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Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus (Brandt, 1833)

  • SOILS, SEC 4 • ECOTOXICOLOGY • RESEARCH ARTICLE
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Abstract

Purpose

Methiocarb and metaldehyde are the most common molluscicides applied in agricultural and horticultural fields in Portugal and elsewhere in Europe. The application of molluscicidal baits to control slug and snail populations can pose a threat to non-target organisms like terrestrial isopods, because they are detritivorous and may feed on the toxic baits applied to the soil surface. The aim of this work was to evaluate the effects and understand the modes of action of these molluscicides to terrestrial isopods.

Materials and methods

In this study, the terrestrial isopod Porcellionides pruinosus was exposed to these two molluscicides, and the time to lethality was evaluated. Biochemical indicators (biomarkers) are known to provide early warning signs of environmental pollution or stress conditions to the organisms, by measuring cellular or molecular responses of the target organism to xenobiotic agents. Therefore, to evaluate modes of action and effects and also to see if biomarkers can be used as early warning tools in molluscicidal exposures, three different enzymes, glutathione S-transferase (GST), acetylcholinesterase (AChE) and catalase (CAT), were analysed upon single exposures and binary mixtures tests.

Results and discussion

These two molluscicides showed to be of extreme concern regarding terrestrial isopods, as all animals died after 24 h of exposure to methiocarb, and only 20% survived after 56 h of exposure to metaldehyde. Results indicate that the carbamate methiocarb inhibited significantly AChE activity, but no effects were observed in CAT and GST levels. The exposure to metaldehyde had no effects on AChE, but a decrease in GST activity as well as a general increase in CAT activity was observed at the higher exposure period tested (32 h). The combined exposure of the two molluscicides resulted in a general decrease in AChE and CAT activity, but no visible effects were observed in terms of GST activity.

Conclusions

The LT50 values found in the single exposures to both molluscicides were very low, especially in the case of the carbamate methiocarb. The use of several biomarkers was a suitable tool to understand the mode of action of these two molluscicides in this isopod species.

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References

  • Bailey SER (2002) Molluscicidal baits for control of terrestrial gastropods. In: Barker GM (ed) Molluscs as crop pests. CABI Publishing, Wallingford, pp 33–54

    Chapter  Google Scholar 

  • Bieri M (2003) The environmental profile of metaldehyde. In: Henderson IF (ed) Slugs and snails. In World Agriculture, British Crop Protection Council, Symposium Proceedings 80, pp 255–260

  • Bocchetti R, Regoli F (2006) Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65:913–921

    Google Scholar 

  • Boran M, Altinok U, Çapkin E, Karaçam H, Biçer V (2007) Acute toxicity of carbaryl, methiocarb, and carbosulfan to the rainbow trout (Oncorhynchus mykiss) and Guppy (Poecilia reticulata). Turk J Vet Anim Sci 31:39–45

    CAS  Google Scholar 

  • Brown PJ, Long SM, Spurgeon DJ, Svendsen C, Hankard PK (2004) Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon. Chemosphere 57:1675–1681

    Article  CAS  Google Scholar 

  • Clairborne A (1985) Catalase activity. In: Greenwald R (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284

    Google Scholar 

  • Crane M, Sildanchandra W, Kheir R, Callaghan C (2002) Relationship between biomarker activity and developmental endpoints in Chironomus riparius Meigen exposed to an organophosphate insecticide. Ecotox Environ Saf 53(3):361–369

    Article  CAS  Google Scholar 

  • Diamantino TC, Almeida E, Soares AVMV, Guilhermino L (2001) Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere 45:553–560

    Article  CAS  Google Scholar 

  • Drobne D, Blažič M, Van Gestel CAM, Lešer V, Zidar P, Jemec A, Trebše P (2008) Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere 71:1326–1334

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres VJ, Featherstone R (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmac 7:88–95

    Article  CAS  Google Scholar 

  • El-Wakil HB, Radwan MA (1991) Biochemical studies on the terrestrial snails Eobania vermiculata (Müller) treated with some pesticides. J Environ Sci Health Part B 26(5–6):479–489

    Article  CAS  Google Scholar 

  • Engenheiro EL, Hankard PK, Sousa JP, Lemos MF, Weeks JM, Soares AMVM (2005) Influence of dimethoate on acetylcholinesterase activity and locomotor function in terrestrial isopods. Environ Toxicol Chem 24(3):603–609

    Article  CAS  Google Scholar 

  • Ferrari A, Venturino A, D'Angelo AMP (2007) Effects of carbaryl and azinphos methyl on juvenile rainbow trout (Oncorhynchus myskiss) detoxifying enzymes. Pest Biochem Physiol 88:134–142

    Article  CAS  Google Scholar 

  • Fischer E, Farkas S, Hornung E, Past T (1997) Sublethal effects of an organophosphorus insecticide dimethoate on the isopod Porcellio scaber. Comp Biochem Physiol 116C(2):161–166

