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Can Local Enhancement in Earthworms Affect the Outcome of the Standard Earthworm Avoidance Test?

  • A. H. Stander
  • A. le Roux
  • P. Voua OtomoEmail author
Article

Abstract

Earthworms exhibit clumping behaviour in and out of the soil. However, it remains unknown if such social behaviour ultimately influences the outcome of ecotoxicological experiments in the laboratory. We performed several overnight avoidance tests to determine whether social behaviour (i.e., local enhancement) is a factor in pollution avoidance behaviour in the earthworm Eisenia fetida. The results showed that there was no clear influence of social behaviour on the choice or avoidance of Cd contaminated soils, although we suspect that 50 mg Cd/kg might not have been high enough to elicit a significant avoidance response. Nevertheless, when offered a choice between clean undisturbed soil and previously inhabited soil, the worms preferred the previously inhabited soil (p < 0.01). While the level of metal pollution investigated in this study did not disrupt or help predict social dynamics, local enhancement, perhaps driven by some sort of habitat imprinting, was successfully documented in Eisenia fetida.

Keywords

Avoidance behaviour Avoidance test Cadmium Earthworms Ecotoxicology 

Notes

References

  1. Amorim MJB, Novais S, Römbke J, Soares AMVM (2008) Avoidance test with Enchytraeus albidus (Enchytraeidae): effects of different exposure time and soil properties. Environ Pollut 155:112–116.  https://doi.org/10.1016/j.envpol.2007.10.028 CrossRefGoogle Scholar
  2. Butt KR, Lowe CN (2007) A viable technique for tagging earthworms using visible implant elastomer. Appl Soil Ecol 35:454–457.  https://doi.org/10.1016/j.apsoil.2006.06.004 CrossRefGoogle Scholar
  3. Caro G, Abourachid A, Decaëns T et al (2012) Is earthworms ’ dispersal facilitated by the ecosystem engineering activities of conspecifics? Biol Fertil Soils.  https://doi.org/10.1007/s00374-012-0694-1 CrossRefGoogle Scholar
  4. Chatelain M, Mathieu J (2017) How good are epigeic earthworms at dispersing? An investigation to compare epigeic to endogeic and anecic groups. Soil Biol Biochem 111:115–123.  https://doi.org/10.1016/j.soilbio.2017.04.004 CrossRefGoogle Scholar
  5. Davis JM, Stamps JA (2004) The effect of natal experience on habitat preferences. Trends Ecol Evol 19:411–416.  https://doi.org/10.1016/j.tree.2004.04.006 CrossRefGoogle Scholar
  6. De Bono M, Tobin DM, Davis MW et al (2002) Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419:899–903.  https://doi.org/10.1038/nature01169 CrossRefGoogle Scholar
  7. Demuynck S, Lebel A, Grumiaux F et al (2016) Comparative avoidance behaviour of the earthworm Eisenia fetida towards chloride, nitrate and sulphate salts of Cd, Cu and Zn using filter paper and extruded water agar gels as exposure media. Ecotoxicol Environ Saf 129:66–74.  https://doi.org/10.1016/j.ecoenv.2016.03.013 CrossRefGoogle Scholar
  8. Dou J, Hu S (2014) Individual and combined toxicity of chromium and cadmium on the earthworm Eisenia fetida. Biotechnol Indian J 10:9737–9742Google Scholar
  9. European Economic Community (1984) Council directive 79/831/EEC Annex V, part C. Method for the determination of ecotoxicity. Level 1. Earthworms: artificial soil test. Commission of the European Communities. DGXI/128/82 Rev. 5Google Scholar
  10. Frankenbach S, Scheffczyk A, Jänsch S, Römbke J (2014) Duration of the standard earthworm avoidance test: are 48 h necessary? Appl Soil Ecol 83:238–246.  https://doi.org/10.1016/j.apsoil.2014.04.006 CrossRefGoogle Scholar
  11. Franks NR, Richardson T (2006) Teaching in tandem-running ants. Nature 439:153–153.  https://doi.org/10.1038/439153a CrossRefGoogle Scholar
  12. Heyes CM, Ray ED, Mitchell CJ, Nokes T (2000) Stimulus enhancement: controls for social facilitation and local enhancement. Learn Motiv 98:83–98.  https://doi.org/10.1006/lmot.1999.1041 CrossRefGoogle Scholar
  13. Hoppitt WJE, Brown GR, Kendal R et al (2008) Lessons from animal teaching. Trends Ecol Evol 23:486–493.  https://doi.org/10.1016/j.tree.2008.05.008 CrossRefGoogle Scholar
  14. Hund-Rinke K, Wiechering H (2001) Earthworm avoidance test for soil assessments. J Soils Sediments 1:15–20.  https://doi.org/10.1007/bf02986464 CrossRefGoogle Scholar
