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Emission of greenhouse gases and soil changes in casts of a giant Brazilian earthworm

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Abstract

Greenhouse gas emissions (CO2, N2O, CH4) and chemical, physical and microbiological properties (pH, macro and micronutrients, texture, moisture, exchangeable NH4+, NO3−, total C and N, organic C, microbial biomass C and metabolic coefficient) were monitored in casts of a large, endogeic native Brazilian earthworm species Rhinodrilus alatus and from non-ingested control soil incubated for up to 32 days. Earthworm casts represented a significantly different chemical and microbiological environment, with higher soil moisture, pH, H + Al, exchangeable NH4, Cu, Fe and Mn contents, lower microbial biomass C and higher metabolic quotient (qCO2), but with few differences in CO2, N2O and CH4 emissions compared with non-ingested control soil. Nonetheless, fermenting, methanogenic and nitrate-reducing microbes encountered ideal conditions for sustained anaerobic activity in the clayey, dense and moist castings of R. alatus, maintaining emission of N2O and CH4 and confirming previous results observed using gut contents. The high exchangeable NH4 and H2O contents influenced the oxy-reduction processes, affected GHG emissions and N transformations and modified soil microbial biomass and activity. In addition, selective ingestion concentrates C and N contents in the casts and transformation processes affect the availability of important plant nutrients, topics that deserve further attention, considering the widespread collection of this species for use as fish-bait in Brazil.

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References

  • Anderson JPE, Domsch KH (1993) The metabolic quotient of CO2 (qCO2) as a specific activity paramenter to assess the effects of environmental condition, such as pH, on the microbial of forest soil. Soil Biol Biochem 25:393–395

    Google Scholar 

  • Anderson JM, Ingram JSI (1993) Tropical soil biological and fertility – a handbook of methods, 2nd edn. CABI, Wallingford

    Google Scholar 

  • Bahl KN (1947) Excretion in the oligochaeta. Biol Rev Camb Philos Soc 22:109–147

    CAS  PubMed  Google Scholar 

  • Barois I, Verdier B, Kaiser P, Mariotti A, Rangel P, Lavelle P (1987) Influence of the tropical earthworm Pontoscolex corethrurus (Glossoscolecidae) on the fixation and mineralization of nitrogen. In: Omodeo P, Bonvicini AM (eds) On earthworms. Mucchi, Bologna, pp 151–158

    Google Scholar 

  • Barois I, Lavelle P, Brossard M, Tondoh J, Martinez MA, Rossi JP, Senapati BK, Angeles A, Fragoso C, Jimenez JJ, Decaens T, Lattaud C, Kanyonyo J, Blanchart E, Chapuis L, Brown G, Moreno A (1999) Ecology of earthworm species with large environmental tolerance and/ or extended distributions. In: Lavelle P, Hendrix P, Brussard L (eds) Earthworm management in tropical agroecosystems. CAB International, Wallingford, pp 57–86

    Google Scholar 

  • Bartz MLC, Costa ACS, Souza IG, Brown GG (2010) Micronutrientes e óxidos de ferro em coprólitos de minhocas produzidos em um Latossolo Vermelho distroférrico (Oxisol) sob diferentes sistemas de manejo. Acta Zool Mex 26:281–294

    Google Scholar 

  • Bayon RC, Binet F (2006) Earthworms change the distribution and availability of phosphorous in inorganic substrates. Soil Biol Biochem 38:235–246

    Google Scholar 

  • Bityutskii NP, Kaidun PI (2008) The influence of earthworms on the mobility of microelements in soil and their availability for plants. Euras Soil Sci 41:1306–1313

    Google Scholar 

  • Bityutskii NP, Kaidun PI, Yakkonem KL (2012) The earthworm (Aporrectodea caliginosa) primes the release of mobile and available micronutrients in soil. Pedobiologia 55:93–99

    Google Scholar 

  • Blanchart E, Lavelle P, Braudeau E, Le Bissonnais Y, Valentin C (1997) Regulation of soil structure by geophagous earthworm activities in humid Savannas of Côte d’Ivoire. Soil Biol Biochem 29:431–439

    CAS  Google Scholar 

  • Blanchart E, Albrecht A, Alegre J, Duboisset A, Gilot C, Pashanasi B, Lavelle P, Brussaard L (1999) Effects of earthworms on soil structure and physical properties. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CAB International, Wallingford, pp 149–172

