Present knowledge on earthworm biodiversity in the State of Paraná, Brazil

European Journal of Soil Biology 42 (2006) S296–S300 http://france.elsevier.com/direct/ejsobi

Original article

Present knowledge on earthworm biodiversity in the State of Paraná, Brazil K.D. Sauttera,*, G.G. Brownb, S.W. Jamesc, A. Pasinid, D.H. Nunesd, N.P. Benitod a

Unicenp, Rua Prof. Pedro V. de Souza, 5300, 81280-330 Curitiba-PR, Brazil b Embrapa Soja, C.P. 231, 89001-970 Londrina-PR, Brazil c Natural History Museum, University of Kansas, Lawrence, KS 66045, USA d State University of Londrina, C.P. 86051-970 Londrina-PR, Brazil Available online 10 August 2006

Abstract In this paper we summarize the current knowledge on earthworm biodiversity in the State of Paraná, Brazil. Up to the present, 54 species of earthworms are known from the State, belonging to seven families and 19 genera. Native species (N = 34), dominated over exotics (N = 20). The most widespread exotics were Pontoscolex corethrurus (Glossoscolecidae) and several Amynthas spp. (Megascolecidae) and Dichogaster spp. (Acanthodrilidae), generally associated with anthropogenic sites. Of the native species, most (17 spp.) were in the genus Glossoscolex, frequently encountered in chronically wet soils. Further work is warranted, particularly more sampling efforts, but also ecological studies, given the potential biodiversity and agro-ecological importance of earthworms in Paraná. © 2006 Elsevier Masson SAS. All rights reserved. Keywords: Oligochaeta; Glossoscolecidae; Native species; Exotic species

1. Introduction The State of Paraná (PR), located in southern Brazil, has a surface area of about 200,000 km2, mostly used for agricultural purposes (28% for crops, 34% for pastures). Plantation forestry and native vegetation (medium- to well-preserved) also cover approximately 28% (14% each) of the State’s surface area. Native vegetation comprises primarily Atlantic Forest of various forms (more than 90% of total; including the Araucaria angustifolia forest), as well as cerrado and native grassland (together representing less than 10%

* Corresponding

author. Fax: +55 41 3362 8917. E-mail address: [email protected] (K.D. Sautter).

of total) [5]. Both the Atlantic Forest and the Cerrado biomes are considered plant and animal biodiversity hot-spots [13]. Up until recently, very few earthworm collections had been made in PR, and prior to the year 2000 only 10 earthworm species were known from the State: the exotics Amynthas corticis (Kinberg, 1867), Amynthas gracilis (Kinberg, 1867), Amynthas morrisi (Beddard, 1892), Pheretima darnleiensis (Fletcher, 1886), Metaphire californica (Kinberg, 1867) and Metaphire schmardae (Horst, 1883) [4,6,9,10,17–19,21], as well as the native species Rhinodrilus duseni Michaelsen, 1918 [11,21], Pontoscolex corethrurus (Müller, 1857), Glossoscolex bergi (Rosa, 1900) and Glossoscolex matogrossensis Righi, 1984 [20]. Beginning in 2001, the authors began an extensive survey, to collect

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K.D. Sautter et al. / European Journal of Soil Biology 42 (2006) S296–S300

and classify the biodiversity of earthworms of PR and assess the level of knowledge on earthworm ecology in the state [3]. The present paper presents the first results of this effort, focusing on earthworm biodiversity. 2. Earthworm biodiversity in Paraná State Earthworms were collected in various environments including annual cropping systems (soybean, maize, wheat, oats) under various tillage management practices, gardens, pastures, marshes, native grasslands and forests (pine plantations, primary and secondary forests) [2,3,8], in the years 2001–2005. Citations on earthworms from PR were gathered from the literature, the entry books of the major collections of earthworms in Brazil were all reviewed, and the information compiled into a database. The mapping of the collection sites of the present authors and those from the literature (Fig. 1), revealed that earthworms had been collected from only 43 counties in the State (11% of the total). Forty-eight species of earthworms were identified from the authors’ and Museum’s collections, and the total number of species for the State increased to 54: 34 native (63%), and 20 exotic (37%) species (Table 1). Another 16 species are expected to be present (found in neighboring States or countries; [1,8,12]), and will probably be encountered with further sampling efforts: the exotics Eisenia fetida (in composting heaps) (Savigny, 1826), Bimastos parvus (Eisen, 1874) and Pontodrilus litoralis (Grubbe,

