Abstract
In this study, we sampled grazed natural grassland and agropastoral systems in two regions (Alegrete and Aceguá) in the highly diverse Brazilian Pampa region which is undergoing significant change in land use cover. By hand sorting the soil, a total of five species were found, belonging to the families Glossoscolecidae (Glossoscolex sp.50 and Glossoscolex sp.51), Ocnerodrilidae (Kerriona sp.6 and Eukerria sp.3), and Lumbricidae (Aporrectodea trapezoides). The former four were identified as native—new to science—and the latter as exotic. Differences were observed in both earthworm species richness and abundance between regions and land-use systems, likely due to environmental conditions and agricultural practices, respectively. Agropastoral systems had higher abundance and species richness than natural grasslands, though these differences varied by location. This suggests that conversion from natural grassland to agropastoral systems can maintain native earthworms and, possibly, enhance ecosystem services. However, an exotic species was found in high abundance at one agropastoral site. These results highlight the need for additional biodiversity studies on earthworms in the Brazilian Pampa and for research on the impacts of land use changes in this region.
References
Almeida, H.S. (2016) Diversidade de ácaros edáficos e minhocas em área de integração lavoura pecuária no centro oeste do Rio Grande do Sul. Mestrado em Agrobiologia, Universidade Federal de Santa Maria (UFSM, RS)
Alvares, C.A., Stape, J.L., Sentelhas, P.C., De Moraes Gonçalves, J.L. & Sparovek, G. (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22, 711–728. https://doi.org/10.1127/0941-2948/2013/0507
Anderson, J.M. & Ingram, J.S.I. (1993) Tropical soil biology and fertility: A handbook of methods 2nd Edition. CAB International, Wallingford, 171 pp.
Andrade, B.O., Marchesi, E., Burkart, S., Setubal, R., Lezama, F., Perelman, S., Schneider, A.A., Trevisan, R., Overbeck, G.E. & Boldrini, I.O. (2018) Vascular plant species richness and distribution in the Río de la Plata grasslands. Botanical Journal of the Linnean Society, 188 (3), 250–256. https://doi/.org/10.1093/botlinnean/boy063
Azevedo, P.T.M. (2010) Minhocas, fungos micorrízicos arbusculares e bactérias diazotróficas em mudas de Araucaria angustifolia. Dissertação Mestrado em Solos e Nutrição de Plantas, Universidade de São Paulo Escola Superior de Agricultura “Luiz de Queiroz”, Piracicaba.
Baker, G., Brown, G.G., Butt, K., Curry, J.P. & Scullion, J. (2006) Introduced earthworms in agricultural and reclaimed land: their ecology and influences on soil properties, plant production and other soil biota. Biological Invasions, 8, 1301–1316. https://doi.org/10.1007/s10530-006-9024-6
Barbosa, J.Z., Demetrio, W.C., Silva, C.M. & Dionísio, J.A. (2017) Earthworms (Amynthas spp.) increase common bean growth, microbial biomass, and soil respiration. Semina: Ciências Agrárias, Londrina, 38, 2887–2898. https://doi.org/10.5433/1679-0359.2017v38n5p2887
Bardgett, R. & van der Putten, W. (2014) Belowground biodiversity and ecosystem functioning. Nature, 515, 505–511. https://doi.org/10.1038/nature13855
Bartz, M.L.C, James, S.W., Steffen, G.P.K., Antoniolli, Z., Steffen, R.B. & Brown, G.G. (2018) New species-group taxa of Glossoscolex (Clitellata: Glossoscolecidae) from Rio Grande do Sul, Brazil. Zootaxa, 4496 (1), 548–561. https://doi.org/10.11646/zootaxa.4496.1.42
Beddard, F.E. (1892) On some aquatic oligochaetous worms. Proceedings of the Zoological Society of London, 25, 349–361. https://doi.org/10.1111/j.1469-7998.1892.tb06834.x
Blakemore, R.J. (2002) Cosmopolitan earthworms-an eco-taxonomic guide to the peregrine species of the world. VermEcology, Kippax, 426 pp.
