Elsevier

Geoderma

Volume 393, 1 July 2021, 115005
Geoderma

The effects of saline toxicity and food-based AD digestate on the earthworm Allolobophora chlorotica

https://doi.org/10.1016/j.geoderma.2021.115005Get rights and content

Highlights

  • Salts present in digestate can induce osmotic stress in an endogeic earthworm.

  • Similar negative impacts to digestate were observed with the addition of water.

  • Adult earthworms were worse affected than juvenile stages.

Abstract

Anaerobic digestion (AD) is used to produce biogas and can offer a solution in waste management. Digestate, the AD by-product, can be applied to soil to improve fertility. However, the response of soil biological communities is not fully understood. There are mixed reports on its impact on earthworm survival. This study aimed to investigate digestate effects on earthworm mortality, and to elucidate potential mechanisms underlying it, if observed, after digestate application to soil. Juvenile and adult Allolobophora chlorotica were used as model organisms and added to microcosms prepared in a glasshouse trial. Five replicated treatments were: liquid Digestate; Osmotic-Stress (i.e. same salt concentration as digestate); Labile-C (i.e. same Biological Oxygen Demand as Digestate); Synthetic-Digestate a mixture of Osmotic-Stress and Labile-C (i.e. same salt concentration and BOD as digestate); and Water as the control. Treatments were applied at two different standardised rates equivalent to the digestate’s N content (i.e. 150 kg N ha−1 eq. or 300 kg N ha−1 eq.). The two development stages of A. chlorotica had different responses to treatments. Adult biomass was significantly greater in the Water control R150 treatment than in Digestate. Significantly lower juvenile biomass was observed in the Digestate R300 treatment than in the Labile-C and Water control treatments. The biomass of adults in the Labile-C R300 treatment was significantly greater than in the Digestate, Osmotic-Stress, Synthetic-Digestate and Water control treatments. Both life-stages exhibited a decline in biomass across all treatments, but the adults had higher mortality rates. The biomass of adults and juveniles declined, respectively, by 90% and 62% for Digestate applied at the lower rate, and by 96% and 90% at the higher rate. Whereas the abundance of adults and juveniles exhibited 80% and 24% drop at the lower rate, and a 90% and 84% drop at the higher rate. This study demonstrates that digestate can have negative impact on earthworm morbidity and mortality when applied to soil at 60% water filed pore space, with most of the total weight loss per pot due to reduced earthworm abundance. A likely hypothesis could be the osmotic stress induced by salts present in the digestate. However, there are other factors that interact with this effect, including possibly anaerobic impacts caused by high water content soils, as well as other mechanisms that have not been fully elucidated through this experimental design. Nevertheless, this work provides the basis for further ecotoxicology studies on the impact of digestate applied to soil. Further, while this works has shown that digestate can negatively impact A. chlorotica survival, whether the same is true for other earthworm species, ecotypes and life-cycle stages warrants further investigation. Considering the important role that worms play in soil health, field scale studies are also required to monitor the impacts of repeated digestate application on earthworm communities.

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.

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