochemistry. The experiments were carried out on experimentally induced arm regenerations in semistatic controlled conditions with exposure concentrations comparable to those of moderately polluted coastal zones. The bulk of results obtained so far provide indications of significant sublethal effects from exposure to TPT-Cl and Fenarimol and mechanisms of toxicity related to developmental physiology, which are associated with variations in steroid levels in the animal tissues. The results indicate that these two substances (1) affect growth and development by interfering with the same basic cellular mechanisms of regeneration, such as cell proliferation, migration and differentiation/dedifferentiation, which are possibly controlled by steroid hormones; and (2) can induce a number of significant modifications in the timing, modalities and pattern of arm regeneration, which may involve the activation of cell mechanisms related to steroid synthesis/metabolism.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aminin DL, Agafonova IG, Federov SN (1995) Biological activity of disulfated polyhydroxysterids from the Pacific brittle star Ophiopholis aculeata. Comp Biochem Physiol 112(C):201–204

    CAS  Google Scholar 

  • Anderson S, Hose JE, Knezovic JP (1994) Genotoxic and developmental effects in sea urchin are sensitive indicators of effects genotoxic chemicals. Environ Toxicol Chem 13:1033–1041

    Article  CAS  Google Scholar 

  • Andersen HR, Vinggard AM, Rasmussen TH, Gjermandsen IM, Bonefeld-Jørgensen EC (2002) Effects of currently used pesticides in assays for estrogenicity, androgenicity and aromatase activity in vitro. Toxicol Appl Pharmacol 179:1–12

    Article  CAS  Google Scholar 

  • Barbaglio A, Sugni M, Mozzi D, Invernizzi A, Doria A, Pacchetti G, Tremolada P, Bonasoro F, Candia Carnevali MD (2004) Exposure effects of organotin compounds (TPT-Cl) on regenerative potential of crinoids. In: Heinzeller, Nebelsick (eds) Echinoderms. Munchen Taylor & Francis Group, London, pp 91–95

    Google Scholar 

  • Békri K, Pelletier E (2004) Trophic transfer and in vivo immunitoxicological effects of tributyltin (TBT) in polar seastar Leptasterias polaris. Aquat Toxicol 66:39–53

    Article  Google Scholar 

  • Bell G (1994) Rubigan 12 EC (EAF 457) acute toxicity to Daphnia magna. DowElanco Company report

  • Bryan GW, Gibbs PE, Hummerstone LG, Burt GR (1986) The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Ass UK 66:611–640

    Article  CAS  Google Scholar 

  • Cadbury D (1998) The feminisation of nature. Our future at risk. Penguin Books, London

    Google Scholar 

  • Candia Carnevali MD (2005) Regenerative response and Endocrine Disrupters in Crinoid Echinoderms: an old experimental model, a new ecotoxicological test. In: Matranga V (ed) Echinodermata. Progress in molecular and subcellular biology. vol 39. Subseries marine molecular biotechnology. Springer, Berlin Heidelberg New York, pp 187–198

  • Candia Carnevali MD, Bonasoro F (2001) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426

    Article  CAS  Google Scholar 

  • Candia Carnevali MD, Lucca E, Bonasoro F (1993) Mechanism of arm regeneration in the feather star Antedon mediterranea: healing of wound and early stages of development. J Exp Zool 267:299–317

    Article  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Lucca E, Thorndyke MC (1995) Pattern of cell proliferation in the feather star Antedon mediterranea. J Exp Zool 272:464–474

    Article  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Biale A (1997) Pattern of bromodeoxyuridine incorporation in the advanced stages of arm regeneration in the feather star Antedon mediterranea. Cell Tissue Res 289:363–374

    Article  CAS  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC, Galassi S (2001a) PCB exposure and regeneration in crinoids (Echinodermata). Mar Ecol Prog Ser 215:155–167

    Article  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC (2001b). Role of the nervous system in echinoderm regeneration. In: Barker M (ed), Echinoderm 2000: Proceedings of 10th international echinoderm conference, Dunedin 2000, Balkema, Rotterdam, pp 5–20