Blouin, M., Hodson, M.E., Delgado, E.A., Baker, G., Brussaard, L., Butt, K.R., Dai, J., Dendooven, L., Peres, G., Tondoh, J.E., Cluzeau, D. & Brun, J. (2013) A review of earthworm impact on soil function and ecosystem services. European Journal of Soil Science, 64, 161–182. https://doi.org/10.1111/ejss.12025
Bottinelli, N., Hedde, M., Jouquet, P., Capowiez, Y. (2020) An explicit definition of earthworm ecological categories– Marcel Bouché’s triangle revisited. Geoderma, 372, 114361. https://doi.org/10.1016/j.geoderma.2020.114361
Braga, L.P.P., Yoshiura, C., Borges, C.D., Horn, M.A., Brown, G.G., Drake, H.L. & Tsai, S.M. (2016) Disentangling the influence of earthworms in sugarcane rhizosphere. Scientific Reports, 6, 38923. https://doi.org/10.1038/srep38923
Brown, G.G., James, S.W., Pasini, A., Nunes, D.H., Benito, N.P., Martins, P.T. & Sautter, K.D. (2006) Exotic, peregrine and invasive earthworms in Brazil: diversity, distribution and effects on soils and plants. Caribbean Journal of Science, 42, 339–358.
Brown, G.G. & Fragoso, C. (2007) Minhocas na América Latina: Biodiversidade e Ecologia. Embrapa Soja, Londrina. 545p.
Brown, G.G. & James, S.W. (2007) Ecologia, biodiversidade e biogeografia das minhocas no Brasil. In: Brown, G.G. & Fragoso, C. (Eds.), Minhocas na América Latina: Biodiversidade e Ecologia. Embrapa Soja, Londrina, pp. 297–381.
Brown, G.G., Callaham, M.A., Niva, C.C., Feijoo, A., Sautter, K.D., James, S.W., Fragoso, C., Pasini, A. & Schmelz, R.M. (2013) Terrestrial oligochaete research in Latin America: The importance of the Latin American Meetings on Oligochaete Ecology and Taxonomy. Applied Soil Ecology, 69, 2–12. https://doi.org/10.1016/j.apsoil.2012.12.006
Brown, G.G., Silva, E., Thomazini, M.J., Niva, C.C., Decaens, T., Cunha, L.F.N., Nadolny, H., Demtrio, W.C., Santos, A. Ferreira, T., Maia, L.S., Conrado, A.C., Segalla, R.F., Ferreira, A.C., Pasini, A., Bartz, M.L.C., Sautter, K.D., James, S.W., Baretta, D., Antoniolli, Z.I., Briones, M.J.I., Sousa, J.P., Rombke, J. & Lavelle, P. (2018) The role of soil fauna in soil health and delivery of ecosystem services. In: Reicosky, D. (Ed.), Managing soil health for sustainable agriculture, v. 1: Fundamentals. Burleigh Dodds Science Publishing, Oxford, pp. 197–241. https://doi.org/10.19103/AS.2017.0033.11
Brown, G.G., James, S.W., Csuzdi, C., Lapied, E., Decaëns, T., Reynolds, J.W., Misirlioðlu, M., Stovanic, M., Trakić, T., Sekulić, J., Phillips, H. & Cameron, E. (2023) A checklist of megadrile earthworm (Annelida: Clitellata) species and subspecies of the world. Zenodo. (Accessed 10 Jan. 2023) https://doi.org/10.5281/zenodo.7301848
Cardoso, G.B.X., Nadolny, H., Feijoo, A. & Brown, G.G. (2014) Earthworm populations in an altitudinal gradient of the coastal Atlantic Rainforest in Paraná State, southern Brazil (Oligochaeta). In: Pavlícek, T., Cardet, P., Almeida, M.T., Pascoal, C & Cássio, F. (Ed.), Advances in Earthworm Taxonomy VI (Annelida: Oligochaeta). Heidelberg: Kasparek Verlag, pp.74–86. Proceedings of the 6th International Oligochaeta Taxonomy Meeting (6th IOTM), Palmeira de Faro, April 22–25, 2013.
