Scientific literature addressing the influence of pesticides on the growth and reproduction of earthworm is reviewed. Earthworms are considered as important bioindicators of chemical toxicity in the soil ecosystem. Studies on this aspect are important because earthworms are the common prey of many terrestrial vertebrate species such as birds and small mammals, and thus they play a key role in the biomagnification process of several soil pollutants. Majority of the studies have used mortality as an endpoint rather than subtler endpoints such as reproductive output. It is now emphasized that, whereas higher concentrations of a pollutant can easily be assessed with the acute (mortality) test, contaminated soils with lower (sublethal) pollutant concentrations require more sensitive test methods such as reproduction test in their risk assessment. 1. Introduction A greater proportion ( 80%) of biomass of terrestrial invertebrates is represented by earthworms which play an important role in structuring and increasing the nutrient content of the soil. Therefore, they can be suitable bioindicators of chemical contamination of the soil in terrestrial ecosystems providing an early warning of deterioration in soil quality [1–3]. This is important for protecting the health of natural environments and is of increasing interest in the context of protecting human health [4] as well as other terrestrial vertebrates which prey upon earthworms [5]. The suitability of earthworms as bioindicators in soil toxicity is largely due to the fact that they ingest large quantity of the decomposed litter, manure, and other organic matter deposited on soil, helping to convert it into rich topsoil [6, 7]. Moreover, studies have shown that earthworm skin is a significant route of contaminant uptake [8] and thus investigation of earthworm biomarkers in the ecological risk assessment (ERA) can be helpful [9] . Eisenia fetida is the standard test organism used in terrestrial ecotoxicology, because it can be easily bred on a variety of organic wastes with short generation times [10–13]. Its susceptibility to chemicals resembles that of true soil organisms. Sensitivity tests of multiple earthworm species have revealed that Eisenia fetida is comparatively less sensitive [14–16]. Although, earthworm species vary in their tolerance, reports have shown a decline in earthworm populations in response to large amounts of organic chemical deposition [17]. Mortality has been the most frequently used parameter to evaluate the chemical toxicity in earthworms [18–20]. It is postulated, however, that
References
[1]
M. D. Culy and E. C. Berry, “Toxicity of soil-applied granular insecticides to earthworm populations in cornfields,” Down to Earth, vol. 50, pp. 20–25, 1995.
[2]
J. Sorour and O. Larink, “Toxic effects of benomyl on the ultrastructure during spermatogenesis of the earthworm Eisenia fetida,” Ecotoxicology and Environmental Safety, vol. 50, no. 3, pp. 180–188, 2001.
[3]
E. Bustos-Obregón and R. I. Goicochea, “Pesticide soil contamination mainly affects earthworm male reproductive parameters,” Asian Journal of Andrology, vol. 4, no. 3, pp. 195–199, 2002.
[4]
A. Beeby, “What do sentinels stand for?” Environmental Pollution, vol. 112, no. 2, pp. 285–298, 2001.
[5]
G. Dell'Omo, A. Turk, and R. F. Shore, “Secondary poisoning in the common shrew (Sorex araneus) fed earthworms exposed to an organophosphate pesticide,” Environmental Toxicology and Chemistry, vol. 18, no. 2, pp. 237–240, 1999.
[6]
S. A. Reinecke and A. J. Reinecke, “Lysosomal response of earthworm coelomocytes induced by longterm experimental exposure to heavy metals,” Pedobiologia, vol. 43, no. 6, pp. 585–593, 1999.
[7]
M. C. Sandoval, M. Veiga, J. Hinton, and B. Klein, “Review of biological indicators for metal mining effluents: a proposed protocol using earthworms,” in Proceedings of the 25th Annual British Columbia Reclamation Symposium, pp. 67–79, 2001.
[8]
K. A. Lord, G. G. Briggs, M. C. Neale, and R. Manlove, “Uptake of pesticides from water and soil by earthworms,” Pesticide Science, vol. 11, no. 4, pp. 401–408, 1980.
[9]
J. C. Sanchez-Hernandez, “Earthworm biomarkers in ecological risk assessment,” Reviews of Environmental Contamination and Toxicology, vol. 188, pp. 85–126, 2006.
[10]
ISO, “Soil quality—effects of pollutants on earthworms (Eisenia fetida)—part 1: determination of acute toxicity using artificial soil substrate,” ISO 11268-1, International Organization for Standardization, Geneva, Switzerland, 1993.