  • Candia Carnevali MD, Galassi S, Bonasoro F, Patruno M, Thorndyke MC (2001c) Regenerative response and endocrine disrupters in crinoid echinoderms: arm regeneration in Antedon mediterranea after experimental exposure to polychlorinated biphenyls. J Exp Biol 204:835–842

    CAS  Google Scholar 

  • Candia Carnevali MD, Bonasoro F, Ferreri P, Galassi S (2003) Regenerative potential and effects of exposure to pseudo-estrogenic contaminants (4-nonylphenol) in the crinoid Antedon mediterranea. In: Feral JP (ed) Echinoderm research 2001. Balkema, Rotterdam, pp 201–207

    Google Scholar 

  • Caricchia AM, Chiavarini S, Cremisini C, Fantini M, Morabito R (1992) Monitoring of organotins in the La Spezia Gulf – II. Results of the 1990 sampling campaigns and concluding remarks. Sci Total Environ 121:133–144

    Article  CAS  Google Scholar 

  • 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 35:174–182

    Article  CAS  Google Scholar 

  • Colborn T, von Saal FS, Soto AM (1993) Developmental effects of endocrine disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378–384

    Article  CAS  Google Scholar 

  • Cooper RL, Kavlock RJ (1997) Endocrine disruptors and reproductive development: a weight-of-evidence overview. J Endocrinol 152:159–166

    Article  CAS  Google Scholar 

  • Coteur G, Danis B, Fowler SW, Teyssié J-L, Dubois Ph, Warnau M (2001) Effects of PCBs on reactive oxygen species (ROS) production by the immune cells of Paracentrotus lividus (Echinodermata). Mar Pollut Bull 42:667–672

    Article  CAS  Google Scholar 

  • D’Andrea AF, Stancyk S, Chandler GT (1996) Sublethal effects of cadmium on arm regeneration in the burrowing brittlerstars, Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Ecotoxicology 5:115–133

    Article  Google Scholar 

  • Degen GH, Botl HM (2000) Endocrine disruptors: update on xenoestrogens. Int Arch Occup Environ Health 73:433–441

    Article  CAS  Google Scholar 

  • den Besten PJ (1998) Cytochrome P450 monooxygenase system in echinoderms. Comp Biochem Physiol 121(C):139–146

    Google Scholar 

  • den Besten PJ, Herwig HJ, Zandee DI, Voogt PA (1989) Effects of cadmium and PCBs on reproduction of the sea star Asterias rubens: aberrations in the early development. Ecotoxicol Environ Saf 18:173–180

    Article  Google Scholar 

  • den Besten PJ, Herwig HJ, Smaal AC, Zandee DI, Voogt PA (1990) Interference of polychlorinated biphenyls (Clophen A50) with gametogenesis in the sea star Asterias rubens L. Aquat Toxicol 18:231–246

    Article  Google Scholar 

  • den Besten PJ, Elenbaas JM, Maas EJR, Dielman SJ, Herwig HJ, Voogt PA (1991a) Effects of cadmium and polychlorinated biphenyls (Clophen A50) on steroid metabolism and cytochrome P-450 monooxygenase system in the sea star Asterias rubens L. Aquat Toxicol 20:95–110

    Article  Google Scholar 

  • den Besten PJ, Mass JR, Livingstone DR, Zandee DI, Voogt PA (1991b) Interference of benzo[α]pyrene with cytochrome P450 mediated steroid metabolism in pyloric caeca microsomes of the sea star Asterias rubens L. Comp Biochem Physiol 100(C):165–168

    Google Scholar 

  • Depledge MH, Billinghurst Z (1999) Ecological significance of endocrine disruption in marine invertebrates. Mar Pollut Bull 39:32–38

    Article  CAS  Google Scholar 

  • Dieleman SJ, Schoenmakers HNJ (1979) Radioimmunoassay to determine the presence of progesterone and estrone in starfish Asterias rubens. Gen Comp Endocrinol 39:534–542