    Google Scholar 

  • Bottinelli N, Hallaire V, Menasseri-Aubry S, Le Guillou C, Cluzeau D (2010) Abundance and stability of belowground earthworm casts influenced by tillage intensity and depth. Soil Tillage Res 106:263–267

    Google Scholar 

  • Bouché MB (1977) Strategies lombriciennes. In: Lohm U, Persson T (eds) Soil organisms as components of ecosystems, vol 25. Ecological Bulletins, Stockholm, pp 122–132

    Google Scholar 

  • Bouché MB, Al-Addan F (1997) Earthworms, water infiltration and soil stability: some new assessments. Soil Biol Biochem 29:441–452

    Google Scholar 

  • Braga LP, Yoshiura CA, Borges CD, Horn MA, Brown GG, Drake HL, Tsai SM (2016) Disentangling the influence of earthworms in sugarcane rhizosphere. Sci Rep 6:38923

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown GG, Doube BM (2004) Functional interactions between earthworms, microorganisms, organic matter, and plants. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, FL, pp 213–239

    Google Scholar 

  • Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:1–23

    Google Scholar 

  • Chang CH, Szlavecz K, Buyer JS (2016) Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon. Soil Biol Biochem 100:129–139

    CAS  Google Scholar 

  • Chapuis-Lardy L, Brossard M, Lavelle P, Schouller E (1998) Phosphorus transformations in a Ferralsol through ingestion by Pontoscolex corethrurus, a geophagous earthworm. Eur J Soil Biol 34:61–67

    Google Scholar 

  • Chapuis-Lardy L, Brauman A, Bernard AL, Pablo J, Toucet MJ, Mano L, Weber L, Brunet D, Razafimbelo T, Chotte JL, Blanchart E (2010) Effect of the endogeic earthworm Pontoscolex corethrurus on the microbial structure and activity related to CO2 and N2O fluxes from a tropical soil (Madagascar). Appl Soil Ecol 45:201–208

    Google Scholar 

  • Clause J, Barot S, Richard B, Decaëns T, Forey E (2014) The interactions between soil type and earthworm species determine the properties of earthworm casts. Appl Soil Ecol 83:149–158

    Google Scholar 

  • Decaëns T, Rangel AF, Asakawa N, Thomas RJ (1999) Carbon and nitrogen dynamics in ageing earthworm casts in grasslands of the eastern plains of Colombia. Biol Fertil Soils 30:20–28

    Google Scholar 

  • Depkat-Jakob PS, Hunger S, Schulz K, Brown GG, Tsai SM, Drake HL (2012) Emission of methane by Eudrilus eugeniae and other earthworms from Brazil. Appl Environ Microbiol 78:3014–3019. https://doi.org/10.1128/AEM.07949-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Depkat-Jakob PS, Brown GG, Tsai SM, Horn M, Drake HL (2013) Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microb Ecol 83:375–391. https://doi.org/10.1111/j.1574-6941.2012.01476.x

    Article  CAS  Google Scholar 

  • Devliegher W, Verstraete W (1997) Microorganisms and soil physicochemical conditions in the drilosphere of Lumbricus terrestris. Soil Biol Biochem 29:1721–1729

    CAS  Google Scholar 

  • Drake HL, Horn MA (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61:169–189. https://doi.org/10.1146/annurev.micro.61.080706.093139

    Article  CAS  PubMed  Google Scholar 

  • Drake H, Schramm A, Horn M (2006) Earthworm gut microbial biomes: their importance to soil microorganisms, denitrification, and the terrestrial production of the greenhouse gas N2O. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Soil Biology, vol 6. Springer, Berlin, pp 65–87. https://doi.org/10.1007/3-540-28185-1_3

    Chapter  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 Package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Drumond MA, Brown GG, Marini-Filho O (2012) Avaliação do risco de extinção do minhocuçu Rhinodrilus alatus Righi, 1971. Biodiversidade Brasileira 2:125–130

    Google Scholar 

  • Drumond MA, Guimarães AQ, El Bizri HR, Giovanetti LC, Sepúlveda DG, Martins RP (2013) Life history, distribution and abundance of the giant earthworm Rhinodrilus alatus RIGHI 1971: conservation and management implications. Braz J Biol 73:699–708

