The earthworm fauna of regenerating forests and anthropogenic habitats in the coastal region of Paraná

A fauna de minhocas em florestas em regeneração e habitats antropogênicos na região costeira do Paraná

SOIL SCIENCE

The earthworm fauna of regenerating forests and anthropogenic habitats in the coastal region of Paraná

A fauna de minhocas em florestas em regeneração e habitats antropogênicos na região costeira do Paraná

Jörg Römbke^I Petra Schmidt^II; Hubert Höfer^II

^IECT Oekotoxikologie GmbH, Böttgerstrasse 2-14, D-65439 Flörsheim, Germany. E-mail: [e-mail]

^IIStaatliches Museum für Naturkunde, Erbprinzenstrasse 13, D-76133 Karlsruhe, Germany. E-mail: [e-mail], [e-mail]

ABSTRACT

The aim of this study was to evaluate abundance, biomass and diversity of earthworms in the southern coast region of the Mata Atlântica biodiversity hotspot. A total of 51 study sites in pastures, banana monocultures, mixed agroforestry systems, secondary forests in succession and old-growth forests near the coast of Paraná, Brazil, were evaluated. Each site was sampled once. Species richness of the earthworms was generally low and varied little between sites. At all sites except for one, the peregrine species Pontoscolex corethrurus (Glossoscolecidae) strongly dominated. Three other peregrine species, Amynthas corticis, Amynthas gracilis (Megascolecidae) and Ocnerodrilus occidentalis (Ocnerodrilidae), were frequent in moist sites. No autochthonous species were found. Abundance and biomass of earthworms varied strongly within and between sites (0-338 individuals m^-2, 0-96 g m^-2 fresh weight). Pastures had significantly lower abundance than all other sites. The forest sites had similar earthworm abundance and biomass, with a tendency to be higher in younger succession stages. The coastal plain region has been strongly altered by human activities. Reasons for the lack of any autochthonous species and the dominance of one peregrine species require further investigation.

Index terms:Pontoscolex corethrurus, Atlantic Forest, biodiversity, Oligochaeta, peregrine species, secondary forest.

RESUMO

O objetivo deste estudo foi avaliar a abundância, a biomassa e a diversidade de minhocas, na região costeira sul do "hotspot" de biodiversidade Mata Atlântica. Um total de 51 locais foram avaliados em pastagens, monoculturas de banana e sistemas agroflorestais de banana com palmito e florestas secundárias próximos à costa do Estado do Paraná. Cada local foi amostrado apenas uma vez. A riqueza de espécies de minhocas, de modo geral, foi baixa e variou pouco entre os locais. Em todos os locais, exceto um, predominou a espécie peregrina Pontoscolex corethrurus (Glossoscolecidae). Não foram encontradas espécies nativas em nenhum local. Três outras espécies peregrinas, Amynthas corticis, Amynthas gracilis (Megascolecidae) e Ocnerodrilus occidentalis (Ocnerodrilidae), foram frequentes em locais úmidos. A abundância e a biomassa das minhocas variaram muito, dentro e entre os sítios amostrais (0-338 indivíduos m^-2, 0-96 g m^-2 de massa fresca). Nas pastagens, observou-se menor abundância do que nos demais ecossistemas. As florestas apresentaram abundância e biomassa similares, sendo que estágios mais jovens da regeneração apresentaram abundância e biomassa mais alta. A planície litorânea já foi fortemente alterada por atividades antrópicas. As razões da falta de espécies nativas e da predominância de uma espécie peregrina, na região, necessitam ser mais pesquisadas.

Termos para indexação:Pontoscolex corethrurus, Mata Atlântica, biodiversidade, Oligochaeta, espécies peregrinas, floresta secundária.

Introduction

Earthworms are a dominant group of soil animals in the humid and subhumid tropics (Fragoso et al., 1999). In recent years, research on this topic increased, particularly in Brazil (González, 2006; Brown & Fragoso, 2007), resulting in major compilations of earthworm diversity (Brown & Fragoso, 2007), assessments of earthworms role in agricultural systems and in secondary and primary forests, the identification of impacts of different land uses on earthworm populations and diversity, and their role as bioindicators. Although these questions have been partly addressed in several parts of Brazil (Lavelle & Lapied, 2003), knowledge on the earthworm fauna of the second largest forest biome in Brazil, the Atlantic Forest (Mata Atlântica) - worldwide recognized as a hotspot of biodiversity - is still scarce. Therefore, earthworms were sampled as important representatives of the soil fauna with an expected high functional importance, as part of the activities of the German-Brazilian project SOLOBIOMA. This project aims to assess the ecosystem quality of secondary forests, in the coastal region of Paraná state, and especially their potential for conservation of biodiversity and provision of ecosystem services.

