Relationship between space distribution of the benthic macroinvertebrates community and trophic state in a Neotropical reservoir (Itupararanga, Brazil)

Relação entre a distribuição espacial da comunidade de macroinvertebrados bentônicos e o estado trófico em um reservatório Neotropical (Itupararanga, Brasil)

ARTICLES

Relationship between space distribution of the benthic macroinvertebrates community and trophic state in a Neotropical reservoir (Itupararanga, Brazil)

Relação entre a distribuição espacial da comunidade de macroinvertebrados bentônicos e o estado trófico em um reservatório Neotropical (Itupararanga, Brasil)

Frederico Guilherme de Souza Beghelli^I,1; André Cordeiro Alves dos Santos^I; Maria Virgínia Urso-Guimarães^I; Maria do Carmo Calijuri^II

^IDepartamento de Biologia, Universidade Federal de São Carlos – UFSCar, Rod. João Leme dos Santos, Km 110, Sorocaba, SP, Brasil. http://www.sorocaba.ufscar.br/ufscar/

^IIDepartamento de Hidráulica e Saneamento, Escola de Engenharia de São Carlos, Universidade de São Paulo – USP, Av. Trabalhador São Carlense, 400, São Carlos, SP, Brasil. http://www.saocarlos.usp.br/

ABSTRACT

The purpose of this work was to verify the benthic macroinvertebrates community responses through environmental factors along a headwater tropical reservoir. Samplings were taken with a Van-Veen grab along the reservoir in littoral and profundal regions and in the headwater, next to the dam and the middle of the reservoir. Samples were taken during both wet and dry seasons. Dissolved oxygen concentrations, electric conductivity, temperature and pH near the sediment have been performed in situ, at every sampling station by using a multiprobe and Secchi disc. Total water phosphorus and chlorophyll a concentrations were analyzed to determine the trophic state index. Sediment's organic matter, total phosphorus, nitrogen concentrations and granulometric composition were measured. In order to verify which environmental variables would have more influence over the benthic macroinvertebrates community, a canonical correspondence analysis (CCA) was performed. The total number of recorded taxa was 28. Among them, the family Chironomidae (Diptera) was the richest group (19 taxa). It can be proposed that the benthic macroinvertebrates community may be influenced by environmental conditions such as nutrient and organic matter availability, as well as dissolved oxygen concentration. Macroinvertebrates are adequate bioindicators of water quality due to their sensibility to environmental changes mentioned before. Chironomus sp, Limnodrilus hoffmeisteri and Branchiura sowerbyi comprises a group that can be considered bio-indicators of eutrophic conditions. A second group can be considered as indicator of mesotrophic conditions. The presence of two or more members from that group which comprises Tanytarsini spp, Fissimentum sp, Pelomus sp and Goeldichironomus sp, like predominant taxa, may indicates mesotrophic conditions.

Keywords: benthos, Chironomidae, Limnology, bioindicator, water quality.

RESUMO

O objetivo deste trabalho foi verificar as respostas da comunidade de macroinvertebrados bentônicos a fatores ambientais ao longo de um reservatório tropical de cabeceira. As amostras foram coletadas com uma draga do tipo Van-Veen ao longo do reservatório nas regiões profunda e litorânea bem como na cabeceira, próximo à barragem e no meio do reservatório. Amostras foram coletadas tanto na estação seca quanto na estação chuvosa. Foram determinadas as concentrações de oxigênio dissolvido, condutividade elétrica, temperatura e pH próximos ao sedimento, in situ, em todas as estações amostrais com a utilização de um multisensor e disco de Secchi. Foram ainda determinadas as concentrações de fósforo e clorofila a da água para cálculo do índice de estado trófico. Com relação ao sedimento, foram determinados o teor de matéria orgânica, concentrações totais de fósforo e nitrogênio bem como a composição granulométrica. Para se verificar quais variáreis ambientais tiveram maior influência sobre a comunidade de macroinvertebrados bentônicos, uma análise de correspondência canônica (ACC) foi realizada. Foram registrados, ao todo, 28 táxons. Dentre estes, o grupo taxonômico com maior riqueza foi a família Chironomidae (Diptera) com 19 táxons. O estudo indicou que a comunidade de macroinvertebrados bentônicos respondeu às condições ambientais como disponibilidade de nutrientes e matéria orgânica, bem como às concentrações de oxigênio dissolvido. Assim sendo, os macroinvertebrados foram considerados bons indicadores da qualidade da água devido à sua sensibilidade frente às possíveis alterações ambientais supramencionadas. Chironomus sp, Limnodrilus hoffmeisteri e Branchiura sowerbyi formaram um grupo que pode ser considerado como bioindicador de condições eutróficas. Um segundo grupo pôde ser considerado como indicador de condições mesotróficas. A presença de dois ou mais membros deste grupo, que inclui os táxons Tanytarsini spp, Fissimentum sp, Pelomus sp e Goeldichironomus sp, como táxons dominantes, pode indicar tais condições.

