Earthworms and their importance to agricultural soils in the inland Pacific Northwest

Scientists estimate that there are approximately 3,000 species of earthworms worldwide (Lee, 1985). The number of species in North America is estimated to be 187, of which 35% are non-native, introduced species (Reynolds, 2020). Distribution of earthworms across the globe is wide and ultimately controlled by properties such as soil temperature, moisture, pH, and texture. At the field or landscape scale, their distribution is extremely patchy or highly variable as a result of the significant influence of these soil properties.

Earthworms are hermaphrodites with both functional female and male organs. Some species are known to be parthenogenetic, reproducing without the exchange of sperm from another individual. An earthworm can produce anywhere from 3 to more than 100 cocoons (Figure 1) per year with the exact number depending on species, environmental conditions, and food quality and quantity (Lee, 1985). Each cocoon, in turn, can contain multiple ova. The number of days it takes for earthworms to hatch from cocoons varies and is based largely on environmental conditions. Delayed hatching during stressful environmental conditions likely serves as an important mechanism protecting against desiccation in warm, dry conditions. Other mechanisms that protect earthworms from dying under adverse environmental conditions include deep burrowing and aestivation, a type of hibernation or resting state (Lee, 1985; Walsh et al., 2019). Earthworms are subject to predation by birds and other soil-dwelling animals but may live anywhere from 1 to 10 years (Coleman & Crossley, 1996).

Earthworms Are Ecosystem Engineers

While the relationship between earthworms and soils has been studied since the time of Darwin, advances in science and technology have only recently allowed us to understand the potential magnitude of their impacts on soil–plant systems (Johnson-Maynard & Strawn, 2016). Because they actively change the soil environment in which they live, through burrowing and the excretion of casts (spherical aggregates containing soil particles, mucilage, and organic matter as show in Figure 2), earthworms influence the numbers and activities of other soil organisms and important processes such as the conversion of organically bound nitrogen to plant-available forms (Blair et al., 1997; van Groenigen et al., 2014). The ability to restructure and modify the soil environment has led to the widespread acknowledgement of earthworms as “ecosystem engineers.”

As we strive to increase the efficiency of agricultural production through conservation of moisture and reduction of synthetic fertilizer inputs, interest in the impacts of earthworms on soil processes and plants has grown. Moreover, given their influence on water and nutrient cycling, soil structural properties, and populations of other soil organisms, earthworms are often considered important indicators of soil health and ecosystem processes (Doran & Zeiss, 2000; Bünemann et al., 2018).

Earthworm Impacts on Soil Properties

The effect that earthworms have on the soil environment varies depending on earthworm density (the number of earthworms present in a specific volume of soil), species composition, and ecological class. Because it reflects how earthworms feed, cast, and burrow, earthworm ecological class is especially important to know when trying to predict earthworm impacts on soil properties. Three major ecological classes are recognized: epigeic, endogeic, and anecic (Bouché, 1977).

Endogeic species live primarily within the upper soil profile (top 6–8 inches) where they feed on organic matter and create complex, horizontal burrows, rarely coming to the soil surface. The dominant endogeic species in the inland Pacific Northwest (iPNW) is Aporrectodea trapezoides (Fauci & Bezdicek, 2002; Walsh & Johnson-Maynard, 2016)—a highly adaptable worm that is found all over the world. One example of its adaptive capacity is that it sometimes deviates from typical endogeic behavior and has been observed to feed on plant residues at the soil surface. Aporrectodea trapezoides also has a high reproductive rate and exhibits parthenogenesis (Fernández et al., 2010, 2011). The dominance of this species in iPNW agricultural fields (Johnson-Maynard et al., 2007; Umiker et al., 2009) suggests that it is not significantly impacted by the typical conservation or reduced-tillage practices used within the region or that it rebounds quickly following a tillage event.

Anecic species tend to be large (3 to 6 inches) and build permanent, deep, vertical burrows that connect to the soil surface where they feed on plant residues. Anecic earthworms create middens, which are small mounds of organic material and casts (earthworm excretions) at burrow openings. Middens are an easy-to-see (Figure 3), physical indication of the presence of anecic species, particularly in the early spring. The only known native species in the iPNW (Driloleirus americanus, or the “giant Palouse earthworm”) is anecic and has only been found in soils that have never been tilled (Sánchez-de León & Johnson-Maynard, 2009). Lumbricus terrestris, commonly known as the “nightcrawler,” is an exotic anecic earthworm found in no-till agricultural soils in the iPNW and throughout the world. Measured densities of L. terrestris in iPNW agricultural soils are low; however, most studies have utilized hand-sorting as a collection method, which is not an optimum method for quantifying populations of deep-burrowing species (Xu et al., 2013; Walsh & Johnson-Maynard, 2016).

