Introduction

Organic waste management is a global problem due to large scale urbanization, economic growth, and population explosion. Environmentally unhealthy disposal of organic wastes can degrade the environment and may cause diseases. Land filling, open dumping, and burning disposal practices are ecologically unsustainable, due to the production of certain toxic gases and leaching which can cause environmental pollution. The management of organic waste is a serious issue for the maintenance of pollution free environment. Globally, each year 3.4–4 billion tons of industrial and municipal waste is generated, of which non-hazardous industrial waste is about 1.2 billion tons [1]. About 960 million tons of solid waste is produced each year in India, of which 290 million tons are of industrial waste [2]. In India open dumping (94%) are the predominant mode of solid waste disposal and only 5% is used for composting [3]. Waste recycling or composting and its use for agricultural purposes is the best method for waste disposal [4]. The conversion of industrial waste into vermicompost is of double interest as along with checking pollution it also converts waste into a fertilizing material [5]. The production of earthworms in organic material is called vermiculture and the bioconversion of organic materials by earthworms is known as vermicomposting/earthworm technology. Vermicompost is one of the highest-grade and most nutrient-rich natural organic fertilizers in the world. Vermicompost contains highly enriched nutrients (nitrogen, potassium, phosphorus, calcium) which gradually make them easily available to plants [6]. Application of vermicompost in sustainable agriculture is thus a well-established choice to chemical fertilizers.

In the present review article, growth and reproduction of earthworms in organic wastes is discussed. Along with this, the paper discusses the earthworm-microbe interaction for stabilization/decomposition of wastes and also the quality of final vermicompost (nutrient status) as compared to composting without earthworms. There are number of research studies on the use of the vermicomposting process for the bioconversion of different organic wastes to produce organic fertilizer (vermicompost) at small scale (lab conditions). Waste management is not possible without earthworms. Practical utilization of earthworms as waste managers in towns, corporations at commercial level/large scale should be taken into consideration. The earthworm technology should be considered for employment of youth as this technology is cost effective and produces two productive outputs (biomass and compost) in stipulated duration.

Earthworm-Microbe Interaction

Earthworms are also called as the ‘farmer’s friend’ or ‘nature’s ploughman’. Sir Charles Darwin described earthworms as the ‘unheralded soldiers of mankind’, Sir Anatoly Igonin called ‘protector and producer’ and Aristotle called them as the ‘intestine of earth’ as they maintain the fertility of the soil and also could digest varieties of organic substrates [7]. More than 4000 species of earthworms are reported in the world and in the India 420 valid species/subspecies belonging to 70 genera are known [8]. India contributes about 10.5 per cent of the world’s earthworm diversity alone [8]. Earthworms are hermaphrodites with bilaterally symmetrical, segmented invertebrates grouped under phylum Annelida and class Oligochaeta with a dark brown body and clitellum for producing cocoons. Earthworms have a gizzard which crushes the organic materials to a smaller size. The gut of the earthworm is inhabited by microbial symbionts (bacteria, protozoa, and fungi) which is responsible for the organic matter degradation [9]. The different types of microflora present in different species of earthworms are listed in Table 1.

Table 1 List of different types of microflora present in different species of earthworms
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Based on feeding habitat, earthworm species have been classified into three types: epigeic, anecic and endogeic worms (Table 2) [19].

