Earthworm activity and soil structure: consequences for erosion and soil water regimes

Soil structure is a critical factor for most soil functions, including soil fertility. Earthworms contribute to soil structure and formation through humus formation, mineral weathering, and mixing of these components to create stable aggregates, i.e., organo-mineral complexes, which are deposited either on the soil surface or within the soil profile (Le Bayon et al. 2002). They also affect soil mechanical and hydraulic properties through their burrowing activities (Fig. 3a), which generate macropores that significantly impact water infiltration and thus are important for supplying crops with water, as well as controlling surface runoff and erosion.

Fig. 3 a Earthworm gallery in a compacted clod of loamy soil in Northern France (credit C. Pelosi). b Anecic earthworm Lumbricus terrestris (credit S. Barot). c Endogeic earthworm Apporectodea rosea (credit C. Pelosi) Full size image

Burrowing is driven by earthworm activities such as feeding, reaction to drought or cold temperatures, avoidance of predators, and soil oxygenation (Jegou et al. 2002). Pore morphology varies depending on the earthworm ecological group. Anecic earthworms (Fig. 3b) dig large (higher than 1-mm diameter) vertically oriented galleries that extend to depths greater than 1 m in the soil profile. Endogeic earthworm (Fig. 3c) galleries are not preferentially oriented in the vertical direction. The burrow diameter is smaller than anecic burrows, and they are not so deep (Bouché 1972). Epigeic earthworms remain in the litter layer and in the first few centimeters of the soil and thus have little effect on soil macroporosity. In a mesocosm experiment, Ernst et al. (2008) showed that earthworm ecological groups affect soil water characteristics. The anecic Lumbricus terrestris and the endogeic Aporrectodea caliginosa enhanced drying in the 0–15-cm soil layer by increasing soil aeration and subsequently evaporation through their burrows. In contrast, the epigeic Lumbricus rubellus tended to favor water storage in the topsoil. This is probably due to the fact that L. rubellus leaves litter at the soil surface rather than burying it, which prevents evaporation. A. caliginosa induced higher water infiltration rates and faster water discharges to the subsoil than other species, probably because its burrows are temporary and continually being rebuilt.

Earthworm burrows affect water availability to crops. Blouin et al. (2007) showed, studying rice growing in a greenhouse, that the presence of the endogeic worm Reginaldia omodeoi, formerly known as Millsonia anomala, had a positive effect on plant growth in a well-watered treatment, but a negative effect in a water-deficient treatment. This was attributed to lower water availability to rice caused by lower soil water retention capacity in the presence of this compacting earthworm. However, preferential water flow occurred in macropores created by earthworms. This has been documented for different soil types: rice paddy soils (Sander et al. 2008), temperate loamy soils (Capowiez et al. 2009), and temperate clay soils (Jarvis et al. 2007). Preferential flow increases the risk of leaching and subsequent contamination of subsurface and groundwater by nitrogen and pesticides (Ritsema and Dekker 2000; Blackwell 2000). However, the action of earthworms on soil porosity generally has a positive effect on the soil water regime (Ehlers 1975; Clements et al. 1991; Pitkänen and Nuutinen 1998). Clements et al. (1991) showed that, after 10 years of earthworm inoculation, the water infiltration rate increased from 15 to 27 mm h−1. In Mediterranean soils, water percolation was found to be positively correlated with earthworm biomass, burrow length, and burrow surface with r value of 0.66, 0.65, and 0.77, respectively (Bouché and Al-Addan 1997). In this study, a significant correlation between infiltration and earthworm biomass was observed: The infiltration rate increased by 150 mm h−1 per 100 g m−2 of earthworms. This correlation was even stronger when only anecic species were considered in the analysis: 282 mm h−1 per 100 g of anecic m−2 (Bouché and Al-Addan 1997). In contrast, in a corn agroecosystem where earthworm populations were deliberately elevated, the infiltration rate did not vary (Lachnicht et al. 1997).