Palavras-chave: bentos, Chironomidae, Limnologia, bioindicadores, qualidade da água.

Introduction

The water quality is a very important issue to the human life nowadays. Because of this, a wide variety of indicators have been employed to monitoring the water quality and the integrity of the aquatic ecosystems. There is not a unique indicator that may point to all the variations and impacts that a water body receives. Furthermore, variables like time, costs, skilled human resources, method's accuracy, extent of the answer, possibility of spatial and temporal identification and mainly what kind of disturbance is necessary to identify or to monitoring in the environment are factors that will determine which will be the more adequate indicator in each case.

The trophic state indices are usually the most used among the water quality indicators. The most traditional indices use phosphorus and chlorophyll concentrations in the water as its components (Carlson 1977, Lamparelli 2004). There are still those, among the biological ones, which show differentiated sensitivity to pollutants concentrations or other impacts such riparian forest suppression. The benthic macroinvertebrates are good examples of this as well as other organisms are as, for instance, the zooplankton (Brito et al. 2011) or fishes' communities (Terra & Araújo 2011). But, the first one, are better when the objective is to localize spatially the influence of the disturbance, due to their low mobility (Mandaville 2002), or is preferable when the goal is to measure the effects of impacts accumulation along the time as, for example, the nutrients or metals in the bottom (Arslan et al. 2010, Bettinetti et al. 2012).

The benthic macroinvertebrates are considered excellent bio-indicators because they can be found in most of the aquatic environments from temporary ponds to large rivers, lakes and deep reservoirs. Further, these animals present an elevated species richness. Since benthic macroinvertebrates, are mainly sedentary or has low mobility, the environmental disturbances can be easily localized. Furthermore, since they are in the sediment and have a long life cycle when compared to others bio-indicators like plankton organisms, the macroinvertebrates can indicate environmental conditions through the time providing long period recordings (Rosenberg 1998). Moreover, they are capable to react to both water column and sediment impacts which amplifies the response to environmental conditions spectrum, since the others indicators usually responses to one or another compartment (Carew et al. 2007).

Natural environmental conditions like sediment grain size, pH, temperature, currents, depth, oxygen as well as organisms interactions like predation, competition or food availability are relevant too and their influence will be according to the macroinvertebrates species populations multidimensional niches (Hutchinson 1965, Cowell & Rangel 2009) and so this influence must be considered in any environment that is being monitored by biological indicators.

Many works demonstrate that benthic macroinvertebrates community can also be altered in response to anthropogenic environmental changes, as land uses (Miserendino et al. 2011), riparian forest impacts and effluents loading (Baptista et al. 2007, Couceiro et al. 2007, Gamito & Furtado 2009, Sharma & Rawat 2009) and also by pollution by industrial effluents (Moreno & Callisto 2006). Several taxa from benthic macroinvertebrates community and a wide range of biological indexes and metrics have been widely employed as environmental indicators (Bode et al. 2002, Mandaville 2002, Fusari & Fonseca-Gessner 2006, Baptista et al. 2007, Baptista 2008, Angradi et al. 2009).

Our hypothesis is that the benthic macroinvertebrates communities' shows significative differences in abundance; distribution and composition when they are under diverging environmental conditions witch could be related to human impacts.

Moreover, there are few works that clearly demonstrates relationship between water and sediment environmental conditions and the benthic macroinvertebrates composition and distribution in the Neotropical region.

Hence, the aim of this work was to verify the responses of macroinvertebrates to environmental conditions and human impacts in a tropical reservoir. In that sense, the present research can provide tools for future studies and in monitoring or in restoring programs.

Materials and Methods

1. Study area

Itupararanga Reservoir is placed on Alto Sorocaba Basin (SP, Brazil), that corresponds to the main headwater of the left margin effluent of Tiete River (Figure 1).

The Itupararanga reservoir is located into an Environmental Preservation Area (EPA) created in 1998, with the main purpose to protect the water resources in the influenced area of the reservoir. More than 1/3 of the (EPA) is occupied by native vegetation fragments in a matrix of rural environment (Beu et al. 2011). The predominant vegetation can be classified as semideciduous forest (Almeida 2009). The EPA is located in the area of dense rainforests, but many of the original vegetation has been removed, and the majority of remaining plants are composed of secondary forest or pioneer formations (Almeida et al. 2011).