[11]
ISO, “Soil quality—effects of pollutants on earthworms (Eisenia fetida)—part 2: determination of effects on reproduction,” ISO 11268-2, International Organization for Standardization, Geneva, Switzerland, 1998.
[12]
OECD, “Guideline for testing of chemicals,” no. 207, Earthworm Acute Toxicity Test. Organization for Economic Co-Operation and Development, Paris, France, 1984.
[13]
OECD, “Guideline for testing of chemicals,” no. 222, Earthworm Reproduction Test (Eisenia fetida/andrei). Organization for Economic Co-Operation and Development, Paris, France, 2004.
[14]
W. C. Ma and J. Bodt, “Differences in toxicity of the insecticide chlorpyrifos to six species of earthworms (Oligochaeta, Lumbricidae) in standardized soil tests,” Bulletin of Environmental Contamination and Toxicology, vol. 50, no. 6, pp. 864–870, 1993.
[15]
H. Kula, “Comparison of laboratory and field testing for the assessment of pesticide side effects on earthworms,” Acta Zoologica Fennica, vol. 196, pp. 338–341, 1995.
[16]
D. G. Fitzgerald, K. A. Warner, R. P. Lanno, and D. G. Dixon, “Assessing the effects of modifying factors on pentachlorophenol toxicity to earthworms: applications of body residues,” Environmental Toxicology and Chemistry, vol. 15, no. 12, pp. 2299–2304, 1996.
[17]
D. E. Bayer and C. L. Foy, “Action and fate of adjuvants in soils,” in Adjuvants for Herbicides, pp. 84–92, WSSA, Champaign, Ill, USA, 1982.
[18]
C. A. M. Van Gestel and W. A. Van Dis, “The influence of soil characteristics on the toxicity of four chemicals to the earthworm Eisenia fetida andrei (Oligochaeta),” Biology and Fertility of Soils, vol. 6, no. 3, pp. 262–265, 1988.
[19]
C. A. M. Van Gestel, W. A. Van Dis, E. M. Van Breemen, and P. M. Sparenburg, “Development of a standardized reproduction toxicity test with the earthworm species Eisenia fetida andrei using copper, pentachlorophenol, and 2,4-dichloroaniline,” Ecotoxicology and Environmental Safety, vol. 18, no. 3, pp. 305–312, 1989.
[20]
P. Y. Robidoux, J. Hawari, S. Thiboutot, G. Ampleman, and G. I. Sunahara, “Acute toxicity of 2,4,6-trinitrotoluene in earthworm (Eisenia andrei),” Ecotoxicology and Environmental Safety, vol. 44, no. 3, pp. 311–321, 1999.
[21]
F. Moriarty, Ecotoxicology: The Study of Pollutants in Ecosystems, Academic Press, London, UK, 1983.
[22]
G. K. Frampton, S. J？nsch, J. J. Scott-Fordsmand, J. R？mbke, and P. J. Van den Brink, “Effects of pesticides on soil invertebrates in laboratory studies: a review and analysis using species sensitivity distributions,” Environmental Toxicology and Chemistry, vol. 25, no. 9, pp. 2480–2489, 2006.
[23]
M. J. B. Amorim, J. R？mbke, and A. M. V. M. Soares, “Avoidance behaviour of Enchytraeus albidus: effects of Benomyl, Carbendazim, phenmedipham and different soil types,” Chemosphere, vol. 59, no. 4, pp. 501–510, 2005.
[24]
J. R？mbke, M. V. Garcia, and A. Scheffczyk, “Effects of the fungicide benomyl on earthworms in laboratory tests under tropical and temperate conditions,” Archives of Environmental Contamination and Toxicology, vol. 53, no. 4, pp. 590–598, 2007.
[25]
F. Riepert, J. R？mbke, and T. Moser, Ecotoxicological Characterization of Waste, Springer, New York, NY, USA, 2009.
[26]
M.G. Paoletti, “The role of earthworms for assessment of sustainability and as bioindicators,” Agriculture, Ecosystems and Environment, vol. 74, no. 1–3, pp. 137–155, 1999.
[27]
C. A. M. Van Gestel, E. M. Dirven-Van Breemen, R. Baerselman, et al., “Comparison of sublethal and lethal criteria for nine different chemicals in standardized toxicity tests using the earthworm Eisenia andrei,” Ecotoxicology and Environmental Safety, vol. 23, no. 2, pp. 206–220, 1992.