The objectives of this study were to: assess the diversity and structure of earthworm assemblages, in the southern Mata Atlântica; evaluate how the earthworm fauna recovers during forest regeneration from pastures; and assess which site properties determine the abundance, biomass and diversity of the earthworm fauna.

Materials and Methods

The study sites were located within an area of about 30x80 km², along the coast of Paraná state, in the municipalities Antonina, Guaraqueçaba and Paranaguá. Most sites are situated within and adjacent to the "Área de Proteção Ambiental" Guaraqueçaba (Ferretti & Britez, 2006). Climate of this coastal region is mesothermic subtropical humid, corresponding to Köppen's Cfa-type (Schröder, 2000; Strahler & Strahler, 2005). Mean annual temperature is above 18ºC, and monthly precipitation is over 60 mm. Frost rarely occurs in areas from sea level to 700 m a.s.l. (Instituto Paranaense de Desenvolvimento Econômico e Social, 2001). Annual rainfall in the region varies between 2,000 and 3,000 mm (Roderjan & Kunyoshi, 1988) and is seasonal. Lower rainfall occurs from the autumn end to winter (April to August), and higher rainfall occurs during the warmer months of Brazilian summer (September to March) (Instituto Paranaense de Desenvolvimento Econômico e Social, 2001). Soils of the region are mainly Cambisols in the submontane range, and Podzols and Gleysols in the lowland range (Food and Agriculture Organization of the United Nations, 1998). These soil types are characterized by low pH, [3.5-4.3 (CaCl2), sometimes reaching 5.0, under pastures], C/N-ratios from 15-40 and organic matter contents of 2-5% in the upper 20 cm of soil.

One group of study sites (1-15 and 19-30, in Table 1) is situated within the "Reserva Natural do Rio Cachoeira" (herein called Cachoeira forest) and includes pastures, secondary forest stages naturally regenerating from pastures, and old-growth forests (>80 years old). The latter were never completely cut down and used as pastures. Pastures and secondary forests were found on the two most frequent soil types: well drained Cambisols (1-15) on slopes, and hydromorphic Gleysols (19-30) in the plain. For every stage on each soil type, three replicate sites were studied, and analyses of variance were done for the effects of stages and soil type. The second group of study sites (31-42), also comprising regenerating secondary forests and old-growth forests on Cambisols, is situated approximately 30 km to the east, within the "Reserva Natural do Itaqui" (herein called Itaqui forest). Likewise for all stages, three replicate sites were studied, allowing statistical analysis of the effect of stage and a comparison of the two areas, Cachoeira and Itaqui, based on Cambisol sites. These 39 sites within the submontane forest region represent the natural regeneration process, covering mosaic-like distributed patches of forests, which differ in age since abandonment of use, as buffalo pastures, from 3 to >80 years and, thus, represent a gradient of decreasing anthropogenic influence. These are the core sites of a large biodiversity study within the German-Brazilian project SOLOBIOMA. All sites are owned and administrated by the Brazilian NGO "Sociedade de Pesquisa em Vida Silvagem e Educação Ambiental".

Within the Cachoeira forest area, three further sites (16-18) of three different regeneration stages on Cambisols were used for functional studies of litterfall, decomposition and nutrient cycling. The same accounts for three sites (43-45) of lowland forest on Podzols, situated in the municipality of Paranaguá, within the reserve "Floresta Estadual do Palmito" (530 ha, herein called Palmito forest). A detailed description of these sites, which represent the forest formations submontane and lowland Atlantic forest, is reported by Schmidt et al. (2008).

Six sites were located just outside the Cachoeira forest reserve, at a place called "Rio Pequeno", about 20 km north of Antonina (Table 1), and represent currently cultivated sites with agroforestry plantations (46-51). Three were banana monocultures, and three mixed systems with bananas and palmito palms (Euterpe edulis), both very frequent smallholder systems in the region. Nearly all these sites stock on gleyic, groundwater-influenced soils.

Earthworms were sampled in a total of 51 sites, situated in two regions with different forest formations - lowland and submontane forest -, different land cover types - plantations, grassland and forest regeneration stages -, on three different soil types, Cambisols, Gleysols, Podzols, covering a gradient of anthropogenic influence, from agricultural sites and pastures to regenerating and old-growth forests.