    Article  CAS  Google Scholar 

  • EEC (1967) Council Directive 67/548/EEC on the approximation of laws, regulations and administrative provisions relating to the classification, packaging and labelling of dangerous substances. Official Journal of the European Communities, Luxemborg, 196, p.1

  • Fairley P, Roberts M, Stringer J (1996). Endocrine disruptor. Chem Week May 8:29–36

    Google Scholar 

  • Fait A, Ferioli A, Barbieri F (1994) Organotin compounds. Toxicology 91:77–82

    Article  CAS  Google Scholar 

  • Federoff NE, Young D, Cowles J, Spatz D, Shamin M (1999) TPTH. Environmental fate and ecological risk assessment. United States Environmental Protection Agency, Washington DC

    Google Scholar 

  • Fitox (1999) Database on physical, chemical and ecotoxicological properties of pesticides. In: Finizio A (ed) Environmental impact of pesticides: risk evaluation for non-target organism. Ampa n 1 Roma

  • Gibbs PE, Pascoe PL, Burt GR (1988) Sex changes in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Ass UK 68:715–731

    Article  Google Scholar 

  • Gray LE Jr, Monosson E, Kelce WR (1996) Emerging issues: the effects of endocrine disrupters on reproductive development. In: Di Giulio RT, Monosson E (eds) Interconnection between human and ecosystem health. Chapman & Hall, London, pp 47–81

    Google Scholar 

  • Heinzeller T, Welsch U (1994) Crinoidea. In: Harrison F (ed) Microscopic anatomy of invertebrates: Echinodermata, vol 14. Wiley-Liss, New York, pp 9–148

  • Hines GA, Watts SA, McClintock JB (1994) Biosynthesis of estrogen derivatives in the echinoid Lytechinus variegates Lamark. In: David, Guille, Féral, Roux (eds) Echinoderms through time. Balkema, Rotterdam, pp 711–716

    Google Scholar 

  • Hoffman DG, Grothe DW, Francis PC (1987) Chronic toxicity of fenarimol to Daphnia magna in a static renewal life cycle test. DowElanco Company report

  • Horiguchi T, Shiraishi H, Shimizu M, Morita M (1995) Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from antifouling paints. Mar Pollut Bull 31:402–405

    Article  CAS  Google Scholar 

  • IPCS (2004) (International programme on chemical safety), by World Health Organization, United Nations Environmental Programme, International Labour Organization, http://www.inchem.org

  • Jackson R, Lewis C (1994) The degradation and retention of 14C Fenarimol in water-sediment systems. DowElanco Company report

  • Janer G, LeBlanc GA, Porte C (2004) A comparative study on the metabolism of androgens in invertebrates and its modulation by xenoandrogens. In: Proceedings of CREDO cluster workshop on ecological relevance of chemically induced endocrine disruption in wildlife, p 23

  • Kline RM, Knox JW (1981) Fenarimol: Interactions with sewage microorganism. DowElanco Company report

  • Kabayashi N (1984) Marine ecotoxicological testing with Echinoderms. In: Persoone G, Jaspers F, Claus C (eds) Ecotoxicological testing for the marine environment. Vol.I, State University of Ghent and Institute of Marine Scientific Research, Bredene, Belgium, pp 341–405

  • LeBlanc GA, Campbell PM, den Besten P, Brown RP, Chang ES, Coats JR, De Fur PL, Dhadialla T, Edwards J, Riddiford Lm, Simpson MG, Snell TW, Thorndyke MC, Matsumura F (1999) The endocrinology of invertebrates. In: deFur P, Crane M, Ingersoll C, Tattersfield L (eds) Endocrine dirsruption in invertebrates: endocrinology, testing and assessment. Workshop on endocrine disruption in invertebrates: endocrinology, testing and assessment: 1998 Dec 12–15. SETAC Noordwijkerhout, The Netherlands, pp 23–106