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1855), as well as the native species Andiorrhinus n. sp. 4, Glossodrilus bresslaui (Michaelsen, 1918), G. catharinensis Michaelsen, 1918, G. colonorum Michaelsen, 1918, G. corrientus Righi, 1984, G. giganteus australis Righi and Lobo, 1979, G. truncatus (Rosa, 1895), G. uruguayensis corderoi Righi, 1968, G. vizottoi Righi, 1971, G. wiengreeni (Michaelsen, 1897), Fimoscolex inurus Cognetti, 1913, F. sacii (Righi, 1971) and Opistodrilus borelli borelli Rosa, 1895. According to Fragoso et al. [7] each 100,000 km2 in the neotropics may have approximately 20 species of earthworms. However, recent counts of the number of species in the State of São Paulo [1], just North of PR, revealed 77 species in 250 thousand km2, or the equivalent of about 31 species for each 100,000 km2. But, considering that much of the State of São Paulo has not yet been sampled for earthworms, and that recent collections revealed several new species [1], the actual total for the state may be even higher, resulting in a larger number of species per unit area. Therefore, extrapolation of these diversity/area relationships for the State of PR, results in estimates from 40 (conservative) to 62 species (upper end). Nevertheless, considering: ● that only a relatively small collection effort has been made so far (covering 11% of the counties of PR); ● that several native habitats and diverse ecosystems in various regions of PR still have to be sampled;

Fig. 1. Counties in the state of Paraná where earthworms have been collected (shaded).

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Table 1 Earthworm species found in the State of Paraná, Brazil Number

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

16 17 18 19 20 21 22 23 24 25 26 27 28

29 30 31 32 33 34 35 36 37 38 39 40 41 42 43

Family Genera/species Megascolecidae Amynthas aeruginosus Kinberg, 1867 Amynthas corticis (Kinberg, 1867) Amynthas gracilis (Kinberg, 1867) Amynthas morrisi (Beddard, 1892) Amynthas sp. (various spp. not identified) Metaphire californica (Kinberg, 1867) Metaphire schmardae (Horst, 1883) Pheretima darnleiensis (Fletcher, 1886) Lumbricidae Eisenia andrei Bouché, 1972 Lumbricidae sp. (not identified) Acanthodrilidae Dichogaster affinis (Michaelsen, 1890) Dichogaster annae (?) (Horst, 1893) Dichogaster bolaui (Michaelsen, 1891) Dichogaster gracilis (Michaelsen, 1892) Dichogaster modigliani (?) (Rosa, 1896) Dichogaster saliens (Beddard, 1892) Dichogaster sp. (various spp. not identified) Eudrilidae Eudrilus eugeniae (Kinberg, 1867) Ocnerodrilidae Belladrilus n. sp. 1 Belladrilus sp. (not identified) Eukerria eiseniana (Rosa, 1895) Eukerria emete Righi and Guerra, 1985 Eukerria saltensis (Beddard, 1895) Haplodrilus michaelseni (Cognetti, 1900) Haplodrilus n. sp. 1 Kerriona n. sp. 1 Kerriona n. sp. 2 Kerriona sp. (not identified) Ocnerodrilus occidentalis Eisen, 1878 Ocnerodrilidae sp. 1 Ocnerodrilidae sp. 2 Ocnerodrilidae sp. (various spp. not identified) Almidae Drilocrius n. sp. 1 Almidae sp. Glossoscolecidae Andiorrhinus n. sp. 2 Andiorrhinus n. sp. 3 Andiorrhinus sp. (various spp. not identified) Fimoscolex n. sp. 2 Fimoscolex n. sp. 3 Fimoscolex sp. (two spp. not identified) Glossoscolex bergi (Rosa, 1900) Glossoscolex matogrossensis Righi, 1984 Glossoscolex n. sp. 3 Glossoscolex n. sp. 4 Glossoscolex n. sp. 5 Glossoscolex n. sp. 6 Glossoscolex n. sp. 7 Glossoscolex n. sp. 8 Glossoscolex n. sp. 10

No counties

Native/ Exotic

Referencesa

1 15 15 2 7 2 1 1

Exotic Exotic Exotic Exotic Exotics Exotic Exotic Exotic

MZUSP [3,4,6,8,10,15,17–19] [3,4,6,8–10,15,17–19,21] [4,15] J&B [4,15] [4] [4]

3 1

Exotic Exotic

[3,8], J&B [15]

2 1 4 2 1 2 8

Exotic Exotic Exotic Exotic Exotic Exotic ?