At each site, five earthworm samples were taken on one occasion (Table 1), by using a combination of hand-sorting of soil, within a quadrate of 50x50 cm, to a depth of approximately 20 cm (International Organization for Standardization, 2007), followed by formol extraction (0.5% aqueous formol). Since almost no worms were caught after formol application, only hand-sorting was performed at the six agroforestry sites. All worms were stored in 70% ethanol before being counted, weighted and determined to the species level. Abundance, biomass and species composition were used as measurement endpoints. The statistical tests (ANOVA) for effects of soil type and for differences between stages were done with Statistica 8.0 (StatSoft, 2007).

Results and Discussion

Earthworms belonging to three families (Glossoscolecidae, Megascolecidae, Ocnerodrilidae) were found. Species richness was generally low (1-4 species per site) and did not differ considerably between the sites or vegetation types. Altogether five species, all of them peregrine, were regularly found. In anthropogenic habitats in Brazil, like pastures, crop and agroforestry systems, as well as secondary forests, 2 to 4 species are usually found, whereas at primary forest sites, species richness is generally higher (on average 5, range: 2-10) (Brown & James, 2007). In all sites, except for banana/palmito plantations, Pontoscolex corethrurus (Müller, 1857) strongly dominated the samples, usually representing 90-99% of abundance (Figure 1). Very moist sites (e.g. close to small creeks) and also some agroforestry sites showed higher proportions of Amynthas spp. - A. corticis (Kinberg, 1867) and A. gracilis (Kinberg, 1867). In the agroforestry sites, Ocnerodrilus occidentalis (Eisen, 1878) or Dichogaster spp. were frequently found. At two banana/palmito sites, Amynthas spp. as well as O. occidentalis reached about 25% of abundance, respectively. One of these sites was located very close to a human settlement, while the other was adjacent to a small river.

Abundance and biomass of earthworms per plot varied between 0 and 338 individuals m^-2 and 0 and 96 g fresh weight m^-2 (Table 1). Within the secondary forests, there was high variance of abundances (Figure 2). Biomass was almost always very similar to abundance, due to the fact that one species (P. corethrurus) dominated all samples and was almost always present with all development stages, from juvenile to adult. The only sites strongly differing from all other sites were the lowland forest sites in Palmito forest (43-45), with very low abundance (and biomass). In one site, no earthworm was found at all. This is readily explained by the very sandy (90 to 98% sand) and nutrient depleted soils in this site (Boeger et al., 2005). In these sandy soils, the upper horizons dry out quickly due to drainage and, in the lower horizons, the high ground water level creates anoxic situations, both of which are fatal for worms. The lack of available nutrients (organic matter), due to the relatively low input (litter fall) from the sparse plant cover, and very irregular (clumped) distribution of litter in the younger stages (Pinto & Marques, 2003) might negatively influence earthworm abundance (Lee, 1985).

In the three corresponding Cachoeira forest sites (16-18), on Cambisols, which were sampled at the same time, earthworm numbers (70-250 individuals m^-2) were distinctly higher and in the range of the other sites in Cachoeira (see Table 1). Especially biomass was surprisingly high (20-70 g m^-2 fresh weight) (Schmidt et al., 2008).

Based on the replicated stages, several designs were analyzed using ANOVA. Comparison of pastures and secondary forests on Gleysols and Cambisols (sites 1-12, 19-30), in the Cachoeira reserve showed a significant effect of regeneration stage, caused by the lower abundance and biomass in the pastures and no effect of the soil type (Figure 3). Comparison of secondary forests and old-growth forests on Cambisols, in Cachoeira, with the same stages in Itaqui, showed a significant effect of stage, with decreasing abundances and biomass from the herbaceous to the old-growth forests (Figure 4). Differences between the two areas were significant for abundance, but not for biomass. In the old-growth forests of Itaqui, abundance and biomass were slightly higher than in the medium old forests. When looking at the whole succession, from pastures to older forests, on Cambisols in the Cachoeira reserve, the increase of earthworm biomass from pastures to the two younger succession stages was significant. In addition, earthworm abundance and biomass were significantly lower in the two older stages (medium, old-growth), in comparison with the two younger succession stages (Figure 5).

The plantations showed high abundances and very high biomass, compared with the forests. They were significantly higher in the mixed banana/palmito plantations than in the banana monocultures. Actually, the highest abundance of all sites (338 individuals m^-2) was found in a banana/palmito plantation (no 50). This site was the most closely located to a house and, also, the only one which was not dominated by P. corethrurus, but by the small peregrine species O. occidentalis.