Table 2 Classification and characteristics of different earthworm species
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Out of these three types of earthworms, epigeic species shows good potential for vermicomposting. The important earthworm species for vermicomposting is Eisenia fetida as it has a high capacity of all environmental conditions, higher rates of decomposition of organic substances and high reproductive rate and short life cycle. Earthworm-microbe interaction is found to be complex. Microbes provide food for earthworms and the protozoa and fungi are of major importance in diet. Worms and microbes work together to increase the organic waste decomposition [20]. Vermicompost has higher microbial population than compost [21]. A large number of bacteria have been reported in vermicomposts produced by different earthworm species like proteobacteria, bacteroidetes, actinobacteria in E. fetida [10]. Azotobacter, autotrophic Nitrosomonas, nitrobacter in Eudrilus species [16]. Pseudomonas oxalaticus in Pheretima species [17]. Bradyrhizobium japonicum in Lumbricus terrestris [13]. Ismail [22] reported that earthworms have collaboration with free living soil bacteria and forms the drilosphere. The ingested material while passing through the gut of earthworms, increases the number of microbes up to 1000 fold [23]. The gut of earthworms contain the ‘nitrogen-fixing’ and ‘decomposer microbes’ which are released along with nutrients in their final excreta [15] and are beneficial to the soil health [24]. Final earthworm casts contains higher activities of protease, phosphatase, peroxidase, dehydrogenase, amylase and cellulose [25] and provides some biological benefits to soil [26]. Several researchers [27, 28] have reported that the microbiota of earthworm gut and cast can digest organic substances and polysaccharides. Earthworms and their microflora increases nitrogen mineralization that favours nitrification in the organic wastes [29]. Monson et al. [30] observed a maximum number of microbes in vermicomposted treated plots. A higher microbiota was also observed in paddy fields applied with vermicompost [31]. Chen et al. [32] observed that earthworms activated lignocelluloses degradation microorganisms (Pseudomonas, Streptomyces, Pseudoxanthomonas, Mucor, and Cryptococcus) there by speedup lignocelluloses decomposition in maize stover. Aira et al. [33] observed that E. fetida promoted fungal growth and fungal biomass depends on the density of worms. Koubova et al. [34] observed that the route of consumed organic substance through the gut of E. fetida and E. andrei increased the biomass of microbes and changed the microbial structure. Vivas et al. [24] observed that microbial diversity of olive waste was enhanced by E. fetida and the final vermicompost was detected by greater bacterial population. Microbiological investigations revealed that the earthworms and their microbiota have strong interactions with each other [35]. The population of microbes is enhanced in earthworm gut and finally in the vermicasts. The earthworm-microbe interaction is interdependent and the relationship can play a great role in producing high quality manure.

Growth and Reproduction of Earthworms in Organic Wastes

It is understood that earthworm species increases the rate of decomposition during vermistabilization of organic wastes [33]. Earthworm species have the ability to consume various types of organic wastes such as livestock excreta, cattle dung, oil palm waste, agricultural residue, sewage sludge and other agro-industrial refuse. Earthworms are hermaphrodites and at maturity develops ring shaped clitellum which secret a thick mucus to form a cocoon [36]. In earthworms production of cocoons starts at the age of 6 weeks till the end of 6 months. Quality and nature of organic material is one of the conditions determining the reproduction and growth of earthworms [37]. Yadav and Garg [38] reported increase in worm biomass at initial stages and later declined at final stages during vermicomposting of food industry sludge and water hyacinth using earthworm E. fetida. Availability of food at initial stages increases the worm biomass whereas exhaustion of food in the final stages decreases the earthworm biomass [39]. Many researchers have revealed that biochemical quality and the kind of food affects the earthworm biomass and reproduction [40–42]. In vermicomposting process, the decomposition and microbial density of organic wastes are important in determining the growth and reproduction of earthworms. Singh et al. [43] observed a continuous decrease of earthworm E. fetida in hundred per cent distillery sludge, but when it was mixed with cattle dung, earthworm biomass and reproduction was increased. Earthworm number and cocoons also decreased with increasing content of distillery sludge [44]. The decrease in earthworm number can be due to the toxic nature or unfavorable environment in feed substrate. Many researchers have reported that earthworm biomass grows faster at lower stocking densities [45–47]. For optimum stocking density 27–53 earthworms per kilogram per feed mixture is effective for vermicomposting process [47]. Many researchers have observed that the cocoon production was more in cow dung, whereas it was low in horse dung due to lower nutritional value [48]. Reinecke et al. [49] suggested that the ideal temperature for earthworm growth and production of cocoons is between 25 and 30 °C. Reinecke and Venter [50] suggested that in vermicomposting system the optimum moisture content for better growth and cocoon production should be maintained between 65–70%. Earthworm biomass and reproduction increases with decreasing carbon to nitrogen ratio in final feed mixtures. Organic wastes having more available forms of nutrients enhance earthworm growth and reproduction. Vermicomposting of different types of organic wastes are shown in Table 3.

