Abstract
The area destined for agricultural production in Paraná state in Brazil is ~6 million hectares, of which 79% are under no-tillage systems (NTS) that can positively affect earthworm populations. Furthermore, earthworm abundance and richness can be valuable soil quality. This study assessed earthworm communities in long-term no-tillage sites (NTS) and nearby secondary Atlantic Forest (SF) fragments. Sampling was performed in June 2018 and May 2019 using the quantitative Tropical Soil Biology and Fertility handsorting method (ISO-TSBF), complemented by qualitative sampling in three municipalities: Faxinal, Mauá da Serra and Palmeira, in NTS and SF. Eleven earthworm species, belonging to five families (Benhamiidae, Glossoscolecidae, Megascolecidae, Ocnerodrilidae, and Rhinodrilidae) were found along with seven native species (Glossoscolex sp.22, Glossoscolex sp.23, Fimoscolex sp.21, Fimoscolex sp.24, Fimoscolex sp.42, Andiorrhinus duseni and Urobenus brasiliensis) and four exotic or cosmopolitan species (Dichogaster gracilis, Amynthas gracilis, Metaphire californica and Pontoscolex corethrurus). The cosmopolitan P. corethrurus dominated Faxinal and Mauá da Serra, while in Palmeira Fimoscolex and Glossoscolex were the most abundant. Six species belonging to Glossoscolex and Fimoscolex were new to science and must be described. Overall, 239 individuals were found. In 2018 126 individuals were found (76 in NTS and 50 in SF) and in 2019, only 112 individuals were found (45 in NTS and 67 in SF). The highest earthworm abundance was in Faxinal (123 individuals), with 76 individuals in NTS and 47 in SF. In Mauá da Serra the same pattern was observed (SF>NTS), while in Palmeira in overall, fewer individuals (38) were collected (24 in NTS and 14 in SF). The NTS at Faxinal and SF Mauá da Serra in 2019 had only/more exotic/cosmopolitan species, while at the other dates and sites >50% of the specimens sampled were native species. Overall, forests had more native species than exotics: in 2018, natives represented > 75% of all specimens, but in 2019 both Faxinal and Mauá da Serra had more exotic species (> 65%), while at Palmeira, they represented 50% of the individuals. Earthworm total biomass for forest sites was higher in Faxinal (3.2 g) and NTS in Mauá da Serra (1.7 g) in 2019. Overall, the total biomass was higher in SF sites than NTS. Using a classification available for earthworm populations in no-tillage systems, all three sites were considered to have poor quality in terms of abundance (ind m-2), while for species richness, they were considered to have moderate (Faxinal and Mauá da Serra) and good quality (Palmeira).
References
Anderson, J.M & Ingram, J.SI. (1993) Tropical soil biology and fertility: a handbook of methods, 2nd Edition. CAB International, Wallingford, 171 pp.
Baretta, D., Brown, G.G., James, S.W. & Cardoso, E.J.B.N. (2007) Earthworm populations sampled using collection methods in Atlantic forests with Araucaria angustifolia. Scientia Agricola, 64, 384–392. https://doi.org/10.1590/S0103-90162007000400009
Bartz, M.L.C., Brown, G.G., Pasini, A., Fernandes, J.D.O., Curmi, P., Dorioz, J. & Ralisch, R. (2009) Earthworm communities in organic and conventional coffee cultivation. Pesquisa Agropecuária Brasileira, 44, 928–933. https://doi.org/10.1590/S0100-204X2009000800019
Bartz H.A., Bartz M.C.L. & Bartz, J. (2010) A experiência pioneira de Herbert no Sistema de Plantio Direto na palha. In: Anais do 12° Encontro Nacional de Plantio Direto na Palha – Tecnologia que mudou a visão do produtor. Federação Brasileira de Plantio Direto na Palha, Foz do Iguaçu, 190 pp.
Bartz M.L.C. & Brown, G.G. (2011) As minhocas e o sistema plantio direto. A Granja, São Paulo, 63 – 65.
Bartz H.A., Bartz, M.L.C., Mello I. & Ralisch R. (2012) Sistema de Plantio Direto é opção de sustentabilidade. Visão Agrícola (USP / ESALQ), 10, 46–48.
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: Pavlícek, T., Cardet, P., Almeida, M.T., Pascola, C. & Cássio, F. (Eds.), Advances in earthworm taxonomy VI (Annelida: Oligochaeta). Kasparek-Verlag, Heidelberg, pp. 59–73.