The region climate can be classified as Cwa according the Köppen classification. That classification is used to describe humid subtropical climates, with average temperatures in the warmest months of summer above 22 º C. With respect to precipitation, there is characteristically a cold, dry season and a warm rainy season. The average annual rainfall in the Basin region of Alto Sorocaba is 1493 mm. The wettest month is January when the average rainfall is 248 mm. August is the driest one and average rainfall of its month is 43 mm (Salles et al. 2008).

The high Sorocaba basin is surrounded mainly by small cities. Those cities usually have the agriculture as their major economic resource (vegetable farming). Despite the forming rivers (Sorocabuçu, Sorocamirim and Una) of the reservoir drain peripheral regions of the Metropolitan Region of São Paulo, where a disordering marginal occupation is observed in almost every cities. The domestic effluents treatment is incipient and, as a consequence, sewage is discharged "in natura" in the forming rivers (Salles et al. 2008, Beu et al. 2011).

There are multiple uses for the water stored by that rivers damming. The main uses are energy supply for a large industry and the water supply for four cities (Votorantim, 2012) providing 85% of the treated water consumed by the city of Sorocaba that has approximately 600,000 habitants. Therefore, the water supply from this reservoir is given to about 850,000 people. In addition, this water body plays an important hydraulic regulatory role to Sorocaba River water, which crosses the metropolitan area of the city of Sorocaba.

The area of Itupararanga Reservoir is about 29.49 km² and its maximum capacity of water reaches 355 × 10⁶ L of water. Its water is also used to some other activities like irrigation, recreation area and fishing (Beu et al. 2011).

2. Collection and identification

The samplings were taken in three distinct zones of the reservoir (Table 1) which were chosen in order to obtain samples longitudinally along the reservoir. The first zone was near the headwater of the reservoir where there is higher turbulence, the edges are near each other and this is the closest region of the former rivers which receives many sewage discharges. The second was in the middle and can be considered as a transitional region and the last samples were taken close to the dam, far away from the impacted rivers and it is lentic as the middle region (Figure 2). The material was sampled twice: one profundal and another littoral in order to detect different degrees of terrestrial environment impact in the communities. All samplings were taken in December 2009 and in February 2010 (wet season) and in June and in August 2010 (dry season) during the day.

The measurements of water pH, dissolved oxygen content, temperature and electric conductance were performed in situ, near the sediment until 15m depth by using an YSI 556 model multiprobe. The water transparency was measured by a Secchi disk and the photic zone extension was calculated multiplying the disk lecture value by 2.27 (Padial & Tomaz 2008).

In order to calculate the trophic state index (TSI) of Carlson (1977) modified by Lamparelli (2004) (Table 2), the samplings taken in three reservoir zones in the central region near the surface to determine the total phosphorus (4500B (item 5) American... 2005) and chlorophyll a (Nush 1980).

At each sample point, it was collected sediment samplings in order to determine the granulometric composition (Camargo et al. 2009), phosphorus (Andersen 1976) and nitrogen concentrations (4500 N_OrgC; American... 2005), and organic matter proportion (Wetzel & Likens 2000).

The macroinvertebrates were collected with a Van Veen grab (0.045 m² sampling area); at each point three sampling units were taken, performing cumulative samples. The samplings were washed over a 212µm pore opening web, sorted and identified usually until genera or species level. The Chironomidae larvae were identified to genera level, because for species safe identification it is necessary to examine larva, pupa and imago and in the present work it was possible to take only larvae. The Tanytarsini tribe was not identified beyond the tribe level because the safe differentiation between Caladomyia and Tanytarsus requires the last instars larvae and most of them was first or second instars larvae. It was reached the species or genera level for Oligochaeta. The morphospecies concept was used to low representative taxa when the identification at genera level was not possible. The identification was performed in the laboratory by using stereomicroscope and optic microscope and it was also used the following identification keys and manuals: Brinkhurst (1971), Saether (1980), Brinkhurst & Gelder (2001), Hilsenhoff (2001), Pinho (2008), Epler (2011), Trivinho-Strixino (2011).

3. Data analysis

The total density per sampling was calculated by dividing the number of specimens sampled by the total sampled area at each point, resulting in the number of organisms per m².

Additionally, a matrix of Correspondence Canonical Analysis among the environmental variables and the density logarithm of the main taxa – considering only the taxa that had abundance higher than 10% in at least one sampling and frequency of, at least 30% – were performed and so, the variables that presented significant correlation with at least one of the analyzed taxa were selected to the Canonical Correlation Analysis (CCA).

