Importance of earthworms

1.1.1. History of earthworms

Intestinal microbes are important to the performance and health of their animal hosts (Shreiner et al., 2015; Blake and Suchodolski, 2016; Fouhse et al., 2016; Liang et al., 2018).

Based on fossil records, worm-like triploblastic metazoans and annelids existed 0.5 to 1.1 billion years ago (Seilacher, 1998; Morris and Peel, 2008). Aristotle (384 to 322 B.C.) was one of the first historically famous persons understanding the importance of earthworms in soil formation and maintenance of soil structure and fertility. He suitably called them “The Intestine of the Earth”

(Yadav, 2017). Approximately three hundred years later Cleopatra VII (69 to 30 B.C.), one of the most famous female rulers in history, was fascinated by these inconspicuous soil creatures and declared them to be sacred after she recognized the strong contribution of earthworms to the Egyptian agriculture (Abul-Soud et al., 2009; Yadav, 2017). At this time, the removal of earthworms from Egypt carried the death penalty (Abul-Soud et al., 2009). However, until the late 1800s, when Charles Darwin published 1881 his book “The Formation of Vegetable Mould through the Action of Worms” (Darwin, 1881), earthworms were commonly underappreciated and considered as garden pest (Brown et al., 2004). Darwin and his work brought finally widespread public attention to the central importance of earthworms in the maintenance of soil structure, aeration, drainage and fertility, including the decomposition of dead plant material and animal matter (Darwin, 1881; Brown et al., 2004).

Soil fertility is defined as the capacity of soil to supply essential nutrients to crops and is strongly associated with the productivity of soils (Stockdale et al., 2002), which is one of the most important aspects regarding the nutrition of 7.7 billion people on the planet, a number which increases year to year (https://www.worldometers.info). More than 98% of the world nutrition originates from terrestrial ecosystems (Schinner and Sonnleitner, 1996), demonstrating the importance of these ecosystems and the need for understanding the factors that influence their functions. An ecosystem can be defined as “a unit of interaction among organisms and between organisms and their physical environments, including all living things within a defined area”

(Lewis, 1992). In this regard, the earthworm is one such factor that influence the functions of the terrestrial ecosystem. With up to 2,000 individuals per square meter, earthworms represent the most dominant marcrofauna in many soils (Figure 1; Edwards and Bohlen, 1996), and their feeding habits result in substantial physical, chemical, and biological alterations of the terrestrial biosphere, including the turnover of elements and diverse effects on plant growth (Tomati et al., 1988; Lavelle et al., 1998; Brown et al., 2000; Bastardie et al., 2003). Since it is known that earthworms lead to alterations in physical structure, nutrient fluxes, and energetic status, earthworms are aptly called soil ecosystem engineers (Jones et al., 1994; Lavelle et al., 1998).

Figure 1. Abundance of earthworms in different pastures. A country listed twice represents two different samplings in that country. Figure based on numbers obtained from Edwards and Bohlen, 1996.

1.1.2. Earthworms and the turnover of elements

The important role of earthworms in the breakdown of complex organic matter, for example dead plant biomass and animal material, is attributable to their high abundance in many soils and their propensity to consume high amounts of their habitat (Edwards and Bohlen, 1996).

Therefore, earthworms influence organic matter and nutrient cycles on four different levels: (a) during the gut passage, (b) in fresh earthworm cast, (c) in aging cast , and (d) during the long-term genesis of the soil profile (Lavelle and Martin, 1992). In this regard, ingested organic matter that passes through the earthworm gut is broken down into much smaller particles, resulting in a greater surface area of organic matter exposed to further microbial decomposition (Martin, 1991).

Previous experiments demonstrated that a 90% decreased earthworm population results in a 43%, 30% and 32% increase of fine, coarse, and total particulate organic matter, respectively (Parmelee et al., 1990). These findings indicate the positive correlation between the annelid biomass and the amount of decomposed organic matter, and furthermore illustrates the high importance of earthworms in the fragmentation and breakdown of complex organic material incorporated in the terrestrial biosphere. The effectivity of organic matter fragmentation and incorporation into soil is dependent on the different feeding habits of earthworms (Section 1.1.4).

Anecic earthworms (e.g., Lumbricus terrestris) incorporate large amounts of organic matter into soil and are able to ingest large litter fragments by pickling off smaller pieces (Edwards and Bohlen, 1996). In contrast, epigeic and endogeic earthworms either do not incorporate organic matter into soil or feed only on already fragmented material (Ferriére, 1980; Judas, 1992).

However, the concomitant occurrence of anecic and endogeic earthworms in many soils, suggesting a synergistic effect on the reallocation of organic matter in the soil profile (Shaw and Pawluk, 1986a, 1986b). Especially in the renewal of forests ecosystems, the mixing and

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INTRODUCTION 3 fragmentation of the litterfall by the activity of earthworms turned out as fundamentally important (Bernier and Ponge, 1994). Beyond that, by the repeated ingestion and turnover of soil and organic matter, earthworms (a) facilitate the rate of mineralization (a process defined as the conversion of organic forms from organic material to plant utilizable inorganic forms) (Edwards and Bohlen, 1996) and (b) enhance nitrogenous gas emission of soil and the nitrogen uptake by plants (Karsten and Drake, 1997; Matthies et al., 1999; Borken et al., 2000; Bertora et al., 2007;

Rizhiya et al., 2007; Lubbers et al., 2011).