[28]
K. Lock and C. R. Janssen, “Cadmium toxicity for terrestrial invertebrates: taking soil parameters affecting bioavailability into account,” Ecotoxicology, vol. 10, no. 5, pp. 315–322, 2001.
[29]
H. Kula and O. Larink, “Development and standardization of test methods for the prediction of sublethal effects of chemicals on earthworms,” Soil Biology and Biochemistry, vol. 29, no. 3-4, pp. 635–639, 1997.
[30]
Q.-X. Zhou, Q.-R. Zhang, and J.-D. Liang, “Toxic effects of acetochlor and methamidophos on earthworm Eisenia fetida in phaiozem, northeast China,” Journal of Environmental Sciences, vol. 18, no. 4, pp. 741–745, 2006.
[31]
O. Espinoza-Navarro and E. Bustos-Obregón, “Effect of malathion on the male reproductive organs of earthworms, Eisenia foetida,” Asian Journal of Andrology, vol. 7, no. 1, pp. 97–101, 2005.
[32]
M. Cikutovic, Pathologies in earthworm: sub lethal biomarkers of xenobiotic toxicity, dissertation, University of North Texas, 1991.
[33]
E. Martikainen, “Toxicity of dimethoate to some soil animal species in different soil types,” Ecotoxicology and Environmental Safety, vol. 33, no. 2, pp. 128–136, 1996.
[34]
A. Haque and W. Ebing, “Toxicity determination of pesticides to earthworms in the soil substrate,” Journal of Plant Diseases and Protection, vol. 90, no. 4, pp. 395–408, 1983.
[35]
J. A. Addison and S. B. Holmes, “Comparison of forest soil microcosm and acute toxicity studies for determining effects of fenitrothion on earthworms,” Ecotoxicology and Environmental Safety, vol. 30, no. 2, pp. 127–133, 1995.
[36]
B. Helling, S. A. Reinecke, and A. J. Reinecke, “Effects of the fungicide copper oxychloride on the growth and reproduction of Eisenia fetida (Oligochaeta),” Ecotoxicology and Environmental Safety, vol. 46, no. 1, pp. 108–116, 2000.
[37]
L. P. D. Choo and G. H. Baker, “Influence of four commonly used pesticides on the survival, growth, and reproduction of the earthworm Aporrectodea trapezoides (Lumbricidae),” Australian Journal of Agricultural Research, vol. 49, no. 8, pp. 1297–1303, 1998.
[38]
C. A. M. Van Gestel, J. Zaal, E. M. Dirven-Van Breemen, and R. Baerselman, “Comparison of two test methods for determining the effects of pesticides on earthworm reproduction,” Acta Zoologica Fennica, vol. 196, pp. 278–283, 1995.
[39]
N. Xiao, B. Jing, F. Ge, and X. Liu, “The fate of herbicide acetochlor and its toxicity to Eisenia fetida under laboratory conditions,” Chemosphere, vol. 62, no. 8, pp. 1366–1373, 2006.
[40]
S. Yasmin and D. D'Souza, “Effect of pesticides on the reproductive output of Eisenia fetida,” Bulletin of Environmental Contamination and Toxicology, vol. 79, no. 5, pp. 529–532, 2007.
[41]
L. H. Booth, V. J. Heppelthwaite, and K. O'Halloran, “Growth, development and fecundity of the earthworm Aporrectodea caliginosa after exposure to two organophosphates,” New Zealand Plant Protection, vol. 53, pp. 221–225, 2000.
[42]
Y. Y. Mosleh, S. M. M. Ismail, M. T. Ahmed, and Y. M. Ahmed, “Comparative toxicity and biochemical responses of certain pesticides to the mature earthworm Aporrectodea caliginosa under laboratory conditions,” Environmental Toxicology, vol. 18, no. 5, pp. 338–346, 2003.
[43]
Y. Y. Mosleh, S. Paris-Palacios, M. Couderchet, and G. Vernet, “Biological effects of two insecticides on earthworms (Lumbricus terrestris L.) under laboratory conditions,” Mededelingen Rijksuniversiteit te Gent. Fakulteit van de Landbouwkundige en Toegepaste Biologische Wetenschappen, vol. 67, no. 2, pp. 59–68, 2002.
[44]
Y. Y. Mosleh, S. Paris-Palacios, M. Couderchet, and G. Vernet, “Acute and sublethal effects of two insecticides on earthworms (Lumbricus terrestris L.) under laboratory conditions,” Environmental Toxicology, vol. 18, no. 1, pp. 1–8, 2003.