Chauvel, A., Grimaldi, M., Barros, E., Blanchart, E., Sarrazin, M. & Lavelle, P. (1999) Pasture degradation by an Amazonian earthworm. Nature, 389, 32–33. https://doi.org/10.1038/17946
Christoffersen, M.L. (2007) Biodiversity and distribution of the Glossoscolex genus-group (Annelida, Clitellata, Lumbricina, Glossoscolecidae) in South America. Neotropical Biology and Conservation, 2 (3), 155–160. https://doi.org/10.13102/neod.21.1
Curry, J.P. (2004) Factors affecting the abundance of earthworms in soils. In: Edwards, C.A. (Ed.), Earthworm Ecology, 2nd Ed. CRC Press, Boca Raton, pp. 91–113. https://doi.org/10.1201/9781420039719.pt3
Dala-Corte, R.B., Giam, X., Olden, J.D., Becker, F.G., Guimarães, T.F. & Melo, A.S. (2016) Revealing the pathways by which agricultural land-use affects stream fish communities in Southern Brazilian Grasslands. Freshwater Biology, 61 (11), 1921–1934. https://doi.org/10.1111/fwb.12825
Decaëns, T. & Jiménez, J.J. (2002) Earthworm communities under an agricultural intensification gradient in Colombia. Plant and Soil, 240, 133–143. https://doi.org/10.1023/A:1015844610604
Demetrio, W.C., Dionísio, J.A. & Maceda, A. (2017) Earthworms and root-knot nematodes: effect on soil biological activity and tomato growth. Semina: Ciências Agrárias, Londrina, 38, 244–2462. https://doi.org/10.5433/1679-0359.2017v38n4SUPLp2449
Depkat-Jakob, P.S., Brown, G.G., Tsai, S.M., Horn, M.A. & Drake, H.L. (2012a) Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microbiology, Ecology, 83, 375–391. https://doi.org/10.1111/j.1574-6941.2012.01476.x
Depkat-Jakob, P.S., Hunger, S., Schulz, K., Brown, G.G., Tsai, S.M. & Drake, H.L. (2012b) Emission of methane by Eudrilus eugeniae and other earthworms from Brazil. Applied and Environmental Microbiology, 7949, 1–6. https://doi.org/10.1128/AEM.07949-11
De Santo, F.B.; Niemeyer, J.K. & Bartz, M.L.C. (in press in this special issue) How earthworm behaves in Native Grassland Pasture converted to Integrated Crop-Livestock system? – a study case in Vale Verde, Rio Grande do Sul, Brazil.
Drilobase (2022) Available from: http://taxo.drilobase.org (accessed 24 May 2022)
FAO [Food and Agriculture Organization of the United Nations] (2007) Informes sobre Recursos Mundiales de Suelos 103. Base Referencial Mundial del Recurso Suelo. Available from: http://www.fao.org/3/a-a0510s.pdf (accessed 11 Nov 2021)
Falco, L. & Momo, F. (2010) Seleccion de habitat: efecto de la cobertura y tipo de suelo en lombrices de tierra. Acta Zoológica Mexicana, 26, 179–187. https://doi.org/10.21829/azm.2010.262886
Feijoo, A. & Brown, G.G. (2023) Three new Glossoscolex (Annelida: Crassiclitellata: Glossoscolecidae) in the truncatus group from the Brazilian Atlantic Forest. Zootaxa, 5255 (1), 220–234. https://doi.org/10.11646/zootaxa.5255.1.21
Ferreira, P.M. A., Andrade, B.O., Podgaiski, L.R., Dias, A.C., Pillar, V.D. & Overbeck, G.E. (2020) Long-term ecological research in southern Brazil grasslands: Effects of grazing exclusion and deferred grazing on plant and arthropod communities. PLoS ONE, 15 (1), e0227706. https://doi.org/10.1371/journal.pone.0227706
Ferreira,T., James, S.W., Bartz, M.L.C., Lima, A.C.R., Dudas, R. & Brown, G.G. (2023) Distribution and diversity of earthworms in different land use systems in Rio Grande do Sul, Brazil. Zootaxa, 5255 (1), 399–416. https://doi.org/10.11646/zootaxa.5255.1.32
Fragoso, C., Brown, G.G., Patron, J.C., Blanchart, E., Lavelle, P., Pashanasi, B., Senapati, B. & Kumar, T. (1997) Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: the role of earthworms. Applied Soil Ecology, 6, 17–35. https://doi.org/10.1016/S0929-1393(96)00154-0
Fragoso, C. & Rojas, P. (2009) A new ocnerodrilid earthworm genus from Southeastern Mexico (Annelida: Oligochaeta), with a key for the genera of Ocnerodrilidae. Megadrilogica, 13 (9) 141–152.
