The Earthworms: Charles Darwin’s Ecosystem Engineer

Abstract

The term ecosystem engineering focuses on how organisms physically change the abiotic environment and how this feeds back to the biota. Charles Darwin was the first naturalist who studied the role of the earthworms and their ecosystem services. Darwin’s last publication on earthworms gave the role of earthworms in global bioturbation. Darwin also used the word ‘friend of farmer’ and ‘nature ploughman’ for the earthworm because of its important role in the soil ecosystem. In modern ecological theory, bioturbation is recognised as ‘ecosystem engineering’. They are called as ecosystem engineers due to their different ecosystem services which cause the physical, chemical and biological changes in the soil. This review highlights the different ecological services provided by the earthworms that make them ecosystem engineers as said earlier by Darwin.

1. Introduction

Charles Darwin (1809–1882) in his 45-year-long career studied the earthworm and gave many experimental results, observations, interpretations and theories. He published a book “The Formation of Vegetable Mould, through the Actions of Worms, With Observations on their Habits” almost six months before his death. His last publication on earthworms demonstrated their role in global soil bioturbation [1]. According to him [2] “It may be doubted whether there are many other animals which have played so important part in the history of the world, as played by these less organized animals.” He carefully examined the activities of earthworms and reported that earthworms play important role in turning over large amounts of soil, maintaining of soil structure, breakdown of forest litter, plant and animal dead material in soil, aeration and fertility etc. All these activities ultimately promote the plant growth [3, 4, 5].

The complex interactions of earthworms with their environment make their study a challenging task [6] like modifying geochemical gradients, humus formation, buffering capacity of their cast, nutrient cycling [3], redistributing food resources, viruses, bacteria, resting stages of various microbes and eggs [7]. Ploughing of soil was a most valuable and ancient invention of man, but there is no doubt that earthworms were ploughing soil from millions of years ago and maintaining the physical condition of the soil. Earthworms are regularly ploughing the soil and continued to plough the soil in which they are present. That’s why these worms are well-known as “farmer’s friends” or “nature’s ploughman” [2, 8, 9].

Bioturbation is the term used for the biological reworking of soil and sediments [10] and its importance for soil processes and geomorphology by all organisms including microbes, burrowing animals and rooting plants. In modern ecological theory, bioturbation is recognised as ‘ecosystem engineering’ [7]. All these pioneering observations and experimental results of Darwin on earthworm makes him founding father of soil science [11]. The concept ‘ecosystem engineering’ refers to modification in the physical environment that strongly affects the other organisms [7]. In the case of earthworms, it mainly affects the physical condition of soil which is an abiotic factor. Earthworms improve soil fertility by modifying the soil environment. Thus ultimately earthworms are capable of structuring, maintaining or restoration of degraded soils [4, 8, 12, 13]. This review paper highlights, how earthworms play an important role in different ecological services that make them ecosystem engineers.

2. General biology and classification of earthworms

Earthworms have dark brownish to red body, covered with cuticle and average body weight 1400–1500 mg after 8–10 weeks. They are soft-bodied, long, narrow, cylindrical, bilaterally symmetrical, metamerically segmented and soil-dwelling invertebrates [14]. Their body contains a large amount of protein approximately 65% (around 70–80% ‘lysine-rich protein’). Their body also has 14% carbohydrates, 14% fats and 3% ash [15]. The gut of an earthworm is an almost straight tube starting from the mouth followed by a muscular pharynx, oesophagus, gizzard, intestine associated digestive glands and ending outside through the anus [3]. Their gut contains some important inorganic nutrients, protein, mucus, various polysaccharides forms and symbiotic microbes like bacteria, protozoa and microfungi. Earthworm’s gut environment provides optimum conditions (increased total organic carbon, nitrogen and moisture) for activation of microbes from the dormant stage and also for germination of endospores [16, 17]. Various digestive enzymes such as cellulase, amylase, protease, chitinase, lipase and urease were identified from the alimentary canal of earthworms. Microbes present in their gut are responsible for cellulase and mannose activities [16, 17]. Their life span varies from species to species with a range of 3–7 years. These are hermaphrodite animals but cross-fertilisation occurs. The average rate of cocoon production was 7.23, 0.99 and 0.53/worm/week in the monsoon season, winter and the summer respectively [4, 18, 19].

