Soil invertebrate organisms are responsible for several biochemical processes indispensable for the correct functioning of ecosystems. Because of the high diversity of animals that occurs in the soil environment, some invertebrates such as earthworms and nematodes are highly important in trophic chains, with high number of species and the effect that they exert on both natural and agricultural systems. However, although numerous studies have evaluated the implications of these organisms in soil processes and their consequences on crop productivity, the interaction between earthworms and nematodes has received little attention in recent years. This chapter reviews studies focusing on the elucidation of the interaction between earthworms and nematodes in diverse situations in which they occur, for example, the vermicompost process and the native and agricultural systems. Several studies have shown that the direct and/or indirect action of earthworms can highly modify nematode populations. In addition, in the presence of earthworms, the damage caused by phytonematodes can be reduced in some crops.
- biological control
- plant growth
- plant parasitic nematode
- soil food web
The first studies on earthworms were initiated by Darwin, with the classic “The Formation of Vegetable Mold through the Action of Worms, with observations on their Habits” . Since then, thousands of studies related to the biology and ecology of earthworms have been performed worldwide. However, even in ancient Rome, these invertebrates had already attracted the attention of Aristotle, who described them as “the intestines of the earth” in 340BC .
At present, the importance of earthworms for the functioning of natural and agricultural ecosystems is recognized [3, 4, 5, 6]. These organisms can influence the growth of plants via several mechanisms, which were described by Edwards  and Scheu , such as increasing soil organic matter mineralization; modifications of soil porosity and aggregation that change the availability of water and oxygen to plants; production of plant growth regulators via the stimulation of microbial activity; pest and parasite control; and stimulation of symbiotic microorganisms.
However, the benefits mediated by these organisms in the soils led to erroneous interpretations, mainly because of their high diversity; there are about 3500 earthworm species described worldwide, with potential of more than 7000 species [8, 9, 10]. In addition, also it is high the diversity of earthworms occurring in an area with natural vegetation or agricultural system. This has already been noted by Steffen et al. , who identified about 56 earthworm species in natural and agricultural ecosystems, of which 26 were native and 30 exotic, belonging to six families. In addition, the greatest diversity of these species was related to the type of ecosystem evaluated: their richness is greater in areas of forest fragments and native fields. Brown et al.  evaluated earthworm populations in different land use systems and observed high earthworm abundance in conservation systems with values ranging from 116 to 179 ind. m−2 in no-tillage and minimum tillage, respectively. The authors suggested that the greater presence of these organisms can be attributed to the lack of soil management in no-tillage, promoting the accumulation of organic material on the soil surface, and small mechanical movement, benefiting the community of these organisms. In addition to the effect of management on earthworm populations, Tanck et al.  found seasonality effects in the communities of
The remarkable diversity of earthworm species can be divided into three distinct ecological categories: epigeic, anecic, and endogeic . Epigeic earthworms comprise animals living on the soil surface, by using the litter and organic horizons as habitat, feeding on organic materials at the beginning of the decomposition process, and incapable of digging galleries in the soil; they are normally used in vermicompost processes. Conversely, endogeic species live in greater depths of soil; are geophageous, taking from the soil the food necessary for their survival; and include most of the earthworms described. The anecic earthworms are organisms that live in the soil-surface interface and are considered the most active of the three categories mentioned above .
These ecological categories are based on the environments in which earthworms live, ingesting and transporting organic and mineral particles at different distances horizontally and vertically in the soil profile [16, 17, 18]. Because of their size and dietary habits, earthworms also unintentionally ingest a large diversity of organisms, ranging from microorganisms such as bacteria and fungi to small animals such as nematodes [15, 19, 20].
Nematodes are highly representative invertebrates in soils, with densities ranging from 106 to 107 m−2 and biomass of up to 100 kg ha−1 . Like earthworms, these organisms also present remarkable ecological diversity, with free-living species—bacteriophages, plant-parasitic, mycophages, omnivores, and predators—responsible for the regulation of several trophic chains in the soil, and parasitic nematodes of plants or animals . Population densities of these animals are of the order of 106 m−2 and can consume up to 800 kg ha−1 of bacteria . However, plant-parasitic nematodes, a group with high agricultural interest, and bacteriophages, nematodes that feed on both pathogenic and saprophytic bacteria and other beneficial species, are the most representative groups in soils .
Considering the small size of free-living and plant-parasitic nematodes, they are inevitably ingested by other organisms, mainly by earthworms . Several studies have attempted to elucidate the interactions between these groups of invertebrates; however, because of the remarkable ecological variability already mentioned, the results have not been consistent, and these interactions have not been clearly defined [26, 27, 28]. Thus, little is known about the effects of earthworms on microbial diversity and soil microfauna .
In this context, a series of studies were performed in order to elucidate the interactions between earthworms and nematodes, as well as the implications of these interactions with other soil organisms and plants in natural and agricultural systems. A simplified version of these interactions is shown in Figure 1.
2. Effects of earthworms on nematode communities
The effects of earthworms on nematode communities (free living or phytonematodes) can be analyzed under four different situations. First, the effects of earthworms on the populations of nematodes during the vermicomposting process of unstabilized organic residues; second, the effects of the products generated by the action of earthworms (vermicompost) or the byproducts (vermicompost tea) as controlling agents of phytonematodes; third, when soil interaction only occurs between worms and nematodes; and fourth, when the interaction of earthworms and phytonematodes occurs in the presence of plants, the latter being more complex, with greater variability of results and thus greater difficulty of interpretation.
