Advertisement

Important Issues in Ecotoxicological Investigations Using Earthworms

  • Mirna Velki
  • Sandra Ečimović
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 239)

Abstract

The importance and beneficial effects of earthworms on soil structure and quality is well-established. In addition, earthworms have proved to be important model organisms for investigation of pollutant effects on soil ecosystems. In ecotoxicological investigations effects of various pollutants on earthworms were assessed. But some important issues regarding the effects of pollutants on earthworms still need to be comprehensively addressed. In this review several issues relevant to soil ecotoxicological investigations using earthworms are emphasized and guidelines that should be adopted in ecotoxicological investigations using earthworms are given. The inclusion of these guidelines in ecotoxicological studies will contribute to the better quantification of impacts of pollutants and will allow more accurate prediction of the real field effects of pollutants to earthworms.

Keywords

Ecotoxicology Earthworms Soil ecosystems Risk assessment Biomarker responses Toxic effects Pollutants Pollutant mixtures Hormesis Microcosmic systems Experimental conditions Temperature change 

References

  1. Abbott I, Parker CA (1981) Interactions between earthworms and their soil environment. Soil Biol Biochem 13:191–197Google Scholar
  2. Abiven S, Menasseri S, Chenu C (2009) The effects of organic inputs over time on soil aggregate stability—a literature analysis. Soil Biol Biochem 41:1–12Google Scholar
  3. Adams SM (2003) Establishing causality between environmental stressors and effects on aquatic ecosystems. Hum Ecol Risk Assess 9:17–35Google Scholar
  4. Alves PR, Cardoso EJ, Martines AM, Sousa JP, Pasini A (2013) Earthworm ecotoxicological assessments of pesticides used to treat seeds under tropical conditions. Chemosphere 90:2674–2682Google Scholar
  5. An YJ (2005) Assessing soil ecotoxicity of methyl tert-butyl ether using earthworm bioassay; closed soil microcosm test for volatile organic compounds. Environ Pollut 134:181–186Google Scholar
  6. Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, Mount DR, Nichols JW, Russom CL, Schmieder PK, Serrrano JA, Tietge JE, Villeneuve DL (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29:730–741Google Scholar
  7. Belmeskine H, Haddad S, Vandelac L, Sauvé S, Fournier M (2012) Toxic effects of PCDD/Fs mixtures on Eisenia andrei earthworms. Ecotoxicol Environ Saf 80:54–59Google Scholar
  8. Bindesbøl A, Holmstrup M, Damgaard C, Bayley M (2005) Stress synergy between environmentally realistic levels of copper and frost in the earthworm Dendrobaena octaedra. Environ Toxicol Chem 24:1462–1467Google Scholar
  9. Bindesbøl A-M, Bayley M, Damgaard C, Hedlund K, Holmstrup M (2009a) Changes in membrane phospholipids as a mechanistic explanation for decreased freeze tolerance in earthworms exposed to sub-lethal copper concentrations. Environ Sci Tech 43:5495–5500Google Scholar
  10. Bindesbøl A-M, Bayley M, Damgaard C, Holmstrup M (2009b) Impacts of heavy metals, PAHs and pesticides on freeze tolerance of the earthworm Dendrobaena octaedra. Environ Toxicol Chem 28:2341–2347Google Scholar
  11. Birkás M, Jolánkai M, Gyuricza C, Percze A (2004) Tillage effects on compaction, earthworms and other soil quality indicators in Hungary. Soil Tillage Res 78:185–196Google Scholar
  12. Bogomolov DM, Chen S-K, Parmelee RW, Subler S, Edwards CA (1996) An ecosystem approach to soil toxicity testing: a study of copper contamination in laboratory soil microcosms. Appl Soil Ecol 4:95–105Google Scholar