Ronald and Donald [20] reported that the earthworms and microorganisms were associated symbiotically and thus enhance the decomposition of organic matter. Due to this relationship, they can break down a large amount of organic material within the time limit and return it to the nutrient cycle which is responsible for the introduction of vermiculture. Earthworms are highly sensitive to pollutants, so they can be used as bio-indicator tools [21].

Evolutionary date of earthworm is about 6 billion years back. They belong to phylum Annelida and class Oligochaeta. Worldwide around 4200–4400 species of oligochaetes and 20 families with 3200 species of earthworms are well known [4, 16, 22, 23]. Some groups are abundantly distributed in the whole world. Different taxonomic groups were found in different ecosystems except for Antarctica. Some species of earthworms can also be noticed in estuarine waters like Pontodrilus bermudensis. Lampito mauritii can be bred and cultured in sandy soils [3]. In the Indian subcontinent, earthworms represent the bulk of the oligochaete fauna. According to Julka [24], there are around 509 species and 67 genera of earthworms. The most abundant earthworms found in grasslands and agricultural ecosystems in the Palearctic region are belonging to the family Lumbricidae [25]. The greatest variety is found in tropical soils with progressively smaller numbers of species in the northern region. Therefore in France, there are about 180 earthworm species [26] and in the U.K. about 25 species [27]. Earthworms are found in almost every part of the world except the driest and the coldest regions because earthworms are sensitive to a range of environmental factors such as pH, temperature, water content, aeration and salinity levels [8, 22, 28]. Edwards [29] reported that earthworms belonging to temperate regions cannot tolerate high temperatures. Eisenia fetida is most productive at 20°C if both reproduction and growth rate are considered. We can say that earthworms are widely distributed creatures in nature and more than 80% of soil invertebrate’s biomass is occupied by the earthworms [30].

2.1 Trophic classification of earthworms

Bouche [31] classified earthworms based on ecological habitat and their feeding habits, into three major groups (Figure 1):

Figure 1.

Trophic classification of earthworms.

3. Ecosystem services of earthworms

The book “The Formation of Vegetable Mould, through the Actions of Worms, With Observations on their Habits” describes the role of earthworms in soil weathering, pedogenesis, nutrient cycling, organic degradation, soil aeration, burrow formation, development of vegetative mould (topsoil), soil profile differentiation, casting, interchange of the top soil profile, soil fertility, plant growth and protection of archaeological remains through their burial activity [12]. Earthworm’s dry powder and its extract are also used as preventive agents and therapeutic agents for various diseases like bladder stone excretion promoting agents, bladder stone reducing agents, tonic agents, hair growth agents, jaundice, antipyretics, aphrodisiacs, therapeutic agents for convulsion, blood circulation promoters, therapeutic agents for hemiplegia, diuretics, indirect analgesics, antihypertensive and antiasthmatics agents [32]. Major ecosystem services of earthworms are: (Figure 2).

Figure 2.

Ecosystem services of earthworms.

3.1 Effect of earthworms on soil properties

Darwin showed that earthworms are important ecosystem engineers in soil formation (pedogenesis), by mixing layers of soil, humus formation, affecting rock weathering rate and soil horizon differentiation. The influence of earthworms on soil properties depends upon the species present in that particular area and the life history of that species. For example, vertical burrows made by L. terrestris (anecic) facilitate the water flow through the soil profile. Thus they can increase the transport of water and nutrients in the deeper part of soil [4, 23]. It has been reported that surface cast play important role in soil profile development whereas cast deposited beneath the soil profile contributed to pedogenesis. Endogeic species Octolasion tyrtaeum lives in upper mineral soil layers and mainly consumes soil organic matter. Jones et al. [33] and Eisenhauer et al. [34] in their study reported that O. tyrtaeum and L. terrestris species act as keystone detritivores and ecosystem engineers.