Gates, G.E (1962) Contributions to a revision of the earthworm family Ocnerodrilidae. IV-V. Revue de Zoologie et de Botanique Africaines, 66, 344–358.
IBGE (2021) Biomas e Sistema Costeiro-Marinho do Brasil. Available from: https://www.ibge.gov.br/apps/biomas/ (accessed 13 August 2021)
James, S.W., Bartz, M.L.C. & Brown, G.G. (2023) New Ocnerodrilidae genera, species and records from Brazil. Zootaxa, 5255 (1), 235–269. https://doi.org/10.11646/zootaxa.5255.1.22
Jamieson, B.G.M. (1967) New records of Ocnerodrilidae and Lumbricidae (Oligochaeta) from South African rivers. Zoologica Africana, 3, 59–86. https://doi.org/10.1080/00445096.1965.11447352
Kobiyama, M., Barick, C. & Santos, H.R. (1995) Influência da minhoca louca (Amynthas spp. Rosa, 1891) sobre o movimento da água no solo, relacionado ao crescimento da bracatinga (Mimosa scabrella Benth.) Dissertação (Doutorado) - Universidade Federal do Paraná, Curitiba.
Kusdra, J.F. (1998) Influência do Oligochaeta edáfico Amynthas spp. e do Rhizobium tropici no feijeiro (Phaseolus vulgaris L.). Tese (Mestrado) Universidade Federal do Paraná, Curitiba.
Lavelle, P., Blouin, M., Boyer, J., Cadet, P., Laffray, D., Pham-Thi, A.-T., Reversat, G., Settle, W. & Zuily, Y. (2004) Plant parasite control and soil fauna diversity, Comptes Rendues de l’Académie des Sciences de Paris, Serie Biologie, 327, 629–638. https://doi.org/10.1016/j.crvi.2004.05.004
Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P., Ineson, P., Heal, O.W. & Ghillion, S. (1997) Soil function in a changing world: The role of invertebrate ecosystem engineers. European Journal of Soil Biology, 33, 159–193.
Lima, A.C.R. de & Rodríguez, C. (2007) Earthworm diversity from Rio Grande do Sul, Brazil, with a new native criodrilid genus and species (Oligochaeta: Criodrilidae). Megadrilogica, 11, 9–20.
Ljungström, P.O., Emiliani, F., Righi, G. (1975) Notas sobre los oligoquetos (lombrices de tierra) argentinos. Revista de la Asocicación de Ciencias Naturales del Litoral, 6, 1–42. https://doi.org/10.14409/natura.v1i6.3282
Maschio, W. (2012) Populações de minhocas em plantios de Eucalyptus spp. e efeitos de P. corethrurus sobre o crescimento de duas espécies de Eucalyptus spp. em casa de vegetação. Mestrado em Ciências do Solo, Universidade Federal do Paraná, Curitiba.
