Oligochaeta (Annelida: Clitellata) associated to aquatic macrophytes in Brazil

Oligochaeta are still characterized as a poorly studied group among the aquatic macroinvertebrates and few studies about their ecology were conducted in Brazil. Thus, our study aimed to provide an overview of the association between Oligochaeta and macrophytes, in Brazilian continental aquatic environments, by means of a literature review along with an inventory of species associated to aquatic macrophytes on marginal lagoons


Introduction
Research relying on information obtained from inventories of species provides a broad knowledge about distribution, richness, and other ecological aspects, establishing relevant tools for biodiversity conservation programs and decision-making with regard to management of natural areas (SILVEIRA et al., 2010).However, in general, the invertebrate fauna is still poorly documented when compared to other animal groups, such as mammals and birds (CHRISTOFFERSEN, 2010).The difficulties of taxonomic identification and the low popularity of these taxa among people make information about them fragmented and scarce (MAGURRAN, 2011).
Aquatic macrophytes are important elements to maintain biodiversity in tropical lakes, increasing habitat complexity and heterogeneity (ROSINE, 1955).Aquatic macrophytes are key in the trophic chain, where many animal groups obtain their food from biomass, organic residue, or periphyton growing on the surface of macrophytes (WELCH, 1952;ROSINE, 1955;POTT;POTT, 2000).Moreover, macrophytes serve as cover for excessive luminosity (WELCH, 1952), shelter against predators, and they can be used as nest for egg deposition (GLOWACKA et al., 1976).Invertebrate density and biomass may change according to the habitat complexity degree, which is optimized by macrophytes (MORMUL et al., 2010;KRAWCZYK et al., 2013).Thus, Oligochaeta are often observed in areas with aquatic vegetation, mainly on decomposing leaves, where they feed on organic matter, as well as on periphyton adhered to the surface (GALIZZI; MARCHESE, 2009;MARTINS et al., 2011).Periphyton is a major source of food for Oligochaeta, especially the Naididae family (LEARNER et al., 1978).Thus, morphological plant structures serve as ilters to catch particles and microorganisms, providing more favorable conditions so that Oligochaeta populations can establish and grow with macrophytes (CORREIA; TRIVINHO-STRIXINO, 1998).Moreover, plant structures are important to provide these organisms with shelter (CHAUVET, 1997), mainly submerged roots (ARMENDÁRIZ, 2008).
Despite the growing interest in studying and expand the ecological and biological knowledge of Oligocaheta, this research area still fragmented and incomplete in Brazilian freshwaters (ALVES et al., 2006).Based on the above, we aimed to inventory the Oligochaeta species associated to macrophytes in Brazilian continental aquatic environments.

Data from articles
We searched Brazilian articles about the association between Oligochaeta and macrophytes in March and April of 2014 on the databases Scopus, Google Scholar, and Web of Science, by using the keywords "aquatic macrophytes" and "Oligochaeta" with no determined period.A total of 10 articles were selected according to the criterion of having Oligochaeta species or genus associated to macrophyte species or genus and we iltered only articles from Brazil.The articles found provide us with an overview from 1997 to 2014.To organize the results, a table was prepared according to the taxonomic level adopted (species or genus).

Sampling of Oligochaeta
We obtained information to inventory Oligochaeta on marginal lagoons in the reservoir Ribeirão das Anhumas (Américo Brasiliense, São Paulo, Brazil), central region of the state of São Paulo, Brazil (21º42'23"S and 48º0'33"W; 544 m high).Macrophytes were sampled in August and December 2012 and in March and April 2013, on the coastal region of lagoons.According to Pott and Pott (2000), we selected and identiied ive We collected 100 g (wet weight) for each macrophyte genus by using a 0.21 mm mesh hand net.Small amounts of each macrophyte were analyzed in trays with water and each Oligochaeta specimen was ixed in 10% formalin and preserved in 70% alcohol (ALVES; GORNI, 2007;PEIRÓ;GORNI, 2010).For identifying Oligochaeta, lamina were prepared with lactophenol and observed criteria adopted by Brinkhurst andJamieson (1971), Righi (1984), Brinkhurst and Marchese (1989).

Results
We inventoried 21 Oligochaeta species on the lagoons in the reservoir Ribeirão das Anhumas, belonging to two families: Naididae and Opistocystidae.Sampling results were entered and 45 taxa were registered (41 species and 4 genera), associated to 20 aquatic macrophyte taxa (Table 1).The articles found included few Brazilian states: Mato Grosso do Sul, São Paulo, Paraná, and Minas Gerais, showing a concentration of studies in the southeastern, southern, and central-western regions in Brazil.Additionally, only one article discussed the occurrence of Oligochaeta on decomposing leaves (MARTINS et al., 2011), showing that most studies still focus on the sampling of living macrophytes.
Therefore, we noticed a predominance of the Naididae family among the species inventoried (literature review and inventory of species), with 93.33% associated to macrophytes and other two families registered: Opistocystidae (4.44%) and Alluroididae (2.22%).Moreover, the species with the highest prevalence in the macrophytes was Dero nivea, which was associated to 15 macrophyte taxa, followed by Dero digitata and Dero raviensis, associated to 11 taxa, and Dero sawayai, associated to 10 taxa.In turn, species such as Brinkhurstia americana and Limnodrilus hoffmesteiri were registered only in 1 macrophyte taxon.The most frequently registered macrophytes in literature review and inventory of species live a submerged life.However, the macrophyte showing the highest richness of Oligochaeta associated was Eichhornia azurea, which lives a loating life.Thus, E. azurea had 51.1% of the richness, while the others were: Egeria sp.(40.0%),Najas sp.(35.6%), and Mayaca luviatilis (31.1%) (Table 2).

