Effects of biochar on earthworms in arable soil: avoidance test and field trial in boreal loamy sand
Introduction
Biochar use as a soil amendment has been proposed as a greenhouse gas mitigation strategy due to the high stability of carbon (C) in it (Cheng et al., 2008, Lehmann et al., 2008, Woolf et al., 2010). The need for evaluating the suitability of biochar technology has increasingly promoted research in this area. Furthermore, biochar may also benefit soil functions (Glaser et al., 2002, Lehmann et al., 2008, Major et al., 2010, Vaccari et al., 2011) and, depending on its properties and those of the soil, it may increase soil pH (Vaccari et al., 2011), improve plant nutrition through the nutrients it contains (Major et al., 2010, Xu et al., 2013) and reduce nutrient leaching (Brockhoff et al., 2010, Güereña et al., 2012, Major et al., 2012). These effects may contribute to enhanced abundance and activity of soil organisms (Liang et al., 2010, Lehmann et al., 2011, Güereña et al., 2012), increased yields of agricultural crops (Major et al., 2010, Vaccari et al., 2011, Zhang et al., 2012) and improved environmental quality (Lehmann et al., 2011, Major et al., 2012).
The effects of biochar on the soil biological community have received little attention, with the exception of the rather well established increase in microbial biomass under most conditions (Liang et al., 2010, Lehmann et al., 2011, Güereña et al., 2012). In particular, the effects of biochar on soil fauna have so far been only sporadically studied (Lehmann et al., 2011). This is a clear shortcoming considering the high potential of soil animals, particularly earthworms, for ingesting, modifying and transporting biochar in the pedosphere (Topoliantz and Ponge, 2003, Topoliantz and Ponge, 2005, Eckmeier et al., 2007) and subsequently influencing the microbial activity (Lehmann et al., 2011). Earthworms are globally common members of soil communities and have favorable influences on soil physical structure, litter decomposition (Lavelle, 1988, Blouin et al., 2013) and soil nutrient availability for plants (Lavelle et al., 1998, Chaoui et al., 2003, Blouin et al., 2013). These functions make earthworms important organisms for assessing the effects of any substances added into soil, including biochar (Yeardley et al., 1996, Hund-Rinke and Wiechering, 2001, Busch et al., 2011, Li et al., 2011).
Favorable effects of biochar on earthworm behavior and activity have been attributed to decreased soil acidity (Topoliantz and Ponge, 2003, Topoliantz and Ponge, 2005, Van Zwieten et al., 2010, Busch et al., 2011) which could, when biochar particles are ingested and the pH in the gut of earthworms increased, assist earthworms in the assimilation of other resources (Weyers and Spokas, 2011). When earthworms ingest biochar particles containing high microbial biomass, it could contribute microbial enzymes to their digestive system (Topoliantz and Ponge, 2003). Negative responses to biochar by earthworms include avoidance and weight loss (Li et al., 2011) and decreased survival of Eisenia fetida Sav. (Liesch et al., 2010). These effects have been related to desiccation caused by high water retention of biochar (Li et al., 2011) or, in the case of poultry manure biochar, to the salinity, toxic effects of ammonia or to a rapid increase in soil pH (Liesch et al., 2010).
Previous experiments have not only given conflicting results on the effects of biochar on earthworms, but they have also been laboratory-based (Topoliantz and Ponge, 2003, Topoliantz and Ponge, 2005, Noguera et al., 2010, Van Zwieten et al., 2010, Busch et al., 2011, Li et al., 2011), and on earthworm species not common in agricultural soils (Van Zwieten et al., 2010, Busch et al., 2011, Gomez-Eyles et al., 2011, Li et al., 2011). Only two studies to our knowledge have been conducted under field conditions, neither of them comprised replicated treatments (Husk and Major, 2010, Weyers and Spokas, 2011).
Most field studies exploring the biochar-mediated changes in soil quality and plant growth have been conducted in (sub-) tropical (Major et al., 2010, Vaccari et al., 2011, Zhang et al., 2012) or temperate (Güereña et al., 2012, Jones et al., 2012) climates. Additional research is needed in colder climates, where soils are less affected by low contents of organic matter. For these reasons, this study explored the effects of spruce chip biochar on the earthworm species common in arable soils under both laboratory and boreal field conditions.
Section snippets
Biochar
The biochar was produced by pyrolising chips of debarked spruce (Picea abies (L.) H. Karst.) in a continuously pressurized carboniser (Preseco Oy, Lempäälä, Finland) at 550–600 °C for 10–15 min. The biochar was cooled overnight in an airtight silo and then ground. The particle size distribution was determined by dry sieving. The ash content and the total elemental composition of the biochar were determined by dry ashing after Miller (1998). A 1.5 g sample was dry-ashed in a laboratory muffle
Biochar properties
The biochar particle size distribution (by weight) was 26% 0–0.25 mm, 22% 0.25–1 mm, 40% 1–5 mm, 10% 5–10 mm and 2% >10 mm. The biochar contained considerable amounts of total Ca, K, P and Mg (Table 1). In contrast, the liming equivalent of the biochar (9 g CaCO3 kg−1) and the carbonate–C content of the biochar (1.2 g kg−1 equivalent to 10 g CaCO3 kg−1) were both low. The high content of Corg (881.3 g kg−1) and low atomic (0.34) H/Corg ratio of the biochar (Table 1) provided evidence of a relatively high
Avoidance test
The lack of effect of 16 g kg−1 of biochar on the habitat choice of A. caliginosa after two days, but significant avoidance of the biochar at 14 days, may be attributable to the increased water retention caused by the biochar application. Li et al. (2011) reported no significant effect of 10 g kg−1 of biochar on Eisenia fetida. in an avoidance test lasting for 48 h, but significant avoidance of 100 g kg−1 of biochar was reported unless the biochar was wetted to its field capacity (2.2 mL water per g
Conclusions
This study is to our knowledge the first where the biochar effects on earthworms were investigated both in a laboratory avoidance test and in a replicated field experiment that allowed statistical evaluation of treatment effects. In the avoidance test, biochar did not affect the habitat choice of earthworms within two days, but after two weeks, the earthworms tended to avoid biochar slightly but significantly. As the liming equivalence and contents of heavy metals and PAH in the biochar were
Acknowledgments
The authors thank Sampo Tukiainen (Preseco Oy) for providing the experimental biochar, Mikko Hakojärvi for his help with the TDR measurements and Johannes Mäkinen for his help during earthworm sampling from the field. The authors acknowledge Ilya Belevich for the scanning electron microscopy imaging, Miia Collander and Johanna Muurinen for technical assistance with the biochar and soil analysis, Festus Anasonye for PAH analyses of the biochar and Arja Tervahauta for the analysis of the H
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