[45]
S.-P. Zhou, C.-Q. Duan, H. Fu, Y.-H. Chen, X.-H. Wang, and Z.-F. Yu, “Toxicity assessment for chlorpyrifos-contaminated soil with three different earthworm test methods,” Journal of Environmental Sciences, vol. 19, no. 7, pp. 854–858, 2007.
[46]
L. H. Booth and K. O'Halloran, “A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos,” Environmental Toxicology and Chemistry, vol. 20, no. 11, pp. 2494–2502, 2001.
[47]
S. Zhou, C. Duan, X. Wang, W. H. G. Michelle, Z. Yu, and H. Fu, “Assessing cypermethrin-contaminated soil with three different earthworm test methods,” Journal of Environmental Sciences, vol. 20, no. 11, pp. 1381–1385, 2008.
[48]
P. M. C. S. De Silva, A. Pathiratne, and C. A. M. van Gestel, “Influence of temperature and soil type on the toxicity of three pesticides to Eisenia andrei,” Chemosphere, vol. 76, no. 10, pp. 1410–1415, 2009.
[49]
E. F. Neuhauser and C. A. Callahan, “Growth and reproduction of the earthworm Eisenia fetida exposed to sublethal concentrations of organic chemicals,” Soil Biology and Biochemistry, vol. 22, no. 2, pp. 175–179, 1990.
[50]
J. M. Venter and A. J. Reinecke, “Dieldrin and growth and development of the earthworm, Eisenia fetida (oligochaeta),” Bulletin of Environmental Contamination and Toxicology, vol. 35, no. 5, pp. 652–659, 1985.
[51]
P. M. C. S. De Silva, A. Pathiratne, and C. A. M. van Gestel, “Toxicity of chlorpyrifos, carbofuran, mancozeb and their formulations to the tropical earthworm Perionyx excavatus,” Applied Soil Ecology, vol. 44, no. 1, pp. 56–60, 2010.
[52]
P. Y. Robidoux, C. Svendsen, J. Caumartin, et al., “Chronic toxicity of energetic compounds in soil determined using the earthworm (Eisenia andrei) reproduction test,” Environmental Toxicology and Chemistry, vol. 19, no. 7, pp. 1764–1773, 2000.
[53]
S. A. Reinecke, M. W. Prinsloo, and A. J. Reinecke, “Resistance of Eisenia fetida (Oligochaeta) to cadmium after long-term exposure,” Ecotoxicology and Environmental Safety, vol. 42, no. 1, pp. 75–80, 1999.
[54]
M. S. Maboeta, A. J. Reinecke, and S. A. Reinecke, “Effects of low levels of lead on growth and reproduction of the Asian earthworm Perionyx excavatus (Oligochaeta),” Ecotoxicology and Environmental Safety, vol. 44, no. 3, pp. 236–240, 1999.
[55]
C. A. M. Van Gestel, “Validation of earthworm toxicity tests by comparison with field studies: a review of benomyl, carbendazim, carbofuran, and carbaryl,” Ecotoxicology and Environmental Safety, vol. 23, no. 2, pp. 221–236, 1992.
[56]
S. K. Gupta and P. N. Saxena, “Carbaryl-induced behavioural and reproductive abnormalities in the earthworm Metaphire posthuma: a sensitive model,” Alternatives to Laboratory Animals, vol. 31, no. 6, pp. 587–593, 2003.
[57]
M. A. Cikutovic, L. C. Fitzpatrick, B. J. Venables, and A. J. Goven, “Sperm count in earthworms (Lumbricus terrestris) as a biomarker for environmental toxicology: effects of cadmium and chlordane,” Environmental Pollution, vol. 81, no. 2, pp. 123–125, 1993.
[58]
O. Espinoza-Navarro and E. Bustos-Obregón, “Sublethal doses of malathion alter male reproductive parameters of Eisenia fetida,” International Journal of Morphology, vol. 22, no. 4, pp. 297–302, 2004.
[59]
M. J. Amorim, J. P. Sousa, A. J. A. Nogueira, and A. M. V. M. Soares, “Comparison of chronic toxicity of Lindane ( -HCH) to Enchytraeus albidus in two soil types: the influence of soil pH,” Pedobiologia, vol. 43, no. 6, pp. 635–640, 1999.
[60]
V. Laabs, W. Amelung, A. Pinto, and W. Zech, “Fate of pesticides in tropical soils of Brazil under field conditions,” Journal of Environmental Quality, vol. 31, no. 1, pp. 256–268, 2002.