Water infiltrating through earthworm burrows can be a source of crop water or percolate through the soil profile, but changes in water infiltration also affect surface hydrological processes. In Ohio, the increase in infiltration rate due to anecic earthworm burrows reduced soil erosion by 50 % (Shuster et al. 2002). In Vietnam on an experimental field with 40 % slope, biogenic aggregates of Amynthas khami were responsible for a 75 % decrease in runoff (Jouquet et al. 2007). Endogeic species also increase soil macroporosity and water infiltration, which tends to reduce runoff. However, it has been shown that some endogeic species also produce small-sized casts, which favor surface sealing and contribute to soil erosion (Blanchart et al. 1999). This effect was shown in tropical conditions with Pontoscolex corethrurus, a tropical earthworm. However, this negative effect resulted from a dramatic population increase of one particular species after the land use was changed from forest to pasture in Brazil (Chauvel et al. 1999). Earthworm species that create water stable casts reduce soil sensitivity to splash effects and runoff, but this may reduce water infiltration by increasing surface bulk density (Reddell and Spain 1991b; Blanchart et al. 1999; Chauvel et al. 1999; Shuster et al. 2002). These contradictions between the results about the impact of earthworms on soil structure, water infiltration, and soil erosion are probably due to the fact that this impact depends on the following: (1) the rainfall regime, (2) earthworm abundance, (3) earthworm species, and (4) the amount of organic matter available at soil surface (Blanchart et al. 1997; Hallaire et al. 2000).

Generally, earthworm burrowing and casting activities contribute efficiently to soil erosion control in temperate and tropical soils. In temperate climates, anecic earthworm casts increased soil roughness, reinforced by the presence of organic residues, forming “middens” that reduced surface runoff (Le Bayon et al. 2002). In Finland, surface runoff during rainfall events was negatively correlated with the dry biomass of L. terrestris (Pitkänen and Nuutinen 1998). In three soil tillage treatments where earthworm populations were reduced, increased, or remained unmanipulated, anecic earthworm biomass was identified as an important independent variable contributing to runoff and erosion diminution, and erosion rates decreased exponentially as a function of anecic earthworm biomass (Valckx et al. 2010). Endogeic and anecic casts on the soil surface improve soil structural stability and give a better resistance to erosion (Le Bayon et al. 2002). They may represent considerable amounts of soil, i.e., 2 to 10 kg m−2 in temperate climate, which corresponds to a 5- to 25-mm-thick layer created by earthworms.

Although some cases of soil degradation due to earthworm compacting species are reported in the literature, earthworms generally improve soil structural stability and soil porosity and reduce runoff.

Effect of earthworms on soil organic matter and nutrient cycling

Earthworms contribute to carbon cycling through several complementary mechanisms (Lavelle and Martin 1992; Marinissen and de Ruiter 1993). Anecic and epigeic earthworms directly ingest poorly decomposed litter at the soil surface, while endogeics ingest soil and assimilate a small fraction of the organic matter it contains. Once ingested, the fraction of litter that is not assimilated is fragmented during the digestion process and mixed with soil. Last, the undigested litter and SOM are returned to the soil in the form of earthworm casts. Fresh casts possess active bacteria and high mineralization rates, at least transiently, and these nutrient cycling processes decline with the age of casts.

SOM decomposition and mineralization depend on processes mediated by soil microorganisms. Earthworms change the structure of soil microbial communities in a way that accelerates SOM decomposition and mineralization (see for example Scheu et al. 2002; McLean and Parkinson 2000). Bacteria are strongly implicated in soil organic carbon (SOC) stabilization and nitrogen cycling due to their population size, turnover rates, and ability to produce enzymes required for decomposition/mineralization. While bacteria directly contribute to SOM mineralization, Winding et al. (1997) observed greater protozoa activity in mesocosms with earthworms, which increased mineralization, presumably due to predation of bacteria in the detrivorous food web. Four mechanisms are generally assumed to be responsible for earthworm-microbial interactions (Brown 1995): (i) Soil ingestion stimulates the growth of some microorganisms through the addition of mucus and brings microorganisms in contact with organic residues. (ii) The incorporation of organic matter into the soil creates hot spots of microbial activity. (iii) Earthworms modify soil structure, creating habitats favorable to microbial activity. (iv) Earthworms are responsible for horizontal and vertical transport of microorganisms, which are either transported on earthworm body or in their gut, ingested with soil or litter. While the stimulation of some bacteria within the earthworm digestive tract and in fresh casts is often reported, the long-term effect of earthworms on bacteria biomass in the bulk soil is still under debate. In some studies, bacterial biomass increased in response to earthworm stimulation (Burtelow et al. 1998; Li et al. 2002; Groffman et al. 2004) and decreased following earthworm consumption in other studies (Hendrix et al. 1998; Groffman et al. 2004).