3.1.1 Soil formation

The importance of earthworms in chemical weathering was first studied by Darwin [2] in an experiment where the red colour of red-oxide sand disappeared after passing through earthworm intestine, and dissolution of this red-oxide occur due to biochemical changes by specific enzymes released in gizzard and intestine [17]. According to Darwin [2], weathering of rock occurs due to physical and chemical changes in the nature of the rock. The physical weathering by earthworms is possible due to the breakdown of rocks in the gizzard of earthworms whereas chemical weathering occurs due to their intestinal enzyme and microflora. Darwin [2] studied that calciferous glands formed calcareous concretions which combine with small stone or sand present in the gizzard. At that time Darwin did not know exactly the role of calcite formed by the calciferous gland but know that it is a true excretory product. Recent studies showed that water balancing might be an important role by these glands [12, 35]. From the gizzard, grinded material (2–4 micron) pass through the intestine where chemical degradation occurs. Thus gizzard and intestine act as “bioreactors”. However, the rest material is excreted out as cast [17].

Darwin [2] observed that earthworms produced almost 1140 kg/ha/year cast. Bertrand et al. [36] studied that 0–15 cm of soil layer drying was enhanced by endogeic species A. calligenosa and anecic species L. terrestris by increasing evaporation through their burrows. Erosion also helps in pedogenesis and earthworm’s casts on soil surfaces have a significant role in this process. Aggregate size distribution is also affected by earthworm activities. For example, Reginaldia omodeoi increased the proportion of aggregate greater than 2 mm in diameter from 24.6 to 42.2% or 29.8 to 53.5% under maize and yam culture respectively [37, 38, 39].

Darwin [2] concluded that the process of ingestion, grinding and digestion in the earthworm’s intestine, excretion of cast with mucus and microflora, mixing of organic nutrients and vegetative mould (topsoil) exposed the rock particles for chemical alteration as a result of which soil formation occur and ultmatelly soil amount increase.

3.1.2 Soil aeration

Air-filled pores are crucial to help the plant roots to thrive because the plant needs O₂ for photosynthesis and expel CO₂ from surrounding soil. Earthworms improve the exchange of these gases with the atmosphere (Figure 3).

Figure 3.

Mechanism for increase soil aeration by earthworms.

Soil aggregation is improved by mixing of organic matter with soil in the earthworms’ gut which is released as cast. These casts are highly stable aggregates which are deposited by some earthworms in their burrows and by others at the surface of the soil. Thus they may form permanent or temporary burrow [4]. Generally, vertical burrows (more than 1 mm in diameter) are formed by anecic earthworm species that can extend upto 1 m depth in the soil. of endogeic species mainly orientated in the horizontal direction and their diameter are smaller than burrows made by anecic species whereas epigeic species are present in a few centimetres of upper soil and they mainly remain in plant litter [26, 36]. Wollny [40] reported that earthworms show an increase of soil volume from 8 to 30%.

3.1.3 Humus formation

Darwin was the first naturalist who recognised that earthworm’s activities help in humus formation on the topsoil profile of the earth. He observed that earthworms were responsible for the breakdown as well as rapid incorporation of organic matter in different layers of soil. Coarse particles are continually used by the epigeic and anecic earthworms and triturated ingested organic particles in their gut [1, 12].

The short-term increase of mineral nutrients is well known however long term effects on soil organic matter (SOM) in the presence of earthworms are less clear [41]. Biodegradation of organic matter in the gizzard and the intestine occurs by proteases, lipases, amylases, cellulases and chitinases which bring about a rapid biochemical conversion of the cellulosic and the proteinaceous organic materials. Cast released by earthworms has many beneficial microbes which further help in the biodegradation of organic matter [17, 42]. Earthworm’s gut alters the soil microflora and processes mediated by these microorganisms accelerate mineralisation and decomposition of soil organic matter. It was observed that soil inhabited by earthworms had more microflora than the soil devoid of earthworms [43].

