Life cycle

The genus Eudrilus is bi-parental, being characterised by internal fertilisation preceding cocoon production (Sims 1964, 1987). Initial life studies are relatively recent, for example by Neuhauser et al. (1979), who found the best growth on horse manure or activated sewage sludge. Its life span can be 1–3 years, with Eudrilus eugeniae possessing a life cycle that ranges from 50–70 days, with sexual maturity reached at 35–50 days in culture (Viljoen & Reineke 1989). Reineke and Viljoen (1988) reported that in a cattle manure substrate at 25°C, cocoons produced by adult worms between the ages of 70–100 days were incubated for ca. 17 days before producing a mean of 2.7 hatchlings per cocoon (range 1–8) with 84 % hatchling success. Dominguez et al. (2001) had similar findings with cocoons hatching in only 12 days at 25°C, and reaching maturity in as little as 35 days (total 47 days). The latter findings concluded that mature worms produced 3.6 cocoons per week with 2.2 viable hatchlings per cocoon (= 6.5 hatchlings per worm per week on average). Viljoen and Reinecke (1989, 1994) reported the first indication of clitella at between 35–45 days; worms with fully developed clitella copulated readily and the formation of cocoons started within 24 hours after copulation, continuing for up to 300 days. In India, Nagavallemma et al. (2004) recorded an 18-fold increase in population (from 55 specimens to 1,007) on legume leaf/cow dung substrate in three months, the highest of three composting species they tested. Also in India, Vasanthi et al. (2013b) report the highest productivity rates in sugarcane filter mud (= pressmud) mixed with sawdust and cattle manure at 26°C. These rates of growth and reproduction are amongst the highest currently reported for any earthworm.

Parasites and disease resistance

Gates (1982: 74) states that, unlike in most earthworm species, parasitic protozoans had not been reported. Internal nematodes (parasitic, paratenic or commensal) are known (e.g. Gates 1974: 74; Poinar 1978; del Valle & Rodriguez 1988; McNeill & Anderson 1990; Spiridonov 1992), but this species is supposedly disease-free apart from records of ammonia lesions on the clitellum (Gerasimov 2007). The functions of the ancillary glands of the female and male organs are not fully worked out; possibly they produce nutrients for eggs/sperm or are in part copulation sentinels preventing intromission of parasites or other disease vectors. Neither is the function of the supra-intestinal glands understood, as already noted.

Regeneration

Gates (1982: 74) reports ‘head' regeneration as well as more easily observed posterior or ‘tail’ regeneration, and sometimes abnormalities like forked tails. Regrowth findings were confirmed, e.g. by Parida and Swain (2011) and Subashini et al. (2014), thus it is plausible for this species to get two viable worms from a single ‘individual’ as with some other species reported by Blakemore (2001).

Ecology and economics

Ecology of the three most common aerobic composting worm species, Eisenia fetida (Savigny, 1826), Eudrilus eugeniae and Perionyx excavatus Perrier, 1872, that are most often bred in worm farms and fed on household vegetable wastes or animal manures, are detailed in reports by Graff (1982), Sabine (1983), Kale and Bano (1991), Reinecke et al. (1992), Kale and Sunitha (1993, mispelt “Sunita” in Edwards 2004 : 388, table 19.3) and by Dominguez et al. (2001). Comparative studies generally show E. eugeniae to be a most productive species in tropical zones or under cover in temperate regions (where it is bred mainly for fish bait) since its large size makes it particularly easy to handle and harvest. As well as its use for fishing bait, this species is also used as a commercial meal high in protein for fish, birds and other animals that reject the taste or smell of Eisenia fetida, as noted below. For example, Gates (1982: 74) says it is the preferred food for duck-billed platypuses [Ornithorhynchus anatinus (Shaw, 1799)] in zoos, and this was confirmed by the Qld National Parks and Wildlife Service in Brisbane (pers. obs.).

In Cuba, India and the Philippines, this worm is favoured most for producing vermicompost fertiliser for organic farming, whereas in North America and Australia the main commercial use is for breeding as fish bait where it is known colloquially as the ‘African Nightcrawler’ or ‘ANC’. The current studies noted a propensity to escape from containers at night and wander, adding justification to this common name. Despite its potential for mobility, there were no records of natural colonisation for North America (Gates 1958, 1972, 1982) or Australia, and such records from New Zealand are now known to be mistaken identities. As Gates (1958: 10) said: “This species, originating in tropical Africa and until very recently known only from the tropics, has been raised and distributed in the United States for several years by earthworm culturists. Sales appear to be mostly to anglers for bait. Escapes of live specimens into natural environments must have been numerous. As yet, however, there are no records to indicate acclimatization and permanent colonization in mainland states.” This was slightly counter-indicated by his later record of specimens from soil under oak trees at Vero Beach Laboratories, Florida (Gates 1982: 72).

