Earthworm species in public parks in Curitiba, Paraná, Brazil Author Ferreira, Talita Author Santos, Alessandra Author Demetrio, Wilian C. Author Cardoso, Guilherme B. X. Author Moraes, Rafael Author Assis, Orlando Author Niva, Cintia Author Smokanit, Manoela Author Knópik, Juliane Author Sautter, Klaus D. Author Brown, George G. Author Bartz, Marie L. C. text Zootaxa 2018 2018-10-05 4496 1 535 547 journal article 29243 10.11646/zootaxa.4496.1.41 24ef32ad-6137-48b7-a616-6b303ac46b99 1175-5326 1447019 DE1A841D-1319-43C3-A350-63CE807A6822 Dichogaster sp. (juvenile) COFMBRPR0926, 1 juvenile, surface horizon ( 0–20 cm ) of a Technosol with grass lawn in Passaúna Park, Curitiba-PR (25°28'33.66"S 49°22'37.39"W), June 2014 , M.L.C. Bartz, K. Sautter and G.B.X. Cardoso, colls. A total of 12 earthworm species were identified, belonging to six families: Glossoscolex sp.1, Fimoscolex sp.1, sp.2 and sp.3 ( Glossoscolecidae ), P. corethrurus (Rhinodrilidae) , Eukerria tucumana (Ocnerodrilidae) , A. gracilis , A. corticis , M. californica (Megascolecidae) , L. rubellus and A. rosea (Lumbricidae) , as well as an unidentified juvenile Dichogaster sp. ( Acanthodrilidae ). Independently of the LUS, park and season, of the total individuals and species identified, the highest frequency was of the families Megascolecidae (40%), followed by Rhinodrilidae (24%), Ocnerodrilidade (18%) and Lumbricidae (6 %). The native family Glossoscolecidae had only 4.5 % of the individuals collected, and the African Dichogaster only 0.1 %. In the grass lawn sites, highest species richness was found in the summer season in Tingui Park, Botanic Garden and Passaúna (6 spp.) and in the winter season in the Botanic Garden (7 spp.). In the forests fragments, highest richness was found in Barigui Park on both sampling dates (4 spp.). The occurrence of exotic species was different in both LUS sampled. In the summer, in both LUS the percentage of exotic species ranged from 50 to 100%. In winter, it ranged from 73 to 100% in the grass lawns and 0 to 100% in the secondary forest fragments. There was a clear dominance of exotic species in the LUS of most of the public parks of the city of Curitiba. This dominance is likely the consequence of anthropic disturbance, soil moving and transplanting of trees and shrubs, as well as grass sod, which promotes the invasion and establishment of these species. However, added to this is the fact that these exotic species are also generally able to support higher variability in soil and environmental conditions than native species. Human colonization is also an active agent of dispersal and invasion of exotic species in several places around the world ( Hendrix 2006 ), including Brazil ( Brown et al . 2006 ). P. corethrurus was the most abundant species collected in the parks in Curitiba (162 individuals), but its presence was higher in grass lawns (25%) than in the forests (19% of total). This species, native to Northern Brazil and the Guyanas region is considered a peregrine species in others Brazilian regions, such as the South, where Curitiba is located ( Righi 1984 , Brown et al . 2006 ). It is widely distributed in Brazil due its tolerance to soil disturbance, and wide range of soil abiotic factors, such as temperature, moisture, texture and fertility ( Brown et al . 2006 ). Specimens in Curitiba area tend to be smaller than average for this species, possibly due to the colder climate ( Buch et al. 2011 ). The earthworm is endogeic and able to live in soil with low organic matter levels ( Hamoui 1991 ), and from dry to waterlogged soils (M.L.C. Bartz—personal observation). These conditions occur quite commonly in the Technosols (human built soils) in some of the Curitiba parks. The prevalence of P. corethrurus in Curitiba parks, with continental Cfb climate (annual mean temperature 17 °C), subject to frequent frosts, means that the species can still expand its distribution into other sub-tropical and temperate climates worldwide, such as tropical mountains ( Ortiz-Gamino et al. 2016 ), the USA and Europe ( Gates 1973 ). Although the species has been associated with some soil disfunctions ( Chauvel et al. 1999 ), P. corethrurus can improve soil physical and chemical properties, and plant growth ( Brown et al. 1999 ), particularly when present with other species. In the Curitiba parks, P. corethrurus was found associated particularly with several Megascolecidae species and E. tucumana . The combined presence and abundance of these species in several of the Curitiba parks, especially the grass lawns implies that they may be having (as of yet unmeasured) important impacts on soil ecosystem functioning and plant production. The Glossoscolecidae family has about 152 species in South America, and the Glossoscolex genus is distributed in Brazil , Paraguay , Argentina and Uruguay , and occurs from Minas Gerais state in Brazil to the lower Plata River Basin region in Argentina ( Fragoso & Brown 2007 ). In 2012, 9 new species of Glossoscolex were described from Northern Paraná ( Bartz et al. 2012 ), highlighting the large number of species in this genus still to be discovered and described. In fact, the single species of this genus found in the Botanic Garden is also a new species. All species in this genus with male pores on segment 17 (such as this one) are endogeic, living within the soil and ingesting mineral material. Some Glossoscolex species can be found in deforested areas and disturbed sites ( Brown & James 2007 ), and Bartz et al. (2013 , 2014 ) found many new species of Glossoscolex in agricultural fields of Paraná and Santa Catarina states. Most species of the genus Fimoscolex are endogeic and the genus has a smaller distribution range than Glossoscolex , which is known from as far south as Uruguay and Argentina ( Fimoscolex are only recorded as far south as Rio Grande do Sul ; Steffen et al. this issue). Many new species in this genus have also been recorded in S and SE Brazil ( Brown & James 2007 , Bartz et al . 