  13. Bohlen PJ, Edwards CA (1995) Earthworm effects on N dynamics and soil respiration in microcosms receiving organic and inorganic nutrients. Soil Biol Biochem 27:341–348Google Scholar
  14. Boyer J, Reversat G, Lavelle P, Chabanne A (2013) Interactions between earthworms and plant-parasitic nematodes. Eur J Soil Biol 59:43–47Google Scholar
  15. Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198Google Scholar
  16. Brown PJ, Long SM, Spurgeon DJ, Svendsen C, Hankard PK (2004) Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a noncarcinogenic polycyclic aromatic hydrocarbon. Chemosphere 57:1675–1681Google Scholar
  17. Burrows LA, Edwards CA (2002) The use of integrated soil microcosms to predict effects of pesticides on soil ecosystems. Eur J Soil Biol 38:245–249Google Scholar
  18. Cahill TM, Cousins I, Mackay D (2003) Development and application of a generalized physiologically based pharmacokinetic model for multiple environmental contaminants. Environ Toxicol Chem 22:26–34Google Scholar
  19. Calabrese EJ (2003) The maturing of hormesis as a credible dose-response model. Nonlinearity Biol Toxicol Med 1:319–343Google Scholar
  20. Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 27:1451–1474Google Scholar
  21. Calabrese EJ, Baldwin LA (2002) Defining hormesis. Hum Exp Toxicol 21:91–97Google Scholar
  22. Calabrese EJ, Baldwin LA (2003) The hormetic dose-response model is more common that the threshold model in toxicology. Toxicol Sci 71:246–250Google Scholar
  23. Calisi A, Lionetto MG, Schettino T (2011) Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Sci Total Environ 409:4456–4464Google Scholar
  24. Calisi A, Zaccarelli N, Lionetto MG, Schettino T (2013) Integrated biomarker analysis in the earthworm Lumbricus terrestris: application to the monitoring of soil heavy metal pollution. Chemosphere 90:2637–2644Google Scholar
  25. Cao X, Song Y, Kai J, Yang X, Ji P (2012) Evaluation of EROD and CYP3A4 activities in earthworm Eisenia fetida as biomarkers for soil heavy metal contamination. J Hazard Mater 243:146–151Google Scholar
  26. Capowiez Y, Dittbrenner N, Rault M, Triebskorn R, Hedde M, Mazzia C (2010) Earthworm cast production as a new behavioural biomarker for toxicity testing. Environ Pollut 158:388–393Google Scholar
  27. Chan KY (2001) An overview of some tillage impacts on earthworm population abundance and diversity—implications for functioning in soils. Soil Tillage Res 57:179–191Google Scholar
  28. Crittenden SJ, Eswaramurthy T, de Goede RGM, Brussaard L, Pulleman MM (2014) Effect of tillage on earthworms over short- and medium-term in conventional and organic farming. Appl Soil Ecol 83:140–148Google Scholar
  29. De Silva PM, Pathiratne A, van Gestel CA (2009) Influence of temperature and soil type on the toxicity of three pesticides to Eisenia andrei. Chemosphere 76:1410–1415Google Scholar
  30. Dittbrenner N, Moser I, Triebskorn R, Capowiez Y (2011) Assessment of short and long-term effects of imidacloprid on the burrowing behaviour of two earthworm species (Aporrectodea caliginosa and Lumbricus terrestris) by using 2D and 3D post-exposure techniques. Chemosphere 84:1349–1355Google Scholar
  31. Doan TT, Ngo PT, Rumpel C, Nguyen BV (2013) Interactions between compost, vermicompost and earthworms influence plant growth and yield: a one-year greenhouse experiment. Sci Hortic 160:148–154Google Scholar