[8,14] J&B [8,14,15] [8] [8] [8,14] J&B

2

Exotic

[8]

1 1 2 1 1 1 1 1 1 1 1 1 1 4

Native? Native? Exotic? Native? Exotic? Native? Native? Native Native Native Exotic Native? Native? ?

[14] J&B [8,14] [8] [14] [8] [8] [8] [8] [8] [8,14] [8] [8,14] J&B

1 1

Native? Native?

[8] [8]

2 3 5 1 1 2 1 1 1 1 1 1 1 1 1

Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native

[8] [8] [8], J&B [8,14] [8] [8], J&B [20] [20] [8] [8] [8] [8] [8] [8] [8] (continued)

K.D. Sautter et al. / European Journal of Soil Biology 42 (2006) S296–S300

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Table 1 (continued) Number 44 45 46 47 48 49 50 51 52 53 54

No counties 2 2 1 1 1 3 1 1 4 20 2 7 3

Family Genera/species Glossoscolex n. sp. 12 Glossoscolex n. sp. 14 Glossoscolex n. sp. 16 Glossoscolex n. sp. 17 Glossoscolex n. sp. 18 Glossoscolex n. sp. 21 Glossoscolex n. sp. 22 Glossoscolex n. sp. 23 Glossoscolex sp. (various spp. not identified) Pontoscolex corethrurus (Müller, 1857) Rhinodrilus duseni Michaelsen, 1918 Urobenus brasiliensis Benham, 1887 Urobenus sp. (not identified)

Native/ Exotic Native Native Native Native Native Native Native Native Native Exotic Native Native Native

Referencesa [8] [8] [8] [8] [8] [8] [8] [8] [8,14] [3,8,14,20] [11,21] [8] [8]

a MZUSP: Museum of Zoology of the University of São Paulo collection, or Righi’s collection, now deposited together with that of the Museum; J&B: S.W. James and G.G. Brown, personal observation.

● the level of endemicity of native species found in the neighboring State of São Paulo (77%, see Ref. [1, 16]) and overall in Brazil (80%, see Ref. [8]); ● that 54 species have already been found—it is likely that even the higher estimate of the species number (62 spp.) for the state is an underestimate of the earthworm biodiversity in PR. Of the native species found in PR, the most widespread was Urobenus brasiliensis Benham, 1887, an epigeic earthworm commonly found in the litter of primary and secondary forest fragments. Of the peregrine or exotic species, P. corethrurus, Amynthas spp. (particularly A. gracilis and A. corticis) and Dichogaster spp. were the most widespread. These species were generally found in disturbed habitats, especially close to human habitations, such as urban and rural gardens and cropping systems [2,3,8]. Therefore, it is highly likely that the distribution of these species in PR is much wider than presently observed. Many of the native species found in the authors’ surveys were from chronically wet soils, belonging to the Almidae (genus Drilocrius), Ocnerodrilidae (genus Haplodrilus, Eukerria, Kerriona) and Glossoscolecidae (genus Glossoscolex) families. While the Almidae were mainly found in marshes, the Ocnerodrilidae may be found in wet grasslands, next to streams and in bromeliads, and the Glossoscolex spp. can be found in both native habitats as well as deforested or otherwise heavily altered land. A typical example is a saturated marsh soil within a grazed pasture. These specially-adapted earthworms may have important influences on gas and water movement within soil profiles that are ordinarily anaerobic at more than a few centimeters depth. This

should be an exciting area for future ecological and biological research with earthworms in PR and Brazil in general. Given the large number of species found in PR so far, even with a reduced sampling effort, much further work is warranted, particularly taxonomic, but also ecological, to enhance the knowledge on biodiversity and ecological importance of earthworms in the State of PR. Acknowledgements The authors thank IAP and IBAMA for permits to collect in state parks, P. Trigo for help on the earthworm database, CNPq for fellowships to G. Brown, Prodetab, CNPq and the Fullbright Commission for funding S. James’ trips and the Museum of Zoology of the University of São Paulo staff for access to the collection and Righi’s bibliography. References [1] [2]

[3]

G.G. Brown, S.W. James, Earthworm biodiversity in São Paulo state, Brazil, Eur. J. Soil Biol. (2006) (this volume). G.G. Brown, N.P. Benito, A. Pasini, K.D. Sautter, M.F. Guimarães, E. Torres, No-tillage greatly increases earthworm populations in Paraná State, Brazil, Pedobiologia 47 (2003) 764– 771. G.G. Brown, S.W. James, K.D. Sautter, A. Pasini, N.P. Benito, D.H. Nunes, V. Korasaki, E.F. Santos, C.Y. Matsumura, P.T. Martins, A. Pavão, S.H. Silva, G. Garbelini, E. Torres, Avaliação das populações de minhocas como bioindicadores ambientais no Norte e Leste do Estado do Paraná, in: O.F. Saraiva (Ed.), Resultados de pesquisa da Embrapa Soja 2003. Manejo de solos, plantas daninhas e agricultura de precisão, Embrapa Soja, Londrina, Série Documentos, no. 253, 2004, pp. 33–46.