    Google Scholar 

  • Lorenzo J (2003) A new hypothesis for how sex steroid hormones regulate bone mass. J Clin Invest 111:1641–1643

    Article  CAS  Google Scholar 

  • Lutz I, Sugni M, Candia Carnevali MD, Lavado R, Porte C, Schulte-Oehlmann U, Kloas W (2004) First evidence for specific [3H]-testosterone and [3H]-estradiol binding sites in echinoderms. In: Proceedings of CREDO cluster workshop on ecological relevance of chemically induced endocrine disruption in wildlife, p 43

  • Mackay D, Shiu WY, Ma KC (1997) Illustrated handbook of physical-chemical properties and environmental fate for organic chemicals. vol 5, Lewis Publishers, New York, p 812

  • Marsh A, Walker C (1995) Effect of estradiol and progesterone on c-myc expression in the sea star testis and the seasonal regulation of spermatogenesis. Mol Reprod Dev 40:62–68

    Article  CAS  Google Scholar 

  • Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17(1):37–43

    Article  CAS  Google Scholar 

  • Moschino V, Marin M (2002) Spermiotoxicity and embriotoxicity of triphenyltin in the sea urchin Paracentrotus lividus Lmk. Appl Organomet Chem 16:175–181

    Article  CAS  Google Scholar 

  • Mu XY, LeBlanc GA (2002) Environmental antiecdysteroids alter embryo development in the crustacean Daphnia magna. J Exp Zool 292(3):287–292

    Article  CAS  Google Scholar 

  • Novelli AA, Argese E, Tagliapietra D, Bettiol C, Volpi Ghirardini A (2002) Toxicity of tributyltin and triphenyltin to early life-stages of Paracentrotus lividus (Echinodermata: Echinoidea). Environ Toxicol Chem 21:859–864

    Article  CAS  Google Scholar 

  • Powers MF, Beavis AD (1991) Triorganotins inhibit the mitochondrial inner membrane anion channel. J Biol Chem 266(26):17250–17256

    CAS  PubMed  Google Scholar 

  • Rippen G (ed) (1990) Handbuch Umweltechemikalien. Stoffdaten, Pfüfverfahren, Vorschirften. 3. Auflage, 5. Ergänzungslieferung 2/90. Ecomed, Landsberg am Lech

  • Schoenmakers HJN (1979) In vitro biosynthesis of steroids from cholesterol by the ovaries and pyloric caeca of the starfish Asterias rubens. Comp Biochem Physiol (B) 63:179–184

    Google Scholar 

  • Schoenmakers HJN (1980) The variation of 3ß-hydroxysteroid dehydrogenase activity of the ovaries and pyloric caeca of the starfish Asterias rubens during the annual reproductive cycle. J Comp Physiol 138:27–30

    Article  CAS  Google Scholar 

  • Schoenmakers HJN, Voogt PA (1980) In vitro biosynthesis of steroids from progesterone by the ovaries and pyloric caeca of the starfish Asterias rubens. Gen Comp Endocrinol 41:408–416

    Article  CAS  Google Scholar 

  • Shirai H, Walker CW (1988) Chemical control of asexual and sexual reproduction in echinoderms. Alan R Liss Inc, New York

    Google Scholar 

  • Shubina LK, Fedorov SN, Levina EV, Andriyaschenko PV, Kalinovsky AI, Stonik VA, Smirnov IS (1998) Comparative study on polyhydroxylated steroids from echinoderms. Comp Biochem Physiol 119(B):505–511

    Article  Google Scholar 

  • Smith AB (1990) Biomineralization in Echinoderms. In: Carler JG (ed) Skeletal biomineralization: patterns, processes and evolutionary trends. vol I, pp 413–435

    Chapter  Google Scholar 

  • Smith DF, Meyer DL, Horner SMJ (1981) Amino acid uptake by the comatulid crinoid Cenometra bella (Echinodermata) following evisceration. Mar Biol 61:207–213