  32. Doube BM, Stephens PM, Davoren CW, Ryder MH (1994) Interactions between earthworms, beneficial soil microorganisms and root pathogens. Appl Soil Ecol 1:3–10Google Scholar
  33. Edwards CA (2004) The importance of earthworms as key representatives of the soil fauna. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, FL, pp 3–11Google Scholar
  34. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman and Hall, LondonGoogle Scholar
  35. Eisenhauer N, Hörsch V, Moeser J, Scheu S (2010) Synergistic effects of microbial and animal decomposers on plant and herbivore performance. Basic Appl Ecol 11:23–34Google Scholar
  36. Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2009) Earthworm and belowground competition effects on plant productivity. Oecologia 161:291–301Google Scholar
  37. Eisenhauer N, Partsch S, Parkinson D, Scheu S (2007) Invasion of a deciduous forest by earthworms: changes in soil chemistry, microflora, microarthropods and vegetation. Soil Biol Biochem 39:1099–1110Google Scholar
  38. Ellis SR, Hodson ME, Wege P (2010) The soil-dwelling earthworm Allolobophora chlorotica modifies its burrowing behaviour in response to carbendazim applications. Ecotoxicol Environ Saf 73:1424–1428Google Scholar
  39. El-Temsah YS, Joner EJ (2012) Ecotoxicological effects on earthworms of fresh and aged nano-sized zero-valent iron (nZVI) in soil. Chemosphere 89:76–82Google Scholar
  40. Ernst G, Emmerling C (2009) Impact of five different tillage systems on soil organic carbon content and the density, biomass, and community composition of earthworms after a ten year period. Eur J Soil Biol 45:247–251Google Scholar
  41. Fayolle L, Michaud H, Cluzeau D, Stawiecki J (1997) Influence of temperature and food source on the life cycle of the earthworm Dendrobaena veneta (Oligochaeta). Soil Biol Biochem 29:747–750Google Scholar
  42. Fraser PM, Beare MH, Butler RC, Harrison-Kirk T, Piercy JE (2003) Interactions between earthworms (Aporrectodea caliginosa), plants and crop residues for restoring properties of a degraded arable soil. Pedobiologia 47:870–876Google Scholar
  43. Garcia M, Römbke J, de Brito MT, Scheffczyk A (2008) Effects of three pesticides on the avoidance behavior of earthworms in laboratory tests performed under temperate and tropical conditions. Environ Pollut 153:450–456Google Scholar
  44. Giska I, van Gestel CA, Skip B, Laskowski R (2014) Toxicokinetics of metals in the earthworm Lumbricus rubellus exposed to natural polluted soils—relevance of laboratory tests to the field situation. Environ Pollut 190:123–132Google Scholar
  45. Gomez-Eyles JL, Svendsen C, Lister L, Martin H, Hodson ME, Spurgeon DJ (2009) Measuring and modelling mixture toxicity of imidacloprid and thiacloprid on Caenorhabditis elegans and Eisenia fetida. Ecotoxicol Environ Saf 72:71–79Google Scholar
  46. Gupta SK, Sundararaman V (1991) Correlation between burrowing capability and AChE activity in the earthworm, Pheretima posthuma, on exposure to carbaryl. Bull Environ Contam Toxicol 46:859–865Google Scholar
  47. Hackenberger BK, Jarić-Perkušić D, Stepić S (2008) Effect of temephos on cholinesterase activity in the earthworm Eisenia fetida (Oligochaeta, Lumbricidae). Ecotoxicol Environ Saf 71:583–589Google Scholar
  48. Hackenberger BK, Velki M, Stepić S, Hackenberger DK (2012) The effect of formalin on acetylcholinesterase and catalase activities, and on the concentration of oximes, in the earthworm species Eisenia andrei. Eur J Soil Biol 50:137–143Google Scholar
  49. Hayashi Y, Heckmann LH, Simonsen V, Scott-Fordsmand JJ (2013) Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida. Ecotoxicol Environ Saf 98:219–226Google Scholar