Brown, G.G., Benito, N.P., Pasini, A., Sautter, K.D., Guimarães, M.F. & Torres, E. (2003) No-tillage greatly increases earthworm populations in Paraná state, Brazil. Pedobiologia, 47, 764–771. https://doi.org/10.1078/0031-4056-00256
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. & 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 (2008) Avaliação das populações de minhocas (Annelida: Oligochaeta) em sistemas agrícolas e naturais, e seu potencial como bioindicadoras ambientais. In: Saraiva, O.F. & Leite, R.M.V.B.C. (Eds.), Resultados de Pesquisa da Embrapa Soja 2005. Londrina: Embrapa Soja, 17–38.
Brown, G.G. & Domínguez, J. (2010) Uso das minhocas como bioindicadoras ambientais: princípios e práticas – o 3º Encontro Latino-Americano de Ecologia e Taxonomia de Oligoquetas (ELAETAO3). Acta Zoológica Mexicana, 26 (2), 1–18. https://doi.org/10.21829/azm.2010.262874
Brown, G.G., Pashanasi, B., Villenave, C., Patron, J.C., Senapati, B.K., Giri, S., Barois I., Lavelle, P., Blanchart, E., Blakemore, R.J., Spain, A.V. & Boyer, J. (1999) Effects of earthworms on plant production in the tropics. Earthworm management in tropical agroecosystems, 5, 87–147.
Brown, G.G., Niva, C.N., Zagatto, M.R., Ferreira, A.S., Nadolny, H., Cardoso, G.B.X., Santos, A., Martinez, G.A., Pasini, A., Bartz, M.L.C., Sautter, K.D., Thomazini, M.J., Baretta, D., Silva, E. da., Antoniolli, Z.I., Decäens, T., Lavelle, P., Sous, J.P. & Carvalho F. (2015) Biodiversidade Da Fauna Do Solo E Sua Contribuição Para Os Serviços Ambientais. In: Parron L.M., Garcia J.R., Oliveira E.B., Brown G.G. & Bardy R.P. (Org.), Serviços ambientais em sistemas agrícolas e florestais do Bioma Mata Atlântica. 1ed. Brasília: Embrapa, 1, pp. 122–154.
Buch, A.C., Brown, G.G., Niva, C.C., Sautter, K.D. & Lourençato, L.F. (2011) Life cycle of Pontoscolex corethrurus in tropical artificial soil. Pedobiologia, 54, 19–25. https://doi.org/10.1016/j.pedobi.2011.07.007
Cardoso, G.B.X., Nadolny, H., Feijoo, A. & Brown, G.G. (2014) Earthworm population in an altitudinal gradient of the coastal Atlantic Rainforest in Paraná State, southern Brazil (Oligochaeta). In: Pavlícek, T., Cardet, P., Almeida, M.T., Pascoalm, C. & Cássiom, F. (Eds.), Advances in Earthworm Taxonomy: 6th International Oligochaeta Taxonomy Meeting. 1.ed. Palmeira do Faro-Portugal: Kasparek Verlag, Germany, pp. 74–86.
Demetrio, W.C., Santos, A., Ferreira, T., Nadolny, H., Cardoso, G.B.X., Torres, J.L., Da Silva, E.S., Brown, G.G. & Bartz, M.L.C. (2018) Earthworm species in various land use systems in the Campos Gerais region of Lapa, Paraná, Brazil. Zootaxa, 4496 (1), 503–516. https://doi.org/10.11646/zootaxa.4496.1.39
Demetrio, W.C., Ribeiro, R.H., Nadolny, H., Bartz, M.L.C. & Brown, G.G. (2020) Earthworms in Brazilian no-tillage agriculture: Current status and future challenges. European Journal of Soil Science. https://doi.org/10.1111/ejss.12918
Doran, J.W. (1997) Soil quality and sustainability. In: Congresso Brasileiro De Ciência Do Solo, 26, Rio de Janeiro. Anais. Rio de Janeiro, Sociedade Brasileira de Ciência do Solo.