Table 3 Vermicomposting of different types of organic wastes and growth features of different earthworm species
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Stabilization of Organic Wastes During Vermicomposting

Many researchers have studied biochemical changes in the organic waste during the process of vermicomposting. The comparison of nutrient content between the traditional compost and vermicompost are shown in Table 4. A brief review of physico-chemical parameters (pH, electrical conductivity, organic carbon, C:N ratio, nitrogen, phosphorus, potassium and heavy metals) is given below:

Table 4 Comparison of nutrient content of traditional compost and vermicompost (cattle dung)
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pH

The pH of organic wastes is an important factor affecting the vermicomposting process. Earthworms can remain alive in a pH range of 5–9 and the most desirable pH during the process of vermicomposting is recommended to be 7.5–8.0 [81]. pH is highly dependent on the initial raw material used for the stabilization process. In vermicomposting pH usually decreases from alkaline to neutral or acidic [40]. The shift in pH towards acidic or neutrality may be due to the formation of organic acids and mineralization of organic nitrogen and phosphorus. Many researchers have reported acidic nature of pH during vermicomposting of organic wastes [48, 82]. Garg et al. [83] have reported that in organic wastes at initial stages the nature of pH is alkaline (8.3–7.2), whereas during vermicomposting process, pH slightly shifts to neutral or acidic (6.3–7.1) conditions due to the intermediate products produced. Elvira et al. [84] concluded that the accumulation of organic acids and evolution of carbon dioxide in vermicomposting process lowers the pH of organic wastes as compared to initial feed mixtures. Vermicomposts of pH range 6–8.5 are capable for soil application [85]. In composting and vermicomposting process, increase in pH is mainly due to the utilization of organic acids and an increase in nutrient constituents of the organic wastes [86]. Datar et al. [87] observed increase in the pH of organic community solid waste using earthworm Eudrilus eugeniae and this increase may be due to the excess of organic nitrogen and later releases as ammonia, which gets dissolved in water and increases the pH of the final vermicompost [88]. Muthukamaravel et al. [89] also reported increase in pH, which may be attributed to the decomposition of nitrogenous materials. In vermicomposting process during initial stages, increase in pH value may be due to the formation of basic hydroxides and in final stages decrease in pH towards neutrality is due to the production of organic acids [90]. A number of reasons can be discussed for the change in pH during bioconversion of wastes by earthworms. The difference in pH among the different feed mixtures of organic wastes may be due to the quality of feed material which affected the mineralization process during vermicomposting.

Electrical Conductivity (EC)

EC reflects the salinity of an organic material. Phytoxicity may be caused by high salt concentrations therefore EC values of a vermicompost is a good indicator for agricultural purposes [91]. Lasaridi et al. [92] reported that the maximum tolerance limit of plants to EC is 4.0 mScm−1 and a lower value than 4.0 mScm−1 can be safely applied for agricultural purposes. Some researchers during vermicomposting process reported decrease in EC values [43, 74, 83] while as others report an increase in EC values [38, 66, 69, 75, 93, 94]. Karmegam and Daniel [95] observed an increase in the final EC values of vermicompost which may be due to the increase in soluble salt level, resulting from the action of worms and microbes. Kaviraj and Sharma [96] also reported an increase in final EC values during vermicomposting of municipal solid wastes and is due to the loss final weight of organic materials and release of mineral salts such as potassium, ammonium, phosphates etc in plant available forms. Kaur et al. [75] observed that in paper mill sludge vermicomposting, increase in sodium and potassium parameters and a decrease in total organic carbon content may be responsible for increased final EC values. Garg et al. [94] reported that increase in final EC values during vermicomposting process is mainly due to the free available minerals and ions produced during the breakdown and excretion by earthworms. Singh et al. [43, 74] observed a decline in final EC values during vermicomposting of beverage and distillery industry sludge. Decrease in EC may be due to the stabilization of final mixtures and a decrease in ions after forming a complex.