The following variables had correlations with greater number of taxa: sediment phosphorus (six taxa) and nitrogen (five taxa); dissolved oxygen (five taxa) and organic matter in the sediment (four taxa). Depth, pH and sediment grain size also had some correlations but, in these cases with less than three taxa. The other environmental variables were omitted once that them had not shown any correlation with the main taxa.

The CCA significance was verified by a permutation test (1,000 permutations). After that, the groups and the main environmental variables that differentiate each one were identified. The softwares Multi Variate Statistical Package 3.12 (Kovach... 2001); Bioestat 5.0 (Ayres 2007) and Past 2.01 (Hammer et al. 2001) were employed to perform that analysis.

Two UPGMA (Unweighted pair-group average) cluster analysis, one for wet season and other for dry season, with binary data and a two-way ANOVA (similarity analysis) considering all samplings were performed in order to verify the spatial heterogeneity of the community based on species composition.

Results

According to the calculated TSI, Itupararanga Reservoir can be classified as meso – eutrophic water body. In general, the headwater of reservoir can be considered eutrophic, whereas the middle and dam are mesotrophic zones (Table 3). The mean water temperature during the wet season was 6.82º higher than during the dry season, the pH was usually neutral in both but higher during the dry season (Table 4). The electric conductivity can be considered intermediate and it was not recorded considerable variations between the seasons (Table 4). The oxygen concentrations were low and had great variation considering the spatial heterogeneity; the lowest values were recorded near the rivers entrance and in the profundal regions (Table 4).

The sediment nutrients concentrations were higher during the wet season. Average granulometric composition shows predominance of the finest grains in the sediment but, with great amplitude considering it was taken littoral and profundal samplings. The organic matter content remained similar in both seasons (Table 5).

A total of 2087 individuals were collected, belonging to 28 taxa (Tables 6 and 7). Densities varied from zero to 2963 ind.m^–2 for sampling. The mean density was 704 ind.m^–2 with a standard deviation of 756 including all samples. The recorded taxa number by period were 13, 12, 20 and 16 taxa, in December 2009, February 2010 (wet season), June and August 2010 (dry season), respectively. During the wet season 17 taxa were recorded, in contrast to the 25 taxa collected during the dry one.

The Tubificinae (Oligochaeta, Naididae) and Chironomidae (Diptera) were the most abundant taxonomic groups and was present in every sampling period and along all reservoir. The Tubificinae here is represented by four taxa: Branchiura sowerbyi Beddard; Bothrioneurum sp; Limnodrilus hoffmeisteri Brinkhurst; Peloscolex sp and one non identified taxa named here as Tubificinae sp1.When considering all reservoir, it was the more abundant taxa during the wet season and the Chironomidae, represented by 19 taxa, was the most abundant during the dry one.

The abundance was concentrated in the headwater during the wet season, while this distribution was more heterogenic during the dry one. The family Chaoboridae (Diptera) was also an abundant taxonomic group (Figure 3; Tables 6 and 7).

Ablabesmyia sp, Corynoneura sp, Cricotopus sp and Nilothauma sp. were found only in dry period on the other hand, 13 taxa were found only in wet period (Tables 6 and 7).

The CCA results indicate that water variables as dissolved oxygen and pH, as well as sediment variables as total nitrogen and phosphorus, organic matter content and granulometric composition may explain the high variation (p < 0.0001 and canonical R = 0.9968) in the distribution, abundance and structure of the benthic macroinvertebrates community (Table 8). Additionally, through CCA values, benthic macroinvertebrates could be separated in three groups compromising different taxa which are influenced by specific environmental conditions (Figure 4). Group I includes taxa which present tolerance to high sediment nutrient concentrations, as well as to lower dissolved oxygen water availability. Group II displays a higher heterogeneity and seems to be less tolerant to water hypoxia and more tolerant to low phosphorus, nitrogen and organic matter concentrations in the sediment. Group III correspond to the genera Chaoborus sp and Procladius sp. Only the first taxa showed significant correlation with the variables that were considered. Chaoborus sp was related to higher organic matter content in the sediment and to a higher proportion of fine granulometric fractions.

The spatial heterogeneity analyzes indicate that this occurs both transversely (littoral and profundal) and longitudinally (Figure 5). The p value for the ANOSIM was 0.049 for heterogeneity in the transverse direction and 0.009 for heterogeneity longitudinal sense.

Discussion

Some researches (Pamplin et al. 2006, Carew et al. 2007, Jorcin & Nogueira 2008, Buss & Vitorino 2010, Cortelezzi et al. 2011, Miserendino et al. 2011) have improved the knowledge of the bio-indicator potential of the benthic macroinvertebrates.

