Earthworms and soil quality
As first documented in Darwin's 1881 book, the earthworm is a classic example of an organism that profoundly alters its external environment, in this case, the "earth" or soil it inhabits (see also C. Jones et al. 1994). Earthworm is the common name for a number of species in the oligochaete subgroup of annelid worms. These species are unusual in being terrestrial, as the vast majority of annelid species inhabit either freshwater or marine environments. In fact, because they are phylogenetically constrained to be "physiologically aquatic" animals (J. Turner 2000; on which the following discussion is based), earthworms must effectively transform their terrestrial habitat in order to exist.
In functional terms, these small creatures are ill- suited to the central stress that characterizes life out of water—desiccation. Like freshwater oligochaetes, earthworms produce large quantities of relatively dilute urine, losing 60%-90% of their body weight in water daily (compared with less than 10% in terrestrial mammals such as humans). As a result, earthworms require an environment that is not too drying, and from which water (as well as oxygen and food) can easily be extracted. It is precisely this kind of moist, aerated, nutrient-rich soil environment that earthworms create in terrestrial habitats, through the humble but collectively powerful daily activities described below. In so doing, they shape the living conditions of countless other terrestrial organisms and microorganisms.
Earthworms tunnel through soil, compacting it and leaving a coating of polysaccharide-rich mucus that acts as an adhesive to aggregate soil particles and provides a ready carbon source that promotes microbial activity (Lavelle 1988; Bossuyt et al. 2005). Their production of this mucus is surprisingly copious: 1 g of earthworms can produce an average of 5.6 mg (dry weight) of these skin secretions per day (Pan et al. 2010 and references therein). As they tunnel, earthworms ingest bits of soil, digesting its constituent organic matter and bacteria and eliminating fecal pellets that are permeated with gut secretions and calcium carbonate (Daniel and Anderson 1992; J. Turner 2000). This complex of digested soil particles, calcium carbonate, and organic secretions dries in the form of durable macroaggregate "casts" that substantially enhance soil fertility (Syers and Springett 1984; Lavelle 1988; additional references in Bossuyt et al. 2005). For example, these fecal castings have higher moisture content, increased microbial activity, and greater concentrations of soluble organic carbon than the same soils that have not passed through a worm gut (Daniel and Anderson 1992). At the same time, worms incorporate into soils additional organic materials such as decomposing bits of leaf litter, gathering them from the soil surface and bringing them into their tunnels to use as an eventual food source (J. Turner 2000; Dempsey et al. 2013). Laboratory studies using radioactively labeled leaf material show that these activities result in the production, from rapidly incorporated organic residues, of large soil macroaggregates with elevated amounts of total carbon (Bossuyt et al. 2005). Interestingly, these macroaggregates within worm casts contain microaggregates in which much of this newly incorporated carbon is held in a protected form, possibly providing long-term stabilization of soil carbon (Bossuyt et al. 2005).
These activities enhance soil nutrient content and promote more rapid nutrient and carbohydrate cycling (Lavelle 1988; Dempsey et al. 2013). By building structurally aggregated soils, earthworm activities also transform the soil's physical and hence water-holding properties. If not for this aggregating action, soils would weather into increasingly fine particles, becoming dense matrices of clay to which water molecules would be very tightly bound and hence biologically unavailable (J. Turner 2000). One evident effect of earthworm activities is to increase the penetrability of soils to plant roots, arthropods, and fungal hyphae (Syers and Springett 1984). This structural effect also improves gas exchange between the soil and the aerial atmosphere (Bossuyt et al. 2005). In addition, worm burrowing activity enhances the moisture content of the soil by creating large structural macropores that make it easier for rain to infiltrate and allow a given soil volume to hold more water (J. Turner 2000). Another key physical effect of aggregation is the formation of larger soil micropores; these hold moisture less tightly, reducing the osmotic forces that could otherwise draw water out of worm bodies.
Together, earthworm activities result in the production of organically rich, structurally aggregated soil— Darwin's highly fertile "vegetable mould." Through their own transformative activities, these small animals "develop, maintain and expand" a soil zone that suits their aquatic physiology (and which can even be viewed as an external organ for water balance): a habitat where rain infiltrates readily; where plenty of water is held, but not so tightly as to be unavailable; and where the pores allow both high humidity and abundant oxygen (J. Turner 2000, 118). In the process, the earthworms create a fertile soil horizon for other soil inhabitants such as terrestrial plants and soil microorganisms. This understanding of how earthworm activities mediate soil conditions could perhaps be expanded to include functional and selective feedback effects, by testing individual and population consequences of soils with various levels of prior mediation by earthworms.
The prodigious soil-transforming capabilities of earthworms may provide urgently needed new benefits to terrestrial ecosystems in the future. Recent work has revealed that earthworm mucus has a high affinity for organic molecules such as certain insecticides and that earthworm activities can change the distribution and biological availability of toxic heavy metal ions (Pan et al. 2010 and references therein). These interactions with soil contaminants raise the intriguing possibility that earthworms may be employed as agents of bioremediation for soils that have been chemically altered by the habitat-constructing activities of human beings.