Organic Carbon and Carbon to Nitrogen Ratio

Earthworms consume various organic wastes and decreases organic carbon during vermicomposting process. This reduction in organic carbon denotes the rate of degradation of organic wastes. The reduction in organic carbon in the final vermicompost is due to the loss of carbon from substrate through respiration by the combined action of earthworms and microbes [61, 76, 97]. In the vermicomposting process earthworms and microbes promote such conditions in the feed mixtures that it activates microbial respiration and degradation of organic wastes, thereby increases the loss of organic carbon [98]. Venkatesh and Eevera [99] reported that a major portion of carbon and nitrogen is used by microbes and earthworms for decomposition of organic wastes and may have decreased the large fractions of organic carbon as CO2. Garg and Gupta [81] suggested that the reduction in organic carbon in initial stages of vermicomposting is more due to the availability of food at initial stages which increases the earthworm and microbial activity in the organic wastes. Ravindran et al. [100] reported the organic carbon decreased from 55.12 to 21.1% during vermicomposting of animal fleshing solid waste generated from leather industries. Earthworms thus bring about significant reduction in organic carbon content of the organic wastes and increase the waste bioconversion process.

Carbon to Nitrogen ratio (C:N ratio) reflect the waste decomposition and mineralization. Reduction in C:N ratio is due to maximum loss of carbon through microbial respiration in the form of CO2 and increase in nitrogen in the form of mucus and stabilization of organic material by the earthworms [73, 93]. However in vermicomposting initial content of nitrogen in the feed mixtures are mainly responsible for the final content of nitrogen and the extent of decomposition. For faster organic waste stabilization, the optimum C:N ratio should be in between 25 and 30. Sinesi [101] suggested that a reduction in C:N ratio to <20 indicates organic waste stabilization and compost maturity which is an important tool for the growth of plants. Many researchers have reported that C:N ratio decreases sharply during vermicomposting and is one of the most widely used indicator for maturity of organic wastes [43, 44, 81, 102]. The loss of carbon and production of nitrogenous excreta increases the nitrogen content, which decreases the C:N ratio of feed mixtures.

Nitrogen

Nitrogen is easily available in vermicomposting technology as compared to other technologies for organic waste degradation. Many researchers have reported that the rearing of earthworms increases soil nitrogen which may be due to the death and decay of earthworms [103, 104]. Cynthia and Rajeshkumar [105] observed an increase in nitrogen content of final vermicompost mixtures of sugar industry and is due to the decomposition of waste by earthworms to increase the nitrogen bioconversion process. Earthworms increases the nitrogen content of final vermicompost through death of some earthworm tissues and microbial mediated nitrogen transformation results in further increase in nitrogen [106]. Tripathi and Bhardwaj [41] reported that during vermicomposting process addition of nitrogen content is due to the release of nitrogenous excretory substances, mucus, growth hormones and enzymes. Losses in organic carbon during decomposition of organic wastes should be responsible for enhancement of nitrogen [107]. Mineralization of carbon-rich materials and action of nitrogen-fixing bacteria during vermicomposting process increases mineral-N forms [108]. Ravindran et al. [100] reported that the nitrogen content of final vermicomposted animal fleshing waste increased from 0.81 to 1.34% from that of control. Yadav and Garg [109] suggested that mineralization of organic waste, decreases in pH, ammonium to nitrate conversion and decrease in organic carbon content should be responsible for addition of nitrogen in final vermicompost. While many researchers revealed that decrease in nitrogen content during the vermicomposting process. This may be due to ammonification, denitrification, NH3 volatilization, leaching or due to release of ammonia [110, 111]. In general, increase in final nitrogen content of vermicompost depends upon the initial nitrogen content and the extent of mineralization.