1.1.3. Earthworms and the effect on plant growth

Earthworms share the soil environment with roots and the impact on plant growth and productivity is therefore unavoidable (Figure 2). These impacts on plant growth including root development and productivity can occur on three levels: physically, biologically, and chemically (Figure 2; Edwards, 2004). While the physical and chemical impact on plants is mostly indirect, the biological effect can be either direct or indirect.

Figure 2. Simplified model connecting the physical, chemical, and biological effects of earthworms on plant growth and nutrition. Figure modified from Edwards, 2004.

In more detail, earthworms have an indirect biological effect on plants when they (a) disperse or change the populations and activity of plant-beneficial microbes (e.g., plant promoting rhizobacteria or nitrogen fixing root symbionts), plant pests, parasites and pathogens (Dash et al., 1980; Brown, 1995; Nakamura et al., 1995 Brown, 1995; Anderson and Bohlen, 1998; Lavelle et 19

Earthworms Plants

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Soil

al., 1998; Maraun et al., 1999; Brown et al., 2000), or (b) produce plant promoting or regulating substances (e.g., hormones and vitamins) (Gavrilov, 1963; Nielson, 1965; Harti et al., 2001b, 2001a). In contrast, root abrasion, ingestion of living plant material or seeds, and burial of seeds by earthworms are examples of direct biological effects (Chen and Lui, 1963; Hameed and Bouchè, 1993; Barrion and Litsinger, 1997; Brown, 1999). Furthermore, earthworm casts lead to aggregation and crust formation, whereas macropores (larger than 30 µm) caused by earthworm burrows, (a) enhance the aeration and erosion of soil, (b) facilitate the root infiltration and elongation, and (c) optimize the water retention (Figure 2; Blanchart et al., 1997; Hirth et al., 1997;

Kretzschmar, 1998; Jiménez, 1999; Decaëns and Rossi, 2001). These are physical changes in soil structure that influence indirectly the plant growth, root development and productivity. The release or immobilization of plant nutrients, denitrification, and mineralization (processes that influence nutrient availability) can be enhanced by earthworm activities, and result in indirect chemical effects on plants (Barois et al., 1999; Brussaard, 1999; Rangel et al., 1999; Cortez and Hameed, 2001). Although earthworms has diverse positive effects on plant growth, and are of value for vermicomposting (Suthar and Singh, 2008; Domínguez et al., 2010), the invasiveness of this invertebrate may have negative environmental consequences (Migge-Kleian et al., 2006;

Addison, 2009).

1.1.4. Morphological features and feeding habits of earthworms

Earthworms (a) belong to the class Oligochaeta, consisting of approximately 800 genera and 8000 species, and (b) constitute up to 90% of invertebrate biomass in soil (Edwards, 2004).

Dependent on the morphological features, habitats and feeding skills the burrows of earthworm can vary in volume, orientation, tortuosity, stability, and connectivity (Capowiez et al., 2003;

Bastardie et al., 2005). Considering the different earthworm lifestyles, earthworms can be divided into three ecotypes, termed as epigeic, endogeic or anecic earthworms (Bouché, 1977).

The epigeic earthworms decomposing litter on the soil surface, whereby only small amounts of soil or no soil is ingested (Palm et al., 2013). Epigeic earthworms are characteristic for their relative small size and heavy ventrally and dorsally pigmentation. Because these worms (a) feed mainly on fresh or partially decomposed litter in the upper organic layer (Figure 3) and (b) form only some horizontally burrow in the upper few centimeters of the top soil (Palm et al., 2013), epigeic earthworms also called litter-dwellers and humus formers (Bouché, 1977; Perel, 1977).

Furthermore, they are short lived, grow rapidly and exhibit relatively high reproduction rates (Edwards and Bohlen, 1996).

In contrast, anecic earthworms form humus while feeding on litter and soil (Perel, 1977).

They are characteristic for pulling organic plant material into their large permanent and semi-permanent vertical burrow system. In this regard, the anecic earthworm L. terrestris is well known for removing significant quantities of litter from forest floors (Curry and Schmidt, 2007). Deduced from the fact that anecic earthworm burrows can extend several meters into the mineral subsoil

INTRODUCTION 5 (Figure 3), they are called as deep-burrowers. Furthermore, they are relative large, and medium to heavy dorsally pigmented (Perel, 1977).

Endogeic earthworms consume, in contrast to anecic and epigeic earthworms, large amounts of mineral soil with preference for material rich in organic matter (e.g., dead roots) (Curry and Schmidt, 2007). Their activity leads to extensive sub-horizontal highly branched and less stable burrows in the upper 10 to 15 cm of top soil (Figure 3, Palm et al., 2013). Endogeic earthworms are unpigmented or lightly pigmented, exhibit a medium size, and termed soil-dwellers or humus feeders (Perel, 1977; Edwards and Bohlen, 1996).

Figure 3. Burrow profile of the different earthworm ecotypes demonstrated at a cross section of soil. Figure based on information obtained from Fraser and Boag, 1998; Schelfhout et al., 2017; Channarayappa and Biradar, 2019.