  15. International Organization for Standardization (2008) ISO 17512-1 - Soil quality – avoidance test for determining the quality of soils and effects of chemicals on behaviour – part 1: test with earthworms (Eisenia foetida and Eisenia andrei). 12:27Google Scholar
  16. International Organization for Standardization (2012a) ISO 11268-1:2012 – Soil quality – effects of pollutants on earthworms – part 1: determination of acute toxicity to Eisenia fetida/Eisenia andrei. 18Google Scholar
  17. International Organization for Standardization (2012b) ISO 11268-2:2012 – Soil quality – effects of pollutants on earthworms – part 2: determination of effects on reproduction of Eisenia fetida/Eisenia andrei Google Scholar
  18. Lukkari T, Haimi J (2005) Avoidance of Cu- and Zn-contaminated soil by three ecologically different earthworm species. Ecotoxicol Environ Saf 62:35–41.  https://doi.org/10.1016/j.ecoenv.2004.11.012 CrossRefGoogle Scholar
  19. Machado RC, Amaral CDB, Schiavo D et al (2017) Complex samples and spectral interferences in ICP-MS: evaluation of tandem mass spectrometry for interference-free determination of cadmium, tin and platinum group elements. Microchem J 130:271–275.  https://doi.org/10.1016/j.microc.2016.09.011 CrossRefGoogle Scholar
  20. Mathieu J, Barot S, Blouin M et al (2010) Habitat quality, conspecific density, and habitat pre-use affect the dispersal behaviour of two earthworm species, Aporrectodea icterica and Dendrobaena veneta, in a mesocosm experiment. Soil Biol Biochem 42:203–209.  https://doi.org/10.1016/j.soilbio.2009.10.018 CrossRefGoogle Scholar
  21. McBride MB (2011) A comparison of reliability of soil cadmium determination by standard spectrometric methods. J Environ Qual 40:1863–1869.  https://doi.org/10.2134/jeq2011.0096 CrossRefGoogle Scholar
  22. Organisation for Economic Co-operation and Development (1984) OECD 207 – earthworm, acute toxicity tests. OECD Guidel Test Chem 207:9.  https://doi.org/10.1787/9789264070042-en CrossRefGoogle Scholar
  23. Reinecke AJ, Reinecke SA (1996) The influence of heavy metals on growth and reproduction of the compost worm Eisenia fetida (Oligochaeta). Pedobiologia 40:439–449Google Scholar
  24. Reinecke SA, Prinsloo MW, Reinecke AJ (1999) Resistance of Eisenia fetida (Oligochaeta) to Cadmium after long-term exposure. Ecotoxicol Environ Saf 42:75–80.  https://doi.org/10.1006/eesa.1998.1731 CrossRefGoogle Scholar
  25. Siekierska E, Ska-Jasik DU (2002) Cadmium effect on the ovarian structure in earthworm Dendrobaena veneta (Rosa). Environ Pollut 120:289–297.  https://doi.org/10.1016/S0269-7491(02)00152-5 CrossRefGoogle Scholar
  26. Spurgeon DJ, Hopkin SP, Jones TD (1994) Effect of cadmium, copper, lead and zinc on growth, reproduction and survival of earthworm Eisenia fetida. Environ Pollut 84:123–130.  https://doi.org/10.1016/0269-7491(94)90094-9 CrossRefGoogle Scholar
  27. Thorpe W (1963) Learning and instinct in animals, 2nd edn. Methuen, LondonGoogle Scholar
  28. USEPA (1988) Protocols for short- term toxicity screening of hazardous waste sites, EPA/600/3-88/029Google Scholar
  29. USEPA (1996) Method 3052: microwave assisted acid digestion of siliceous and organically based matrices. https://www.epa.gov/sites/production/files/2015-12/documents/3052.pdf. Accessed 5 Oct 2019
  30. Voua Otomo P, Reinecke SA (2010) Increased cytotoxic and genotoxic tolerance of Eisenia fetida (Oligochaeta) to cadmium after long-term exposure. Ecotoxicology 19:362–368.  https://doi.org/10.1007/s10646-009-0418-y CrossRefGoogle Scholar
  31. Zirbes L, Brostaux Y, Mescher M et al (2012) Self-assemblage and quorum in the earthworm Eisenia fetida (oligochaete, lumbricidae). PLoS ONE 7:1–11.  https://doi.org/10.1371/journal.pone.0032564 CrossRefGoogle Scholar
  32. Zirbes L, Deneubourg J, Brostaux Y, Haubruge E (2010) A new case of consensual decision: collective movement in earthworms. Ethology 116:546–553.  https://doi.org/10.1111/j.1439-0310.2010.01768.x CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Zoology & EntomologyUniversity of the Free StatePhuthaditjhabaSouth Africa
  2. 2.Afromontane Research UnitUniversity of the Free StatePhuthaditjhabaSouth Africa

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