The interpretation of these findings is facilitated by the fact that the earthworm assemblage was so strongly dominated by P. corethrurus, which is the best studied tropical earthworm species. Its high tolerance for a wide range of soil properties is confirmed by the absence of differences in abundance and biomass between sites on Cambisols and Gleysols. Low earthworm abundance and biomass in pastures can be explained by unfavourable conditions: the soil is compacted by buffalos, which impedes burrowing. The negative effect of soil compaction on the activities of P. corethrurus has been confirmed in laboratory tests (Zund et al., 1997). In addition, the daily temperature amplitude is higher than in shaded environments, causing low moisture values, at least in the uppermost soil layers. According to Lavelle et al. (1987), P. corethrurus can tolerate temperatures between 15 and 35ºC, but reproduces only between 23 and 27ºC. Significantly higher temperatures, in the 0-10 cm soil layer in pastures compared to forests, were cited as a possible reason for impacts on earthworm feeding, burrowing and reproductive activities in Puerto Rico (Liu & Zou, 2002).

The increase of P. corethrurus abundance in the two younger regeneration stages may partly be caused by a decrease of soil density and improved moisture levels caused by the emergence of shading higher vegetation. Both this increase of P. corethrurus and the decrease in earthworm abundance and biomass at the two oldest succession stages are probably caused by changes in the chemical composition of the residues and soil organic matter available as food. Originally, P. corethrurus has been classified as a mesohumic endogeic species, which means that it consumes intermediate quality organic matter and not fresh or slightly decomposed litter. The discrepancy between using such low energy food and its often high abundance and biomass has been explained by the presence of a highly efficient gut microflora, well adapted to this type of food as well as to root and fungal (including arbuscular mycorrhizal fungi) substrates (Lattaud et al., 1998). Based on studies with labelled sugarcane material, it was proposed that this species may derive much of its tissue C from rhizosphere sources, which due its energy-rich composition would better explain its astonishing success in many different soils (Spain et al., 1990). In our study sites, in the coastal rainforest region, P. corethrurus seems to find its ideal C-sources only in the younger succession stages and, in particular, in the agroforestry sites. Lapied & Lavelle (2003) also found higher numbers in banana plantations (361 individuals m^-2), compared to different forest sites (50 - 250 individuals m^-2), in Costa Rica.

Studies of earthworm populations along forest succession in the tropics, with a replicated design, are rare. A study in Puerto Rico using three replicates of pastures (about 60 years old) young secondary forests (25 - 40 years old) and "mature secondary" forests (>77 years old) (Sanchez-De Leon et al., 2003) revealed strong dominance of P. corethrurus, in the two early stages, and co-occurrence with five anecic endemic species in mature forest. Number and biomass of the endemic species, all together reaching about one-third of P. corethrurus, were positively correlated with the amount of litter mass. Abundance and biomass were highest in the pastures and decreased significantly along the succession. Similar findings, in a nearby sequence of sites, were reported by Zou & González (1997). While no causal explanation was given, a positive correlation was found between earthworm density and fine-root biomass, thus pointing to root exudates as the most important factor. Interestingly, no negative effects on soil bulk density were found at the pasture sites in Puerto Rico, in contrast to Amazonia (Barros et al., 2004). In the study, we also observed a decrease along the succession, although it must be remembered that our "old growth" forests were never cut and used as pastures. But, even so, they did not contain any native species.

Almost no data on abundance or biomass of earthworms were available from eastern Paraná state. Therefore, we compare the data from the coastal region of Paraná with abundance data from western and central Paraná, representing mainly highland areas (Table 2) (Brown & James, 2007), being aware of the differences in climate, geology, soils, human activities etc. It seems that abundance and biomass of earthworms, at the agroforestry sites, are higher than those at other sites in Paraná, while there are no differences for pastures and secondary forests. Abundance and biomass data from the old-growth forests were higher than the ones reported in the literature (Table 2). This might be due to the fact that in our sites P. corethrurus dominated, while other "old" forest sites had endemic species. But it should also be considered that the category "old-growth/native/primary forest" is not well defined and, in most cases, no site history is known or reported.

It is likely that the coastal region of Paraná was originally inhabited by endemic glossocolecid species, as this has been observed in other coastal regions with Atlantic Forest of Brazil (Brown & James, 2007). Using a relationship first proposed by Fragoso (2001) for Mexico, and later modified for the state of São Paulo (31 spp. per 100 thousand km²), the Atlantic Forest, which originally covered approximately 1.3 million km² of Brazil, could have up to 400 species of earthworms. Currently, 144 species are known from this region (35 peregrine and 109 endemic) (Brown & James, 2007). For the state of Paraná, 55 species are known today (20 peregrine and 35 endemic), implying that there are probably many species not yet been discovered (Sautter et al., 2006). Most samples taken up to the present date have been taken in highland areas of western and central Paraná, with few samples from the lowland coastal rainforest (Brown & James, 2008).