    CAS  PubMed  Google Scholar 

  • Drumond MA, Guimarães AQ, Silva RHP (2015) The hole of local knowledge and traditional extraction practices in the management of giant earthworms in Brazil. PLoS One 10:e0123913

    PubMed  PubMed Central  Google Scholar 

  • Elliott PW, Knight D, Anderson JM (1990) Denitrification in earthworm casts and soil from pasture under different fertilizer and drainage regimes. Soil Biol Biochem 22:601–605

    CAS  Google Scholar 

  • Elliott PW, Knight D, Anderson JM (1991) Variables controlling denitrification from earthworm casts and soil in permanent pasture. Biol Fertil Soils 11:24–29

    CAS  Google Scholar 

  • Eriksen-Hamel NS, Whalen JK (2007) Impacts of earthworms on soil nutrients and plant growth in soybean and maize agroecosystms. Agric Ecosyst Environ 120:442–448

    CAS  Google Scholar 

  • Fischer K, Hahn D, Honerlage W, Zeyer J (1997) Effect of passage through the gut of the earthworm Lumbricus terrestris L. on Bacillus megaterium studied by whole cell hybridization. Soil Biol Biochem 29:1149–1152

    CAS  Google Scholar 

  • Fiuza SS, Kusdra JF, Furtado DT (2011) Caracterização química e atividade microbiana de coprólitos de Chibui bari (Oligochaeta) e do solo adjacente. Rev Bras Ciên Solo 35:723–728

    CAS  Google Scholar 

  • Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed) Methods of soil analysis, 2nd ed. American Society Agronomy, Madison, pp 383-411

  • Hernández-Castellanos B, Barois I, Brown GG, García-Pérez JÁ (2010) Modificaciones químicas inducidas por dos especies de lombrices geófagas em suleos de Veracruz, México. Acta Zool Mex (ns) 26:295–308

    Google Scholar 

  • Hmar L, Ramanujam S (2014) Earthworm cast production and physic-chemical properties in two agroforestry systems of Mizoram (India). Trop Ecol 55:77–86

    Google Scholar 

  • Hue NV, Evans CE (1986) Procedures used for soil and plant analysis by the Auburn University soil testing laboratory no. 106. Department of Agronomy and Soils, Auburn, AL.

  • Hulugalle NR, Ezumah HC (1991) Effects of cassava-based cropping systems on physic-chemical properties of soil and earthworm casts in a tropical Alfisol. Agric Ecosyst Environ 35:55–63

    CAS  Google Scholar 

  • IUSS (2015) World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome

  • James SW, Brown GG (2006) Earthworm ecology and diversity in Brazil. In: Moreira FMS, Siqueira JO, Brussaard L (eds) Soil biodiversity in Amazonian and other Brazilian ecosystems. CABI, Wallingford, pp 56–116

    Google Scholar 

  • Jégou D, Cluzeau D, Balesdent J, Tréhen P (1998) Effects of four ecological categories of earthworms on carbon transfer in soil. Appl Soil Ecol 9:249–255

    Google Scholar 

  • Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil V. A method for measuring soil biomass. Soil Biol Biochem 8:209–213

    CAS  Google Scholar 

  • Jiménez JJ, Cepeda A, Decaëns T, Oberson A, Friesen DK (2003) Phosphorus fractions and dynamics in surface earthworm casts under native and improved grasslands in a Colombian savanna Oxisol. Soil Biol Biochem 35:715–727

    Google Scholar 

  • Kawaguchi T, Kyoshima T, Kaneko N (2011) Mineral nitrogen dynamics in the casts of epigeic earthworms (Metaphire hilgendorfi: Megascolecidae). Soil Sci Plant Nutr 57:387–339

    CAS  Google Scholar 

  • Kernecker M, Whalen JK, Bradley RL (2014) Endogeic earthworms lower net methane production in saturated riparian soils. Biol Fertil Soils 51:271–275

    Google Scholar 

  • Koubova A, Goberna M, Simek M, Chronakova A, Pizl V, Insam H, Elhottova D (2012) Effects of the earthworm Eisenia andrei on methanogens in a cattle-impacted soil: a microcosm study. Eur J Soil Biol 48:32–40