The short-term increase in mineral nutrient availability in the presence of earthworms is well documented, but the long-term effect of earthworms on SOM content is less clear (Lavelle et al. 1992; Don et al. 2008). Incorporation of organic matter into the soil profile by earthworms might lead to a partial protection of surface litter within the SOM. The evidence for this phenomenon comes first from the lower mineralization observed in old and stable earthworm casts (Pulleman et al. 2005; Bossuyt et al. 2005). Second, the organic matter that reaches a deeper soil layer is less prone to decomposition, which might be due to the lower provision of fresh organic matter to these soil layers that suppresses positive priming effects (Fontaine et al. 2007), i.e., the enhancement of SOM decomposition through inputs of labile organic matter that stimulates microbial activities.

Bohlen et al. (1997) calculated that a population of about 100 individuals per m2 of L. terrestris could ingest 840 kg ha−1 year−1 of surface litter in a temperate cornfield. Eriksen-Hamel and Whalen (2007) reported that the availability of soil mineral N, and subsequently the N concentration in soybean grain, is increased with the abundance of earthworms, mostly A. caliginosa. The increase in N availability with increasing earthworm abundances can be significant: A field with high earthworm abundance, 300 individuals m−2, could have 14 kg N ha−1 more in the 0–15-cm soil layer than a field with low earthworm abundance, 30 individuals m−2. The availability of some of the water-soluble nutrients (K, Ca, Mg,…) is also enhanced as SOM and litter pass through earthworm gut, because these nutrients are solubilized and dissolved from soil minerals during the grinding/rearrangement of organo-minerals during gut transit (Carpenter et al. 2007).

Earthworms may also cause N losses from ecosystems. For example, earthworms have been shown, in some cases, to increase denitrification (Horn et al. 2006; Costello and Lamberti 2009; Lubbers et al. 2013) and the leaching of mineral N (Domínguez et al. 2004). However, the stabilization of organic N in earthworm casts could offset these N losses. Such effects of earthworms on the nitrogen balance have not been assessed thoroughly in agroecosystems, and this knowledge gap needs to be addressed.

In summary, processes underlying earthworm’s effects on SOM cycling and nutrient availability are complex, and the balance between positive and negative effects is not clearly established and probably depends on the time of sampling at a specific site.

Effects of earthworms on crop growth and health

Earthworms have inhabited soils for several hundred million years and represent the most abundant belowground biomass in most terrestrial ecosystems (Lavelle and Spain 2001); so, it is likely that coevolution between earthworms and plants could have occurred. The beneficial effect of earthworms on plant growth was recognized more than a century ago (Darwin 1881). Consequently, the effect of earthworms on primary production has been extensively investigated in the laboratory or in the field, respectively, 46 and 54 % of the studies reviewed by Brown et al. (1999), with some experiments monitored for several years (Giri 1995; Blanchart et al. 1997). Here, we give a brief overview of some of the vast literature available on this topic (Lee 1985; Edwards and Bohlen 1996; Lavelle et al. 2001; Edwards 2004).

Brown et al. (1999; 2004) reviewed 246 experiments in tropical countries and concluded that in 53 % of the studies, there was less than 20 % difference in biomass production with and without earthworms. In 4 % of studies, there was more than 20 % reduction in biomass production in the presence of earthworms, such that earthworms were detrimental to plant growth. In the remaining 43 % of studies, there was more than 20 % improvement in biomass production where earthworms enhanced plant growth. Several environmental factors were identified as responsible for variation in biomass production in the presence of earthworms (Brown et al. 1999, 2004). A major determinant is soil type, especially soil texture and carbon content, which account for 43 % of the variation in plant yield response. Sandy soils with a slightly acidic pH show the greatest increase in biomass production in the presence of earthworms (Brown et al. 2004), which was confirmed by Laossi et al. (2010a). Plant functional group is also an important driver: Earthworms induce higher biomass production in perennial species, especially trees, than that in annual species, whereas biomass of legumes is sometimes negatively affected by the presence of earthworms (Brown et al. 2004).