  50. Heckmann L-H, Hovgaard M, Sutherland D, Autrup H, Besenbacher F, Scott-Fordsmand J (2011) Limit-test toxicity screening of selected inorganic nanoparticles to the earthworm Eisenia fetida. Ecotoxicology 20:226–233Google Scholar
  51. Hirano T, Tamae K (2011) Earthworms and soil pollutants. Sensors 11:11157–11167Google Scholar
  52. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V, Köhler HR, Loureiro S, Soares AM, Ferreira AL, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762Google Scholar
  53. Holmstrup M, Petersen BF, Larsen MM (1998) Combined effects of copper, desiccation, and frost on the viability of earthworm cocoons. Environ Toxicol Chem 17:897–901Google Scholar
  54. Hooper HL, Jurkschat K, Morgan AJ, Bailey J, Lawlor AJ, Spurgeon DJ, Svendsen C (2011) Comparative chronic toxicity of nanoparticulate and ionic zinc to the earthworm Eisenia veneta in a soil matrix. Environ Int 37:1111–1117Google Scholar
  55. Hu CW, Zhang LJ, Wang WL, Cui YB, Li M (2014) Evaluation of the combined toxicity of multi-walled carbon nanotubes and sodium pentachlorophenate on the earthworm Eisenia fetida using avoidance bioassay and comet assay. Soil Biol Biochem 70:123–130Google Scholar
  56. Hu CW, Li M, Cui YB, Li DS, Chen J, Yang LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42:586–591Google Scholar
  57. Jager T, Vandenbrouck T, Baas J, De Coen WM, Kooijman SA (2010) A biology-based approach for mixture toxicity of multiple endpoints over the life cycle. Ecotoxicology 19:351–361Google Scholar
  58. Jensen D, Bayley M, Holmstrup M (2009) Synergistic interaction between 4-nonylphenol and high but not low temperatures in Dendrobaena octaedra. Ecotoxicol Environ Saf 72:10–16Google Scholar
  59. Jones OA, Spurgeon DJ, Svendsen C, Griffin JL (2008) A metabolomics based approach to assessing the toxicity of the polyaromatic hydrocarbon pyrene to the earthworm Lumbricus rubellus. Chemosphere 71:601–609Google Scholar
  60. Jonker MJ, Svendsen C, Bedaux JJM, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environ Toxicol Chem 24:2701–2713Google Scholar
  61. Jusselme MD, Miambi E, Mora P, Diouf M, Rouland-Lefèvre C (2013) Increased lead availability and enzyme activities in root-adhering soil of Lantana camara during phytoextraction in the presence of earthworms. Sci Total Environ 445–446:101–109Google Scholar
  62. Kammenga JE, Dallinger R, Donker MH, Köhler H-R, Simonsen V, Triebskorn R, Weeks JM (2000) Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Rev Environ Contam Toxicol 164:93–147Google Scholar
  63. Khan MA, Ahmed SA, Salazar A, Gurumendi J, Khan A, Vargas M, von Catalin B (2007) Effect of temperature on heavy metal toxicity to earthworm Lumbricus terrestris (Annelida: Oligochaeta). Environ Toxicol 22:487–494Google Scholar
  64. Kılıç GA (2011) Histopathological and biochemical alterations of the earthworm (Lumbricus Terrestris) as biomarker of soil pollution along Porsuk River Basin (Turkey). Chemosphere 83:1175–1180Google Scholar
  65. Klobučar GI, Štambuk A, Šrut M, Husnjak I, Merkaš M, Traven L, Cvetković Z (2011) Aporrectodea caliginosa, a suitable earthworm species for field based genotoxicity assessment? Environ Pollut 159:841–849Google Scholar
  66. Kurelec B (1998) Biomarkers and the ecological risk assesment paradigm. In: Werner E, Muller G (eds) Modern aspects in monitoring of environmental pollution in the sea. Akademie gemeinnutziger Wissenschaften zu Erfurt, ErfurtGoogle Scholar