3.1.4 Soil nutrient cycle

The cycling of nutrients is a critical function that is possible due to the decomposition of organic matter. The decomposition process is mediated by different types of microbes. Earthworms ingest plant debris and release it as casts. These casts have further beneficial microbes and important nutrients such as, nitrogen (N) and phosphorus (P) which can be used by microbes for their multiplication and vigorous action. Due to the symbiotic activities of earthworms and microbes, organic content which is unavailable to plants becomes available for plant growth in the form of inorganic nutrients. Earthworms also influence the supply of nutrients through their tissues but mainly through their burrowing activities [4, 17, 19, 44]. In earthworm’s gut, casts and burrows; different groups of bacterial species were reported such as, Aeromonas hydrophila in Eisenia fetida [45], Actinobacteria in L. rubellus [46] and fluorescent Pseudomonas in Lumbricus terrestris [47].

During their function as ecosystem engineers; anecic and endogeic earthworms create semi-permanent burrows that permit the transport of O₂ into deeper soil profiles which may alter the principal nitrogen transformation reaction [48]. Haimi and Hutha [49] observed that L. rubellus stimulated microbial respiration by 15–28% whereas Dendrobaena octaedra stimulated it slightly. Both of these species increase nitrogen mineralisation within the soil environment. There are many cases in which carbon cycling occurs through the complementary mechanism of earthworms [41]. Decomposition of organic matter increases mineralisation of carbon upto 90% which is carried out by microorganisms such as bacteria and fungi [50].

3.1.5 Water infiltration

Water infiltration is regulated mainly by the soil porosity. Soil moisture and water infiltration rate decreased in a grass sward, when earthworms were experimentally removed [37, 51]. Soil mechanical and hydraulic properties are also affected by the earthworms, mainly through their burrowing activities which generate macropores. These macropores appreciably impact water infiltration and thus are important for supplying water to crops, in addition to controlling surface runoff and erosion [36]. Baker et al. [52] studied that sub soil properties like drainage and infiltration were improved in Australia with the introduction of A. longa.

The epigeic L. rubellus tends to favour water storage in the topsoil, because it leaves the litter at the soil surface rather than burying it, thus prevents evaporation. Compared to other species, A. caliginosa forms temporary burrows and continually rebuilt which cause a higher infiltration rate to the subsoil [36]. This infiltrated water can be a source of agricultural crop water or percolate through the soil horizon. The surface hydrological processes were also affected by water infiltration in the presence of earthworms [12].

In Ohio, anecic earthworm burrows greatly reduced soil erosion up to 50% due to an increase in infiltration rate [53]. Endogeic species R. omodeoi and Dichogaster terraenigrae improved weakly (+22 to 27%) water infiltration rate and in the case of Hyperiodrilus africanus it was strongly improved +77% [54].

3.2 Effect of earthworm on plant growth

According to Darwin [2] “earthworms help in preparation of soil in an excellent manner which enhances the growth of fibrous-rooted plants and seedlings of all kinds”. Earthworms play a key role in nutrient rich manure production [55], mineral soil formation, soil porosity, water infiltration, amorphous colloidal humus formation and nutrient cycle which directly affect the plant’s growth. Earthworms are known for engineering seed bed conditions for plants. Some recent studies highlight direct and indirect interactions between earthworms and plant seeds which is responsible for plant community composition [4, 19, 34]. Krishnamoorthy and Vajranabhaiah [56] reported that earthworm’s casts have some plant growth regulators such as cytokinins and auxins. Vesicular Arbuscular Mycorrhizae (VAM) population is enhanced due to the presence of earthworms and which is effective for the growth of wheat and other crops. VAM helps in the uptake of phosphate by plants [3]. Earthworms also help in controlling various types of pests in different crops. For example, A. rosea and A. trapezoids reduced the population of soil-borne fungal pathogens and the earthworm R. omodeoi reduced the damage caused by plant-parasitic nematodes Heterodera sacchari on rice plants [36, 57, 58, 59].