The present study implies that the endemic species expected for the Atlantic Forest, in this region, have been replaced by the peregrine invasive species P. corethrurus, or by South-Eastern Asian Amynthas spp. (Blakemore, 2002) exotic species, since these were the main species found at the sampling sites, which represented different vegetation types, soil types and land use forms. Thus, it seems that even the old forests of the coastal plain region (which is the oldest colonization front of settlers in the state of Paraná, beginning in the 1600s), have been affected by anthropogenic activities, leading to the loss of native species and the invasion by peregrine and exotic ones.

Similar findings have also been made in other Latin American natural forests as in Costa Rica (Lapied & Lavelle, 2003; Brown et al., 2006). The coastal region of Brazil was strongly colonized for centuries and, consequently, P. corethrurus has been reported in almost every agriculturally used area of the Mata Atlântica for about 150 years (Müller, 1857; Brown & James, 2006), including near-natural, old-growth forests like our study sites. Today, P. corethrurus is probably the most widely distributed earthworm species in tropical areas, where it is often the dominant species, at least in anthropogenic disturbed soils (Fragoso et al., 1999). Due to its very wide ecological preferences and some morphological variability, it was proposed that this is a species complex, consisting of at least four species (Moreno, 2004) - a view, which has not been proven so far. This species has expanded over the Neotropics during the European expansion, and is still colonizing plantations and secondary forests throughout Brazil, for example in central Amazonia (Zicsi et al., 2001). The species has already been associated with negative effects on soil structure due to its casting activities (Sparovek et al., 1999; Barros et al., 2004), on plant production (Brown et al., 1999), and on native earthworm communities (Lapied & Lavelle, 2003). However, it seems that in agricultural soils its net effect is mainly positive, while in native ecosystems the net effect of invasion may be negative (Brown & James, 2007). It is still not known to which extent P. corethrurus colonized "empty" soils after the native earthworm fauna was annihilated by human activities, or whether this species invaded pristine sites because it is simply more competitive than native species (González et al., 2006). The latter could be caused by the fact that the species is able to survive even in nutrient-poor soils (Lavelle et al., 1999). This explanation is supported by the results of a mesocosm study in Puerto Rico, which indicates that the recolonization of disturbed sites by native species Estherella spp. (epigeic and anecic) is possible, but only if peregrine species are not present (Huang et al., 2006). In this context, it is worthwhile to mention that at some sites a co-existence between P. corethrurus and native species is possible, simply by living at different layers (soil depths, litter) (Sanchez-De Leon et al., 2003). Based on field studies in Puerto Rico, Sanchez-De León et al. (2003) also pointed out that a recovery of native species is possible only if there are primary forest patches in close distance, in order to allow their recolonization, which, as far as we know today, was not the case of our study sites.

Much less is known about the invasive ocnerodrilids or megascolecids, the latter being often associated with human settlements. Based on laboratory experiments, Garcia & Fragoso (2003) concluded that A. corticis thrives best when feeding on a mixture of high and low quality organic material, while P. corethrurus is less demanding. This may partly explain why Amynthas spp. are usually less abundant. No data are known from eastern Paraná or from the coastal lowlands, but abundance values of 0 to 200 individuals m^-2 of Amynthas spp. were reported from the highlands of Paraná (Brown & James, 2007). Especially at no-tillage treated crop sites, farmers acknowledge the occurrence of megascolecid worms (Peixoto & Marochi, 1996). The high ecological tolerance of these peregrine species, in terms of soil properties, vegetation types and climatic factors explains why they are so wide-spread in the secondary forests studied here.

The often very high abundance and, in particular, biomass (by far the biggest part of the whole soil invertebrate community) of the earthworms, at almost all sites (except for the forests with sandy Podzol soils), underlines their important role for the provision of ecological services (Schmidt et al., 2008). This is rather interesting, since for a long time, the contribution of earthworms to soil structure, organic matter decomposition and soil fertility was considered less important in the tropics than in temperate regions, as it was assumed that their biomass in tropical soils was lower than in temperate soils, and that the tropical earthworm community did not contain vertical burrowers (Beck, 1971). However, within the last two decades, the existing knowledge on earthworms, in different tropical ecosystems (pastures, secondary or primary forests) and, in particular, their role in decomposition processes increased considerably, mainly due to work in Latin America (Höfer et al., 2001; Liu & Zou, 2002). The latter authors pointed out that P. corethrurus can significantly increase litter decomposition indirectly by its casting activity at the soil surface: organic material is covered by the casts, which firstly enhances microbial activity by providing better moisture conditions and, secondly, may facilitate feeding by the worms. Despite this progress, the contribution of species like P. corethrurus to processes like organic matter decomposition are far from understood. Further research is necessary, in particular regarding the role which secondary forests as well as agroforestry sites can play for the long-term protection of earthworm biodiversity in Mata Atlântica.