  67. LaCourse EJ, Hernandez-Viadel M, Jefferies JR, Svendsen C, Spurgeon DJ, Barrett J, Morgan AJ, Kille P, Brophy PM (2009) Glutathione transferase (GST) as a candidate molecular-based biomarker for soil toxin exposure in the earthworm Lumbricus rubellus. Environ Pollut 157:2459–2469Google Scholar
  68. Langdon CJ, Hodson ME, Arnold RE, Black S (2005) Survival, Pb-uptake and behaviour of three species of earthworm in Pb treated soils determined using an OECD-style toxicity test and a soil avoidance test. Environ Pollut 138:368–375Google Scholar
  69. Łaszczyca P, Augustyniak M, Babczyńska A, Bednarska K, Kafel A, Migula P, Wilczek G, Witas I (2004) Profiles of enzymatic activity in earthworms from zinc, lead and cadmium polluted areas near Olkusz (Poland). Environ Int 30:901–910Google Scholar
  70. Lee KE (1985) Earthworms. Their ecology and relationships with soils and land use. Academic, SydneyGoogle Scholar
  71. Leveque T, Capowiez Y, Schreck E, Mazzia C, Auffan M, Foucault Y, Austruy A, Dumat C (2013) Assessing ecotoxicity and uptake of metals and metalloids in relation to two different earthworm species (Eiseina hortensis and Lumbricus terrestris). Environ Pollut 179:232–241Google Scholar
  72. Lima MP, Cardoso DN, Soares AM, Loureiro S (2015) Carbaryl toxicity prediction to soil organisms under high and low temperature regimes. Ecotoxicol Environ Saf 114:263–272Google Scholar
  73. Lionetto MG, Calisi A, Schettino T (2012) Earthworm biomarkers as tools for soil pollution assessment. In: Hernandez-Soriano MC (ed) Soil heath and soil use management. InTech—Open Access Publisher, Rijeka (Croatia), pp 305–332Google Scholar
  74. Lukkari T, Marjo Aatsinki M, Väisänen A, Haimi J (2005) Toxicity of copper and zinc assessed with three different earthworm tests. Appl Soil Ecol 30:133–146Google Scholar
  75. Lydy MJ, Linck SL (2003) Assessing the impact of triazine herbicides on organophosphate insecticide toxicity to the earthworm Eisenia fetida. Arch Environ Contam Toxicol 45:343–349Google Scholar
  76. Ma WC, Bodt J (1993) Differences in toxicity of the insecticide Chlorpyrifos to six species of earthworms (Oligochaeta, Lumbricidae) in standardized soil tests. Bull Environ Contam Toxicol 50:864–870Google Scholar
  77. Martin NA (1982) The interaction between organic matter in soil and the burrowing activity of three species of earthworms (Oligochaeta: Lumbricidae). Pedobiologia 24:185–190Google Scholar
  78. Mikhailov AT, Torrado M (1999) Carboxylesterase overexpression in the male reproductive tract: a universal safeguarding mechanism? Reprod Fertil Dev 11:133–145Google Scholar
  79. Morgan AJ, Stürzenbaum SR, Winters C, Grime GW, Aziz NAA, Kille P (2004) Differential metallothionein expression in earthworm (Lumbricus rubellus) tissues. Ecotoxicol Environ Saf 57:11–19Google Scholar
  80. OECD (1984) Guidelines for testing of chemicals, earthworm, acute toxicity tests. Filter paper test and artificial soil test, vol 207. Organization for Economic Cooperation and Development, ParisGoogle Scholar
  81. Pal R, Chakrabarti K, Chakraborty A, Chowdhury A (2006) Degradation and effects of pesticides on soil microbiological parameters-a review. Int J Agric Res 1:240–258Google Scholar
  82. Pastorok RA, Akçakaya R, Regan H, Ferson S, Bartell SM (2003) Role of ecological models in risk assessment. Hum Ecol Risk Assess 9:939–972Google Scholar
  83. Pelosi C, Barot S, Capowiez Y, Hedde M, Vandenbulcke F (2013) Pesticides and earthworms. A review. Agron Sustain Dev 34:199–228Google Scholar
