Skip to main content
Log in

Dose-dependent effects of chlorpyriphos, an organophosphate pesticide, on metamorphosis of the sea urchin, Paracentrotus lividus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The effect of exposures to the insecticide chlorpyrifos on the larval stages of Paracentrotus lividus (Echinodermata, Euechinoidea) up to metamorphosis was investigated with the aim to identify novel risk biomarkers and a new promising model for toxicity tests. The planktonic sea urchin larvae have the ability to undergo a variable exploratory period, up to the choice of a suitable substrate for adult benthonic life. The juvenile bud (called rudiment) is built inside the larval body that, on environmental cues represented by a variety of signal molecules, is reabsorbed by apoptosis and releases the juvenile on the substrate. In this dialogue between larvae and environment, contaminants interfere with the signals reception, and may alter in dose-dependent way the correct regulation of environment-larva-rudiment interaction. Such interaction is shown by larval plasticity, i.e. the ability of the larva to change body proportions according to the environmental conditions. When exposed to low doses of chlorpyriphos (10−7 to 10−10 M) since 2-days after fertilization, the larvae showed altered size and shape, but all reached the metamorphosis at the same time as controls, and in the same percentage. Exposures to high concentrations such as 10−4 to 10−6 M since 2-days after fertilization did not allow larval growth and differentiation. Exposures at later stages caused reabsorption of larval structures within a few hours and precocious release of the immature rudiments, followed by death of the juveniles. Although the mechanism of chlorpyriphos toxicity in sea urchin larvae is still rather unclear, the measurable stress biomarkers can constitute the basis for new toxicity tests.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agnello M, Filosto S, Scudiero R, Rinaldi AM, Roccheri MC (2007) Cadmium induces an apoptotic response in sea urchin embryos. Cell Stress Chaperones 12(1):44–50

    Article  CAS  Google Scholar 

  • Aluigi MG, Sgro M, Franzoni M, Angelici C, Gallus L, Falugi C (2006) Metamorphosis of the sea urchin. A multi-signal endocrine regulated event. CREDO cluster of research into endocrine disruption in Europe, issue 6 www.credocluster.info July 2006, pp 6–7

  • Aluigi MG, Angelini C, Corte G, Falugi C (2008) The sea urchin, Paracentrotus lividus, embryo as a “bioethical” model for neurodevelopmental toxicity testing: effects of diazinon on the intracellular distribution of OTX2-like proteins. Cell Biol Toxicol 24(6):587–601

    Article  CAS  Google Scholar 

  • Burke RD (1978) The structure of the nervous system of the pluteus larva of Strongylocentrotus purpuratus. Cell Tissue Res 191(2):233–247

    Article  CAS  Google Scholar 

  • Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T, Liang S, Mu X, Agca C, Klein WH, Brandhorst BP, Rowe M, Wilson K, Churcher AM, Taylor JS, Chen N, Murray G, Wang D, Mellott D, Olinski R, Hallböök F, Thorndyke MCA (2006) Genomic view of the sea urchin nervous system. Dev Biol 300(1):434–460

    Article  CAS  Google Scholar 

  • Buznikov GA, Nikitina LA, Bezuglov VV, Lauder JM, Padilla S, Slotkin TA (2001) An invertebrate model of the developmental neurotoxicity of insecticides: effects of chlorpyrifos and dieldrin in sea urchin embryos and larvae. Environ Health Perspect 109(7):651–661

    Article  CAS  Google Scholar 

  • Casida JE, Quistad GB (2004) Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chem Res Toxicol 17:983–998

    Article  CAS  Google Scholar 

  • Coniglio L, Morale A, Angelini C, Falugi C (1998) Cholinergic activation of settlement in Ciona intestinalis metamorphosing larvae. J Exp Zool 280:314–320

    Article  CAS  Google Scholar 

  • Drews U (1975) Cholinesterase in embryonic development. Prog Histochem Cytochem 7(3):1–52

    CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Faimali M, Falugi C, Gallus L, Piazza V, Tagliafierro G (2003) Involvement of acetylcholine in settlement process of Balanus amphitrite. Biofouling 19(Suppl):213–220

    Article  CAS  Google Scholar 

  • Falugi C (1993) Localization and possible role of molecules associated with the cholinergic system during “non-nervous” developmental events. Eur J Histochem 37(4):287–294

    CAS  Google Scholar 

  • Falugi C, Angelini C (2002) Sea urchin development from the egg to metamorphosis: an integrated model for cell-to-cell and environment interaction. In: Yokota Y, Matranga V, Smolenicka Z (eds) The sea urchin. From basic biology to aquaculture. Balkema Publication, Lisse, pp 73–94

    Google Scholar 

  • Falugi C, Lammerding-Koppel M, Aluigi MG (2008) Sea urchin development: an alternative model for mechanistic understanding of neurodevelopment and neurotoxicity. Birth Defects Res C Embryo Today 84(3):188–203

