Earthworm Impact: History
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Subjects: Agronomy
Contributor:
Sami ur Rehman
,
Federica De Castro
,
Alessio Aprile
,
Michele Benedetti
,
Francesco Paolo Fanizzi

Earthworms serve as ecological mediators influencing soil structures and microbial activities. The role played by earthworms in improving organic matter decomposition, soil fertility, and soil microorganisms’ activity is discussed herein.

  • earthworms
  • soil fertility
  • soil microbes
  • organic matter decomposition
  • vermicomposting

1. Introduction

Due to their priming effects, earthworms (EWs) serve as ecological mediators influencing soil structures and microbial activities [1]. They are considered among the largest soil species in tropical and temperate regions, accounting for 40–90% of soil macro-fauna [2]. EWs are classified into three main niche groups: epigeic, endogeic, and anecic. Anecic species inhabit deep mineral layers, endogeic species are active in the uppermost mineral layers, and epigeic species feed on surface litter. They promote organic matter decomposition by enhancing microbial activity and population in the soil [3]. EWs such as Eisenia fetida and Eudrilus sp. have been found to increase bacterial diversity during the early stages of vermicomposting [4][5]. EWs play a vital role in breaking down organic matter (OM) and converting macro and micronutrients [6]. 

2. Soil Structure

Among different soil characteristics, its structure is the most important parameter determining fertility. For example, an ideal soil structure improves water-holding capacity, reducing water and soil loss [7]. EWs improve soil structure through humus production, mineral weathering, and the mixing of OM to form soil aggregates. Although it has been demonstrated that E. fetida increases the weathering of kaolinite, biotite, smectite, and anorthite [8], the effect of EWs on mineral weathering still needs to be fully understood. Further studies are required to determine whether the EWs, the microbes in their gut, or both induce an increase in mineral weathering.
A recent study on soil aggregate formation by Al-Maliki and Scullion [9] focused on the relationship between kaolinite and organic material in the presence of EWs. Researchers found that EWs regulate soil structure by improving aggregate stability and stabilizing aliphatic carbon in kaolinite. The burrowing activities of EWs influence the mechanical and hydraulic properties of soil, creating macropores for water percolation in soil profiles and reducing surface runoff [10]. In tropical and temperate soils, the casting and burrowing practices of the anecic EWs control erosion by increasing soil structural stability and porosity [11]. The effect of EWs on soil compaction and loss depends on species type and their interaction with the soil. The long-term interaction with the Eudrilidae family (de-compacting EWs) and Reginaldia omodeoi (compacting EWs) helps maintain soil structure in tropical regions [1]. The cast production in horizontal and vertical burrows by endogeic and anecic EWs influences soil bulk density and porosity. For instance, Rhyacodrilus omodeoi, an anecic earthworm, increased the bulk density from 1.12 to 1.23 g cm−3, and Pontoscolex corethrurus, an endogeic earthworm, reduced the soil porosity from 58% to 53% [12][13].

3. Organic Matter Decomposition

Decomposition is a crucial process that regulates nutrient cycling in terrestrial environments through decomposers such as nematodes, protozoa, microbes, and EWs. EWs are efficient members of the decomposers’ community and play a significant role in plant residue decomposition and the turnover of other organic materials [14][15]. EWs considerably impact decomposition by modifying OM and microbes that pass through their gut and are released in the cast [16][17]. During the gut passage, mucus is added, accelerating microbial and enzymatic activities, thereby increasing OM mineralization [18][19]. Through the vertical distribution of grounded material in the soil profile, EWs’ activity increases surface area for microbial colonization and faster decomposition [20]. Organic matter breakdown by EWs is closely related to the material’s chemical properties. The palatability of material for EWs increases with a reduction in the C/N ratio. Ernst et al. confirmed that residue decomposition by EWs was highest in maize litter (C/N: 34.8) compared to Miscanthus litter (C/N: 134.4) [14]. Epigeic EWs inhabit litter, ingest, and transform OM from various habitats such as forest litter and livestock dung. They interact with microbes and other organisms within the habitat, affecting decomposition processes [16][21]. EWs contribute to decomposition processes through fragmentation, incorporation, and mixing organic material into the soil.