Phosphorus

Phosphorus plays an important role in plant maturation. It is required for photosynthesis, root establishment, good flowering, energy transfer, fruit quality and fruit growth of various crops and plants. Hesse [112] reported that phosphorus in the form of orthophosphates (H2PO4 − and H2PO4 2−) is taken up by plants. Phosphorus usually increases in the final vermicompost than initial wastes. Singh et al. [43] observed an increase of 13.83% in total phosphorus of distillery sludge after vermicomposting with E. fetida for 150 days. Hameeda et al. [113] reported that at different pH various types of microbes act on phosphorus for its solubilisation during composting and vermicomposting. In vermicomposting process, increase in phosphorus is mainly due to acid formation during organic waste decomposition by microbes and is responsible for solubilisation of insoluble phosphorus [114]. Earthworm increases the availability of phosphorus in the vermicomposting system. This release of phosphorus is performed by earthworm gut phosphatases and phosphate-solubilizing microbes present in the final feed mixtures of vermicompost [115]. Yadav and Garg [116] reported that vermicomposting process increases phosphorus content through decomposition and mineralization of phosphorus by phosphate and bacterial activity of worms. Microflora present in vermicompost feed mixtures plays an important role in increased content of phosphorus of final earthworm casts [117]. Bhat et al. [66] reported 22.60% increase in total phosphorus in the final vermicompost products of pressmud sludge. Kaur et al. [75] also reported that vermicomposting feed mixtures had higher phosphorus content as compared to the mixtures of composting without earthworms. Ravindran and Sekaran [118] revealed that the net loss of dry mass which concentrates the phosphorus in the final feed mixtures of vermicomposting process increases the phosphorus content. Yadav and Garg [38] also reported 30–60% increase in phosphorus content in the final products of vermicomposting than the initial raw waste.

Potassium

Potassium along with phosphorus and nitrogen plays an important role for plant growth. It is an essential nutrient used in cell division and root development by plants [109]. Many researchers have also reported that vermicomposting significantly increases the potassium concentrations in the final feed mixtures of organic wastes [5, 44]. Kaviraj and Sharma [96] suggested that the potassium is increased by the enhanced microflora present in earthworm gut. Increase in potassium concentration was also observed in the final vermicompost of distillery sludge [43]. Yadav and Garg [38] observed an increase in potassium content of industrial solid wastes and weeds. Increased potassium content in final feed mixtures ranged from 41.2 to 60% as compared to the initial raw waste mixtures. Some studies regarding potassium concentration in final vermicomposts are contradictory as potassium may release due to leaching of soluble elements by excess water of bottom [84, 119]. Singh et al. [43] suggested that the earthworm may use the available potassium, as potassium was more in feed mixtures without earthworms as compared to feed mixtures with earthworms. Leachates collected during vermicomposting of sewage sludge had higher content of potassium [110]. Bhat et al. [66, 68] have reported 15.78 and 66.7% decline in total potassium content in the final vermicompost feed mixtures of dyeing sludge and pressmud sludge respectively. Rise in pH during vermicomposting process may be responsible for decrease in potassium ions, as it is more susceptible to fixation by colloids at higher pH [120].