Michaelsen, W. (1892) Terricolen der Berliner Zoologischen Sammlung II. Archiv für Naturgeschichte, 1 (3), 209–261. https://doi.org/10.5962/bhl.part.8321
Nadolny, H., Santos, A., Demetrio, W., Ferreira, T., Maia, L.S., Conrado, A.C., Bartz, M., Garrastazu, M., da Silva, E., Lavelle, P., Baretta, D., Pasini, A., Vezzani, F., Sousa, J.P., Cunha, L., Mathieu, J., Rombke, J. & Brown, G.G. (2020) Recommendations for assessing earthworm populations in Brazilian ecosystems. Pesquisa Agropecuária Brasileira, 55, e01006. https://doi.org/10.1590/S1678-3921.pab2020.v55.01006
Oliveira de, T.E., de Freitas, D.S., Gianezini, M., Ruviaro, C.F., Zago, D., Mércio, T.Z., Dias, E.A., Lampert, V., Otávio, J. & Barcellos, J. (2017) Agricultural land use change in the Brazilian Pampa Biome: The reduction of natural grasslands. Land Use Policy, 63, 394–400. https://doi.org/10.1016/j.landusepol.2017.02.010
Overbeck, G.E., Müller, S.C., Fidelis, A., Pfadenhauer, J., Pillar, V.R.D., Blanco, C.C., Boldrini, I.I., Both, R. & Forneck, E.D. (2007) Brazil’s neglected biome: the South Brazilian Campos. Perspectives in Plant Ecology, Evolution and Systematics, 9, 101–116. https://doi.org/10.1016/j.ppees.2007.07.005
Peixoto, R.T. & Marochi, A.I. (1996) A influência da minhoca Pheretima sp. nas propriedades de um latossolo vermelho escuro álico e no desenvolvimento de culturas em sistema de plantio direto em Arapoti-PR. Revista Plantio Direto, 35, 23–35.
Pelosi, C., Pey, B., Hedde, M., Caro, G., Capowiez, Y. & Guernion, M. (2014) Reducing tillage in cultivated fields increases earthworm functional diversity. Applied Soil Ecology, 83, 79–87. https://doi.org/10.1016/j.apsoil.2013.10.005
Pelosi, C., Bertrand, M., Thenard, J. & Mougin, C. (2015) Earthworms in a 15 year agricultural trial. Applied Soil Ecology, 88, 1–8. https://doi.org/10.1016/j.apsoil.2014.12.004
Phillips, H.R.P. et al. (2019) Global distribution of earthworm density. Science, 366, 480–485. https://doi.org/10.1126/science.aax4851
Phillips, H.R.P., Bach, E.M., Bartz, M.L.C. et al. (2021) Global data on earthworm abundance, biomass, diversity and corresponding environmental properties. Scientific Data, 8 (1), 136. https://doi.org/10.1038/s41597-021-00912-z
Reeves, W.K. & Reynolds, J.W. (1999) New records of cave-dwelling earthworms (Oligochaeta: Lumbricidae, Megascolecidae and Naididae) and other annelids (Aeolosomatida, Banchiobdellida and Hirudinea) in the Southeastern United States, with notes on their ecology. Megadrilogica, 7 (10), 65–71.
Righi, G. (1971) Sobre a Familia Glossoscolecidae (Oligochaeta) no Brasil. Arquivos de Zoologia, 20 (1), 1–96. https://doi.org/10.11606/issn.2176-7793.v20i1p1-95
Righi, G. (1978) Alguns Oligochaeta Megadrili da Argentina. Fave, 1 (3), 167–178. https://doi.org/10.14409/fave.v1i3.2932
Righi, G. (1995) Colombian earthworms. In: van der Hammen, T. (Ed.), Studies on Tropical Andean Ecosystems. Vol. 4. Cramer (Borntraeger), Berlin-Stuttgart, pp. 485–607.