4. Soil Fertility

Various species of EWs can produce different soil biological profiles and fertility levels. The combined activity of these species ensures the maintenance of soil fertility throughout the soil profile [22][23]. EWs play a vital role in producing soil aggregates and biostructures such as pores for better movement of nutrients and water. They also increase N mineralization by encouraging the microbial population both directly and indirectly [24][25]. EWs effectively contribute to nitrogen recycling and enhance the availability of essential plant nutrients. They consume an abundance of substrate but retain only a tiny portion of it (5–10%); the remaining substrate is excreted as vermicompost, which is enriched in N, P, K, and other micronutrients and beneficial microbes. These microbes increase the nitrogen fixation process, providing more nitrogen in worm casts [11][26]. A meta-analysis of casts reveals higher nutrient contents in casts than soil [27]. EWs are also well-known for increasing phosphorus availability in their casts and burrows [28]. P is an essential nutrient for plants, helping to accumulate and transform energy in the metabolic activities of living organisms. It also promotes seedling growth and crop maturity. Earthworm casts contain more P than the soil without them, so EWs have a positive association with P acquisition in soil [29].
Van Groenigen et al. [27] focused on the increase in soil fertility properties in earthworm casts and coined a new term, “relative cast fertility (RCF)” [27]. RCF explains the relative difference in fertility and soil properties, such as nutrient availability and pH, between the EWs casts and the soil. This difference can result from two key processes: concentration and transformation. Firstly, EWs can enhance the RCF by concentrating existing soil fertility towards earthworm-influenced pools of soil fertility. EWs are selective in choosing their food, and this food selection varies among species [30]. The choice of EWs’ diet centers around the size, age, biochemical properties, and microbial population in the feeding mixture [31][32][33][34]. Secondly, RCF can be increased by the transformation process in the gut or casts. The earthworm gut is home to various microbes effectively involved in several biochemical processes [35][36], which affect soil fertility properties. Due to the transformation process, nutrient availability and pH are usually higher in worm casts than in the soil. For instance, N and P contents are higher in the gut or casts [37][38], and the availability of other nutrients such as Ca, Mg, and K may also increase during gut transit [8].

5. Soil Microorganisms

EWs positively or negatively impact microbial populations and their ecological diversity. They influence the functions of microbial decomposers by feeding on microorganisms and making adjacent areas more susceptible to microbial attack after organic matter is broken down. Microorganisms such as bacteria, fungi, and protozoa are essential food sources for the EWs. The combined action of EWs and microorganisms accelerates the decomposition of organic matter [39]. The function of microorganisms and organic matter decomposition is affected by gut-associated processes. The composition of gut-associated microbes (GAM) is related to the ingested material. In addition, the number and behavior of the microbes in EWs’ gut differ from those in uninterrupted material. Hong et al. [40] analyzed the community structure of GAM and explained the impact of enzyme-producing microbes on EWs biomass. They detected 57 bacterial clones in EWs gut using PCR-DGGE analysis. Aeromonas hydrophila, Paenibacillus motobuensis, and Photobacterium ganghwense were active in enzyme production. The mixture inoculated with Aeromonas hydrophila and Paenibacillus motobuensis showed the highest survival rate (100%) and increased the EWs’ growth and cast production, demonstrating a symbiotic relationship between EWs and microorganisms. Specific microorganisms respond differently to the gut environment, and the selective impact on microorganisms during the passage through the EWs’ gut has been analyzed [41]. For example, some bacteria became activated during passage to EWs’ gut, while others remain unchanged or are digested, thus reducing their number [35][42]. Monroy et al. [43] observed a 98% decline in coliforms density after pig slurry passed through the gut of Eisenia fetida. Earthworms can modify microbial physiology and stimulate enzymatic activity during the vermicomposting of pig slurry [4][5][23]. Studies on soil and six species of earthworms and fungi showed that EWs process the soil efficiently by increasing the fungal species involved in faster decomposition processes [44][45].

