Oligochaeta ( Annelida : Clitellata ) in the Juruena River , MT , Brazil : species indicators of substrate types

Oligochaeta assemblages are important components in freshwater environments, where their abundance and composition may indicate aspects related to water quality and sediment. The lack of information about these communities in Brazilian aquatic environments, as well as the application of native species as bioindicators of lotic environmental, stimulated the conception of this paper. Thus, the aim was to study the community of aquatic Oligochaeta in selected stretches of the Juruena River (MT), thereby generating grounds for future environmental monitoring action in lotic ecosystems. For this purpose, samples were analyzed at bimonthly intervals during the period from January to November 2009, in stretches of the Juruena River (Amazon River Basin) located in the State of Mato Grosso (MT). Two methods were used to collect the organisms: a) “D” network in small clusters of fixed macrophytes in the sediment on the river banks; and b) Ekman-Birge dredge in fine sediment. Preliminary results were 584 organisms distributed in 22 taxa. Of these, 22 valid species were identified. This number corresponds to approximately 25% of the aquatic oligochaete species registered in Brazil. Of these species, Limnodrilus hoffmeisteri, Dero nivea and Pristina rosea can be associated with organic enrichment conditions and/or some level of environmental degradation.


Introduction
Oligochaeta are some of the most abundant groups in continental aquatic macrofauna and play an important role in the process of decomposition and cycling of organic matter in freshwater ecosystems (Ragonha & Takeda, 2014, Cesar & Henry 2017).These organisms are found in almost all fresh aquatic environments (Cesar & Henry 2017), living in sediment and water columns (Rodriguez & Reynoldson 2011), and in association with other organisms (Corbi et al. 2004, Alves & Gorni 2007, Gorni & Alves 2007, Gorni & Alves 2008, Oda 2015).
In addition, these worms have limited mobility and are influenced by the habitat characteristics in which they are found (Behrend et al. 2012).Thus, the richness and abundance of Oligochaeta is directly related to environmental variables (Marchese & Drago 1999, Jablonska, 2014), such as availability of food resources (Martins & Silveira, Alves 2011); dissolved oxygen (Dornfeld et al. 2006); type of substrate (Moretto et al. 2013); water temperature (Nascimento & Alves 2009), thus being considered indicators of specific habitats.
However, although common in freshwater environments (Timm et al. 2001), knowledge about Oligochaeta fauna in Brazilian fresh waters is still fragmented and incomplete (Alves et al. 2008, Takeda et al. 2017).This lacuna is mainly due to the concentration of studies related to the spatial distribution of benthic invertebrate fauna, with emphasis on insect larvae (Roque & Trivinho-Strixino 2001, Sanseverino & Nessimian, 2001), the great extent of the still unexplored parts of the Brazilian hydrographic basins (Joly et al. 2011) and the low financial investment in scientific research in the country (Agostinho et al. 2005, Magurran 2011).
However, the lack of information about these organisms in Brazilian aquatic environments is still evident in many regions (Gomes et al. 2017), as well as the use of native species as bioindicators of the quality of the country's aquatic ecosystems.Thus, the main objective of this paper was to study the aquatic Oligochaeta community in selected stretches of the Juruena River (MT), providing information for future action of environmental monitoring in lotic ecosystems.

Study area
For the analysis of the Oligochaeta assemblages, samples were analyzed at bimonthly intervals during the period from January to November 2009.For the regular samplings, five sites were selected from the Juruena River (Amazon River Basin), located in the State of Mato Grosso (MT) (Figure 1).
The region is demarcated by humid tropical climates to contrasting seasons.Regionally the rainy season has its beginning, usually in the month of September until the month of April.From December to March are characterized by a increase in regional rainfall (Tardy, 1986).The basin is mainly sheltered by Ombrophilous Forest (Instituto Brasileiro de Geografia Estatística, 1992).In the upper portion of the basin, close to the Juruena, the vegetation is classified as "Cerrado".The soils in the basin are largely composed of red-yellow Acrisols (29%), red-yellow Oxisols (27%) and Arenosols (18%) (Empresa Brasileira de Pesquisa Agropecuária, 1980).
The headwaters of Rio Juruena are situated at the Parecis Plateau, in a savanna ecosystem ("cerrado").In this area the water is totally transparent and poor in nutrients (N, P, and Ca).Biochemical oxygen demand (BOD) and fecal coliform bacteria are low, demonstrating that anthropic contributions are insignificant.Macrophytes are not abundant and are distributed in discrete and sparse stands, sometimes covering a sand plateau onshore.
The collection sites were selected considering: i) prevailing habitats, ii) easy access, and iii) adequate sites for the use of benthic fauna samplers (details of the geographical location of the sites are shown in Table 1).