Nevertheless, the spread of Eudrilus eugeniae may require closer monitoring as it is a widely cultivated species in Brazil too and there are some records of its survival away from worm farms, mainly in areas of high organic matter, but also in gardens and fields. It was also collected from waterfalls and river sites in Guadeloupe (Csuzdi & Pavlicek 2009). A novice report from mountainous forests in Negros Occidental, Philippines (Flores 2007) is unsubstantiated, being based on a simplistic, non-specialist key only to families, and re-surveys (unpub.) by the current author have not found it far from culture beds.

Preferring bedding material rich in organic matter in culture, this savannah worm also survives in unamended soils (M'ba 1978); and Blakemore (1994) successfully maintained it for six months with reproduction in mesocosms of heat-sterilised but unamended clays (vertisol and kraznozem) and sandy (podzol) soils in the glasshouse. Parthasarathi (2007) showed that over a year it will grow in clay loam but not as well as in composts where its biomass may be six times as high; thus it is considered adaptable to a wide range of soil types, unlike most other highly restricted earthworms that coevolve with their soils (Michaelsen 1922).

Such environmental tolerance was investigated by way of soil selections by Madge (1969) who introduced Eudrilus eugeniae and another tropical species to gradients of soil texture and found a marked preference for the 0.25 mm particle size fraction (fine sand) over both coarse and very fine sand. A series of choice trials conducted by Blakemore (1994) showed that it, along with Eisenia fetida, had a tendency to select soil amended with manure when given a choice and compared to other species; it was found in clay soil rather than loam or sandy soil in 25 % of all its observations. Habitat requirements were also tested by Madge (1969), who introduced E. eugeniae and another tropical African species to a soil moisture gradient and found 65 % of the earthworms in the 12–17 % moisture sectors after 48 hours; tolerated pH range was between 5.6–9.2 and for temperatures, he found an optimal range between 23°C and 31.5°C. In growth experiments, Viljoen and Reinecke (1992) reported that no E. eugeniae juveniles survived below 12°C or above 30°C, and optimal temperature for growth and reproduction was around 25°C. Attempts to establish it in natural environments show that the worms do well until the temperature drops to 40°F (4.4°C), at which time they die (Gates 1972: 52). Sims and Gerard (1985, 1999) say that temperatures below 10°C are not tolerated and that the optimum breeding temperature range is 21–27°C. Domingues et al. (2001) confirmed optimum moisture and temperature ranges for growth of near saturation at 80–82 % and 25–30°C. These moisture and temperature levels correspond well to findings by Blakemore (1994), except the preferred moisture range was 20–25 % in a light sandy loam (10 % clay) and the preferred temperature was 25°C, in gradient cylinders laid horizontally to circumvent depth affects.

Nature of Eudrilus casts

Eudrilus eugeniae is plentiful in the coastal, shaded savannah grasslands of its West African homeland where copious surface pellets are produced — remarkably, up to 140 t ha^-1 per annum is deposited (Madge 1969) or equivalent to 156.8 t ha^-1 per annum according to Gates (1972: 52), during the rainy season only.

In a series of mesocosm soil cores trials with combinations of species, soils and test crops, Blakemore (1994, 2008a) determined that E. eugeniae produces distinctive elongated pellet-like casts (2–3 mm × 1 mm) on the surface of the soil, especially near container edges where the worms burrowed, and had the highest surface cast production (equivalent to between 9.8–14.0 kg m^-2) of a dozen species tested, supporting the findings for a high casting rate of E. eugeniae estimated by Cook et al. (1980) of up to 2.43 g soil per gram fresh weight worm per day. The casting rates in the 23 cm diameter (0.0434 m²) by 33 cm deep mesocosms were as high as 610.5 g per pot in kraznozem soil in just six months, equivalent to 281.3 t ha^-1 per annum, if extrapolated to the field, or about twice the rate reported by Madge (1969).

Blakemore (1994, 2008a) observed that, where casts for this species were deposited on the surface, adventitious plant roots sought them out and that casts fallen over the lip of the cores into the base tray also had root hairs firmly attached to the pellets at the base too; when the roots were lifted cast pellets looked like miniature bunches of grapes dangling on a vine. This may be explained by Eudrilus eugeniae having significantly higher nutrients and trace elements in its casts compared to the clay soil matrix, especially nitrate-N, K and Zn, which were about twice that of the soil (Blakemore 1994, also Table 1), and possibly other plant attractant compounds.

