The effects of herbicides on soil life Part 4: Earthworms

1205

December 2018

DR MARYKE CRAVEN, CHARNÉ MYBURGH, OWEN RHODE and DR JEANETTA SAAYMAN-DU TOIT, ARC-Grain Crops, Potchefstroom

Whilst the use of effective herbicides may provide a feasible option for enhancing weed control, it can become a toxicological risk to invertebrates such as earthworms. It is unavoidable that herbicides will affect earthworms because they are an important component of the soil system that occurs at different soil depths where they interact with plants and other organisms.

Not only can herbicides cause immediate death in some instances, but it can also influence the function, growth, reproduction and overall health of earthworms. Therefore, it is important to be aware of the possible effects that any chemical may have on earthworms before applying it to the soil or on crops.

In the fourth part of our series of articles, we focus on international research findings regarding the impact of herbicides on earthworms. Information presented here represents only a fraction of published results, however.

Why earthworms matter
Earthworms are important components in temperate ecosystems where they influence nutrient cycling and overall ecosystem functioning. They are, furthermore, considered as ecosystem engineers because they increase overall soil fertility by shredding and redistributing organic material in soil and increase soil penetrability for plant roots.

Because of this role that they play in soil formation and maintenance of soil structure and fertility, earthworms are accordingly viewed as a very important group of soil biota in many agroecosystems and natural environments.

Earthworms represent up to 80% of the total invertebrate biomass, and because they can incorporate toxic substances through their skin or by consumption of large amounts of soil, they are the ideal organisms to be used as bio-indicators of soil pollution.

The close relationship between earthworms and the soil enables them to serve as indicators and early warning systems in field studies if soil quality deteriorates. In such field studies, variables such as earthworm density, biomass changes, diversity and reproduction serve as soil quality parameters. As a result, numerous studies were conducted to determine the impact of agrochemicals on earthworm populations. Pesticides1,2, particularly fungicides3 and herbicides4, prove to have negative effects on earthworms that include death, stunted growth and/or poor reproduction.

Herbicide and earthworm mortality
Internationally, research findings published regarding the effect of herbicides on earthworm mortality are contradictory. A 100% mortality rate was reported in Eisenia fetida (the model earthworm species used in studies of annelid toxicology) during a laboratory study where soil was treated with 500 mg/kg and 1 000 mg/kg of 2,4-D, respectively5. In contrast to the laboratory study, no measurable effect was reported on earthworm numbers in a similar field study published during 19906.

According to Wardle7 who published his article during 1995, such discrepancies between laboratory and field studies can partially be explained by the unrealistically high herbicide concentrations that are used in many laboratory studies. Unfortunately, the interpretation of the relevance of findings is much more complex. Factors such as soil characteristics (pH, texture and organic matter content) play a role in the persistence of herbicides and have an effect on soil biological activity. All of these factors must be taken into account during research studies and in the interpretation of their findings.

A research study which focused on the impact of acetochlor on earthworm populations during 2004 suggested that the mortality of earthworms was dependent on the time period of exposure to the herbicide. They stated that the mortality of earthworms increased with increased exposure time to any given concentration acetochlor8.

Therefore, the fatality of a specific herbicide will accordingly depend on factors such as pH, texture and organic matter which play a role in the persistence of a specific herbicide in the soil. Unfortunately, the latter aspect is rarely taken into consideration during research studies.

Numerous studies that focused on glyphosate also showed contradictory findings. Generally, glyphosate is regarded as an environmentally friendly herbicide due to its biodegradation and strong adsorption to soil9,10. However, Domínguez and her research group based in South America11 indicated that the effects of glyphosate on soil fauna remains far from conclusive.

Several studies consistently found very low mortality in certain earthworm species tested12 while others state significant mortality at very high concentrations (50 000 mg/kg)13. A third group found that lethal doses were dependent on the commercial formulation used14. The Domínguez research group conceded that, based on results already available on glyphosate and different earthworm species, it is unlikely that there will be major effects of acute toxicity11.

Herbicide impact on earthworm reproduction and weight
International research findings suggest sub-lethal parameters, such as reproduction or weight of the earthworms to be generally more sensitive than mortality when assessing the effect of herbicides. Although the earthworms accordingly do not necessarily die from exposure, they can be affected, for example, with regard to their capability to reproduce. As a result, various studies report on the effect (or lack of effect) of herbicides on the number of earthworm juveniles or cocoons.

Atrazine drastically reduced growth and cocoon production in E. fetida when applied at 100 parts per million (ppm) and completely stopped growth and reproduction at 200 ppm. Paraquat also slowed down weight gain and cocoon production at 200 ppm15. Similar to the contradictory results obtained by mortality studies, the effect of glyphosate application on earthworm reproduction varies between no significant effect12, a decrease in number of juveniles and/or cocoons16 and increase in cocoon production17.

Several international studies similarly report concentration-dependent weight loss in various earthworm species because of glyphosate intoxication14,18. Aminomethylphosphonic acid (AMPA) is one of the main metabolites of glyphosate and is classified as being persistent in soils. The Domínguez research group11 found that the biomass loss experienced by the earthworms at various AMPA dosages appeared to be related to the higher reproduction rate in these treatments.

