The effects of saline toxicity and food-based AD digestate on the earthworm Allolobophora chlorotica
Introduction
Earthworms are ecosystem engineers with functional roles within the soil profile that affect ecological processes and properties. They modify soil properties through bioturbation processes, including their burrowing and feeding action (Huber et al., 2008, Ritz et al., 2009, Blouina et al., 2013). As such, they have been widely used as bioindicators in soil monitoring networks and environmental assessments (Huber et al., 2008).
Allolobophora chlorotica Savigny (Lumbricidae), is an intermediate earthworm (in the epi-endo-anecic ecological category), that develops as a pale or green morph (Satchell, 1967; Bottinelli et al., 2020). They are the most commonly found earthworm in England, especially in neutral to base-rich grasslands and arable soils, where they are usually found in the rhizosphere (Jones and Eggleton, 2014). Their tolerance to various degrees of soil moisture is morph dependent, and both morphs can be found in different soil types of pH ranging from 4.5 to 8.2 (Satchell, 1967, Sims and Gerard, 1999). They create horizontal burrows and excrete casts, usually within the soil rather than on the surface. Earthworm casts are rich in plant available nutrients (Lee, 1985, Vos et al., 2014) and their feeding action can facilitate the formation of soil aggregates (Kavdir and Ilay, 2011).
Soil organisms known to be beneficial ecosystem engineers like earthworms are often used in toxicity studies. These studies generally rely on commercially available epigeic and anecic earthworms. However, these are not best suited to soil toxicity studies or for determining the impact of nutrient mobility and availability (Sizmur and Hodson, 2009). For example, epigeics can be directly exposed to soil amendments but, like anecics, feed mostly on plant matter. Conversely, epi-endo-anecic, such as A. chlorotica, are exposed to and feed on accumulated residues within the soil profile and so may be better models for soil toxicity and nutrient mobility studies (Van-Camp et al., 2004, Sizmur et al., 2017).
It has been estimated that 180 million tonnes of digestate, a by-product of anaerobic digestion (AD), are produced in the EU28 every year. A variety of feedstocks can be used to produce energy through AD processes, such as manures, crop residues, energy crops and food waste (Corden et al., 2019). Digestate is mostly used as a soil amendment in agricultural systems. Its composition is variable, mainly dependent on the feedstock digested. Its application to land has potential environmental risks, such as ammonia emissions, heavy metal contamination and/or a high salt content, and its impact on soil biological communities is not well understood (Taylor et al., 2011, EA and WRAP, 2014, Möller, 2015, Corden et al., 2019). The impact on earthworm survival following the application of food-based digestate to land has been shown to be site dependent (WRAP, 2015); abundance reduced in some sites, whereas in others no significant difference was observed. Another study found that the spreading of digestate could reduce the abundance of endogeics, and that A. chlorotica was missing from such treatment at a particular site (Koblenz et al. 2015). Sizmur et al. (2017) observed an increase in the biomass of anecic earthworms following the application of digestate incorporated with straw.
The main factors affecting digestate impacts on earthworm populations remain unknown but are likely to include osmotic stress due to salts present, increased anaerobicity due to digestates’ biochemical oxygen demand (BOD), chemical oxygen demand and pH impacts due to the presence of volatile fatty acids (WRAP, 2015).
This study aimed to elucidate mechanisms associated with the effect of BSI PAS 110 (British Standards Institution Publicly-Available Specification) food-based digestate on A. chlorotica survival following application to soil, and whether there is a different response between the juvenile and adult stages. This was done to test the following hypotheses:
- 1.
Digestate application to soil increases A. chlorotica mortality
- 2.
Increased A. chlorotica mortality is caused by salt stress
- 3.
Increased A. chlorotica mortality is caused by anaerobicity resulting from the digestate application
Section snippets
Experimental design
The experiment used independent measures in a randomised block design. Microcosms were constructed using 10.3 L white food-safe polypropylene boxes (28.6 × 19.8 × 27.3 cm) with six 1.5 mm drainage holes. The hook side of self-adhesive hook & loop tape, 2.5 cm wide, was attached around the internal rim of each box to prevent earthworms escaping (Lubbers and van Groenigen, 2013).
The boxes were filled with loamy sand topsoil (80.6% sand, 14.2% silt, 5.2% clay, 3.0% SOM, pH 6.6 H2O) collected from
Earthworm biomass response to treatments
The combined initial biomass of both juvenile and adult stages before they were added to boxes did not differ across treatments applied at R150 lower rate (p = 1.0, ANOVA) or R300 higher rate (p = 0.9, ANOVA).