S300 [4] [5] [6]

[7]

[8]

[9]

[10]

[11] [12]

[13]

K.D. Sautter et al. / European Journal of Soil Biology 42 (2006) S296–S300 Y.-C. Chang, Minireview: natural history of Amynthas hawayanus (Rosa, 1891), Acta Biol. Paran. Curitiba 26 (1997) 39–50. A.A. Cigloni, P.R. Castella, C.B. Jaster, Atlas de vegetação do Estado do Paraná, SEMA, Curitiba, 2002. J.A. Dionísio, B.C.B. Tanck, A. Santos, V.I. Silveira, H.R. Santos, Avaliação da população de Oligochaeta terrestres em áreas degradadas, Rev. Set. Ciênc. Agrár. (Curitiba) 13 (1995) 35–40. C. Fragoso, Las lombrices de tierra de México (Oligochaeta; Annelida): Diversidad, ecología y manejo, Acta Zool. Mex. (n.s.) 1 (2001) 131–171 (no especial). S.W. James, G.G. Brown, Earthworm ecology and diversity in Brazil, in: F.M.S. Moreira, J.O. Siqueira, L. Brussaard (Eds.), Soil biodiversity in Amazonian and other Brazilian ecosystems, CABI, Wallingford, 2006, pp. 56–116. M. Kobiyama, C. Barcik, H.R. Santos, Influência da minhoca (Amynthas hawayanus) sobre a produção de matéria seca de bracatinga (Mimosa scabrella Benth), Rev. Set. Ciênc. Agrár. (Curitiba) 13 (1995) 199–203. R.T. Peixoto, A.I. Marochi, 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 (1996) 23–25. J.W. Michaelsen, Die Lumbriciden, Zool. Jahrb. 41 (1918) 1– 398. C.C. Mischis, Las lombrices de tierra (Annelida, Oligochaeta) de la República Argentina, Natura Neotropicalis 31 (2000) 17– 27. R.A. Mittermeier, N. Myers, P. Robles Gil, C.G. Mittermeier, Hotspots, CEMEX, Mexico City, 1999.

[14] D.H. Nunes, A. Pasini, N.P. Benito, G.G. Brown, Earthworm diversity in four land use systems in the region of Jaguapitä, Paraná state, Brazil, Carib. J. Sci. 42 (2006) (in press). [15] R.R. Ressetti, Determinação da dose de alil isotiocianato em substituição à solução de formol na extração de Oligochaeta edáficos, MSc. Thesis, Universidade Federal de Curitiba, 2004. [16] G. Righi, Oligochaeta, in: C.R. Brandão, E.M. Cancello (Eds.), Biodiversidade do Estado de São Paulo, Brasil: Síntese do conhecimento ao final do século XX. 5. Invertebrados Terrestres, FAPESP, São Paulo, 1999, pp. 13–21. [17] K.D. Sautter, B.C.B. Tanck, J.A. Dionísio, H.R. Santos, Estudo da população de Oribatei (Acari: Cryptostignata), Collembola (Insecta) e Oligochaeta, em diferentes ambientes de um solo degradado pela mineração de xisto a céu aberto, Rev. Setor Ciênc. Agrár. (Curitiba) 13 (1995) 171–174. [18] B.C.B. Tanck, H.R. Santos, J.A. Dionísio, Influência de diferentes sistemas de uso e manejo do solo sobre a flutuação populacional do oligoqueta edáfico Amynthas spp., Rev. Bras. Ciê. Solo 24 (2000) 409–415. [19] M. Voss, Populações de minhocas em diferentes sistemas de plantio, Plantio Direto 4 (1986) 6–7. [20] A. Zicsi, C. Csuzdi, Neue und bekannte Glossoscoleciden-Arten aus Südamerika. 2. Oligochaeta: Glossoscolecidae, Acta Zool. Hung. 33 (1987) 269–275. [21] A. Zicsi, C. Csuzdi, Neue und bekannte regenwürmer aus verschiedenen Teilen Südamerikas. Regenwürmer aus Südamerika 26, Senckenb. Biol. 78 (1999) 123–134.