    CAS  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20(1):37–45

    Article  CAS  Google Scholar 

  • Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM (1996) Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna. Chemosphere 32:727–738

    Article  CAS  Google Scholar 

  • Habig H, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Hayes JD, Pulford DJ (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol 30:445–600

    Article  CAS  Google Scholar 

  • Henderson I, Triebskorn R (2002) Chemical control of terrestrial gastropods. In: Barker GM (ed) Molluscs as crop pests. CABI Publishing, Wallingford, pp 1–31

    Chapter  Google Scholar 

  • Howcroft CF, Amorim MJB, Gravato C, Guilhermino L, Soares AMVM (2009) Effects of natural and chemical stressors on Enchytraeus albidus: can oxidative stress parameters be used as fast screening tools for the assessment of different stress impacts in soils? Environ Int 35:318–324

    Article  CAS  Google Scholar 

  • Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol Environ Saf 54:366–374

    Article  CAS  Google Scholar 

  • Jemec A, Drobne D, Tišler T, Trebše P, Ros M, Sepčić K (2007) The applicability of acetylcholinesterase and glutathione S-transferase in Daphnia magna toxicity test. Comp Biochem Physiol Part C: Toxicol Pharmacol 144:303–309

    Article  Google Scholar 

  • Jemec A, Drobne D, Remskar M, Sepčić K, Tisler T (2008) Effects of ingested nano-sized titanium dioxide on terrestrial isopods (Porcellio scaber). Environ Toxicol Chem 27(9):1904–1914

    Article  CAS  Google Scholar 

  • Jensen S (1998) Acetylcholinesterase activity associated with methiocarb resistance in a strain of Western Flower Thrips, Frankliniella occidentalis (Pergande). Pestic Biochem Physiol 61:191–200

    Article  CAS  Google Scholar 

  • Khessiba A, Roméo M, Aïssa P (2005) Effects of some environmental parameters on catalase activity measured in the mussel (Mytilus galloprovincialis) exposed to lindane. Environ Poll 133:275–281

    Article  CAS  Google Scholar 

  • Köhler HR, Hiittenrauch K, Berkus M, Gräff S, Alberti G (1996) Cellular hepatopancreatic reactions in Porcellio scaber (Isopoda) as biomarkers for the evaluation of heavy metal toxicity in soils. Appl Soil Ecol 3(1):1–15

    Article  Google Scholar 

  • Köhler HR, Knödler C, Zanger M (1999) Divergent kinetics of hsp70 induction in Oniscus asellus (Isopoda) in response to four environmentally relevant organic chemicals (B[a]P, PCB52, g-HCH, PCP): suitability and limits of a biomarker. Arch Environ Contam Toxicol 36:179–185

    Article  Google Scholar 

  • Loureiro S, Sousa JP, Nogueira AJA, Soares AMVM (2002) Assimilation efficiency and toxicokinetics of 14C-lindane in the terrestrial isopod Porcellionides pruinosus: the role of isopods in degradation of persistent soil pollutants. Ecotoxicol 11:481–490

    Article  CAS  Google Scholar 

  • Loureiro S, Soares AMV, Nogueira AJA (2005) Terrestrial avoidance behaviour tests as screening tool to assess soil contamination. Environ Poll 138:121–131

    Article  CAS  Google Scholar 

  • Loureiro S, Amorim MJB, Campos B, Rodrigues SMG, Soares AMVM (2009) Assessing joint toxicity of chemicals in Enchytraeus albidus (Enchytraeidae) and Porcellionides pruinosus (Isopoda) using avoidance behaviour as an endpoint. Environ Pollut 157(2):625–632

    Article  CAS  Google Scholar 

  • Maran E, Fernández M, Barbieri P, Font G, Ruiz MJ (2009) Effects of four carbamate compounds on antioxidant parameters. Ecotox Environ Saf 72:922–930

    Article  CAS  Google Scholar 

  • Massa R, Blevins S, Chao SL (2008) Role of acetylcholinesterase and glutathione S-transferase following exposure to nicosulfuron and diazinon in Helicoverpa zea. Ecotoxicol Environ Saf 71:230–235

    Article  CAS  Google Scholar 

  • Meredith RH (1996) Testing bait treatments for slug control. In: Henderson IF (ed) Slug and snail pests in agriculture. British Crop Protection Council, Farnham, pp 157–164

    Google Scholar 

  • Mills JD, McCrohan CA, Bailey SER, Wedgwood MA (1990) Effects of metaldehyde and acetaldehyde on feeding responses and neuronal activity in the snail Lymnaea stagnalis. Pestic Sci 28:189–199

    Article  Google Scholar 

  • Mills JD, McCrohan CR, Bailey SER (1992) Electrophysiological responses to metaldehyde in neurones of the feeding circuitry of the snail Lymnaea stagnalis. Pestic Biochem Physiol 42(1–2):35–42