The third ecological class is referred to as epigeic and consists of species that live and feed very close to the soil surface. Since these earthworms live at or near the soil surface, their habitat is more highly disturbed by agricultural practices. Their shallow burrowing habit also makes them susceptible to desiccation during the long, dry summer months experienced in dryland agricultural fields in the iPNW. Likely due to their susceptibility to desiccation and tillage, epigeic species have not been found in surveys of iPNW agricultural fields (Fauci & Bezdicek, 2002; Walsh & Johnson-Maynard, 2016).

Through feeding, burrowing, and casting, earthworms can significantly alter soil physical, chemical, and biological properties. Earthworms ingest soil particles as they burrow through the soil. As ingested soil aggregates move through an earthworm’s gut, they are largely destroyed, mixed with mucilage and gut bacteria and excreted as relatively stable casts (Shipitalo & Le Bayon, 2004). Earthworm casts generally have higher water storage, aggregate stability, and nitrogen and carbon mineralization rates than do non-cast aggregates (Ketterings et al., 1997; Blouin et al., 2013; Abail et al., 2017; Hallam & Hodson, 2020). Casts can make up a significant portion of the soil when high densities of earthworms are present and strongly influence soil behavior, including creating hot spots for nutrient cycling. Earthworms can ingest up to 25% of the soil in an A horizon soil (organic matter enriched-mineral soil or topsoil) in a year (Shipitalo & Le Bayon, 2004), and casts have been reported to make up more than 90% of A horizon material in soils with very high earthworm density (Johnson-Maynard et al., 2002). Thus, over time, the accumulation of casts can lead to surface soil with greater nutrient-cycling capacity, water-holding capacity, and structure favorable to crop growth.

Like casting, burrowing activity also has direct influences on soil properties. The deep, vertical burrows of anecic species create pathways that can increase water infiltration into the soil profile (Shipitalo & Butt, 1999; Capowiez et al., 2009) and percolation of water throughout the soil profile (Figure 4). Roots oftentimes grow preferentially though old or even active earthworm channels. The relatively deep channels created by anecic earthworms can provide a route for roots to extend beyond dense, compacted, or clay-enriched soil horizons, which are common in the iPNW (Figure 4). Roots that are limited to old earthworm channels are not uncommon in deep soil cores collected from agricultural fields in the iPNW (Figure 5). Deep rooting increases opportunities for water and nutrient uptake, likely benefiting crop growth. Extensive horizontal burrows created by endogeic species can also increase water infiltration as a high density of large pores near the soil surface, though discontinuous, allows water movement (Ernst et al., 2009; Capowiez et al., 2014).

Results can be mixed, however, as pores created by some endogeic species may be completely backfilled with casts (Figure 6). While earthworm burrowing behavior can increase the amount of water entering the soil profile, it also incorporates organic matter into the soil, which can influence water-holding capacity. Earthworms increase soil organic matter content by ingesting plant residues and incorporating this material into casts that are distributed throughout the soil profile (anecic and epigeic species). Endogeic species can then further decompose and mix organic matter already in the soil profile. As soil organic matter content increases, water-holding capacity can also increase (Ketterings et al., 1997; Hallam & Hodson, 2020).

Population Size and Climate Limitations

In addition to population density and ecological class, the effects of earthworms on soil properties in the iPNW may be limited due to dry periods and soil temperatures above or below thresholds that bring about aestivation. In the iPNW, environmental conditions that allow earthworms to be active generally exist for relatively short periods of time in the spring and fall, especially in dryland agricultural fields where irrigation is not utilized. Walsh et al. (2019) found that earthworm activity in iPNW dryland farming systems was limited to approximately 60 days during the active growing period of wheat. Additionally, the patchy distribution of earthworms across fields makes it difficult to assess the direct and indirect impacts of earthworms on soils and plant growth at field scales.

Another factor that influences the extent which earthworms alter the soil environment is the size of their population. It is suggested that densities greater than 400 earthworms m^–2 (1 m^–2 = 10.76 ft^–2) will have the greatest measurable impact on plant growth; however, densities between 200 and 400 earthworms m^–2 can have a smaller but measurable impact on crop growth (van Groenigen et al., 2014). Earthworm densities in wheat cropping agricultural fields across the iPNW generally range from approximately 50 to 200 earthworms m^–2 with the highest densities reported being around 450 earthworms m^–2 (Walsh & Johnson-Maynard, 2016). Earthworm densities reported in iPNW wheat fields are, therefore, high enough that they could conceivably have a positive impact on crop production. However, given the limited time that they are active each year, positive impacts on plant growth and soil properties may not be easily detected. This could explain results of studies reporting no change in soil physical properties despite increases in earthworm density due to either reduced tillage (Johnson-Maynard et al., 2007) or organic, reduced tillage management (Kahl, 2014) in the iPNW.