Results indicated that although a higher number of cocoons were produced, the cocoons had lower levels of fertility17 or that the juveniles and cocoons produced had a decreased biomass. These studies concluded that the physiological ability of earthworms growing in soils contaminated with high doses of AMPA decreases in terms of development, growth, reproduction and their ability to accomplish key ecosystem functions11.

Herbicide impact on locomotor activity of earthworms
The skin of oligochaete worms is richly supplied with chemoreceptors and many species exhibit a capacity for considerable locomotor activity (i.e. movements or methods that earthworms use to move from one place to another). It was speculated that earthworms likely have the capability to both detect contaminated soil and move away from it. In a laboratory study, researchers observed that the earthworm E. fetida migrates away from soil contaminated by the fungicide Mancozeb19.

During 2004 a Washington State University research group20 made similar observations when glyphosate contaminated soil was incorporated in their trial. They also suggested that exposure to recommended glyphosate concentrations results in low to negligible acute toxicity in E. fetida. It was, however, also demonstrated that glyphosate appeared to alter the locomotor activity of these earthworms. The exposure of the earthworms to glyphosate stimulated avoidance activity, with the worms appearing to migrate to uncontaminated soils.

Based on these results researchers speculated that under natural field conditions, these earthworms would most likely migrate onto the surface of contaminated soil where they will be exposed to predation, UV radiation and/or desiccation. Therefore, although the glyphosate might not directly kill the earthworms, the application thereof might alter their locomotor activity in such a way that it could potentially compromise their survival20.

Points to ponder
Critique expressed by some researchers in earthworm related research is that most studies make use of compost earthworms (Eisenia species) that commonly do not inhabit agroecosystems and that more studies should be done on the species that are more common to agroecosystems21. A study conducted during 2016 further concluded that chemical uptake by earthworms cannot be generalised between species because the influence of species’ traits can vary depending on the nature of the studied chemicals22.

Studies report that some earthworm species such as Aporrectodea caliginosa and Allolobaphora chlorotica demonstrate the ability to adapt to residual glyphosate and atrazine contamination in agricultural soils by activating detoxification and antioxidant enzymes faster23,24. It is therefore entirely possible that species shifts could (or have) occurred over time to favour certain species of earthworm as a result of herbicide application. The dynamics associated with such a shift warrant further investigation.

There is accordingly much we don’t know as to what is happening with the earthworms. One reason might be that current research does not cast the net wide enough to include more earthworm species. A second reason may be that the studies undertaken fail to investigate a more comprehensive scenario that would accurately reflect a true on-farm scenario. Such a comprehensive study would typically have to include different soil types, soil pH, organic matter, various agricultural tillage practices, crop rotation effects and the whole range of agrochemicals that are annually applied.

For instance, no-till practices regulate soil temperature to a greater extent than tilled soils. Recent studies suggested that exposure to the same pesticide concentration at different temperatures lead to different toxicity responses in earthworms, with increase in temperature exposure generally resulting in an increase in toxicity while a decrease in temperature leads to a decrease in toxicity25.

Although various studies showed that herbicides as well as fungicides have a potential detrimental impact on earthworms under laboratory conditions, it remains unclear exactly what takes place under field conditions. The question also remains whether certain soil characteristics or cultivation practices provide a buffer effect that minimises the potential detrimental effects of agrochemicals on earthworms.

Readers are welcome to contact the authors at ARC-Grain Crops with any enquires they might have at 018 299 6100.