[61]
L. C. Paraíba, A. L. Cerdeira, E. F. Da Silva, J. S. Martins, and H. L. Da Costa Coutinho, “Evaluation of soil temperature effect on herbicide leaching potential into groundwater in the Brazilian Cerrado,” Chemosphere, vol. 53, no. 9, pp. 1087–1095, 2003.
[62]
W. Klein, “Mobility of environmental chemicals, including abiotic degradation,” in Ecotoxicology and Climate. SCOPE 38, P. Bordeau, J. A. Haines, W. Klein, and C. R. Krishna Murti, Eds., pp. 65–78, John Wiley & Sons, Chichester, UK, 1989.
[63]
P. Bourdeau, J. A. Haines, W. Klein, and C. R. Krishnamurti, “Ecotoxicology and climate,” in SCOPE 38 IPCS Joint Symposia 9, p. 392, John Wiley & Sons, Chichester, UK, 1989.
[64]
P. N. Viswanathan and C. R. Krishnamurti, “Effects of temperature and humidity on ecotoxicology of chemicals,” in Ecotoxicology and Climate with Special Reference to Hot and Cold Climates, P. Bourdeau, J. A. Haines, W. Klein, and C. R. Krishanamurti, Eds., pp. 139–154, John Wiley & Sons, New York, NY, USA, 1989.
[65]
P. J. Van den Brink, S. N. Sureshkumar, M. A. Daam, et al., “Environmental and human risk of pesticide use in Thailand and Sri Lanka. Results of a preliminary risk assessment,” Alterra Report 789. MAMAS Report Series No. 3/2003, Research Institute for the Green World, Wageningen Alterra, The Netherlands, 2003.
[66]
M. V. B. Garcia, Effects of Pesticides on Soil Fauna: Development of Ecotoxicological Test Methods for Tropical Regions, vol. 19 of Ecology and Development Series, University of Bonn, Bonn, Germany, 2004.
[67]
M. Garcia, J. R？mbke, M. T. de Brito, and A. Scheffczyk, “Effects of three pesticides on the avoidance behavior of earthworms in laboratory tests performed under temperate and tropical conditions,” Environmental Pollution, vol. 153, no. 2, pp. 450–456, 2008.
[68]
P. M. C. S. De Silva, Pesticide effects on earthworms: a tropical perspective, Ph.D. thesis, Department of Ecological Science, VU University, Amsterdam, The Netherlands, 2009.
[69]
M. Holmstrup, “Field assessment of toxic effects on reproduction in the earthworms Aporrectodea longa and Aporrectodea rosea,” Environmental Toxicology and Chemistry, vol. 19, no. 7, pp. 1781–1787, 2000.
[70]
J. R？mbke, C. Bauer, and A. Marschner, “Hazard assessment of chemicals in soil—proposed ecotoxicological test strategy,” Environmental Science and Pollution Research, vol. 3, no. 2, pp. 78–82, 1996.
[71]
J. R？mbke and J. Notenboom, “Ecotoxicological approaches in the field,” in Environmental Analysis of Contaminated Sites, G. I. Sunahara, A. Y. Renoux, C. Thellen, C. L. Gaudet, and A. Pilon, Eds., pp. 181–195, John Wiley & Sons, Chichester, UK, 2002.
[72]
F. Heimbach, “Correlation between data from laboratory and field tests for investigating the toxicity of pesticides to earthworms,” Soil Biology and Biochemistry, vol. 24, no. 12, pp. 1749–1753, 1992.
[73]
S. J？nsch, G. K. Frampton, J. R？mbke, P. J. Van den Brink, and J. J. Scott-Fordsmand, “Effects of pesticides on soil invertebrates in model ecosystem and field studies: a review and comparison with laboratory toxicity data,” Environmental Toxicology and Chemistry, vol. 25, no. 9, pp. 2490–2501, 2006.
[74]
A. R. Abdullah, C. M. Bajet, M. A. Matin, D. D. Nhan, and A. H. Sulaiman, “Ecotoxicology of pesticides in the tropical paddy field ecosystem,” Environmental Toxicology and Chemistry, vol. 16, no. 1, pp. 59–70, 1997.
[75]
B. K. Singh, A. Walker, J. A. W. Morgan, and D. J. Wright, “Effects of soil pH on the biodegradation of chlorpyrifos and isolation of a chlorpyrifos-degrading bacterium,” Applied and Environmental Microbiology, vol. 69, no. 9, pp. 5198–5206, 2003.