2.1. Earthworms and nematodes in vermicomposting process
Because of the high diversity of organisms involved and the ecological complexity of soils, the interactions between earthworms and nematodes have been completely dependent on the particularities of the surveys conducted. Domínguez et al.  evaluated the effects of
The effect of earthworms on nematode populations can be attributed to the direct ingestion and digestion, or reduction by indirect effects . The indirect effect is attributed to the reduction of fungal populations by integrating the diet of the earthworms, thereby reducing communities of fungivorous nematodes .
2.1.1. Vermicomposting and byproducts in the control of nematodes
Although the action of vermicompost earthworms shows the reduction of populations of free-living nematodes, the application of vermicompost in soils has shown to have adverse effects. Arancon et al.  observed a reduction of the communities of plant-parasitic nematodes after the application of vermicompost from different plant materials. However, considering the effect similar to the use of organic compounds in this experiment, the addition of organic materials to the soil was assumed to increase the availability of food for fungivorous and bacteriophage nematodes, increasing the competition between them with other groups. Gabour et al.  also observed this effect of vermicompost application on the populations of the plant-parasitic nematode
In addition to vermicompost, recent studies have shown that the application of vermicompost tea has the potential to control plant parasitic nematodes. In this sense, Edwards et al.  observed a significant suppression in the number of galls caused by
Mechanisms of nematode control by vermicompost tea are still poorly understood. The effects of this substance are likely caused by the death of nematodes by the release of toxic substances such as hydrogen sulfate, ammonia, and nitrite produced during vermicomposting process ; promotion of the growth of nematode predatory fungi that attack their cysts ; favoring of rhizobacteria that produce toxic enzymes and toxins ; or indirectly by favoring populations of microorganisms, bacteria, and fungi, which serve as food for predatory or omnivorous nematodes, or arthropods such as mites, which are selectively opposed to parasitic nematodes of the plant .
2.2. Earthworms and nematodes in the soils
Poinar  reviewed several works and published a list regarding the natural relationships between oligochaetes and nematodes, with more than 150 nematode citations, also containing a brief summary of the groups of nematodes, mainly endoparasite species, found in earthworms. However, it does not present information on these endoparasites in presence of some tropical earthworm species such as
The effects of geophageous earthworms on soil nematodes also differ across studies, and this variability occurs among studies that use the same worm species, which is probably related to the high diversity of these organisms, especially nematodes found in situ. Dash et al.  observed reductions of nematode populations in the soil in the presence of
Studies by Boyer et al.  on
Further, Villenave et al.  evaluated the interaction between nematodes and
The effect of earthworms on the environment are not only restricted to the changes that occur in the soil ingested by these animals. Tiunov et al.  evaluated the populations of nematodes on the walls of the galleries of
In addition to all the results cited above, earthworms can also act as a transport vehicle for these small invertebrates. Shapiro et al.  reported the ability of
2.3. Interaction between earthworms and nematodes and their effects on plants
Dionísio et al.  evaluated the effect of the inoculation of earthworms
The authors indicated that the action of the earthworms occurred probably after the inoculation of the nematodes, because tomato is highly susceptible to attack by nematodes, especially at the seedling stage . Thus, two explanations were presented. First, the earthworms
Contrary results are cited by Lafont et al.  evaluating the effects of
The reduction of nematode damage in plants in the presence of earthworms was also observed by Demetrio et al. , who evaluated the potential of the earthworm
The better development of plants even with the formation of galls in the presence of earthworms can be attributed to several factors: physical changes of the soil by the action of these invertebrates, since galleries formed are normally used by plants as a preferred route for root growth, in addition to facilitate the infiltration of water and oxygen throughout the soil profile . Second, chemical changes, which might increase the availability of P and N mainly, because of the acceleration of nutrient cycling, as well as the continuous deposition of NH4+ by earthworms, both by the production of casts and organo-mineral excrements. These processes could stimulate communities of nitrifying bacteria and growth-regulating-hormone producers, as well as the deposition of mucus-rich nitrogen compounds on the walls of the galleries [7, 47, 48].
The physico-chemical variations promoted by the earthworms alter the biological component of the soil, thereby mainly stimulating the microorganisms (Figure 8b) that can be reflected in the colonization of the roots by arbuscular mycorrhizal fungi . This contributes to the greater absorption of nutrients, mainly phosphorus; the development of plant growth-promoting rhizobacteria  such as
The results of these studies showed that earthworms have a remarkable potential to be used as an alternative in the biological control of plant-parasitic species in several crops; however, further studies are needed to elucidate the mechanisms involved in this process as well as to reveal the interactions with other plants.
3. Final considerations
The complete understanding of the effects of earthworms on nematode communities requires further studies. Considering the studies performed in controlled systems, earthworms seem capable of altering the communities of these invertebrates; however, the effects of other factors such as non-sterilization of the soil and addition of vegetal components could change the number of interactions that exist in this environment, often leading to the generation of contradictory results. The lack of adequate and standardized methodologies for determining the interaction between these organisms and the different habits of life of the nematodes and earthworm species are factors that contribute to the differences found among studies. Nevertheless, this ecological complexity is a part of the soil; therefore, it should be considered in future studies.
Because of the potential to reduce the damage caused by plant-parasitic species, studies with different ecological categories of earthworms need to be performed to understand the interactions occurring in different species and the use of these invertebrates as a tool in the biological control of plant-parasitic nematodes.