The results of the present work raise new questions concerning the impacts of human activities on (soil organism) biodiversity in the coastal plain forests. How many species of native earthworms were formally present at these sites? Is there a threshold for a regeneration of native fauna? Why is one peregrine species so abundant and dominant? Will endemic species be kept to a few isolated spots, or is it possible to manage sites, in particular secondary forests, in a way that more diverse earthworm communities can thrive there?

Conclusions

1. The coastal Mata Atlântica of Paraná state, in Brazil, presents a depleted earthworm fauna in terms of species richness and diversity, while abundance and biomass values observed in this region reconfirm the importance of earthworms for the functioning of the ecosystems.

2. Endemic species expected for the Atlantic Forest have been replaced by the peregrine invasive species Pontoscolex corethrurus, or by South-Eastern Asian Amynthas spp. exotic species. This fact indicates that even the old forests of the Brazilian coastal plain region have been affected by anthropogenic activities.

3. Reasons for the overwhelming dominance of the peregrine species P. corethrurus and for the fact that not one native earthworm species was found in the 51 studied sites remain as a challenge for further research on the conservation and sustainable management of biodiversity, in lowland Atlantic rainforests of Brazil.

Acknowledgements

To the German Federal Ministry of Education and Research and to the Conselho Nacional de Desenvolvimento Científico Tecnológico, for support within the Brazilian-German Mata Atlântica program; to the Brazilian NGO "Sociedade Brasileira de Pesquisa em Vida Selvagem e Educação Ambiental", for permitting and supporting the field work at their reserves "Reserva Natural Rio Cachoeira" and "Reserva Natural Serra do Itaqui". To all our SOLOBIOMA colleagues, for helping during our sampling campaigns, in particular Adriana Souza dos Santos, Bernhard Förster, Florian Raub, Juliano Schwarzbach, Luis Scheuermann, Phillip Hopp, and Stephan Meyer.