    CAS  Google Scholar 

  • Kuczak CN, Fernandes ECM, Lehmann J, Rondon MA, Luizão FJ (2006) Inorganic and organic phosphorus pools in earthworm casts (Glossoscolecidae) and a Brazilian rainforest Oxisol. Soil Biol Biochem 38:553–560

    CAS  Google Scholar 

  • Kusel K, Drake HL (1995) Effects of environmental parameters on the formation and turnover of acetate by forest soils. Appl Environ Microbiol 61:3667–3675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lavelle P (1981) Stratégies de reproduction chez les vers de terre. Acta Oecol Oec Gen 2:117–133

    Google Scholar 

  • Lavelle P (1984) The soil system in the humid tropics. Biol Int 9:4–19

    Google Scholar 

  • Lavelle P (1988) Earthworm activities and the soil system. Biol Fertil Soils 6:237–251

    Google Scholar 

  • Lavelle P, Martin A (1992) Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics. Soil Biol Biochem 24:1491–1498

    Google Scholar 

  • Lavelle P, Melendez G, Pashanasi B, Schaefer R (1992) Nitrogen mineralization and reorganization in casts of the geophagous tropical earthworm Pontoscolex corethrurus (Glossoscolecidae). Biol Fertil Soils 14:49–53

    CAS  Google Scholar 

  • Lavelle P, Bignell D, Lepage M, Wolters V, Roger P, Ineson P, Heal OW, Ghillion S (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33:159–193

    CAS  Google Scholar 

  • Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15

    Google Scholar 

  • Lubbers IM, Brussaard L, Otten W, Groenigen JW (2011) Earthworm-induced N mineralization in fertilized grassland increases both N2O emission and crop-N uptake. Eur J Soil Sci 62:152–161

    CAS  Google Scholar 

  • Lubbers IM, van Groenigen KJ, Fonte SJ, Six J, Brussaard L, van Groenigen JW (2013) Greenhouse-gas emissions from soils increased by earthworms. Nat Clim Chang 3:187–194

    CAS  Google Scholar 

  • Mariani L, Jiménez JJ, Asakawa N, Thomas RJ, Decaëns T (2007) What happens to earthworm casts in the soil? A field study of carbon and nitrogen dynamics in Neotropical savannahs. Soil Biol Biochem 39:757–767

    CAS  Google Scholar 

  • Martin A (1991) Short-term and long-term effect of the endogeic earthworm Millsonia anomala (Omodeo) (Megascolecidae, Oligochaeta) of a tropical savanna, on soil organic matter. Biol Fertil Soils 11:234–238

    Google Scholar 

  • Medina-Sauza RM, Álvarez-Jiménez M, Delhal A, Reverchon F, Blouin M, Guerrero-Analco JA, Cerdán CR, Guevara R, Villain L, Barois I (2019) Earthworms building up soil microbiota, a review. Front Environ Sci 7:81. https://doi.org/10.3389/fenvs.2019.00081

    Article  Google Scholar 

  • Mehring AS, Cook PLM, Evrard V (2017) Pollution-tolerant invertebrates enhance greenhouse gas flux in urban wetlands. Ecol Appl 27:1852–1861

    PubMed  Google Scholar 

  • Mitra P, Kaneko N (2017) Impact of aquatic earthworms on methane emission reduction from the paddy field soil in Japan. J Agric Sci 9:36–46

    Google Scholar 

  • Moon KE, Lee SY, Lee SH, Ryu HW, Cho KS (2010) Earthworm cast as a promising filter bed material and its methanotrophic contribution to methane removal. J Hazard Mater 176:131–138

    CAS  PubMed  Google Scholar 

  • Mulvaney RL (1996) Nitrogen – inorganics forms. In: Bartels JM, Bigham JM, Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltampam PN, Tabatai MA, Johnson CT, Summer ME (eds) Methods of soil analysis, Part 3 - Chemical methods, 5th edn. Soil Science Society of American Book Series, Madison, pp 1123–1184

    Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Google Scholar 

  • Parkin TB, Berry EC (1994) Nitrogen transformations associated with earthworm casts. Soil Biol Biochem 26:1233–1238

    Google Scholar 

  • Parle JN (1963) A microbiological study of earthworm casts. J Gen Microbiol 31:13–22