Data collection
The collection of organisms followed the methodology described by Dowing (1984) and Peckrasky (1984).Thus, two methods of collecting zoobenthos were used: a) the D-net sampler in small groups of fixed macrophytes on the river margin; and b) Ekman-Birge dredge in fine sediment to collected sediment and associated organisms.
The net, with 0.30 m mesh openings, was dragged 1.0 m by the macrophyte roots, making a capture area of 0.3 m 2 .The dredge, with an area of 0.0225 m 2 , was launched in locations close to the margins in depths of up to 3 m.As an adopted procedure, two samples (replicas) were made with the net and dredge at each sampling site (a total of 50 sample units).Still at the sites, the collected samples were washed in a sieve with a mesh of 0.21 mm opening, fixed in 10% formalin and preserved in 70% alcohol.In the laboratory, the samples were washed again on a 0.021mm mesh granulometric sieve.The organisms were screened in a WILD ® stereomicroscope with a maximal increase of 30 times.For the identification of Oligochaeta, taxonomic criteria adopted by Brinkhurst & Jamieson (1971), Righi (1984), Brinkhurst & Marchese (1989), Pinder & Brinkhurst (1994) and Timm (2009) were followed.The list of species in synonymy was based on the catalog proposed by Christoffersen (2007).
All biological material identified was deposited in the Laboratory of Ecology and Aquatic Ecotoxicology (LEEA) linked to the Department of Hydraulics and Sanitation, School of Engineering of São Carlos, University of São Paulo.
In order to verify the sensitivity of the species to the different habitats, fixed macrophytes, mainly Podostemacean species on the river margin (collected with a D-net sampler) and fine sediment (Ekman-Birge dredge) we applied Indicator Species Analysis (ISA) (Dufrene & Legendre, 1997) (alpha = 0.05).This analysis combines species relative abundance with their relative frequency of occurrence in the various groups of samplers.This analysis was made using the ''indicspecies'' package (De Caceres & Legendre, 2009) in R software (R Core Team, 2017), with 10,000 permutations.

Results
A total of 584 organisms were identified in 22 valid species comprising 11 genera.This number corresponds to less than 1% of the aquatic species described in the world and approximately 1/4 of the species registered in Brazil (Christoffersen 2007, Martin et al. 2008).The relative abundance of the Oligochaeta species are shown in Table 1.The specie Brinkhurstia americana showed a relative abundance greater than 50% of the total fauna in all the points sampled.

Discussion
Listed below are the species, according to the nomenclature proposed by Timm (2017) with respective records from the Brazilian territory and ecological considerations.

Pristina rosea
Distribution -São Paulo: Pinheiros River and the campus of the University of São Paulo associated with bromeliads (Marcus 1943), in the Tietê River associated to the plant of the genus Calathea sp.(Marcus 1944); in urban streams and a rural stream (Alves et al. 2006); in the Monjolinho reservoir, organically enriched (Fusari & Fonseca-Gessner 2006); associated with bryophytes of the genus Fissidens sp. and Philonotis sp.(Gorni & Alves 2007); in streams of low order of the Campos do Jordão State Park, characterized by cold waters, rapids and stony bed (Gorni & Alves 2008b), in mesohabitats of the Galharada stream (Gorni & Alves 2012) and was evidenced in impacted urban streams (Gorni et al., 2017).Minas Gerais: occurred in first-order streams of preserved areas (Rodrigues et al. 2013); associated with bryophytes (Rodrigues et al. 2016) and in a stream of the Atlantic Forest (Rosa et al. 2015).Pernambuco: city of Recife, in pools of water (Marcus 1944) and in Tegipió (Marcus 1943).
Based on species distribution patterns and habitat preference (ISA) in the Juruena River, we concluded that Dero species are associated with marginal regions of aquatic ecosystems, mainly occurring as aquatic macrophytes.This condition demonstrates the susceptibility of this species group to samplers such as D-net.Limnodrilus hoffmeisteri, Aulodrilus pigueti, Narapa bonettoi and Aulophorus lodeni were related with depositional zones, where fine sediments occur.L. hoffmeisteri are also registered as being associated to organic enrichment conditions and/or some degree of environmental degradation.
Thus, in order to increase the efficiency of future environmental quality monitoring programs carried out in the region, cautious monitoring of these species in other parts of the Amazon River Basin is advisable.

Figure 1 .
Figure 1.Map showing the location of the study area with highlight of the sampled section.

Table 2 .
Indicator Species in two collected habitats on the Juruena River (fixed macrophites and fine sediment).IV (%): species indicator value obtained by 10,000 permutations (using the Monte Carlo Method).