    Article  CAS  Google Scholar 

  • Fenaux L, Cellario C, Rassoulzadegan F (1988) Sensitivity of different morphological stages of the larva of Paracentrotus lividus (Lamarck) to quantity and quality of food. In: Burke D, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology. A.A. Balkema, Rotterdam, pp 259–266

    Google Scholar 

  • Fenaux L, Strathmann MF, Strathmann RR (1994) Five tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnol Oceanogr 39:84–98

    Article  Google Scholar 

  • Filosto S, Roccheri MC, Bonaventura R, Matranga V (2008) Environmentally relevant cadmium concentrations affect development and induce apoptosis of Paracentrotus lividus larvae cultured in vitro. Cell Biol Toxicol 24(6):603–610

    Article  CAS  Google Scholar 

  • Karnovsky MJ, Roots L (1964) A ‘‘direct colouring’’ thiocholine method for cholinesterase. J Histochem Cytochem 12:219–221

    CAS  Google Scholar 

  • Meshorer E, Soreq H (2006) Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends Neurosci 29(4):216–224

    Article  CAS  Google Scholar 

  • Miller BA, Emlet RB (1997) The influence of nearshore hydrodynamics on larval abundance and settlement of the sea urchins Strongylocentrotus franciscanus and S. purpuratus in the Oregon upwelling zone. Mar Ecol Prog Ser 148:83–94

    Article  Google Scholar 

  • Minchinton TE, Scheibling RE (1991) The influence of larval supply and settlement on the population structure of barnacles. Ecology 72:1867–1879

    Article  Google Scholar 

  • Minganti A, Falugi C (1980) An epithelial localization of acetylcholinesterase in the ascidian, Ciona intestinalis, embryos and larvae. Acta Embryol Morphol Exp 1:143–155

    CAS  Google Scholar 

  • Morse DE (1993) Signalling in planktonic larvae. Nature 363:406

    Article  Google Scholar 

  • Pedrotti ML (1995) Food selection (size and flavor) during development of echinoderm larvae. Invertebr Reprod Dev 27:29–39. (Invertebrate reproduction & development ISSN 0792-4259) Cote INIST: 18005, 35400005599981.0040) publisher: Balaban

  • Pedrotti ML, Fenaux L (1993) Effects of food diet on the survival, development and growth rates of two cultured echinoplutei (Paracentrotus lividus and Arbacia lixula). Invertebr Reprod Dev 24:59–70. (ISSN 0792-4259Cote INIST : 18005, 35400004839164.0080) (publisher: Balaban)

  • Perry C, Soreq H (2006) ACHE gene expression in human brain tumors involves alternative splicing and CREB-induced proliferative signals. Isr Med Assoc J 8(5):364–5

    Google Scholar 

  • Piomboni P, Baccetti B, Moretti E, Gambera L, Angelini C, Falugi C (2001) Localization of molecules related to cholinergic signaling in eggs and zygotes of the sea urchin, Paracentrotus lividus. J Submicrosc Cytol Pathol 33(1–2):187–193

    CAS  Google Scholar 

  • Rakonczay Z, Falugi C, Layer P, Genever P, Thielecke H, Nagy K (2009) In vitro inhibition of acetyl and butyrylcholinesterases by carbamates, organophosphates and their derivatives in different invertebrate and vertebrate tissues, including human. 10th International meeting on cholinesterases, Sibenik, Croatia, 20–25 Sept 2009

  • Roccheri MC, Tipa C, Bonaventura R, Matranga V (2002) Physiological and induced apoptosis in sea urchin larvae undergoing metamorphosis. Int J Dev Biol 46:801–806

    Google Scholar 

  • Shah N, Khurana S, Cheng K, Raufman JP (2009) Muscarinic receptors and ligands in cancer. Am J Cell Physiol 296(2):C221–C232

    Article  CAS  Google Scholar 

  • Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea-urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986

    Article  Google Scholar 

  • Sultatos LG (1994) Mammalian toxicology of organophosphorous pesticides. J Toxicol Environ Health 43:271–289

    Article  CAS  Google Scholar 

  • Vaïtilingon D, Morgan R, Grosjean Ph, Gosselin P, Jangoux M (2001) Effects of delayed metamorphosis and food rations on the perimetamorphic events in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J Exp Mar Bio Ecol 262(1):41–60

  • Zhang XJ, Yang L, Zhao Q, Caen JP, He HY, Jin QH, Guo LH, Alemany M, Zhang LY, Shi YF (2002) Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell death diff 9(8):790–800

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been carried out as a scientific basis in preparation for the project EC 222492, for the benefit of SMEs (responsible person: Mariachiara Chiantore).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carla Falugi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aluigi, M.G., Falugi, C., Mugno, M.G. et al. Dose-dependent effects of chlorpyriphos, an organophosphate pesticide, on metamorphosis of the sea urchin, Paracentrotus lividus . Ecotoxicology 19, 520–529 (2010). https://doi.org/10.1007/s10646-009-0433-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-009-0433-z

Keywords

Navigation