Carew et al. (2007) analyzed the response of Chironomidae taxa indicators to pollution, especially in the sediment. These authors identified taxa Riethia stictoptera Kieffer, Tanytarsus inextentus Skuse, Coelopynia, and Chironomus februarius Martin as potential low anthrophic pressure environment bio-indicators and Chironomus duplex Walter species as a high sediment pollution condition indicator.

In this study, Tubificinae and Chironomidae were the predominant taxa during both seasons reaching 66 and 29%, respectively, of the total organisms sampled during the wet season, and 35 and 40% during the dry one. Other studies suggest that these two groups, as well as most of macrobenthic components in lentic environments (including reservoirs) have some predominance variation due to both environmental conditions and historical factors (Callisto et al. 2005, Pamplin et al. 2006, Lucca et al. 2010).

The richness observed in Itupararanga Reservoir, which has eutrophic and mesotrophic conditions, suffering human impacts especially in the headwater, can be considered intermediate when compared with that described to other lentic environments in Neotropical Regions. Lucca et al. (2010) analyzed the benthic macroinvertebrates communities in an oligotrophic lake and recorded 23 taxa. Fusari & Fonseca-Gessner (2006) reported 20 and 34 taxa in an eutrophic and an oligotrophic reservoir, respectively. In the present study, we have recorded 19 Chironomidae among the 27 taxa identified. The major importance of that taxonomic group for the total richness may be understood as a standard for benthic macroinvertebrates when lentic environments or reservoirs are analyzed (Callisto et al. 2005, Fusari & Fonseca-Guessner 2006, Pamplin et al. 2006, Shostell & Williams 2007, Jorcin & Nogueira 2008, Lucca et al. 2010).

The benthic macroinvertebrates respond quickly and locally to the disturbances by changing the structure and the composition of the community, as well as altering the taxa distribution (Mandaville 2002). The abiotic analyses provided evidences that Itupararanga Reservoir is a heterogenic water body and that many relevant differences could be noticed. Because of this heterogeneity the reservoir can be analyzed as having at least three distinct areas as evidenced by ANOSIM and UPGMA analyses when considered together. The riverine (entrance) zone is evidenced as the most differing one in a longitudinal sense while in a transversal sense the heterogeneity is more pronounced in the middle of the reservoir and near the dam where the margins are farther each other.

In general, we could identify an eutrophicated zone that comprises the headwater profundal and littoral regions; a mesotrophic littoral one which comprises the middle and the near the dam areas in the littoral regions and a mesotrophic profundal zone with the profundal regions of the middle and near the dam areas.

In the present study, a significant correlation among environmental factors with the abundance and the distribution of the main taxa that formed the benthic macroinvertebrates communities of Itupararanga Reservoir was observed. These taxa can be divided into three groups according to their relationship with environmental factors. Group I has been formed by L. hoffmeisteri, Chironomus sp and B. sowerbyi; this group acts as an eutrophication bioindicator. L. hoffmeisteri is considered the Oligochaeta species that is the most tolerant to pollution according to Verdonschot (1989). High densities of them followed by the decrease of the diversity of other taxa may be seen as an organic enrichment indicator to continental water bodies (Dornfeld et al. 2006, Martins et al. 2008). In the same way, some studies pointed out the Chironomus genera as one of the most resistant benthic organisms to organic pollution (Adriansens et al. 2004, Simião-Ferreira et al. 2009). B. sowerbyi was reported in impacted environments (Suriani et al. 2007).

The relevant abundance of these organisms can be associated to high trophic level environmental conditions such as sediment nutrients accumulation and low dissolved oxygen concentrations in the water. This group has been recorded as predominant only in the headwater zone where it was present in every sampling. This zone was the only classified as eutrophic by TSI. Therefore, this data suggests that the group I is characteristic of impacted areas, then reflecting eutrophication of water and sediment.

Group II is a more diverse one. It comprises the Chironomidae Fissimentum sp, Goeldichironomus sp, Pelomus sp, Saetheria sp and Tanytarsini spp. The distribution of these animals is related to water conditions as well to the sediment. There is some preference for high oxygenated waters and low nutrient and organic matter content in the sediment. These organisms are also related to less clay and silt proportion in the sediment. Altogether, these conditions suggest that these organisms are indicators of oligo or mesotrophic environments, since nutrients or organic matter accumulation is not observed in littoral areas of the samples taken in the middle or near the dam zones. Group II organisms were recorded in mesotrophic littoraneous areas with, at least, two members in the same sample dominating the community. In general Tanytarsini spp. or Goeldichironomus sp. In contrast, this group are almost absent in the eutrophicated headwater – even in the deep or littoral region – and, when some group II member was recorded, it appears isolated from the other taxa that characterizes its group and never as predominant taxon. Moreover, the results point out that there are some more equitative taxa distributions, corroborating that metrics like richness or indexes like dominance and diversity may be considered as environmental quality indicators.