2013 , 2014 ), including in disturbed sites such as agricultural fields. In fact, the three species encountered here, from the grass lawn in the Botanic Garden, in the secondary forests in Tinguí Park and in Passaúna Park are also new to science, although the last one, in Passaúna, was represented by only one individual. Interestingly, both Fimoscolex sp.1 and sp.2 were found living together at all sites. All species found were endogeic and relatively small ( 5 to 8 cm long). Little is known of the biology and ecology of these small native Glossoscolex and Fimoscolex species, and much further work is warranted to determine their long-term resistance to perturbation, and their potential impacts on soil structure and fertility. This may be particularly important for sites where they are abundant and possibly contributing more to ecosystem functions. The family Ocnerodrilidae has numerous genera and species living in South America, Africa and India , with several peregrine or exotic species, which are distributed in tropical and subtropical regions. Many of native species from Brazil , found living in waterlogged soils belong to Ocnerodrilidae family ( Brown & James 2007 ). Nonetheless, some species live in drier soils, and the species identified here, Eukerria tucumana , was found in grass lawns and forest in Barigui, and from the grass lawns in Tinguí, the Botanic Garden and Passaúna Park. It has also been found in farmlands in Southern Brazil ( Bartz et al . 2013 , 2014 , M.L.C. Bartz personal observation), but was originally known only from Tucumán , Argentina ( Mischis, 2007 ). Unfortunately, the original habitat where the worm was described from is not known, but the fact that it was now collected in disturbed sites means that it is resistant to disturbance, and an excellent candidate for further work, both ecological and biological, to determine its potential importance for soil processes. The species was found commonly co-inhabiting with other exotic/peregrine species ( P. corethrurus and several Megascolecidae ) in the Curitiba Parks. Lumbricidae and Megascolecidae are exotic families in Brazil , and the species encountered in the present study ( Amynthas corticis , A. gracilis , Metaphire californica , Lumbricus rubellus , Lumbricus terrestris and Aporrectodea rosea ) originated in Asia and Europe (Laurasia). The Lumbricidae family includes species that are usually restricted to regions with colder temperatures, and most records of this family are from sites in Southern Brazil ( Rio Grande do Sul , Santa Catarina and Paraná states), that have Cfb type climate ( Brown & James 2007 ). In the present study, L. rubellus and A. rosea are widespread species in temperate regions. L. rubellus was found only in the Barigui and Botanic Garden lawns and the Barreirinha secondary forest, and A. rosea was found only in grass lawn in Tingui and Passaúna parks. This is evidence of the European colonization prevalent in Curitiba, that probably imported soil with earthworms from their native countries. These earthworms became established in the town and were probably imported into the parks with soil of potted plants (e.g., trees), or with the planting of grass sod containing these species. This is the first record of L. rubellus for Brazil and the second for A. rosea , which was only found in Porto Alegre, Rio Grande do Sul state. The Megascolecidae family has many species widely adapted to different soil and climate regions throughout the world, and the three species encountered in the present study had already been reported for Curitiba by Chang (1997) , and have probably been around for a very long time. In fact, A. gracilis was described by Kinberg (1867) from specimens originally collected in the Rio de Janeiro Botanic garden. All three species are epi-anecic and generally more dependent on organic matter contents in soil. They usually occur in gardens, as well as no-tillage cropping systems in the colder climate regions of Southern Brazil ( Brown et al. 2006 ). In these systems they can cause important changes to soil function, as well as improvements in plant production ( Peixoto & Marochi 1996 ). Therefore, their abundance in the Curitiba Parks may be leading to important impacts in soil-based ecosystem services. In the present study, these species were more prevalent in the grass lawns than in the secondary forests. This may be evidence of a greater spread of these species through the planting of grass sod in these urban parks. A. gracilis is widely distributed in Brazil ( Brown & James 2007 ), and was found in all parks and LUS, except the Passaúna Park secondary forest. A. corticis is also widely distributed in Brazil ( Brown & James 2007 ), but this worm was only found in the Tinguí and Passaúna grass lawns and the Barigui lawn and secondary forest. M. californica was found in all the grass lawns except at Barreirinha Park, but was less prevalent in the secondary forests, being found only at the Barigui and Botanic Garden forests. Native species in the Acanthodrilidae family in Brazil include a few Dichogaster spp., but these are known only from the Amazon region ( Csuzdi 1995 ). All species encountered in S and SE Brazil are exotic ( Brown & James 2007 ), generally of very small size (mostly less than 6 cm long and thin), and classified as epigeic or epiendogeic. These species have been commonly found in pastures and no-tillage agricultural fields ( Bartz et al. 2013 , 2014 ) in Southern Brazil , and are dependent on the presence of a litter layer for survival. The individual found in the present study was juvenile and could not be identified to species level. It was encountered only in one qualitative sample from the grass lawn of Passaúna Park on one occasion (2014). Once again, this may be testament to the probable importance of grass sod transplants as exotic earthworm species inocula in the Curitiba parks, particularly in the Technosols, were soil and plants and grasses are brought in from other locations.