Abstract
Integrated agricultural systems have been greatly expanding in Brazil and currently cover over 30 million hectares. Although these land use systems help soil and environmental quality, little is known of their impacts on earthworm communities. In the present study we evaluated earthworm abundance, biomass and species richness in various integrated and conventional agricultural production systems (pasture, crops), as well as native forest and Eucalyptus plantations. The research was carried out at Fazenda Canchim (Embrapa Livestock Southeast) and at the neighboring campus of the University de São Carlos (UFSCar), in São Carlos municipality in São Paulo state, Brazil. Two earthworm sampling methods, i.e., quantitative (25 x 25 x 20 cm deep monoliths) and qualitative (holes of similar size and niche sampling), were used in three integrated production systems, three conventional systems and two forest systems, totaling 232 quantitative samples and over 160 qualitative samples. Earthworms were counted and identified using available keys. Eight earthworm species of five families (Rhinodrilidae, Ocnerodrilidae, Megascolecidae, Benhamiidae and Glossoscolecidae) were found, with most of the 2,145 individuals being exotic or peregrine species, particularly Pontoscolex corethrurus (88% of total) and various Dichogaster spp. (8% of total). Two native species were encountered in low abundance (55 individuals), both of which are new to science (Fimoscolex n.sp.7 and Glossoscolex n.sp.9) and must still be formally described. The new species were found in the agricultural systems, but not in the native forest and the Eucalyptus plantation, where P. corethrurus and Megascolecids predominated. One unidentified Ocnerodrilid sp. was found only in the intensive pasture. Species richness was highest in the intensive pasture (7 spp.), followed by the agrosilvopastoral and agropastoral systems, highlighting the importance of integrated and pastoral systems in preserving earthworm richness and native species.
References
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. 2 edition. Oxford: Oxford University Press.
Assis, P.C.R., Stone, L.F., Medeiros, J.C., Madari, B.E., Oliveira, J.M. & Wruck, F.J. (2015) Atributos físicos do solo em sistemas de integração lavoura-pecuária-floresta. Revista Brasileira de Engenharia Agrícola e Ambiental, 19, 309–316. https://doi.org/10.1590/1807-1929/agriambi.v19n4p309-316
Baretta, D., Bartz, M.L.C., Fachini, I., Anselmi, R., Zortéa, T. & Maluche-Baretta, C.R.D. (2014) Soil fauna and its relation with environmental variables in soil management systems. Revista Ciência Agronômica, 45, 871–879. https://doi.org/10.1590/S1806-66902014000500002
Bartz, M.L.C., Brown, G.G., Rosa, M.G., Locatelli, M., James, S.W. & Baretta, D. (2011) Minhocas Urobenus sp.: das matas para as áreas sob plantio direto. Revista Plantio Direto, 124, 6–7.
Bartz, M.L.C., Pasini, A. & Brown, G.G. (2013) Earthworms as soil quality indicators in Brazilian no-tillage systems. Applied Soil Ecology, 69, 39–48. https://doi.org/10.1016/j.apsoil.2013.01.011
Bartz, M.L.C., Pasini, A. & Brown, G.G. (2014) Earthworm richness, abundance and biomass in different land use systems in northern Paraná, Brazil (Oligochaeta). In: T. Pavlícek, P. Cardet, M.T. Almeida, C. Pascola & F. Cássio (Eds), Advances in earthworm taxonomy VI (Annelida: Oligochaeta). Kasparek Verlag, Heidelberg, pp. 59–73.
Blakemore, R.J. (2002) Cosmopolitan Earthworms—An Eco-Taxonomic Guide to the Peregrine Species of the World. VermEcology, Kippax, 426. [CD-ROM]
Brown, G.G. & James, S.W. (2007) Ecologia, biodiversidade e biogeografia das minhocas no Brasil. In: G.G. Brown & C. Fragoso (Eds.), Minhocas na América Latina: Biodiversidade e Ecologia. Embrapa Soja, Londrina, pp. 297–381.
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 (3), 339–358.
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
Bünemann, E.K., Bongiorno, G., Bai, Z., Creamer, R.E., De Deyn, G., De Goede, R., Fleskens, L., Geissen, V., Kuyper, T.W., Mäder, P., Pulleman, M., Sukkel, W., Van Groenigen, J.W. & Brussaard, L. (2018) Soil quality – a critical review. Soil Biology and Biochemistry, 120, 105–125. https://doi.org/10.1016/j.soilbio.2018.01.030
Calderano Filho, B., Santos, H.G., Fonseca, O.O.M., Santos, R.D., Primavesi, O. & Primavesi, A.C. (1998) Os solos da Fazenda Canchim, Centro de Pesquisa de Pecuária do Sudeste, São Carlos, SP: Levantamento semi-detalhado, propriedades e potenciais. Rio de Janeiro: Embrapa CNPS/São Carlos (Embrapa-CNPS. Boletim de Pesquisa, 7; Embrapa-CPPSE. Boletim de Pesquisa, 2), 1–107.