    Article  CAS  Google Scholar 

  • Peakall DB (1999) The use of biomarkers in hazard assessment. In: Peakall DB, Colin HW, Migula P (eds) Biomarkers: a pragmatic basis for remediation of severe pollution in Eastern Europe. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 123–133

    Google Scholar 

  • Putachakayala SM, Ram JL (2000) Toxic and excitatory effects of the molluscicide metaldehyde on the biofouling bivalve Dreissena polymorpha Pallas. Pest Manag Sci 56:39–42

    Article  Google Scholar 

  • Radwan MA, Essawy AE, Abdelmeguied NE, Hamed SS, Ahmed AE (2008) Biochemical and histochemical studies on the digestive gland of Eobania vermiculata snails treated with carbamate pesticides. Pestic Biochem Physiol 90:154–167

    Article  CAS  Google Scholar 

  • Ribeiro S, Guilhermino L, Sousa JP, Soares AMVM (1999) Novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods. Ecotoxicol Environ Saf 44:287–293

    Article  CAS  Google Scholar 

  • Ribera D, Narbonne JF, Arnaud C, Saint-Denis M (2001) Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil, effects of carbaryl. Soil Biol Biochem 33:1123–1130

    Article  CAS  Google Scholar 

  • Roberts AP, Oris JT (2004) Multiple biomarker response in rainbow trout during exposure to hexavalent chromium. Comp Biochem Physiol Part C: Toxicol Pharmacol 138:221–228

    Article  Google Scholar 

  • Schlenk D (1999) Necessity of defining biomarkers for use in ecological risk assessments. Mar Pollut Bull 39(1–12):48–53

    Article  CAS  Google Scholar 

  • Schreck E, Geret F, Gontier L, Treilhou M (2008) Neurotoxic effect and metabolic responses induced by a mixture of six pesticides on the earthworm Aporrectodea caliginosa nocturna. Chemosphere 71:1832–1839

    Article  CAS  Google Scholar 

  • Stanek K, Gabrijelcic E, Drobne D, Trebše P (2003) Inhibition of acetylcholinesterase activity in the terrestrial isopod Porcellio scaber as a biomarker of organophosphorous compounds in food. Arh Hig Rada Toksikol 54:183–188

    CAS  Google Scholar 

  • Stanek K, Drobne D, Trebše P (2006) Linkage of biomarkers along levels of biological complexity in juvenile and adult diazinon fed terrestrial isopod (Porcellio scaber, Isopoda, crustacea). Chemosphere 64:1745–1752

    Article  CAS  Google Scholar 

  • Stroomberg GJ, de Knecht JA, Ariese F, van Gestel CAM, Velthorst NH (1999) Pyrene metabolites in the hepatopancreas and gut of the isopod Porcellio scaber, a new biomarker for polycyclic aromatic hydrocarbon exposure in terrestrial ecosystems. Environ Toxicol Chem 18:2217–2224

    CAS  Google Scholar 

  • Taylor P (1996) Agents acting at the neuromuscular junction and autonomic ganglia. In: Hardman JG, Limbird LE, Molinoff PB, Ruddon RW, Goodman GA (eds) The pharmacological basis of therapeutics. McGraw-Hill, New York, pp 177–198

    Google Scholar 

  • Tiwari F, Singh K, Singh DK (2008) Enzyme inhibition by different bait formulations in the nervous system of the snail Lymnaea acuminate. In: Joshi BD, Joshi PC, Joshi N (eds) Environmental pollution and toxicology. A.P.H. Publishing Corporation, New Dehli, pp 115–128

    Google Scholar 

  • Triebskorn R, Christensen K, Heim I (1998) Effects of orally and dermally applied metaldehyde on mucus cells of slugs (Deroceras reticulatum) depending on temperature and duration of exposure. J Molluscan Stud 64:467–487

    Article  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Wellmann P, Heimbach F (1996) The effects of methiocarb slug pellets on the earthworm Lumbricus terrestris in a laboratory test. In: Henderson IF (ed) Slug and snail pests in agriculture. British Crop Protection Council, Farnham, pp 181–188

    Google Scholar 

  • 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 Differ 9:790–800

    Article  CAS  Google Scholar 

  • Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda:Oniscidea): an evolutionary-ecological approach. Biol Rev Camb Philos Soc 77:455–493

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by a PhD grant (SFRH/BD/31562/2006) attributed to Miguel J.G. Santos by the Portuguese Science and Technology Foundation (FCT) and by the project AGROMIX, Evaluation of the toxicity of mixtures of chemical compounds in agricultural soils (PTDC/AGR-AAM/68676/2006) funded by FCT.

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Correspondence to Miguel João G. Santos.

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Santos, M.J.G., Ferreira, N.G.C., Soares, A.M.V.M. et al. Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus (Brandt, 1833). J Soils Sediments 10, 1335–1343 (2010). https://doi.org/10.1007/s11368-010-0246-y

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