  84. Pelosi C, Pey B, Hedde M, Caro G, Capowiez Y, Guernion M, Peigné J, Piron D, Bertrand M, Cluzeau D (2014) Reducing tillage in cultivated fields increases earthworm functional diversity. Appl Soil Ecol 83:79–87Google Scholar
  85. Perreault JM, Whalen JK (2006) Earthworm burrowing in laboratory microcosms as influenced by soil temperature and moisture. Pedobiologia 50:397–403Google Scholar
  86. Presley ML, McElroy TC, Dieh WI (1996) Soil moisture and temperature interact to affect growth, survivorship, fecundity, and fitness in the earthworm Eisenia fetida. Comp Biochem Physiol 114A:319–326Google Scholar
  87. Reinecke AJ, Reinecke SA (2004) Earthworm as test organisms in ecotoxicological assessment of toxicant impacts on ecosystems. In: Edwards CA (ed) Earthworm ecology. CRC Press LLC, Boca Raton, FL, USA, pp 299–320Google Scholar
  88. Reinecke SA, Reinecke AJ (2007) Biomarker response and biomass change of earthworms exposed to chlorpyrifos in microcosms. Ecotoxicol Environ Saf 66:92–101Google Scholar
  89. Ricketts HJ, Morgan AJ, Spurgeon DJ, Kille P (2003) Measurement of annetocin gene expression: anew reproductive biomarker in earthworm toxicology. Ecotoxicol Environ Saf 57:4–10Google Scholar
  90. Riley H, Pommeresche R, Eltun R, Hansen S, Korsaeth A (2008) Soil structure, organic matter and earthworm activity in a comparison of cropping systems with contrasting tillage, rotations, fertilizer levels and manure use. Agr Ecosyst Environ 124:275–284Google Scholar
  91. Robidoux PY, Svendsen C, Sarrazin M, Thiboutot S, Ampleman G, Hawari J et al (2004) Assessment of a 2,4,6-trinitrotoluene contaminated site using Aporrectodea rosea and Eisenia andrei in mesocosms. Arch Environ Contam Toxicol 48:56–67Google Scholar
  92. Rodríguez-Castellanos L, Sanchez-Hernandez JC (2007) Earthworm biomarkers of pesticide contamination: current status and perspectives. J Pest Sci 32:360–371Google Scholar
  93. Rosenbluth J (1972) Myoneural junctions of two ultrastructurally distinct types in earthworm body wall muscle. J Cell Biol 54:566–579Google Scholar
  94. Sanchez-Hernandez JC (2006) Earthworm biomarkers in ecological risk assessment. Rev Environ Contam Toxicol 188:85–126Google Scholar
  95. Sanchez-Hernandez JC, Martinez Morcillo S, Notario del Pino J, Ruiz P (2014) Earthworm activity increases pesticide-sensitive esterases in soil. Soil Biol Biochem 75:186–196Google Scholar
  96. Santos MJG, Ferreira V, Soares AMVM, Loureiro S (2011a) Evaluation of the combined effects of dimethoate and spirodiclofen on plants and earthworms in a designed microcosm experiment. Appl Soil Ecol 48:294–300Google Scholar
  97. Santos MJG, Morgado R, Ferreira NGC, Soares AMVM, Loureiro S (2011b) Evaluation of the joint effect of glyphosate and dimethoate using a small-scale terrestrial ecosystem. Ecotoxicol Environ Saf 74:1994–2001Google Scholar
  98. Sarkar A, Ray D, Amulya NS, Subhodeep S (2006) Molecular biomarkers; their significant and application in marine pollution monitoring. Ecotoxicology 15:333–340Google Scholar
  99. Schnug L, Ergon T, Jakob L, Scott-Fordsmand JJ, Joner EJ, Leinaas HP (2015) Responses of earthworms to repeated exposure to three biocides applied singly and as a mixture in an agricultural field. Sci Total Environ 505:223–235Google Scholar
  100. Schnug L, Jakob L, Hartnik T (2013) The toxicity of a ternary biocide mixture to two consecutive earthworm (Eisenia fetida) generations. Environ Toxicol Chem 32:937–947Google Scholar
  101. Schnug L, Jensen J, Scott-Fordsmand JJ, Leinaas HP (2014) Toxicity of three biocides to springtails and earthworms in a soil multi-species (SMS) test system. Soil Biol Biochem 74:115–126Google Scholar