Earthworm biomass at the end of the experiment significantly declined compared to initial biomass for both stages at both application rates, R150 (juveniles p < 0.001, adults p < 0.001) or R300 (juveniles p < 0.001, adults p < 0.001), across all treatments, including the Water control (
Discussion
This study aimed to elucidate mechanisms associated with the effect of PAS 110 food-based digestate on A. chlorotica survival following application to soil, and whether there is a different response between the adult and juvenile stages. Digestate has properties that can contribute towards improving soil nutrition (Wallace et al., 2011, WRAP, 2015). However, its impact on soil biological communities is not fully understood. Based on the findings of this study, earthworm biomass and survival may be
Conclusion
This study demonstrates that digestate can cause increased mortality of A. chlorotica. However, the experimental setup was not conducive to earthworm survival, although it was not unrealistic for field conditions. A combination of different factors may have explained the variable mortality rates amongst earthworms. Those factors could have been: Horizontal stratification through the soil profile; the application of high-water content amendments or just water to soils that are already wet;
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors would like to thank Mr Andrew P. Cooley and Mr Kevin Jones for their demonstration work on analytical techniques of chemical analyses, and Dr Lucy Crockford on BOD analysis.
References (50)
- et al.
Oxygen uptake of active and aestivating earthworm Glosso scolex paulistus (Oligochaeta, Glossoscolecidae)
Comp. Biochem. Physiol.
(1985) - et al.
An explicit definition of earthworm ecological categories – Marcel Bouché’s triangle revisited
Geoderma
(2020) - et al.
Complementary irrigation with saline water and soil organic amendments modified soil salinity, leaf Na+, productivity and oil phenols of olive trees (cv. Chemlali) grown under semiarid conditions
Agric. Water Manag.. Elsevier
(2020) - et al.
Using earthworms as model organisms in the laboratory: Recommendations for experimental implementations
Pedobiologia
(2010) - et al.
Influence of biogas digestate on density, biomass and community composition of earthworms
Ind. Crops Prod.
(2015) - et al.
A simple and effective method to keep earthworms confined to open-top mesocosms
Appl. Soil Ecol.
(2013) - et al.
Differences in ionic properties of salts affect saline toxicity to the earthworm Eisenia fetida
Appl. Soil Ecol.
(2014) Anion adsorption by soils and soil materials
Adv. Agron.
(1979)- et al.
Inclusion complexes of starches with hydrocarbons
Carbohydr. Polym.
(2000) - et al.
Selecting biological indicators for monitoring soils: A framework for balancing scientific and technical opinion to assist policy development
Ecol. Ind.
(2009)
Do earthworms impact metal mobility and availability in soil? - A review
Environ. Pollut.
Milled cereal straw accelerates earthworm (Lumbricus terrestris). growth more than selected organic amendments
Appl. Soil Ecol.
Do earthworms affect phosphorus availability to grass? A pot experiment
Soil Biol. Biochem.
Effects of Biosolids at Varying Rates on Earthworms (Eisenia fetida) and Springtails (Folsomia candida)
Applied and Environmental Soil Science
Fitting Linear Mixed-Effects Models Using lme4
J. Stat. Softw.
A review of earthworm impact on soil function and ecosystem services
Eur. J. Soil Sci.
Digestate and compost as fertilisers: Risk assessment and risk management options
Edited by V. Bertato. European Commission, Directorate General – Environment, Brussels
Eophila oculata at Verulamium: a Roman Earthworm Population?
Nature
Biology of Earthworms
Studies on the Relationships Between Earthworms and Soil Fertility: IV. On the Life Cycles of Some British Lumbricidae
Ann. Appl. Biol.
An R Companion to Applied Regression
Cited by (4)
The impact of anaerobic digestate on soil life: A review
2023, Applied Soil EcologyBiochar-enhanced agricultural application of liquid digestate from food waste anaerobic digestion for celery cultivation
2023, Science of the Total EnvironmentShort- and long-term impacts of anaerobic digestate spreading on earthworms in cropped soils
2021, Applied Soil EcologyCitation Excerpt :At the lethal doses of the territorial digestate in the microcosms, the ammoniacal N soil content was too low to completely explain the observed toxicity: this suggests that other compounds originating from the inputs may also affect digestate toxicity to earthworms. Urine degradation products such as benzoic acids or sulphides (Curry, 1976) could also be toxic, as could diverse ionic compounds through salinity or CEC (Natalio et al., 2021; Pivato et al., 2016; Tigini et al., 2016). However, it is unlikely that heavy metal contamination was involved in the observed short-term toxicity.
The effects of inflow of agricultural biogas digestate on bivalves’ behavior
2021, Environmental Science and Pollution Research