Effects on plant yield and soil moisture after deliberate introduction of this species

Comparative glasshouse experiments and field trials (Blakemore 1994, 1997, 2008a) showed statistically significant yield increases when this worm was introduced to soil cores ranging from +21–74 % for oats and +15–50 % for grass shoots (and up to +50 % for grass roots), compared to uninoculated pots. Infiltrations rates were increased 19.0× in clay and 3.6× in sandy soil cores in the glasshouse, this partly attributed to absorption by surface casts and also drainage in worm burrows. As one of a dozen candidate species later tested in two field inoculation trials, Eudrilus eugeniae significantly increased pasture grass yield by 83.9 % (i.e. nearly doubled compared to controls). However, these preliminary results were considered inconclusive due to background variation and lack of survivors after one year during a particularly severe drought in tropical eastern Australia that precluded irrigation even from cattle stock reservoirs.

Inadvisability of deliberate introductions of alien species

The ethics of releasing an exotic species such as Eudrilus eugeniae into the Australian field were approved by PhD supervisors at CSIRO Tropical Agriculture, Qld, since this was an objective of the project that aimed to enhance improved pasture production naturally (Blakemore 1994). Possible risks were considered acceptable on the grounds that this species was present in Australia, having been legally imported from Canada by a worm grower some years previously; moreover, it was already widely sold for fishing bait, including in the Mundubbera township nearest to the release site (pers. obs.). This vermicomposting species is sexual (i.e. it requires mutual partners to reproduce rather than being parthenogenetic) and the upland release area, classed as dry, arid sub-tropical, was several kilometres from a water course that may have aided dispersal. Thus the likelihood that the species would persist due to the single release event, especially in the prevailing drought, was considered negligible. However, increasing concerns about the spread of alien species would mean it is inadvisable to contemplate such a release or deliberate introduction in the future in Australia or elsewhere. Commercial solutions for the worm bait/compost market could be found from the pool of native species, some of which are already bred as bait in Australia (Blakemore 1999, 2012b) but, again, redistribution of these natives is also ill-advised albeit less objectionable and less regulated (by import/quarantine restrictions) than the use of exotics.

TABLE 1

Composition of Eudrilus eugeniae casts produced from two types of unamended soils: (A) a sandy podzol and (B) a clay vertisol (Blakemore, 1994: tables 4.3.22/23) compared to (C) 100 % ANC vermicast mainly from horse manure (data courtesy of Kahariam farms). Ratios in square braces are relative to the source soil medium; 1 % = 10,000 mg/kg or 10,000 ppm (parts per million); ‘∼’ = conversion estimates.

Microbial aspects

Sruthy et al. (2013) determined that the intestinal microbial populations of Eudrilus eugeniae in the foregut, mid and hindgut were dominated by bacteria, actinomycetes and fungi, respectively. These authors reviewed the diversity of types and number of these microbes, plus yeasts and protozoans in the casts of E. eugeniae and other vermicomposting species reported on by other researchers (see next section below). Use of earthworms in vermistabilisation of sewage sludge and other wastes have had favourable results when attempted in various regions (e.g. Neuhauser et al. 1988; Blakemore 2000b, c). Monroy et al. (2008) showed that processing of pig manure slurry with E. eugeniae eliminated nematodes and reduced coliform bacteria by up to 98 %.

Composition of ANC vermicompost

The chemical and microbial characteristics of E. eugeniae vermicast/vermicompost differ depending upon the nature of the substrate and the age of the casts. Chemical composition is determined by the source material on which the worms are fed but is often enhanced in terms of natural plant nutrients, these changes relating to physical, chemical and microbial activities during and after passage through the worms’ intestines. Table 1 summarises data from experiments by Blakemore (1994: tables 4.3.22, 4.3.23) that found that plant nutrients in casts of clay soil increased by about +20 %, whereas casts from a sandy soil were depleted in nutrients (by -20 %) probably due to assimilation by the worms, although structural characteristics of the soil matrix were improved by the worm activities too, increasing plant yields as noted above. Several authors, have confirmed phytohormone-like effects of casts as reported by Tomati et al. (1988). For instance, Nagavallemma et al. (2004) found generic vermicomposts to have higher percentages (nearly double) of both macro- and micronutrients and higher microbial activity compared with garden composts, plus they detected these plant-growthpromoting agents. Data from Parthasarathi (2006) is summarised in Table 2.

It is from the microbial activity that most of the benefits of worm casts accrue, relating to mineralisation and the gradual release of nutrients, as well as plant-growth-promoting enzymatic agents. As vermicompost ages, this biological activity declines, but the vitamin content may double with time (Prabha et al. 2007). Studies by Parthasarathi and Ranganathan (2000) showed that enzymes (cellulase, amylase, invertase, protease and phosphatase) declined as the casts aged. Parthasarathi (2006) found that Eudrilus eugeniae fed on sugar cane pressmud had a more than four-fold increase (significant p<0.05) in microbial population (fungi + bacteria + actinomycetes) and dehydrogenase enzyme activity in fresh casts, leading to enhanced nutrient mineralisation, but this activity gradually decreased over the period of a month as the casts aged (see Table 2).