  102. Schreck E, Geret F, Gontier L, Trilhou M (2008) Neurotoxic effect and metabolic responses induced by a mixture of six pesticides on the earthworm Aporrectodea caliginosa nocturna. Chemosphere 71:1832–1839Google Scholar
  103. Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011a) Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida). Nanotoxicology 5:432–444Google Scholar
  104. Shoults-Wilson WA, Zhurbich O, McNear D, Tsyusko O, Bertsch P, Unrine J (2011b) Evidence for avoidance of Ag nanoparticles by earthworms (Eisenia fetida). Ecotoxicology 20:385–396Google Scholar
  105. Six J, Elliott E, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103Google Scholar
  106. Spurgeon DJ, Jones OA, Dorne JL, Svendsen C, Swain S, Stürzenbaum SR (2010) Systems toxicology approaches for understanding the joint effects of environmental chemical mixtures. Sci Total Environ 408:3725–3734Google Scholar
  107. Spurgeon DJ, Ricketts H, Svendsen C, Morgan AJ, Kille P (2005) Hierarchical responses of soil invertebrates (earthworms) to toxic metals stress. Environ Sci Tech 39:5327–5334Google Scholar
  108. Stepić S, Hackenberger BK, Velki M, Hackenberger DK, Lončarić Ž (2013a) Potentiation effect of metolachlor on toxicity of organochlorine and organophosphate insecticides in earthworm Eisenia andrei. Bull Environ Contam Toxicol 91:55–61Google Scholar
  109. Stepić S, Hackenberger BK, Velki M, Lončarić Ž, Hackenberger DK (2013b) Effects of individual and binary-combined commercial insecticides endosulfan, temephos, malathion and pirimiphos-methyl on biomarker responses in earthworm Eisenia andrei. Environ Toxicol Pharmacol 36:715–723Google Scholar
  110. Svendsen C, Hankard PK, Lister LJ, Fishwick SK, Jonker MJ, Spurgeon DJ (2007) Effect of temperature and season on reproduction, neutral red retention and metallothionein responses of earthworms exposed to metals in field soils. Environ Pollut 147:83–93Google Scholar
  111. Tao J, Griffiths B, Zhang S, Chen X, Liu M, Hu F, Li H (2009) Effects of earthworms on soil enzyme activities in an organic residue amended rice-wheat rotation agro-ecosystem. Appl Soil Ecol 42:221–226Google Scholar
  112. Tripathi G, Kachhwaha I, Dabi I (2010a) Ecophysiological category based toxicological responses in metabolism of earthworms: Impact of a pyrethroidal insecticide. Pestic Biochem Physiol 98:333–341Google Scholar
  113. Tripathi G, Kachhwaha N, Dabi I (2010b) Comparative studies on carbofuran-induced changes in some cytoplasmic and mitochondrial enzymes and proteins of epigeic, anecic and endogeic earthworms. Pestic Biochem Physiol 96:30–35Google Scholar
  114. Tripathi GKN, Dabi I, Bandooni N (2011) Temperature-dependent alterations in metabolic enzymes and proteins of three ecophysiologically different species of earthworms. Braz Arch Biol Tech 54:769–776Google Scholar
  115. Tsyusko OV, Hardas SS, Shoults-Wilson WA, Starnes CP, Joice G, Butterfield DA, Unrine JM (2012) Short-term molecular-level effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environ Pollut 171:249–255Google Scholar
  116. van Gestel CA (2012) Soil ecotoxicology: state of the art and future directions. Zookeys 176:275–296Google Scholar
  117. van Gestel CA, Koolhaas JE, Hamers T, van Hoppe M, van Roovert M, Korsman C, Reinecke SA (2009) Effects of metal pollution on earthworm communities in a contaminated floodplain area: linking biomarker, community and functional responses. Environ Pollut 157:895–903Google Scholar