Finally, Group III is composed by Chaoborus sp and Procladius sp. While Chaoborus sp presented a significant correlation with sediment variables (higher organic matter content and finer sediments), it was not observed to Procladius sp. Considering that both taxa belong to the trophic guild of the predators, it can be suggested that prey availability, as well as the presence of the predators, regulate the distribution of these organisms that have migratory ability and a varied diet. Chaoborus sp eats mainly planktonic organisms and usually migrates daily in the water column (Castilho-Noll & Arcifa 2007) while Procladius sp eats as benthic organisms as rotifers, ostracods and cladocerans (Vodopich & Cowell 1984). Despite of the fact that these taxa were mainly recorded in mesotrophic areas, the groups have only two members and one of them was recorded in the eutrophicated headwater area too. So, it is more plausible that the main environmental factors that influenced their predominance were the depth and oxygen availability. So, this group can be considered more like a profundal specialists group that an indicator of other environmental conditions.

Pamplin et al. (2006), studying the benthic macroinvertebrates of Tropical Reservoir, Americana, SP, Brazil, observed that there was a strong correlation among fine sediment fractions (silt and clay) and high organic matter contents with Chironomus decorus Johansen and Limnodrilus hoffmeisteri. These results are different of that obtained in Itupararanga Reservoir. The Itupararanga Reservoir's data show also L. hoffmeisteri from group I associated with sediment granulometric composition but, here, the association is with sand fractions while the results from Pamplin et al. (2006) shown association of Chironomus sp and L. hoffmeisteri with the finest sediment fractions.

Some hypotheses can be considered when comparing these results: firstly, in Itupararanga Reservoir, sediment nitrogen and phosphorus concentrations were included in the analysis whereas in Americana Reservoir they were not included. So, it is plausible that when the sediment's nutrients are considered, the relative importance of the sediment granulometry loses some importance.

Another fact that must be mentioned is that in the present study, the L. hoffmeisteri group is composed in association with Chironomus sp and B. sowerbyi but in the Pamplin et al. (2006) research, the L. hoffmeisteri is associated with more three different taxa and B. sowerbyi is in another group, indicating that the communities structures are someway different.

On the other hand, Chironomus sp and L. hoffmeisteri were correlated in both reservoirs with high organic matter content and low oxygen conditions corroborating the hypothesis that these organisms are good indicators for these conditions, which usually are influenced by human activities.

Moreover, these authors demonstrated that other important factors that can influence macroinvertebrate composition and distribution are the depth and sand proportion in the sediments. The high density from the group I species is generally correlated to the water eutrophication (Martins et al. 2008, Simião-Ferreira et al. 2009).

Shostell & Williams (2007) analyzed the benthic macroinvertebrates community patterns in relation to the physical and chemical parameters in a shallow eutrophic reservoir (Lake Conway, AR, USA). In this study, spatial and seasonal variations in biomass, diversity and organisms' abundance were observed and the explanation was the proximity to the land environment corroborating with the Itupararanga Reservoir's data when considering the transversal heterogeneity separating communities from littoral and profundal regions as evidenced by CCA analysis.

In sum, this research demonstrated the influence of the environmental factors over the benthic macroinvertebrates community of Itupararanga Reservoir. Some of these factors (e.g., nutrient concentrations, organic matter content or the oxygen concentrations) may be greatly influenced by human activities. Therefore, anthropogenic actions can alter indirectly the composition and distribution of those organisms. The results provide strong evidences that groups I and II can be used as biological indicators. The record of the entire group is a more feasible indicator than analyzing only one member studied separately. However, it must be also emphasized the influence of some other non-anthropogenic impacts on benthic macroinvertebrates distributions, such as depth and mineral grains size of the sediment are. As a consequence, environmental peculiarities must be considered to perform a study with monitoring.

Acknowledgements

The authors thank CAPES (Federal Agency of Support and Evaluation of Postgraduate Education) and FAPESP (Sao Paulo Research Foundation) for funding this research (process number 08/55636-9).We are grateful to Drs. Odete Rocha, Luiz Carlos de Pinho, Maurício Cetra, Susana Trivinho-Strixino and Mônica Jones Costa for comments and suggestions done during the development of this research.