3.3 Effect of insecticides on growth, reproductive potential and avoidance behviour of earthworm

Insecticides have major effect on the reproductive, growth and avoidance behviour of earthworm. Due to use insecticides, benifical bacteria in earthworm’s gut and its surrounding soil are decrease that ultimatelety effect the physiological activities of earthworm. Therefore the growth and reproductive potential of earthworm in contaminated decresed drastically [60] (Figure 4). Due to presences of protostomium, earthworms try to avoid the contaminated soil having the insecticides like chlorantraniliprole, fipronil, etc. (Figure 5). But in higly contaiminted, they are unble to avoid, because decrease in energy and die ultimately [4]. So we can say insecticides have decremental effect on trhe earthworm.

Figure 4.

Effect of insecticides on the beneficial bacteria on earthworms.

Figure 5.

Effect of insecticides on the avoidance behviour of earthworms.

4. Techniques used to identify the beneficial attributes of earthworms as ecosystem engineers

Earthworms can consume a wide range of unstable organic matter such as animal waste, industrial waste, sewage sludge, etc. [61, 62]. The burrowing activity of earthworms enhances decomposition, formation of humus, development of soil structure, and cycling of nutrients. Effect of these different kinds of processes done by earthworms are estimated by various techniques which are described below as:

4.1 HPLC-MS/MS

High-Performance Liquid Chromatography-Mass Spectrometry (HPLC-MS) is an excellent technique for component identification, quantification, and mass analysis, and it is frequently used to analyse chemical composition and purity. HPLC-MS has high sensitivity and is ideal for precise and repeatable quantitative analysis. For heat-labile chemicals in soil, such as insecticides and their metabolites, high-performance liquid chromatography techniques are suited. In HPLC-MS, the two techniques (HPLC and MS) are linked by an interface that transmits the separated components from the liquid chromatograph column into the mass spectrometer ion source, allowing the target compound to be identified and quantified. In a study, the enantioselective acute toxicity to earthworms of racemic fipronil and its enantiomers was done by Qu et al., [63]. For this reason, fipronil is released into the soil, where it is consumed by earthworms and degraded. HPLC was used to estimate the amount of pesticide ingested by the earthworm. For the determination of residues, HPLC analysis of extracts from earthworm samples collected at various times after fipronil application was performed.

4.2 GC-MS/MS

GC is a separation science technique that is used to separate the chemical components of a sample mixture and then detect them to determine their presence or absence and/or how much is present. GC detectors are limited in the information that they give; this is usually two-dimensional giving the retention time on the analytical column and the detector response. Identification is based on a comparison of the retention time of the peaks in a sample to those from standards of known compounds, analysed using the same method. However, GC alone cannot be used for the identification of unknowns, which is where hyphenation to an MS works very well. MS is an analytical technique that measures the mass-to-charge ratio (m/z) of charged particles and therefore can be used to determine the molecular weight and elemental composition, as well as elucidate the chemical structures of molecules. Data from a GC-MS is three-dimensional, providing mass spectra that can be used for identity confirmation or to identify unknown compounds plus the chromatogram that can be used for qualitative and quantitative analysis. Chang et al., [64] estimated the Bioaccumulation and enantioselectivity of type I and type II pyrethroid pesticides in earthworms by using GC-MS/MS. The earthworms treated with the two pyrethroids were processed and the residues were extracted in an n-hexane solvent. This extract was further cleaned up by using the adsorbents to remove any interfering substances coming at the retention time of the two pyrethroids. Then, this processed extract was subjected to residue analysis and the estimation of the residues of pyrethroids was done by using GC-MS/MS.