Managing for Earthworms

Agricultural practices directly influence earthworm habitats, primarily through the types of inputs used, the crops grown, and mechanical operations. Overall, agricultural practices influence two main factors: (1) the quality and quantity of food available to earthworm populations and (2) the amount of disturbance caused to their habitat. In general, reducing tillage disturbance or adopting no-till practices results in larger earthworm population density (Chan, 2001; Emmerling, 2001; Ernst & Emmerling, 2009). In a side-by-side comparison, the density of endogeic earthworms ranged from 22–42 earthworms m^–2 in chisel-plowed soils compared with 62–111 earthworms m^–2 under no-till after three years of divergent management (Johnson-Maynard et al., 2007). This study, which was conducted within the iPNW, suggests that reduced tillage can nearly double earthworm density in as little as three years (Figure 7) in systems dominated by endogeic species. This result is likely due to differences in direct mortality, environmental conditions, or crop residue (food source) between the two tillage treatments.

Returning high levels of plant biomass to the soil (cash crop residue, cover crop biomass, etc.) or using organic-based fertilizers (i.e., manure) provides good sources of food for earthworms. Research has shown that endogeic species, which are commonly found in iPNW agricultural soils, are more resilient to tillage disturbance when abundant, high quality food sources are available (Schmidt et al., 2003; Simonsen et al., 2010; Kahl, 2014). Endogeic species also tend to be more resilient to disturbance compared with anecic species (Pelosi et al., 2014b), particularly if the tillage is shallow and if the disturbance occurs while populations are dormant. In the iPNW, this might be in the fall when soils are either dry or too cold for earthworms to be active. Avoiding tillage during the spring and after fall rains will also help limit damage to earthworm populations.

In the iPNW, anecic species are predominately found in agricultural fields managed under zero tillage. This is likely due to the fact that anecic species must maintain connectivity to the soil surface where their food source is located. Recreating burrows destroyed by tillage is an energy-intensive activity for earthworms. Their sensitivity to disturbance is likely why these types of earthworms are less common in iPNW fields where true zero tillage is less common than other forms of conservation tillage. However, given their ability to incorporate plant residues into the soil profile, anecic earthworms could be beneficial for increasing soil carbon storage and soil health in general.

Overall, decreased mechanical disturbance caused through tillage allows earthworm populations to flourish, and in time, increased population density may impart a similar effect as the foregone tillage (aeration, incorporation of crop residues, etc.).

Another important management practice to consider is the use of pesticides and their associated impacts on earthworm populations. Much of the research suggests that pesticides can decrease earthworm population density and impact their physiology and behavior (Pelosi et al., 2014a). However, the impact that pesticides have on earthworms depends on several factors, including the specific chemical compound, concentration of the compound, earthworm ecological class, activity levels of the earthworm, and the vertical distribution of earthworms during application. Although research on the direct and indirect effects of different classes of pesticides on earthworms is somewhat limited, insecticides appear to effect mortality most strongly, whereas fungicides appear to impact reproduction to a greater degree (Pelosi et al., 2014a).

The pesticide families reported to be most harmful to earthworms include nicotinoide, carbamate, and oganophosphate insecticides; strobilurin and triazol fungicides; and sulfonylureas herbicides (Pelosi et al., 2014a). Earthworm species that have more contact with the soil surface tend to be most affected, which can include both epigeic and anecic species (Pelosi et al., 2014a). Herbicides tend to be less harmful than other forms of pesticides though effects vary with species and soil environments (Pelosi et al., 2014a). Glyphosate in its proprietary formulation of Roundup, for example, did not significantly harm epigeic earthworms (Pochron et al., 2020) though it decreased activity in anecic species and reproduction in anecic and endogeic species (Gaupp-berghausen et al., 2015). While research shows that earthworm response to pesticides is nuanced, the existence of earthworm populations in Palouse dryland wheat cropping systems after decades of annual pesticide applications suggests some level of resilience to these compounds. However, direct comparisons to earthworm population density in environments without pesticides are generally lacking.

Conclusions

Earthworms are important to the proper function of soils and in the cycling of organic matter to release nutrients for plant growth. An understanding of earthworm population size, number of years that active populations have existed, and types of earthworm species present in a field can help agricultural producers and their CCAs estimate the type and extent of potential impacts to the soil environment. Reducing tillage, returning crop biomass to the soil, and minimizing the use of pesticides known to be harmful are management practices that can help support healthy populations of earthworms.