Heavy Metals

Heavy metals (Cd, Cr, Cu, Fe, Mn, Ni, Zn) are important trace elements for growth, metabolism and development of plants and animals. Heavy metals in excess concentrations have toxic effects [121]. Metal toxicity depends on metal concentration, mobility, bioavailability and metal uptake mechanism [122]. During vermicomposting process earthworms ingest organic materials and are therefore exposed to metals from the wastes and bio accumulates in their bodies [44]. Earthworms have the ability to accumulate heavy metals in polluted soils [123]. Intestinal microflora and chloragocyte cells of earthworms have the ability to detoxify the heavy metals [124]. So vermicomposting technique can be used for the removal of toxic pollutants and the breakdown of toxic wastes to nontoxic forms. Saxena et al. [123] revealed that during vermicomposting process, earthworms can accumulate metals at superior concentrations. Jain et al. [124] have successfully converted flyash into vermicompost. The results suggested that E. fetida accumulates heavy metals and also reduces Cr(VI) to Cr(III). The vermicomposting of flyash was an efficient technology for decreasing the metal concentrations in fly ash. Gupta et al. [125] also observed reduction in heavy metal content during vermicomposting of flyash. The study revealed that earthworm bodies retain heavy metals and decreases heavy metal content in the final vermicompost. Suthar and Singh [115] reported that vermicomposting of distillery sludge reduced total metal content than initial raw substrate. The authors suggested that reduction in metal content was higher in feed mixtures which show better decomposition and earthworm growth. Many researchers have reported that earthworms accumulate heavy metals and retained within worm bodies if reared for a longer duration in contaminated soils [126–128]. Comparative assessment of heavy metals during the composting and vermicomposting of municipal solid waste has been studied by Soobhany et al. [129]. The authors concluded that metal loss was more in vermicomposting due to earthworm activity in the waste mineralization than the composting process. Soobhany et al. [130] also observed heavy metal reduction (Cd, Cr, Cu, Co, Zn) during vermicomposting of organic wastes by Eisenia eugeniae in the final feed mixtures. Heavy metal concentration was increased in the tissues of earthworms from initial to final process (677.5–6791.4 mg/kg for Cd, 2345.4–2355.0 mg/kg for Cr, 1042.0–1060.55 mg/kg for Cu, 723.8–741.7 mg/kg for Co, 486.7–620.6 mg/kg for Zn, 35.4–68.6 mg/kg for Ni). Singh and Kaur [131] reported decrease in metal content in the final vermicompost mixtures of chemical sludge and spent carbon wastes generated from soft drink industries. Decline in heavy metal contents corresponded with an increase in earthworm weight. Cells of yellow tissue in earthworm body have an ability to accumulate heavy metals [132]. Gupta et al. [133] revealed that during vermicomposting of water hyacinth, decline in heavy metal content could be due to leaching or retained by earthworms. Ravindran et al. [134] reported that in final products of tannery solid waste, heavy metals were highly decreased by earthworms as compared to without earthworm feed mixtures. The highest reduction of heavy metals after 25 days of processing was in order of Cu 58.5%, Cr 55.8%, Zn 35.7%, Mn 23.4% and Fe 19%.

Some researchers reported increased heavy metal content in the products of vermicomposting [38, 61, 63, 69–71]. Deolalikar et al. [135] suggested that increase in heavy metal concentrations of the final feed mixtures of vermicomposting may be due to decline in the volume and weight in the final feed mixtures. Earthworm casts obtained from cultivated lands and sewage soils have higher concentration of heavy metals [126]. Yadav and Garg [38] reported increased content of heavy metals during vermicomposting of industrial solid wastes and weeds by E. fetida. The authors revealed that mineralization and reduction of waste biomass during vermicomposting process may increase heavy metal content in the final feed mixtures. Increase in heavy metals (Zn, Fe, Mn, Ni) during vermicomposting of paper mill sludge have also been observed by Elvira et al. [84]. Although there was an increase in the heavy metal concentrations in vermicomposting process but the contents were less than the international standards, which indicated that the vermicompost can be applied for agricultural purposes without any harmful effects.

Conclusion and Future Prospects

From the information provided in this review, it can be concluded that vermicomposting is economically sound, environmentally safe technology for organic waste degradation. The earthworms improved the physico-chemical characteristics of waste materials, indicating that the application of vermicompost can significantly improve the fertility of soil. In most of the studies, organic waste when applied in combination with other bulking material has improved the growth of earthworms as well as quality of the final vermicompost. The earthworm-microbe interaction is interdependent and the relationship between earthworm and microbes can play a major role in producing high quality manure. The final vermicompost was higher in available nutrients than traditional compost and has a huge potential for agricultural purposes. So, farmers must be educated regarding the useful role of earthworms as waste managers and biofertilizer producers. Keeping the above advantages in mind, vermicompost in near future should be applied to agricultural crops to replace chemical fertilizers. The organic farming continues to grow at world level and the crop made by organic fertilizers sustains the yield and fertility of soil. The studies reported by many authors described earthworms as ecological engineers in utilizing the organic wastes and also the final vermicompost as a powerful biofertilizer for sustainable development.