Received 29/03/2012

Revised 03/12/2012

Accepted 04/12/2012

• ADRIANSENS, V., SIMONS, F., NGUYEN, L.T.H., GODDEERIS, B., GOETHALS, P.L.M. & DE PAUW, N. 2004. Potential of bio-indication of chironomid communities for assessment of running water quality in Flanders (Belgium). Belg. J. Zool. 134:31-40.
• ALMEIDA, V.P. 2009. Análise dendrológica de espécies arbóreas tropicais presentes em fragmento de floresta estacional semidecidual. In Seminário da Área de Proteção Ambiental de Itupararanga (S.E. Beu, coord.). Fundação Florestal, Ibiúna.
• ALMEIDA, V.P., CARVALHO, R.B. & CATHARINO, E.L.M. 2011. Flora. In Biodiversidade na APA de Itupararanga (S.B. Beu, A.C.A. dos Santos, & S.A. Casali, orgs.). SMA/FF/UFSCar, CCR, Via Oeste, p.72-77.
• AMERICAN PUBLIC HEALTH ASSOCIATION APHA. 2005. Standard Methods for Examination of Water and Wastewater. 25th ed. Washington.
• ANDERSEN, J.M. 1976. An ignition method for determination of total phosphorus in lake sediments. Water Res. 10:329-331. http://dx.doi.org/10.1016/0043-1354(76)90175-5
• ANGRADI, T.R., PEARSON, M.S., BOLGRIEN, D.W., JICHA, T.M., TAYLOR, B.H, & HILL, D.L. 2009. Multimetric macroinvertebrate indices for mid-continent US great rivers. J. N. Am. Benthol. Soc. 28:785-804. PMid:20623086. http://dx.doi.org/10.1899/09-003.1
• ARSLAN, N., KOÇ1, B. & ÇIÇEK, A. 2010. Metal Contents in Water, Sediment, and Oligochaeta-Chironomidae of Lake Uluabat, a Ramsar Site of Turkey. ScientificWorldJournal. 10:1269-1281. http://dx.doi.org/10.1100/tsw.2010.117
• AYRES, M, 2007. Bioestat: Aplicações estatísticas nas áreas das ciências bio-médicas. Belém, Brasil.
• BAPTISTA, D.F, 2008. Uso de macroinvertebrados em procedimentos de biomonitoramento em ecosistemas aquáticos. Oecol. Bras. 12:425-441.
• BAPTISTA, D.F., BUSS, D.F., EGLER, M., GIOVANELLI, A., SILVEIRA, M.P. & NESSIMIAN, J.L. 2007. A multimetric index based on benthic macroinvertebrates for evaluation of Atlantic Forest streams at Rio de Janeiro State, Brazil. Hydrobiologia. 575:83-94. http://dx.doi.org/10.1007/s10750-006-0286-x
• BETTINETTI, R., PONTI, B., MARZIALI, R. & ROSSARO, P., 2012. Biomonitoring of lake sediments using benthic macroinvertebrates. Trends Anal. Chem. 36:92-102. http://dx.doi.org/10.1016/j.trac.2011.12.008
• BEU, S.E., DOS SANTOS, A.C.A. & CASALI, S.A. 2011. Biodiversidade na APA Itupararanga: Condições Atuais e Perspectivas Futuras. SMA, UFSCAR/FF/CCR, São Carlos, 152p. PMCid:3008738.
• BODE, W.P., NOVAK, M.A., ABELE, L.E., HEITZMAN, D.L. & SMITH, A.J. 2002. Quality assurance work plan for biological stream monitoring in New York State. Stream Biomonitoring Unit Bureau of Water Assessment and Management Division of Water NYS Department of Environmental Conservation, Albany.
• BRINKHURST, R.O. 1971. A guide for identification of British aquatic oligochaeta. 2nd ed. University of Toronto. Scientific publication no 22.
• BRINKHURST, R.O. & GELDER, S.R. 2001. Annelida: Oligochaeta including Branchiobidellidae. In (J.H. Thorp & A.P. Covich). Orlando, p.431-463.
• BRITO, S.L., MAIA-BARBOSA, P.M., PINTO-COELHO, R.M. 2011. Zooplankton as an indicator of trophic conditions in two large reservoirs in Brazil. Lake Reservior Manage. 16:253-264. http://dx.doi.org/10.1111/j.1440-1770.2011.00484.x
• BUSS, D.F. & VITORINO, A.S. 2010. Rapid Bioassessment Protocols using benthic macroinvertebrates in Brazil: evaluation of taxonomic sufficiency. J. N. Am. Benthol. Soc. 29:562-571. http://dx.doi.org/10.1899/09-095.1