Rocha Silva, E. (2016) Diversidade de Oligochaetas terrestres em sistema ILP (Integração Lavoura-Pecuária). Trabalho do BSc. Zootecnia, Universidade do Estado de Santa Catarina.
Santos, A., dos Maia, L.S., Ferreira, T., Demetrio, W.C., Nadolny, H.S., Ribeiro, L.V., Schiedeck, G., da Costa, F.A., Bartz, M.L.C. & Brown, G.G. (2019) Minhocas como bioindicadoras da qualidade do solo em ecossistemas na Embrapa Clima Temperado. Embrapa Clima Temperado, Pelotas, 37 pp.
Schwert, D.P. (1990) Active and passive dispersal of lumbricid earthworms. In: Dindal, D.L. (Ed.), Soil Biology as Related to Land Use Practices. EPA, Washington, DC, pp. 182–189.
Smith, R.G., McSwiney, C.P., Grandy, A.S., Suwanwaree, P., Snider, R.M. & Robertson, G.P. (2008) Diversity and abundance of earthworms across an agricultural land-use intensity gradient. Soil and Tillage Research, 100, 83–88. https://doi.org/10.1016/j.still.2008.04.009
Souza, C.M., Shimbo, J.Z., Rosa, M.R., Parente, L.L., Alencar, A.A., Rudorff, B.F.T., Matsumoto, H.H., Ferreira, M., SouzaFilho, L.G., De Oliveira, P.W.M., Rocha, S.W., Fonseca, W.F., Marques, A.V., Diniz, C.B., Costa, C.G., Rosa, D., Rosa, D., Vélez-Martin, E.R. & Azevedo, T. (2020) Reconstructing three decades of land use and land cover changes in Brazilian biomes with Landsat archive and earth engine. Remote Sensing, 12 (17), 2735. https://doi.org/0.3390/rs12172735
Sparovek, G., Lambais, M., Silva, A.P. & Tormena, C.A. (1999) Earthworm (Pontoscolex corethrurus) and organic matter effects on the reclamation of an eroded oxisol. Pedobiologia, 43, 698–704.
Staude, I.R., Vélez-Martin, E., Andrade, B.O., Podgaiski, L.R., Boldrini, I.I., Mendonça Jr, M., Pillar, V.D. & Overbeck, G.E. (2018) Local biodiversity erosion in south Brazilian grasslands under moderate levels of landscape habitat loss. Journal of Applied Ecology, 55, 1241–1251. https://doi.org/10.1111/1365-2664.13067
Staude, I.R., Overbeck, G.E., Fonta, C.S., Bencke, G.A., Silva, T.W., Mimet, A. & Pereira, H.M. (2021) Specialist Birds Replace Generalists in Grassland Remnants as Land Use Change Intensifies. Frontiers in Ecology and Evolution, 8, 597542. https://doi.org/10.3389/fevo.2020.597542
Steffen, G.P.K., Steffen, R.B., Bartz, M.L.C, James, S.W., Jacques, R.J.S., Brown, G.G. & Antoniolli, Z.I. (2018) Earthworm diversity in Rio Grande do Sul, Brazil. Zootaxa, 4496 (1), 562–575. https://doi.org/10.11646/zootaxa.4496.1.43
Stephenson, J. (1930) The Oligochaeta XVI. Clarendon Press, Oxford, 978 pp.
Wandeler de, H., Sousa-Silva, R., Ampoorter, E., Bruelheide, H., Carnol, M., Dawud, S.M., Dănilă, G., Finer, L., Hättenschwiler, S., Hermy, M., Jaroszewicw, B., Joly, F.X., Muller, S., Pollastrini, M., Ratcliffe, S., Raulund-Raasmussen, K., Selvi, F., Valladares, F., Van Meerbeek, M., Verheyen, K., Vesterdal, L. & Muys, B. (2016) Drivers of earthworm incidence and abundance across European forests. Soil Biology and Biochemistry, 99, 167–178. https://doi.org/10.1016/j.soilbio.2016.05.003