This entry is adapted from the peer-reviewed paper 10.3390/agronomy13041134

References

  1. Ahmed, N.; Al-Mutairi, K.A. Earthworms Effect on Microbial Population and Soil Fertility as Well as Their Interaction with Agriculture Practices. Sustainability 2022, 14, 7803.
  2. Fragoso, C.; Kanyonyo, J.; Moreno, A.; Senapati, B.K.; Blanchart, E.; Rodriguez, C. A survey of tropical earthworms: Taxonomy, biogeography and environmental plasticity. Earthworm Manag. Trop. Agroecosyst. 1999, 1–26.
  3. Eggleton, P.; Inward, K.; Smith, J.; Jones, D.T.; Sherlock, E. A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture. Soil Biol. Biochem. 2009, 41, 1857–1865.
  4. Vivas, A.; Moreno, B.; Garcia-Rodriguez, S.; Benitez, E. Assessing the impact of composting and vermicomposting on bacterial community size and structure, and microbial functional diversity of an olive-mill waste. Bioresour. Technol. 2009, 100, 1319–1326.
  5. Gopal, M.; Bhute, S.S.; Gupta, A.; Prabhu, S.; Thomas, G.V.; Whitman, W.B.; Jangid, K. Changes in structure and function of bacterial communities during coconut leaf vermicomposting. Antonie Van Leeuwenhoek 2017, 110, 1339–1355.
  6. Edwards, C.A.; Bohlen, P.J. Biology and Ecology of Earthworms; Springer Science & Business Media: London, UK, 1996; Volume 3.
  7. Vickers, N.J. Animal communication: When i’m calling you, will you answer too? Curr. Biol. 2017, 27, R713–R715.
  8. Carpenter, D.; Hodson, M.E.; Eggleton, P.; Kirk, C. Earthworm induced mineral weathering: Preliminary results. Eur. J. Soil Biol. 2007, 43, S176–S183.
  9. Al-Maliki, S.; Scullion, J. Interactions between earthworms and residues of differing quality affecting aggregate stability and microbial dynamics. Appl. Soil Ecol. 2013, 64, 56–62.
  10. Ritsema, C.J.; Dekker, L. Preferential flow in water repellent sandy soils: Principles and modeling implications. J. Hydrol. 2000, 231, 308–319.
  11. Atiyeh, R.M.; Domínguez, J.; Subler, S.; Edwards, C.A. Changes in biochemical properties of cow manure during processing by earthworms (Eisenia andrei, Bouché) and the effects on seedling growth. Pedobiologia 2000, 44, 709–724.
  12. Lavelle, P.; Charpentier, F.; Villenave, C.; Rossi, J.-P.; Derouard, L.; Pashanasi, B.; André, J.; Ponge, J.-F.; Bernier, N. Effects of earthworms on soil organic matter and nutrient dynamics at a landscape scale over decades. Earthworm Ecol. 2004, 2, 145–160.
  13. Alegre, J.; Pashanasi, B.; Lavelle, P. Dynamics of soil physical properties in Amazonian agroecosystems inoculated with earthworms. Soil Sci. Soc. Am. J. 1996, 60, 1522–1529.
  14. Ernst, G.; Henseler, I.; Felten, D.; Emmerling, C. Decomposition and mineralization of energy crop residues governed by earthworms. Soil Biol. Biochem. 2009, 41, 1548–1554.
  15. Lubbers, I.M.; Pulleman, M.M.; Van Groenigen, J.W. Can earthworms simultaneously enhance decomposition and stabilization of plant residue carbon? Soil Biol. Biochem. 2017, 105, 12–24.
  16. Aira, M.; Domínguez, J. Earthworm effects without earthworms: Inoculation of raw organic matter with worm-worked substrates alters microbial community functioning. PLoS ONE 2011, 6, e16354.
  17. Aira, M.; Monroy, F.; Domínguez, J. Changes in bacterial numbers and microbial activity of pig slurry during gut transit of epigeic and anecic earthworms. J. Hazard. Mater. 2009, 162, 1404–1407.
  18. Chapuis-Lardy, L.; Bayon, R.-C.L.; Brossard, M.; López-Hernández, D.; Blanchart, E. Role of soil macrofauna in phosphorus cycling. In Phosphorus in Action; Springer: Berlin/Heidelberg, Germany, 2011; pp. 199–213.
  19. Blouin, M.; Hodson, M.E.; Delgado, E.A.; Baker, G.; Brussaard, L.; Butt, K.R.; Dai, J.; Dendooven, L.; Pérès, G.; Tondoh, J. A review of earthworm impact on soil function and ecosystem services. Eur. J. Soil Sci. 2013, 64, 161–182.
  20. Seeber, J.; Seeber, G.; Langel, R.; Scheu, S.; Meyer, E. The effect of macro-invertebrates and plant litter of different quality on the release of N from litter to plant on alpine pastureland. Biol. Fertil. Soils 2008, 44, 783–790.
  21. Sampedro, L.; Domínguez, J. Stable isotope natural abundances (δ13C and δ15N) of the earthworm Eisenia fetida and other soil fauna living in two different vermicomposting environments. Appl. Soil Ecol. 2008, 38, 91–99.
  22. Thakuria, D.; Schmidt, O.; Finan, D.; Egan, D.; Doohan, F.M. Gut wall bacteria of earthworms: A natural selection process. ISME J. 2010, 4, 357–366.