Feijoo, A., Brown, G.G. & James, S.W. (2017) New species of Andiorrhinus Cognetti, 1908 (Oligochaeta: Rhinodrilidae) from Venezuela and Brazil. Zootaxa, 4363 (1), 55–78. https://doi.org/10.11646/zootaxa.4363.1.2
Ferreira, T., Santos, A., Demetrio, W.C., Cardoso, G.B.X., Moraes, R., Assis, O., Niva, C.C., Smokanit, M., Knópik, J., Sautter, K.D., Brown, G.G. & Bartz, M.L.C. (2018) Earthworm species in public parks in Curitiba, Paraná, Brazil. Zootaxa, 4496 (1), 535–547. https://doi.org/10.11646/zootaxa.4496.1.41
Ferreira, T., James, S.W., Bartz, M.L.C., de Lima, A.C.R., Dudas, R. & Brown, G.G. (2023) Distribution and diversity of earthworms in diferente land use systems in Rio Grande do Sul, Brazil. Zootaxa, 5255 (1), 399–416. https://doi.org/10.11646/zootaxa.4363.1.32
Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 294–299.
Food and Agriculture Organization of the United Nations. (2014) Word reference base for soil resources. International soil classification system for naming soils and creating legends for soil maps, 203 pp.
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.
Franchini, J.C., Saraiva, O.F., Debiasi, H. & Gonçalves, S.L. (2009) Contribuição de sistemas de manejo do solo para a produção sustentável da soja. Embrapa Soja, Londrina. [Embrapa Soja. Circular técnica, 58]
Fuentes-Llanillo, R., Telles, T.S., Junior, D.S., de Melo, T.R., Friedrich, T. & Kassam, A. (2021) Expansion of no-tillage practice in conservation agriculture in Brazil. Soil and Tillage Research, 208, 104877, 1–9. https://doi.org/10.1016/j.still.2020.104877
González, G., Huang, C.Y., Zou, X. & Rodríguez, C. (2006) Earthworm invasions in the tropics. Biological Invasions, 8, 1247–1256. https://doi.org/10.1007/s10530-006-9023-7
Kochhann, R.A. & Denardin, J. (2000) E. Implantação e manejo do sistema plantio direto. Embrapa Trigo.
Köppen, W. (1931) Climatologia. México, Fundo de Cultura Econômica.
Lavelle, P. (1988) Earthworm activities and the soil system. Biology Ferility Soil, 6, 237–251. https://doi.org/10.1007/BF00260820
Lavelle, P. (1996) Diversity of soil fauna and ecosystem function. Biology International, 33, 3–16.
Lavelle, P. (1997) Faunal activities and soil processes: adaptive strategies that determine ecosystem function. Advances in Ecological Research, 27, 93–132. https://doi.org/10.1016/S0065-2504(08)60007-0
Lavelle, P. & Spain, A.V. (2001) Soil ecology. Springer Science & Business Media. https://doi.org/10.1007/978-94-017-5279-4
Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Blouin, M., Bureau, F., Margerie, P., Mora, P. & Rossi, J.P. (2006) Soil invertebrates and ecosystem services. European Journal of Soil Biology, 42, 3–15. https://doi.org/10.1016/j.ejsobi.2006.10.002
Marichal, R., Grimaldi, M., Feijoo, A., Oszwald, J., Praxedes, C., Cobo, D.H.R., Hurtadom M.del.P., da Silva Junior, M.L., Costa, L.G.da.S., Miranda, I.S, Oliveira, M.N.D., Brown, G.G., Tsélouiko, S., Martins, M.B., Decaëns., Velasquez, E. & Lavelle, P. (2014) Soil macroinvertebrate communities and ecosystem services in deforested landscapes of Amazonia. Applied Soil Ecology, 83, 177–185. https://doi.org/10.1016/j.apsoil.2014.05.006
Misirlioğlu, M., Reynolds, J.W., Stovanić, M, Trakić, T, Sekulić, J., James, S.W., Csuzdi, C., Decaëns, T., Lapied, E., Phillips, H.R.P., Cameron, E.K & Brown, G.G. (2023) Earthworms (Clitellata, Megadrili) of the world: an updated checklist of valid species and families, with notes on their distribution. Zootaxa, 5255 (1), 417–438. https://doi.org/10.11646/zootaxa.5255.1.33
Motter, P. & Almeida, H.G.de (2015) Plantio Direto: A Tecnologia Que Revolucionou A Agricultura Brasileira. Parque Itaipu, Foz do Iguaçu, 144 pp.
Muzilli, O. (2006) Manejo do solo em sistema de plantio direto. Sistema plantio direto com qualidade. Londrina: IAPAR; Foz do Iguaçu: ITAIPU Binacional.
Nadolny, H.S. (2017) Estado da arte das minhocas como bioindicadoras da qualidade dos solos brasileiros. Tese de Doutorado, Universidade Federal do Paraná.
Nunes, D.H., Pasini, A., Benito, N.P. & Brown, G.G. (2006) Earthworm diversity in four land use systems in the region of Jaguapitã, Paraná State, Brazil. Carribean Journal of Science, 43, 331–338.