Reference

  1. Lüscher, G, Jeanneret, P, Schneider, MK, Turnbull, LA, Arndorfer, M, Balázs, K, Báldi, A, Baily, D, Bernhardt, KG, Choisis, JP, Elek, Z, Frank, T, Friedel, JK, Kainz, M, Kovács-Hostyánszki, A, Oschatz, ML, Paoletti, MG, Papaja-Hülsbergen, S, Sarthou, JP, Siebrecht, N, Wolfrum, S and Herzog, F. 2014. Responses of plants, earthworms, spiders and bees to geographic location, agricultural management and surrounding landscape in European arable fields. Agric. Ecosyst. Environ. 186, 124 – 134.
  2. Mosleh, YY, Ismail, SMM, Ahmed, MT and Ahmed, YM. 2003. Comparative toxicity and biochemical responses of certain pesticides to the mature earthworm Aporrectodea caliginosa under laboratory conditions. Environ. Toxicol. 18, 338 – 346.
  3. Paoletti, MG, Sommaggio, D, Favretto, MR, Petruzzelli, G, Pezzarossa, B and Barbafieri, M. 1998. Earthworms as useful bioindicators of agroecosystem sustainability in orchards and vineyards with different inputs. Appl. Soil Ecol. 10, 137 – 150.
  4. Pizl, V. 1988. Interactions between earthworms and herbicides 1. Toxicity of some herbicides to earthworms in laboratory tests. Pedobiologia 32, 227 – 232.
  5. Correia, FV and Moreira, JC. 2010. Effects of glyphosate and 2,4-D on earthworms (Eisenia foetida) in laboratory tests. Bull. Environ. Contam. Toxicol. 85, 264 – 268.6
  6. Potter, DA, Buxton, MC, Redmond, CT, Patterson, CG and Powell, AJ. 1990. Toxicity of pesticides to earthworms (Oligochaeta: Lumbricidae) and effect on thatch degradation in Kentucky bluegrass turf. J Econ. Entomol. 83, 2 362 – 2 369.
  7. Wardle, DA. 1995. Impacts of disturbance on detritus food webs in agro-ecosystems of contrasting tillage and weed management practices. Adv Ecol Res 26, 105 – 185.
  8. Xiao, H, Zhou, QX and Liang, JD. 2004. Single and joint effects of acetochlor and urea on earthworm Eisenia fetida populations in phaiozem. Environ Geochem Health 26, 277 – 283.
  9. Barja, BC and Santos, MA. 2005. Aminomethylphosphonic acid and glyphosate adsorption onto goethite: A comparative study. Environ. Sci. Technol. 39, 585 – 592.
  10. Vereecken, H. 2005. Mobility and leaching of glyphosate: A review. Pest Manag. Sci. 61, 1 139 – 1 151.
  11. Domínguez, A, Brown, GG, Sautter, KD, Oliveira, CMR, Vasconcelos, EC, Niva, CC, Bartz, MLC and Bedano, JC. 2016. Toxicity of AMPA to the earthworm Eisenia andrei Bouché, 1972 in tropical artificial soil. Sci. Rep. 6, 19731. Retrieved from: DOI:10.1038/srep19731.
  12. Dalby, PR, Baker, GH and Smith, SE. 1995. Glyphosate, 2,4-DB and dimethoate: effects on earthworm survival and growth. Soil boil. Biochem. 27, 1 661 – 1 662.
  13. Garcia-Torres, T, Guiffré, L, Romaniuk, R, Ríos, RP and Pagano, EA. 2014. Exposure assessment to glyphosate of two species of annelids. Bull. Environ. Contam. Toxicol. 93, 209 – 214.
  14. Piola, L, Fuchs, J, Oneto, ML, Basack, S, Kesten, E and Casabé, N. 2013. Comparative toxicity of two glyphosate-based formulations to Eisenia andrei under laboratory conditions. Chemosphere 91, 545 – 551.
  15. Fisher, E. 1989. Effects of atrazine and paraquat-containing herbicides on Eisenia fetida (Annelida. Oligochaeta). Zool. Anz 223, 291 – 300.
  16. Correia, FV and Moreira, JC. 2010. Effects of glyphosate and 2,4-D on earthworms (Eisenia foetida) in laboratory tests. Bull. Environ. Contam. Toxicol. 85, 264 – 268.
  17. Santadino, M, Coviella, C and Momo, F. 2014. Glyphosate sub lethal effects on the population dynamics of the earthworm Eisenia fetida (Savigny, 1826). Water soil Pollut. 225, 2207. Retrieved from: Doi 10.1007/s11270-014-2207-3.
  18. Yasmin, S and D’Souza, D. 2007. Effect of pesticides on the reproductive output of Eisenia fetida. Bull. Environ. Contam. Toxicol. 79, 529 – 532.
  19. Reinecke, AJ, Maboeta, MS, Vermeulen, LA and Reinecke, SA. 2002. Assessment of lead nitrate and Mancozeb toxicity in earthworms using the avoidance response. Bull. Environ. Contam. Toxicol. 68, 779 – 786.
  20. Verrell P and Van Buskirk, E. 2004. As the worm turns: Eisenia fetida avoids soil contaminated by a glyphosate-based herbicide. Bull Environ. Contam. Toxicol 72, 219 – 224.
  21. Gaupp-Berghausen M, Hofer M, Rewald B and Zaller JG. 2015. Glyphosate-based herbicides reduce the activity and reproduction of earthworms and lead to increased soil nutrient concentrations. Sci. Rep. 5, 12886. Retrieved from: DOI:10.1038/srep12886.
  22. Carter LJ and Boxall ABA. 2016. Does uptake of pharmaceuticals vary across earthworm species? Bull Environ Contam. Toxicol. 97, 316 – 322.
  23. Bon D, Gilard V, Massou S, Pérès G, Malet-Martino M, Martino R and Desmoulin F. 2006. In vivo 31P and 1H HR-MAS NMR spectroscopy analysis of the unstarved Aporrectodea caliginosa (Lumbricidae). Biol. Fertil. Soils 43, 191 – 198.
  24. Givaudan N, Binet F, Le Bot B and Wiegand C. 2014. Earthworm tolerance to residual agricultural pesticide contamination: field and experimental assessment of detoxification capabilities. Environ. Pollut. 192, 9 – 18.
  25. Velki, M and Ečimovič, S. 2015. Changes in exposure temperature lead to changes in pesticide toxicology to earthworms: A preliminary study. Environmental Toxicology and Pharmacology 40, 774 – 784.

Publication: December 2018

Section: On farm level