Received on November 12, 2008 and accepted on June 30, 2009

• BARROS, E.; GRIMALDI, M.; SARRAZIN, M.; CHAUVEL, A.; MITJA, D.; DESJARDINS, T.; LAVELLE, P. Soil physical degradation and changes in macrofaunal communities in Central Amazon. Applied Soil Ecology, v.26, p.157-168, 2004.
• BECK, L. Bodenzoologische Gliederung und Charakterisierung des amazonischen Regenwaldes. Amazoniana, v.3, p.69-132, 1971.
• BLAKEMORE, R.J. Cosmopolitan earthworms: an eco-taxonomic guide to the peregrine species of the world. Canberra: [s.n.], 2002. 1 CD ROM.
• BOEGER, M.R.T.; WISNIEWSKI, C.; REISSMANN, C.B. Nutrientes foliares de espécies arbóreas de três estádios sucessionais de floresta ombrófila densa no Sul do Brasil. Acta Botanica Brasilica, v.19, p.167-181, 2005.
• BROWN, G.G.; FRAGOSO, C. (Ed.). Minhocas na América Latina: biodiversidade e ecologia. Londrina: Embrapa Soja, 2007. 545p.
• BROWN, G.G.; JAMES, S.W. Biodiversidade de minhocas. In: Lopes, M.I.M.S.; Kirizawa, M.; Melo, M.M.R.F. (Ed.). A reserva biológica de Paranapiacaba: a estação biológica de Alto da Serra. São Paulo: Secretaria do Meio Ambiente do Estado de São Paulo, 2008.
• BROWN, G.G.; JAMES, S.W. Earthworm biodiversity in São Paulo state, Brazil. European Journal of Soil Biology, v.42, p.145-149, 2006.
• BROWN, G.G.; JAMES, S.W. Ecologia, biodiversidade e biogeografia das minhocas no Brasil. In: Brown, G.G.; Fragoso, C. (Ed.). Minhocas na América Latina: biodiversidae e ecologia. Londrina: Embrapa Soja, 2007. p.297-383.
• BROWN, G.G.; JAMES, S.W.; PASINI, A.; NUNES, D.H.; BENITO, N.P.; MARTINS, P.T.; SAUTTER, K.D. Exotic, peregrine, and invasive earthworms in Brazil: diversity, distribution, and effects on soils and plants. Caribbean Journal of Science, v.42, p.339-358, 2006.
• BROWN, G.G.; PASHANASI, B.; VILLENAVE, C.; PATRÓN, J.C.; SENAPATI, B.K.; GIRI, S.; BAROIS, I.; LAVELLE, P.; BLANCHART, E.; BLAKEMORE, R.J.; SPAIN, A.V.; BOYER, J. Effects of earthworms on plant production in the tropics. In: LAVELLE, P.; BRUSSAARD, L.; HENDRIX, P.F. (Ed.). Earthworm management in tropical agroecosystems Wallingford: CAB International, 1999. p.87-147.
• EISEN, G. On the anatomy of Ocnerodrilus. Nova Acta Regiae Societatis Scientiarum Upsaliensis, v.10, p.10, 1878.
• FERRETTI, A.R.; BRITEZ, R.M. de. Ecological restoration, carbon sequestration and biodiversity conservation: the experience of the Society for Wildlife Research and Environmental Education (SPVS) in the Atlantic Rain Forest of Southern Brazil. Journal for Nature Conservation, v.14, p.249-259, 2006.
• FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS. World reference base for soil resources Rome: FAO, 1998. (FAO. World Soil Resources Reports, 84).
• FRAGOSO, C. Las lombrices de tierra de México (Annelida: Oligochaeta): diversidad, ecología y manejo. Acta Zoológica Mexicana, v.1, p.131-171, 2001.
• FRAGOSO, C.; KANYONYO, J.; MORENO, A.; SENAPATI, B.K.; BLANCHART, E.; RODRIGUEZ, C. A survey of tropical earthworms: taxonomy, biogeography and environmental plasticity. In: Lavelle, P.; Brussaard, L.; Hendrix, P. (Ed.). Earthworm management in tropical agroecosystems. Wallingford: CAB International, 1999. p.1-26.
• GARCIA, J.A.; FRAGOSO, C. Influence of different food substrates on growth and reproduction of two tropical earthworm species (Pontoscolex corethrurus and Amynthas corticis). Pedobiologia, v.47, p.754-763, 2003.
• GONZÁLEZ, G. Earthworms as invasive species in Latin America - the 2nd Latin American Meeting on Oligochaeta (Earthworm) ecology and taxonomy. Caribbean Journal of Science, v.42, p.281-284, 2006.
• GONZÁLEZ, G.; HUANG, C.Y.; ZOU, X.M.; RODRÍGUEZ, C. Earthworm invasions in the tropics. Biological Invasions, v.8, p.1247-1256, 2006.
• HÖFER, H.; HANAGARTH, W.; GARCIA, M.; MARTIUS, C.; FRANKLIN, E.; RÖMBKE, J.; BECK, L. Structure and function of soil fauna communities in Amazonian anthropogenic and natural ecosystems. European Journal of Soil Biology, v.37, p.229-235, 2001.
• HUANG, C.Y.; GONZÁLEZ, G.; HENDRIX, P.F. The re-colonization ability of a native earthworm, Estherella spp., in forsts and pastures in Puerto Rico. Caribbean Journal of Science, v.42, p.386-396, 2006.
• INSTITUTO PARANAENSE DE DESENVOLVIMENTO ECONÔMICO E SOCIAL. Zoneamento da área de proteção ambiental de Guaraqueçaba Curitiba: IPARDES, 2001. 150p.