  118. Vejares SG, Sabat P, Sanchez-Hernandez JC (2010) Tissue-specific inhibition and recovery of esterase activities in Lumbricus terrestris experimentally exposed to chlorpyrifos. Comp Biochem Physiol C Toxicol Pharmacol 151:351–359Google Scholar
  119. Velki M, Ečimović S (2015) Changes in exposure temperature lead to changes in pesticide toxicity to earthworms: a preliminary study. Environ Toxicol Pharmacol  10.1016/j.etap.2015.09.009. Accepted for Publication
  120. Velki M, Hackenberger BK (2012) Species-specific differences in biomarker responses in two ecologically different earthworms exposed to the insecticide dimethoate. Comp Biochem Physiol C Toxicol Pharmacol 156:104–112Google Scholar
  121. Velki M, Hackenberger BK (2013a) Different sensitivities of biomarker responses in two epigeic earthworm species after exposure to pyrethroid and organophosphate insecticides. Arch Environ Contam Toxicol 65:498–509Google Scholar
  122. Velki M, Hackenberger BK (2013b) Biomarker responses in earthworm Eisenia andrei exposed to pirimiphos-methyl and deltamethrin using different toxicity tests. Chemosphere 90:1216–1226Google Scholar
  123. Velki M, Hackenberger BK, Lončarić Ž, Hackenberger DK (2014) Application of microcosmic system for assessment of insecticide effects on biomarker responses in ecologically different earthworm species. Ecotoxicol Environ Saf 104:110–119Google Scholar
  124. Venkateswara Rao J, Kavitha P (2004) Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environ Res 96:323–327Google Scholar
  125. Wang Y, Chen C, Qian Y, Zhao X, Wang Q, Kong X (2015) Toxicity of mixtures of λ-cyhalothrin, imidacloprid and cadmium on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Ecotoxicol Environ Saf 111:242–247Google Scholar
  126. Wever LA, Lysyk TJ, Clapperton MJ (2001) The influence of soil moisture and temperature on the survival, aestivation, growth and development of juvenile Aporrectodea tuberculata (Eisen) (Lumbricidae). Pedobiologia 45:121–133Google Scholar
  127. Wieczorek-Olchawa E, Niklinska M, Miedzobrodzki J, Plytycz B (2002) Effects of temperature and soil pollution on the presence of bacteria, coelomocytes and brown bodies in coelomic fluid of Dendrobaena veneta. Pedobiologia 47:702–709Google Scholar
  128. World Health Organization (WHO) (2001) Environmental Health Criteria 222. Biomarkers in risk assessment: validity and validation. World Health Organization, Geneva, SwitzerlandGoogle Scholar
  129. Wu S, Zhang H, Zhao S, Wang J, Li H, Chen J (2012) Biomarker responses of earthworms (Eisenia fetida) exposured to phenanthrene and pyrene both singly and combined in microcosms. Chemosphere 87:285–293Google Scholar
  130. Wurst S, Langel R, Reineking A, Bonkowski M, Scheu S (2003) Effects of earthworms and organic litter distribution on plant performance and aphid reproduction. Oecologia 137:90–96Google Scholar
  131. Zhang Y, Shen G, Yu Y, Zhu H (2009) The hormetic effect of cadmium on the activity of antioxidant enzymes in the earthworm Eisenia fetida. Environ Pollut 157:3064–3068Google Scholar
  132. Zhou S, Duan C, Michelle WH (2011) Individual and combined toxic effects of cypermethrin and chlorpyrifos on earthworm. J Environ Sci 23:676–680Google Scholar
  133. Zhou SP, Duan CQ, Fu H, Chen YH, Wang XH, Yu ZF (2007) Toxicity assessment for chlorpyrifos-contaminated soil with three different earthworm test methods. J Environ Sci (China) 19:854–858Google Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.Department of BiologyJosip Juraj Strossmayer University of OsijekOsijekCroatia

Personalised recommendations