Curry, J.P. (2004) Factors affecting the abundance of earthworms in soils. In: C.A. Edwards (Ed.), Earthworm ecology. 2nd ed. CRC Press, Boca Raton, pp. 91–113. https://doi.org/10.1201/9781420039719.pt3
Da Silva, L.Á. & Soares, J.J. (2003) Composição florística de um fragmento de floresta estacional semidecídua no município de São Carlos-SP. Revista Árvore, Viçosa-MG, 27 (5), 647–656.
Decaëns, T., Jiménez, J.J., Gioia, C., Measey, G.J. & Lavelle, P. (2006) The value of soil animals for conservation biology. European Journal of Soil Biology, 42, S23–S38. https://doi.org/10.1016/j.ejsobi.2006.07.001
Demetrio, W.C., Da Fonseca, P.M., Dudas, R., Zagatto, M.G.R., Feijoo, A. & Brown, G.G. (2023) Earthworm species in native and planted forests in Brazil. Zootaxa, 5255 (1), 304–323. https://doi.org/10.11646/zootaxa.5255.1.25
Demetrio, W., Brown, G., Pupin, B., Novo, R., Dudas, R., Baretta, D., Rombke, J., Bartz, M. & Borma, L. (2022) Are exotic earthworms threatening soil biodiversity in the Brazilian Atlantic Forest? Applied Soil Ecology, 182. https://doi.org/10.1016/j.apsoil.2022.104693
Embrapa (2016) ILPF em números. Embrapa Agrossilvopastoril, Sinop, Brazil. 12 pp.
FAO (2020) State of knowledge of soil biodiversity - Status, challenges and potentialities, Report 2020. Rome, FAO. https://doi.org/10.4060/cb1928en
Fragoso, C., Brown, G.G., Patrón, J.C., Blanchart, E., Lavelle, P., Pashanasi, B., Senapati, B.K. & 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)00149-7
González, G., Huang, C.-Y., Zou, X. & Rodríguez, C. (2006) Earthworm invasions in the tropics. Biological Invasions, 8, 247–256. https://doi.org/10.1007/s10530-006-9023-7
Lee, K.E. (1885) Earthworms. Their Ecology and Relationships with Soils and Land Use. Academic Press, London, 411.
Lee, K.E. (1987) Peregrine species of earthworms. In: A.M. Bonvicini-Pagliai & P. Omodeo (Eds.), On Earthworms. Selected Symposia and Monographs. Mucchi, Modena, Italy, pp. 315–328.
Marichal, R., Martinez, A.F., Praxedes, C., Ruiz, D., Carvajal, A.F., Oszwald, J., Del Pilar Hurtado, M., Brown, G.G., Grimaldi, M., Desjardins, T., Sarrazin, M., Decaëns, T., Velásquez, E. & Lavelle, P. (2010) Invasion of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta) in landscapes of the Amazonian deforestation. Applied Soil Ecology, 46, 443–449. https://doi.org/10.1016/j.apsoil.2010.09.001
Maschio, W., Vezzani, F.M. & Brown, G.G. (2014) Earthworm populations in Eucalyptus spp. plantations at Embrapa Forestry, Brazil (Oligochaeta). In: T. Pavlíček, P. Cardet, M.T. Almeida, C. Pascoal & F. Cássio (Eds.), Advances in Earthworm Taxonomy VI (Annelida: Oligochaeta). Kasparek Verlag, Heidelberg, pp. 114–126.
Nadolny, H., Santos, A., Demetrio, W.C., Ferreira, T., Maia, L.D.S., Conrado, A.C., Bartz, M., Garrastazu, M., Silva, E., Lavelle P., Baretta, D., Pasini, A., Vezzani, F., Sousa, J.P., Cunha, L., Mathieu, J., Römbke, J. & Brown, G.G. (2020) Recommendations for assessing earthworm populations in Brazilian ecosystems. Pesquisa agropecuária Brasileira, 55, p.01006. https://doi.org/10.1590/S1678-3921.pab2020.v55.01006
Pulleman, M., Creamer, R., Hamer, U., Helder, J., Pelosi, C., Pérès, G. & Rutgers, M. (2012) Soil biodiversity, biological indicators and soil ecosystem services – an overview of European approaches. Current Opinion in Environmental Sustainability.