  23. De Menezes, A.B.; Prendergast-Miller, M.T.; Macdonald, L.M.; Toscas, P.; Baker, G.; Farrell, M.; Wark, T.; Richardson, A.E.; Thrall, P.H. Earthworm-induced shifts in microbial diversity in soils with rare versus established invasive earthworm populations. FEMS Microbiol. Ecol. 2018, 94, fiy051.
  24. Fujii, K.; Ikeda, K.; Yoshida, S. Isolation and characterization of aerobic microorganisms with cellulolytic activity in the gut of endogeic earthworms. Int. Microbiol. 2012, 15, 121–130.
  25. Johnsen, A.R.; Wick, L.Y.; Harms, H. Principles of microbial PAH-degradation in soil. Environ. Pollut. 2005, 133, 71–84.
  26. Chan, K.; Baker, G.; Conyers, M.; Scott, B.; Munro, K. Complementary ability of three European earthworms (Lumbricidae) to bury lime and increase pasture production in acidic soils of south-eastern Australia. Appl. Soil Ecol. 2004, 26, 257–271.
  27. Van Groenigen, J.W.; Van Groenigen, K.J.; Koopmans, G.F.; Stokkermans, L.; Vos, H.M.; Lubbers, I.M. How fertile are earthworm casts? A meta-analysis. Geoderma 2019, 338, 525–535.
  28. Le Bayon, R.-C.; Milleret, R. Effects of earthworms on phosphorus dynamics–a review. Dyn. Soil Dyn. Plant 2009, 3, 21–27.
  29. Nuutinen, V.; Pitkänen, J.; Kuusela, E.; Widbom, T.; Lohilahti, H. Spatial variation of an earthworm community related to soil properties and yield in a grass–clover field. Appl. Soil Ecol. 1998, 8, 85–94.
  30. Curry, J.P.; Schmidt, O. The feeding ecology of earthworms–a review. Pedobiologia 2007, 50, 463–477.
  31. Neilson, R.; Boag, B. Feeding preferences of some earthworm species common to upland pastures in Scotland. Pedobiologia 2003, 47, 1–8.
  32. Lowe, C.N.; Butt, K.R. Influence of food particle size on inter-and intra-specific interactions of Allolobophora chlorotica (Savigny) and Lumbricus terrestris: The 7th international symposium on earthworm ecology Cardiff Wales·2002. Pedobiologia 2003, 47, 574–577.
  33. Satchell, J.E. Lumbricidae. In Soil Biology; Burges, A., Raw, F., Eds.; Academic Press: London, UK, 1967; pp. 259–322.
  34. Moody, S.; Briones, M.; Piearce, T.; Dighton, J. Selective consumption of decomposing wheat straw by earthworms. Soil Biol. Biochem. 1995, 27, 1209–1213.
  35. Drake, H.L.; Horn, M.A. As the worm turns: The earthworm gut as a transient habitat for soil microbial biomes. Annu. Rev. Microbiol. 2007, 61, 169–189.
  36. Tiwari, S.; Tiwari, B.; Mishra, R. Microbial populations, enzyme activities and nitrogen-phosphorus-potassium enrichment in earthworm casts and in the surrounding soil of a pineapple plantation. Biol. Fertil. Soils 1989, 8, 178–182.
  37. Decaëns, T.; Rangel, A.; Asakawa, N.; Thomas, R.J. Carbon and nitrogen dynamics in ageing earthworm casts in grasslands of the eastern plains of Colombia. Biol. Fertil. Soils 1999, 30, 20–28.
  38. Brossard, M.; Lavelle, P.; Laurent, J.-Y. Digestion of a vertisol by the endogeic earthworm Polypheretima elongata, Megascolecidae, increases soil phosphate extractibility. Eur. J. Soil Biol. 1996, 32, 107.
  39. Edwards, C.; Lofty, J. Biology of Earthworms; Chapman and Hall: London, UK, 1977.
  40. Hong, S.W.; Lee, J.S.; Chung, K.S. Effect of enzyme producing microorganisms on the biomass of epigeic earthworms (Eisenia fetida) in vermicompost. Bioresour. Technol. 2011, 102, 6344–6347.
  41. Schönholzer, F.; Hahn, D.; Zeyer, J. Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol. Ecol. 1999, 28, 235–248.
  42. Pedersen, J.C.; Hendriksen, N.B. Effect of passage through the intestinal tract of detritivore earthworms (Lumbricus spp.) on the number of selected Gram-negative and total bacteria. Biol. Fertil. Soils 1993, 16, 227–232.
  43. Monroy, F.; Aira, M.; Domínguez, J. Reduction of total coliform numbers during vermicomposting is caused by short-term direct effects of earthworms on microorganisms and depends on the dose of application of pig slurry. Sci. Total Environ. 2009, 407, 5411–5416.
  44. Brown, G.G.; Barois, I.; Lavelle, P. Regulation of soil organic matter dynamics and microbial activityin the drilosphere and the role of interactionswith other edaphic functional domains. Eur. J. Soil Biol. 2000, 36, 177–198.
  45. Hoeffner, K.; Monard, C.; Santonja, M.; Cluzeau, D. Feeding behaviour of epi-anecic earthworm species and their impacts on soil microbial communities. Soil Biol. Biochem. 2018, 125, 1–9.
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