In a review of 67 studies reporting 83 cases located in temperate countries, Scheu (2003) showed that aboveground production increased significantly with earthworms in 79 % of cases, while it decreased significantly in 9 % of cases. Belowground production increased significantly in 50 % of cases and decreased in 38 % of cases. The shoot-root ratio was assessed in 24 % of cases and increased with earthworm abundance in all cases but one study reported by Atiyeh et al. (2000). To summarize, aboveground biomass generally increases in the presence of earthworms, but belowground biomass exhibits a variable response to the presence of earthworms.

The positive correlation between earthworm abundance and crop production is not systematic, and contrasting effects on yields have been observed. For example, a study by Baker et al. (1999) showed that pasture production increased linearly with increasing earthworm abundance, A. caliginosa, Aporrectodea longa, and Aporrectodea trapezoides, being each introduced at 114, 214, 429, and 643 earthworms per m−2. Conversely, Chan et al. (2004) reported that the highest grass production, +49 % higher than that in control without earthworms, was measured in the low abundance treatment, 212 A. longa per m2, not in the high abundance treatment, 424 worms per m−2. This negative effect of high earthworm abundance on crop production is not fully understood, but it could be that adding earthworms above the soil carrying capacity will lead to soil compaction, as observed in Amazonia (Chauvel et al. 1999).

Five mechanisms, reviewed in Brown et al. (2004), are likely responsible for the positive effect of earthworms on plant production. Earthworm-induced changes in soil physicochemical properties, reviewed in Sect. 1, include the following: (i) modification of soil porosity and aggregation, which changes water and oxygen availability to plants, and (ii) greater mineralization of SOM, which increases nutrient availability to the plants. The other three mechanisms involve interactions with other organisms: (iii) biocontrol of pests and parasites, (iv) stimulation of symbionts, and (v) production of plant growth regulators via the stimulation of microbial activity.

Earthworms could be effective for pest biocontrol. For example, earthworms Aporrectodea rosea and A. trapezoides reduced the severity of take all, due to a soil-borne fungal pathogen (Stephens et al. 1994; Stephens and Davoren 1997), and the earthworm R. omodeoi reduced the damage caused by plant parasitic nematodes Heterodera sacchari on rain-fed rice plants (Blouin et al. 2005). Earthworms influenced the development of aphids through their effects on plant growth and nutrient content (Scheu et al. 1999; Eisenhauer and Scheu 2008). While the increase in nutrient availability in the presence of earthworms could increase plant resistance against herbivores, this effect has never been demonstrated in the field. Another way that earthworms could benefit agricultural crop production would be to control weeds, which is possible through their ability to modify seed germination by burial, ingestion, and maternal effects (Laossi et al. 2010b). This idea is supported by the influence of earthworms on natural plant community structure, which can increase or decrease plant density depending on the plant and earthworm species (Decaëns et al. 2003; Hale et al. 2008; Laossi et al. 2009; Eisenhauer et al. 2009), but needs to be confirmed in agroecosystems to determine whether a reduction in herbicide use is possible when earthworms are abundant.

Earthworm interactions with other soil organisms have received less investigation. For instance, the spreading of symbionts, i.e., mycorrhizae, carried by earthworms colonizing new fields was shown by Gange (1993), and Doube et al. (1994) demonstrated that earthworms can increase the nodulation of legume plants by Rhizobium. However, to our knowledge, crop production in response to an earthworm-enhanced redistribution of mycorrhizae or Rhizobium has never been assessed.

Greater production of plant growth regulators in the presence of earthworms was demonstrated (Canellas et al. 2002; Muscolo et al. 1998). These compounds could include signal molecules such as auxin or ethylene produced in earthworm casts, as demonstrated with loss-of-function mutants of Arabidopsis thaliana and transcriptome analysis of earthworm effects on plant development and defense (Puga-Freitas et al. 2012a). The stimulation of cultivable bacteria producing indoleacetic acid, an auxin compound, was also demonstrated (Puga-Freitas et al. 2012b).

Most of these findings regarding effects of earthworms on plant growth and health are positive but tend to be from studies under controlled conditions. Due to the great number of processes involved and the variability of field conditions, it is difficult to confirm these effects in agroecosystems, indicating that more research is needed on earthworm-plant interactions in real environments.