• INTERNATIONAL ORGANIZATION FOR STANDARDIZATION. ISO 23611-1: soil quality - sampling of soil invertebrates - Part 1: hand-sorting and formalin extraction of earthworms. Geneve: ISO, 2007.
• KINBERG, J.G.H. Annulata nova. Ofversigt af Kongliga Vetenskaps-Akademiens Forhandlingar, v.23, p.256-257, 1867.
• LAPIED, E.; LAVELLE, P. The peregrine earthworm Pontoscolex corethrurus in the east coast of Costa Rica. Pedobiologia, v.47, p.471-474, 2003b.
• LATTAUD, C.; LOCATI, S.; MORA, P.; ROULAND, C.; LAVELLE, P. The diversity of digestive systems in tropical geophagous earthworms. Applied Soil Ecology, v.9, p.189-195, 1998.
• LAVELLE, P.; BAROIS, I.; CRUZ, I.; FRAGOSO, C.; HERNANDEZ, A.; PINEDA, A.; RANGEL, P. Adaptive strategies of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta), a peregrine geophagous earthworm of the humid tropics. Biology and Fertility of Soils, v.5, p.188-194, 1987.
• LAVELLE, P.; BRUSSAARD, L.; HENDRIX, P. (Ed.). Earthworm management in tropical agroecosystems. Wallingford: CAB International, 1999. 300p.
• LAVELLE, P.; LAPIED, E. Endangered earthworms of Amazonia: an homage to Gilberto Righi. Pedobiologia, v.47, p.419-427, 2003.
• LEE, K.E. Earthworms: their ecology and relationships with soils and land use. Sidney: Academic Press, 1985. 411p.
• LIU, Z.G.; ZOU, X.M. Exotic earthworms accelerate plant litter decomposition in a Puerto Rican pasture and a wet forest. Ecological Applications, v.12, p.1406-1417, 2002.
• MORENO, A.G. What is Pontoscolex (Pontoscolex) corethrurus (Annelida, Glossoscolecidae)? In: MORENO, A.G.; BORGES, S. (Ed.). Advances in earthworm taxonomy. Madrid: Editorial Complutense, 2004. p.69-73.
• MÜLLER, F. Lumbricus corethrurus, Bürstenschwanz. Archiv für Naturgeschichte, v.23, p.113-116, 1857.
• PEIXOTO, R.T. DOS G.; MAROCHI, A.I. 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, v.35, p.23-35, 1996.
• PINTO, C.B.; MARQUES, R. Aporte de nutrientes por frações da serapilheira em sucessão ecológica de um ecossistema da Floresta Atlântica. Revista Floresta, v.33, p.257-264, 2003.
• RODERJAN, C.V.; KUNYOSHI, Y.S. Macrozoneamento florístico da área de proteção ambiental - APA - Guaraqueçaba Curitiba: Fundação de Pesquisas Florestais do Paraná, 1988. (FUPEF. Série Técnica, 15).
• SANCHEZ-DE LEON, Y.; ZOU, X.; BORGES, S.; RUAN, H. Recovery of native earthworms in abandoned tropical pastures. Conservation Biology, v.17, p.999-1006, 2003.
• SAUTTER, K.D.; BROWN, G.G.; JAMES, S.W.; PASINI, A.; NUNES, D.H.; BENITO, N.P. Present knowledge on earthworm biodiversity in the State of Paraná, Brazil. European Journal of Soil Biology, v.42, p.296-300, 2006.
• SCHMIDT, P.; DICKOW, K.; ROCHA, A.A.; MARQUES, R.; SCHEUERMANN, L.; RÖMBKE, J.; FÖRSTER, B.; HÖFER, H. Soil macrofauna and decomposition rates in Southern Brazilian Atlantic rainforests. Ecotropica, v.14, p.89-100, 2008.
• SCHRÖDER, P. Die Klimate der Welt: aktuelle Daten und Erläuterungen. Stuttgart: Thieme, 2000. 159p.
• SPAIN, A.V.; SAFFIGNA, P.G.; WOOD, A.W. Tissue carbon sources for Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) in a sugarcane ecosystem. Soil Biology and Biochemistry, v.22, p.703-706, 1990.
• SPAROVEK, G.; LAMBAIS, M.R.; SILVA, A.P. da; TORMENA, C.A. Earthworm (Pontoscolex corethrurus) and organic matter effects on the reclamation of an eroded Oxisol. Pedobiologia, v.43, p.698-704, 1999.
• STATSOFT. Statistica for Windows: software-system for data analysis. Version 8.0. 2007. Available at: <www.statsoft.com>. Acess on: 19 Aug. 2009.
• STRAHLER, A.H.; STRAHLER, A.N. Physische Geographie Stuttgart: Eugen Ulmer, 2005. 686p.
• ZICSI, A.; RÖMBKE, J.; GARCIA, M.V. Regenwürmer (Oligochaeta) aus der Umgebung von Manaus (Amazonien). Regenwürmer aus Südamerika 32. Revue Suisse de Zoologie, v. 108, p.153-164, 2001.
• ZOU, X.M.; GONZÁLEZ, G. Changes in earthworm density and community structure during secondary succession in abandoned tropical pastures. Soil Biology and Biochemistry, v.29, p.627-629, 1997.
• ZUND, P.R.; PILLAI-MCGARRY, U.; MCGARRY, D.; BRAY, S.G. Repair of a compacted Oxisol by the earthworm Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta). Biology and Fertility of Soils, v.25, p.202-208, 1997.

Publication Dates

• Publication in this collection
  12 Nov 2009
• Date of issue
  Aug 2009

History

• Accepted
  30 June 2009
• Received
  12 Nov 2008