Perez-Losada, M., Ricoy, M., Marshall, J.C. & Dominguez, J. (2009) Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 52, 293–302. https://doi.org/10.1016/j.ympev.2009.04.003
Plaas, E., Meyer, F.W., Banse, M., Bengtsson, J., Bergmann, H., Faber, J.H. Potthoff, M., Runge, T., Schrader, S. & Taylor, A. (2019) Towards valuation of biodiversity in agricultural soils: A case for earthworms. Ecological Economics. 159, 291–300. https://doi.org/10.1016/j.ecolecon.2019.02.003
Santos, H.G. dos, Carvalho Junior, W.D., Dart, R.D.O., Áglio, M.L.D., De Sousa, J.S., Pares, J.G., Fontana, A., Martins, A.L. Da S. & De Oliveira, A.P. (2011) O novo mapa de solos do Brasil: legenda atualizada. Embrapa Solos-Documentos (INFOTECA-E).
Santos, A., Gorte, T., Demetrio, W., Ferreira, T., Nadolny, H., Cardoso, G., Tonetti, C., Ralisch, R., Pit Nunes, A., Coqueiro, A., Leandro, H., Wandscheerm C., Bortoluzzi, J., Brown, G.G. & Bartz, M.L.C. (2018) Earthworm species in no-tillage agroecosystems and native Atlantic forests in Western Paraná, Brazil. Zootaxa, 4496 (1), 517–534. https://doi.org/10.11646/zootaxa.4496.1.40
Santos, A., Maia, L. dos S., Ferreira, T., Demetrio, W.C., Nadolny, H.S, Ribeiro, L.V, Schiedeck, G., Costa, F.A. da., Bartz, M.L.C. & Brown, G.G. (2019). Minhocas como biondicadoras da qualidade do solo em ecossistemas na Embrapa Clima Temperado. Documentos 482, Pelotas, 39 pp.
Sautter, K.D., Brown, G.G., Pasini, A., Benito, N.P., Nunes, D.H. & James, S.W. (2007) Ecologia e biodiversidade das minhocas no Estado do Paraná, Brasil. In: Brown, G.G. & Fragoso, C. (Ed.), Minhocas na América Latina: biodiversidade e ecologia. Londrina: Embrapa Soja, 2007. Embrapa Soja-Capítulo em livro científico, 14 pp.
Silva, E., Lima, O.G., Andrade, D.P. & Brown, G.G. (2019) Earthworm populations in forestry plantations (Araucaria angustifolia, Pinus elliottii) and Native Atlantic forest in Southern Brazil compared using two sampling methods. Pedobiologia, 72, 1–7. https://doi.org/10.1016/j.pedobi.2018.10.002
da Silva, K.A., Nicola, V.B., Dudas, R.T., Demetrio, W.C., Maia, L.D.S., Cunha, L., Bartz, M.C.L., Brown, G.G., Pasini, A., Kille, P., Ferreira, N. & de Oliveira, C.M.R. (2021) Pesticides in a case study on no-tillage farming systems and surrounding forest patches in Brazil. Scientific reports, 11, 1–14. https://doi.org/10.1038/s41598-021-88779-3
Sistema De Informações Hidrológicas – SIH – Instituto ÁGUASPARANÁ. Disponível em: http://www.sih-web.aguasparana.pr.gov.br/sih-web/ (Último acesso em 10 de outubro de 2019)
Sistema de Tecnologia e Monitoramento Ambiental do Paraná – SIMEPAR. Disponível em: http://www.simepar.br/prognozweb/simepar (Último acesso em 10 de outubro de 2019)
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
Righi, G. (1990) Minhocas de Mato Grosso e Rondônia. Brasília, DF: SCT/PR–CNPq 77p. [Programa do Trópico Úmido, Programa Polonoroeste, Relatório de pesquisa, 12]
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.
Van Groenigen, J.W., Lubbers, I.M., Vos, H.M., Brown, G.G., De Deyn, G.B. & Van Groenigen, K.J. (2014) Earthworms increase plant production: a meta-analysis. Scientific reports, 4, 1–7. https://doi.prg/10.1038/srep06365
Van Groenigen, J.W., Van Groenigen, K.J., Koopmans, G.F., Stokkermans, L., Vos, H. M. & Lubbers, I.M. (2019) How fertile are earthworm casts? A meta-analysis. Geoderma, 338, 525–535. https://doi.org/10.1016/j.geoderma.2018.11.001