Discussion
Our study provides an overview of the association between Oligochaeta and macrophytes in Brazilian continental aquatic environments.We highlighted the Naididae family, which obtained 93% of the species richness.Similarly, our results showed the Eichhornia azurea macrophyte with a higher richness of associated Oligochaeta species.
Regarding the Naididae family, perhaps the higher representativeness is due to the inclusion of recent subfamilies (Tubiicinae, Rhyacodrilinae, Phallodrilinae, Limnodrilinae, and Telmatodrilinae) to the group (CHRISTOFFERSEN, 2007).However, this pattern is conirmed by the literature, which regards Naididae as the main family among the Oligochaeta (PAMPLIN et al., 2005).
Naididae is a group adapted to many environmental conditions and it has a wide distribution, all over the world.Moreover, these organisms are free swimmers, a feature which allows them to explore a broader diversity of habitats, including macrophytes (VERDONSCHOT et al., 1982;ALVES;GORNI, 2007).The main food source of these organisms consist of periphyton accumulated in organic matter on plants and sediment (BRINKHURST; JAMIESON, 1971;SCHENKOVÁ;HELESIC, 2006).Thus, some authors reported that the Naididae family is favored at sites with the presence of aquatic vegetation (LEARNER et al., 1978;SMOCK;STONEBURNER, 1980;ALVES;GORNI, 2007).
Our results revealed that Dero species obtained the highest prevalence in the macrophytes, they were observed in plants with different life forms: emergent, loating, and submerged, demonstrating the adaptive capacity of this group to various habitats.In this study, the species Dero nivea had the highest prevalence and it is associated to 15 macrophyte taxa.According to other studies, this species is commonly found in regions rich N. A. O. Sanches et al. in aquatic vegetation (DAVIS, 1982) and it is usually one of the most abundant species (CORREIA; TRIVINHO-STRIXINO, 1998;TRIVINHO-STRIXINO et al., 2000;ALVES;GORNI, 2007).In turn, the species with lower prevalence, such as Brinkhurstia americana and Limnodrilus hoffmeisteri, are more adapted to live on sediment and the substratum composition and particle size was a major determinant of their distribution (MORETTO et al., 2013).
The three-dimensional complexity of macrophytes provides periphyton accumulation and, as a consequence, greater abundance and richness of Naididae, when compared to other aquatic invertebrates (THOMAZ;CUNHA, 2010;HANSEN et al., 2011).Moreover, plant position in the water column may affect the occurrence of organisms.Floating macrophytes, for instance, develop a dense root system, which provides many aquatic organisms with shelter (HECKMAN, 1998), including some Naididae species, which can build small tubes with root fragments, connected by tegument secretions (ARMENDÁRIZ, 2008).Thus, this structural complexity form slits that serve as hiding places and nests, reducing river low (GREGG; ROSE, 1982) and protecting against predators (FERREIRO et al., 2011).Additionally, the Oligochaeta also occurred on exotic macrophytes, Hydrilla verticillata, which according to Behrend et al. (2013) provide these organisms with favorable conditions.
Eichhornia azurea, which had the highest richness of associated Oligochaeta species, is commonly found in studies associating macroinvertebrates to aquatic macrophytes (FULAN;HENRY, 2006;COPATTI et al., 2013;SILVA;HENRY, 2013).This species lives a loating life, providing organisms with spatial stability, it also has thick roots and submerged leaves, providing microhabitats to aquatic fauna (POTT; POTT, 2000).Among all features reported above, it is worth highlighting the submerged rhizome biomass, which absorb and store nutrients, keeping continued productivity and regular food sources to macroinvertebrates (OLIVEIRA et al., 2005).Other factors, such as the decomposition mechanisms of these macrophytes and release of particulate nutrients in aquatic environments may explain the high richness of Oligochaeta species registered for this macrophyte.
This study registered about 48% of the aquatic Oligochaeta diversity observed in Brazil, and this result highlights the relevance of macrophytes as a resource for these invertebrates, mainly for the Naididae family.The literature review also revealed a small number of studies conducted in Brazil associating Oligocheta to macrophytes.Thus, this study corroborates Christoffersen (2010), who reported that information on these worms in South America are regarded as insuficient and further investigation is needed to increase knowledge on the distribution and ecology of this taxon.Therefore, this article contributes to the collection of scientiic data on the Oligochaeta in Brazilian continental aquatic environments.
N. A. O.Sanches et al.