4.3 GC-ECD/FID/NPD

Most of the organic analyses that we conduct are for organic-priority pollutants such as pesticides, PCBs, PHCs, BTEX, and other petroleum products. Gas Chromatography (GC) is the standard methodology. From sample matrices such as soil, water, plants, fish, and earthworms, the analytes are extracted into organic solvents, separated from interfering substances (cleaned up), concentrated, and run on the GC. The detector was selected based on the type of analyte to be detected in the case of nitrogen and phosphorous-containing analytes, the NPD detector is used and in the case of analytes containing halogens, the ECD detector is used. For the estimation of hydrocarbons, an FID detector coupled with gas chromatography was used. Martinkosky et al., [65] demonstrated the bioremediation of soil by increasing the degradation rates of heavy crude oil hydrocarbons by the earthworms. This study demonstrated that earthworms accelerate the bioremediation of crude oil in soils, including the degradation of the heaviest polyaromatic fractions.

4.4 LC-MS/MS

It is a powerful analytical technique that combines the resolving power of liquid chromatography with the detection specificity of mass spectrometry. Liquid chromatography (LC) separates the sample components and then introduces them to the mass spectrometer (MS). The MS creates and detects charged ions. When a sample is injected, it is adsorbed on the stationary phase, and the solvent passes through the column to separate the compounds one by one, based on their relative affinity to the packing materials and the solvent. The component with the most affinity to the stationary phase is the last to separate. This is because high affinity corresponds to more time to travel to the end of the column. The difference between traditional LC and HPLC is that the solvent in LC travels by the force of gravity. In the application of HPLC, the solvent travels under high pressure obtained employing a pump to overcome the pressure drop in the packed column, which reduces the time of separation. As will be discussed, a continuous flow syringe pump is very useful in HPLC. Hu et al., [66] studied the behaviour of the imidacloprid herbicide in the earthworms by estimating the residues of this herbicide in soil via LC-MS/MS. Bioaccumulation and degradation of imidacloprid were estimating the concentration of this herbicide in the treated soil and earthworms after a few days of the treatment. Samples of the treated soil and earthworms present in it were taken at regular intervals of time and these samples were processed for further residue analysis using LC-MS/MS.

4.5 AAS

AAS is an analytical technique used to determine how many certain elements are in a sample. It uses the principle that atoms (and ions) can absorb light at a specific, unique wavelength. When this specific wavelength of light is provided, the energy (light) is absorbed by the atom. Electrons in the atom move from the ground state to an excited state. The amount of light absorbed is measured and the concentration of the element in the sample can be calculated. Ekperusi et al., [67] conducted a study to assess the levels of heavy metals present in crude oil-contaminated soil, and the application of the earthworm - H. africanus with an interest in the bioremediation of metals from the contaminated soil was investigated within 90 days under laboratory conditions. Selected heavy metals such as zinc, manganese, copper, nickel, cadmium, vanadium, chromium, lead, mercury, and arsenic were determined using AAS. Assessment of heavy metals indicated that heavy metals are present in crude oil at elevated levels beyond national regulatory guidelines. There was a significant (P < 0.05) decreasing trend in the percentage of heavy metals present in the soil after inoculation with an earthworm in zinc (57.66%), manganese (57.72%), copper (57.64%), nickel (57.69%), cadmium (57.57%), vanadium (57.68%), chromium (57.67%), lead (57.64%), arsenic (1.36%) and mercury (57.41%) after 90 days period. The bioaccumulation factor showed that zinc, manganese, copper, cadmium, vanadium, chromium, and lead had a factor of 1.36, while nickel, arsenic, and mercury had 1.37, 0.01, and 1.35 respectively. The results showed that the earthworms H. africanus can be effectively used to bioremediate heavy metals from crude oil-polluted soil.

5. Conclusion

Earthworms cause physical, chemical and biological changes in the soil and improve soil fertility mainly by increasing soil weathering, soil porosity, water infiltration and humus formation. All these activities of earthworms help in plant growth. Apart from these, they also protect the plants from various types of pathogens. Thus we can conclude that earthworms significantly modify their environment by improving the chemical, biological and physical properties of soil and because of these activities, Charles Darwin used the term “ecosystem engineer” for them.