Effects of ANC vermicompost on plant yield

A study by Kale et al. (1992) commented on applications of Eudrilus eugeniae vermicompost on crops: application equivalent to 5 t ha^-1 plus half of the recommended chemical fertiliser gave a significantly higher yield of rice in outdoor pots. The rice results are similar to those reported by Pontillas et al. (2009) from the Philippines. However, the combination of vermicomposts with artificial fertilisers and other agri-chemicals may actually reduce efficacy, since there is often a need to adopt wholly organic methods, not just for organic certification, but also based on certain long-term studies, such as Blakemore (2000a) which found that a partly organic section of Haughley Farm was not as productive as a wholly organic section. Unpublished data from Kahariam organic farm in the Philippines show that ANC vermicast application to paddy at rates of just 1.5–3 t ha^-1 are adequate to increase rice yields to 90–120 cavans ha^-1, well above the typical local range of 20–90 cavans ha^-1 but without the need for chemical additions (Mr Danny Rubio, farm manager, pers. comm.). Similarly, an organic sugarcane fields on Negros applying up to 30 t ha^-1 Eudrilus vermicompost yields 90 t ha^-1 (Mr R. Peñalosa, pers. comm.), above the regional average yield of 50 t ha^-1, i.e. +80 %. In current studies by the author, the resident earthworms on both farms were enhanced in terms of biomass and biodiversity when compared with neighbouring farms that use conventional chemical fertilisers and biocides. Such findings attest to the sustainability of organic farming using vermicomposts as primary fertilisers.

TABLE 2

Microbes in ANC vermicompost (after Parthasarathi, 2006: table 1); CFU = Colony Forming Units.

Composition of fish bait, stock feed and worm meal

Worms can be fed to stock directly, or dried and added to worm meal. Composition is provided by several authors, for example Hertrampf and Piedad-Pascual (2000) who show 85.3 % moisture in E. eugeniae worms with 56 % protein when dried, and ten essential amino acids plus macro and trace minerals of freeze-dried vermimeal. Although earthworm feeds tend to be a rich source of vitamins A, B and D, specific data for E. eugenia are not presently available.

Radioactivity and biocide effects

Eno (1966) found E. eugeniae to be less susceptible than Lumbricus terrestris Linnaeus, 1828 to irradiation in the range 16–64 kR. In Nigerian soils, this worm had much higher concentrations of DDT and its products, compared with the surrounding soil, and its production of surface casts virtually ceased in DDT-treated plots, which was considered a contributory factor to the overall decline in fertility of these plots (Cook et al. 1980). The concentration of heavy metals (Cu, Zn, Pb, Cd and Hg) in the tissue of E. eugeniae fed on municipal wastes accumulated beyond acceptable levels for protein-meal production (Graff 1982), although this trait could be utilised for soil bioremediation.

Pharmaceutical or cosmetics uses

Earthworm fibrinolytic enzymes are a group of serine proteases that are used as anticoagulent or thrombolytic drugs to treat and prevent cardiac and cerebrovascular diseases in heart and stroke patients. In original 1982 Japanese patents (e.g. US4568545A) extracts were said to come from “Lumbricus rebellus” (sic), but Indian researchers (Sharma et al. 2011a) have since cloned and sequenced the fibrinolytic protease (Efp-0) gene from E. eugeniae as well as Eisenia fetida. The antimicrobial, antioxidant, anti-inflammatory and anticoagulant properties of E. eugeniae and its extracts have been variously studied (e.g. Mathur et al. 2010a; Packia Lekshmi et al. 2014). When Eudrilus eugeniae was dried and powdered, it produced antimicrobial responses of between 45–90 % inhibition on agar plates when assayed against seven human pathogens (Anjana et al. 2013). Extracts from this worm showed antibacterial and antifungal properties that varied depending on the formulation (Mathur et al. 2010b). Preliminary studies by Shobha and Kale (2008) found indications of possible control of plant soil-borne fungal and bacterial pathogens using E. eugeniae exudates. These findings are supported by Vasanthi et al. (2013a) using a paste from this worm to inhibit the growth of resistant/recalcitrant human pathogens of bacteria such as Staphylococcus aureus Rosenbach, 1884 (‘Golden staph’) and of fungi such as Candida albicans (Robin, 1853) (‘Thrush’), indicating its antimicrobial properties.

Emulating the works of Cooper et al. (2004a, b), but specifically using E. eugeniae as the source, Dinesh et al. (2013) report on the cytotoxic effect of coelomic fluid on cancer cell lines of human HeLa cells, colon cancer cells, WBC malignant tumour cells and brain tumour cells, with reduction by up to 33 %. Such studies indicate novel use of this earthworm for treatment of cancers.

Azmi et al. (2014) recently found earthworm extracts, including those from E. eugeniae, to have anti-wrinkling properties as potential new ‘anti-aging’ agents.