    Article  Google Scholar 

  • Soto AM, Sonnenschein C, Chung KL (1995) The E-Screen as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ Health Perspect 103(Suppl):113–122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorndyke MC, Candia Carnevali MD (2001) Regeneration and neurohormones and growth factors in echinoderms. Can J Zool 79:1171–1208

    Article  CAS  Google Scholar 

  • Tolosa I, Readman JW, Blaevoet A, Ghilini S, Bartocci J, Horvat M (1996) Contamination of Mediterranean (Côte d’Azur) coastal waters by organotins and Irgarol 1051 used in antifouling paints. Mar Pollut Bull 32:335–341

    Article  CAS  Google Scholar 

  • Tremolada P, Bristeau S, Mozzi D, Sugni M, Barbaglio A, Dagnac T, Candia Carnevali MD (2005) A simple model to predict compound loss processes in aquatic ecotoxicological tests: calculated and measured TPT-Cl levels in water and biota. Int J Env Anal Chem 86:171–184

    Article  Google Scholar 

  • Voogt PA, Oudejans RCHM, Broertjes JJS (1984) Steroids and reproduction in starfish. In: Engels W, Clark WH, Fischer A, Olive PJM, Went DF (eds) Advances in invertebrate reproduction. Elsevier North-Holland Inc, New York, pp 151–161

    Google Scholar 

  • Voogt PA, den Besten PJ, Jansen M (1990) The Δ5 –pathway in steroid metabolism in the sea star Asterias rubens L. Comp Biochem Physiol 97(B):555–562

    Google Scholar 

  • Voogt PA, den Besten PJ, Jansen M (1991) Steroid metabolism in relation to the reproductive cycle in Asterias rubens L. Comp Biochem Physiol 99(B):77–82

    Google Scholar 

  • Walsh GE, McLaughlin LL, Louie MK, Deans CH, Lores EM (1986) Inhibition of arm regeneration by Ophioderma brevispina (Echinodermata, Ophiuroidea) by tributyltin oxide and triphenyltin oxide. Ecotoxicol Environ Saf 12:95–100

    Article  CAS  Google Scholar 

  • Yallapragada PR, Vig PJS, Desaiah D (1990) Differential effects of triorganotins on calmodulin activity. J Toxicol Environ Health 29:317–327

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The present work has received financial support from the EU (COMPRENDO Project n° EVK1-CT-2002-00129). The authors are particularly grateful to Dr Ulrike Shulte-Oehlmann for her valuable coordinating activity and to all the partners of the COMPRENDO project for their direct or indirect support and advice. Special thanks are addressed to Drs Simona Ceriani and Angelita Doria for their valuable help and technical assistance. All the experiments carried out for the research work are in accord with the current laws of our country. The authors are grateful to the anonymous reviewers for their invaluable suggestions and careful revision of the manuscript.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia, Università degli Studi di Milano, Via Celoria 26, 20133, Milano, Italy

    Alice Barbaglio, Daniela Mozzi, Michela Sugni, Paolo Tremolada, Francesco Bonasoro & M. Daniela Candia Carnevali

  2. Environmental Chemistry Department, IIQAB-CSIC, C/ Jordi Girona, 18, 08034, Barcelona, Spain

    Ramon Lavado & Cinta Porte

Authors
  1. Alice Barbaglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniela Mozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michela Sugni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paolo Tremolada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesco Bonasoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ramon Lavado
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cinta Porte
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M. Daniela Candia Carnevali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Daniela Candia Carnevali.

Additional information

Communicated by R. Cattaneo-Vietti, Genova

Physical and Chemical Impacts on Marine Organisms, a Bilateral Seminar Italy-Japan held in November 2004

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbaglio, A., Mozzi, D., Sugni, M. et al. Effects of exposure to ED contaminants (TPT-Cl and Fenarimol) on crinoid echinoderms: comparative analysis of regenerative development and correlated steroid levels. Marine Biology 149, 65–77 (2006). https://doi.org/10.1007/s00227-005-0205-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0205-0

Keywords

Search

Navigation