    CAS  Google Scholar 

  • Piearce TG (1972) The calcium relations of selected Lumbricidae. J Anim Ecol 41:167–188

    Google Scholar 

  • Righi G (1971) Sobre a Familia Glossoscolecidae (Oligochaeta) no Brasil. Arq Zool 20:1–96

    Google Scholar 

  • Scheu S (1987) Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae). Biol Fertil Soils 5:230–234

    Google Scholar 

  • Scheu S, Schlitt N, Tiunov AV, Newington JE, Jones TH (2002) Effects of the presence and community composition of earthworms on microbial community functioning. Oecologia 133:254–260

    PubMed  Google Scholar 

  • Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31

    Google Scholar 

  • Šustr V, Šimek M (2009) Methane release from millipedes and other soil invertebrates in Central Europe. Soil Biol Biochem 41:1684–1688

    Google Scholar 

  • Svensson BH, Boström U, Klemedtson L (1986) Potential for higher rates of denitrification in earthworm casts than in the surrounding soil. Biol Fertil Soils 2:147–149

    Google Scholar 

  • Van Groenigen JW, Van Groenigen KJ, Koopmans GF, Stokkermans L, Vos HJJ, Lubbers IM (2019) How fertile are earthworm casts? A meta-analysis. Geoderma 338:525–535

    Google Scholar 

  • Vos HMJ, Koopmans GF, Beezemer L, de Goede RGM, Hiemstra T, van Groenigen JW (2019) Large variations in readily-available phosphorus in casts of eight earthworm species are linked to cast properties. Soil Biol Biochem 138:107583

    CAS  Google Scholar 

  • Zeibich L, Schmidt O, Drake HL (2018) Protein- and RNA-enhanced fermentation by gut microbiota of the earthworm Lumbricus terrestris. Appl Environ Microbiol 84:657–618

    Google Scholar 

  • Zeibich L, Schmidt O, Drake HL (2019a) Dietary polysaccharides: fermentation potentials of a primitive gut ecosystem. Environ Microbiol 21:1436–1451

    CAS  PubMed  Google Scholar 

  • Zeibich L, Schmidt O, Drake HL (2019b) Fermenters in the earthworm gut: do transients matter? FEMS Microbiol Ecol 95:221

    Google Scholar 

  • Zeibich L, Staege M, Schmidt O, Drake HL (2019c) Aminoacids and ribose: drivers of protein and RNA fermentation by ingested bacteria of a primitive gut ecosystem. Appl Environ Microbiol 85:01297–01219

    Google Scholar 

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Acknowledgements

The authors thank Anne Dotaf, Marie Bartz, Lilianne Maia, Siu Tsai, Glaciela Kaschuk, Marcela Guiotoku, Peter Depkat-Jacob, Timo Oppermann, Antonio Carlos Motta, Jeferson Dieckow and the Paropeba National Forest staff for help in various phases of this study.

Funding

Support for this study was provided by the National Council for Scientific and Technological Development (CNPq grants 310690/2017-0, 401824/2013-6 and 307486/2013-3), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Araucária Foundation, Embrapa Forestry and the Federal University of Paraná. Luis Cunha was supported by Fundação para a Ciência e Tecnologia (CEECIND/01986/2017).

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Authors and Affiliations

  1. Soil Science Departament, Federal University of Paraná, Curitiba, Paraná, Brazil

    Alessandra Santos, Marcus Vinicius Cremonesi & George Gardner Brown

  2. Embrapa Forestry, Colombo, Paraná, Brazil

    Josiléia Acordi Zanatta & George Gardner Brown

  3. Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal

    Luis Cunha

  4. School of Applied Sciences, University of South Wales, Pontypridd, Wales, CF37 4BD, UK

    Luis Cunha

  5. Department of Environmental Microbiology, University of Bayreuth, Bayreuth, Germany

    Harold L. Drake

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  1. Alessandra Santos
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  2. Marcus Vinicius Cremonesi
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Santos, A., Cremonesi, M.V., Zanatta, J.A. et al. Emission of greenhouse gases and soil changes in casts of a giant Brazilian earthworm. Biol Fertil Soils 57, 617–628 (2021). https://doi.org/10.1007/s00374-021-01552-6

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