• CALLISTO, M., GOULART, M., BARBOSA, F.A.R. & ROCHA, O. 2005, Biodiversity assessment of benthic macroinvertebrates along a reservoir cascade in the Lower São Francisco River (Northeastern Brazil). Braz. J. Biol. 65:229-240. PMid:16097725. http://dx.doi.org/10.1590/S1519-69842005000200006
• CAMARGO, O.A., MONIZ, A.C., JORGE, J.A. & VALADARES, J.M.A.S. 2009. Métodos de Análise Química, Mineralógica e Física de Solos do Instituto Agronômico de Campinas. Instituto Agronômico, Campinas.
• CARLSON, R.E. 1977. A trophic state index for lakes. Limnol. And Oceanogr. 22:361-369. http://dx.doi.org/10.4319/lo.1977.22.2.0361
• CASTILHO-NOLL, M.S.M. & ARCIFA, M.S. 2007. Chaoborus diet in a tropical lake and predation of microcrustaceans in laboratory experiments. Acta Limnol. Bras. 19:163-174.
• CAREW, M.E., PETTIGROVE, V., COX, R.L., & HOFFMANN, A.A. 2007. The response of Chironomidae to sediment pollution and other environmental characteristics in urban wetlands. Freshwater Biol. 52:2444-2462. http://dx.doi.org/10.1111/j.1365-2427.2007.01840.x
• CORTELEZZI, A., PAGGI, A.C., RODRÍGUEZ, M. & CAPÍTULO, M. 2011. Taxonomic and nontaxonomic responses to ecological changes in an urban lowland stream through the use of Chironomidae (Diptera) larvae. Sci. Total Environ. 409:1344-1350. PMid:21276601. http://dx.doi.org/10.1016/j.scitotenv.2011.01.002
• COUCEIRO, S.R.M., HAMADA, N., LUZ, S.L.B., FORSBERG, B.R. & PIMENTEL, T.P. 2007. Deforestation and sewage effects on aquatic macroinvertebrates in urban streams in manaus, amazonas, brazil. Hydrobiologia. 575:271-284. http://dx.doi.org/10.1007/s10750-006-0373-z
• COWELL, R.K. & RANGEL, T.F. 2009. Hutchinson's duality: the once and future niche. PNAS (Early Edition): 1-8.
• DORNFELD, C.B., ALVES, R.G., LEITE, M.A. & ESPÍNDOLA, E.L.G. 2006. Oligochaeta in eutrophic reservoir: the case of Salto Grande reservoir and their main affluent (Americana, São Paulo, Brazil). Acta Limnol. Bras. 18:189-197.
• EPLER, J.H. 2011. Identification manual for the larval chironomidae (Diptera) of North and South Carolina. North Carolina Department of Environment and Natural Resources.
• FUSARI, L.M. & FONSECA-GESSNER, A.A. 2006.Environmental assessment of two small reservoirs in southeastern Brazil, using macroinvertebrate community metrics. Acta Limnol. Bras. 18:89-99.
• GAMITO, S. & FURTADO, R. 2009. Feeding diversity in macroinvertebrate communities: A contribution to estimate the ecological status in shallow waters. Ecol. Indic. 9:1009-1019. http://dx.doi.org/10.1016/j.ecolind.2008.11.012
• HAMMER, Ø., HARPER, D.A.T. & RYAN, P.D. 2001. PAST Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4(1):1-9.
• HUTCHINSON, G.E., 1965. The niche: An abstractly inhabited hyper-volume, in: The Ecological Theatre and the Evolutionary Play. Yale University Press, New Haven, p.26-78.
• HILSENHOFF, W.L. 2001. Diversity and classification of insects and collembola. In Ecology and Classification of North American Freshwater Invertebrates (J.P. Thorp & A.P. Covich). Academic Press, Fort Colins, p.661-731.
• JORCIN, A. & NOGUEIRA, M.G. 2008. Benthic macroinvertebrates in the Paranapanema reservoir cascade (southeast Brazil). Braz. J. Biol. 68:1013-1024. PMid:19197472. http://dx.doi.org/10.1590/S1519-69842008000500009
• KOVACH COMPUTER SERVICES. 2001. Multi Variate Statistical Package 3.12.
• LAMPARELLI, M.C. 2004. Grau de trofia em corpos d'água do Estado de São Paulo: avaliação dos métodos de monitoramento. Tese de doutorado, Instituto de Biociências da Universidade de São Paulo, 238p.
• LUCCA, J.V., PAMPLIN, P.A.Z., FONSECA-GESSNER, A., TRIVINHO-STRIXINO, S., SPADANO-ALBUQUERQUE, A.L. & ROCHA, O. 2010. Benthic macroinvertebrates of a tropical lake: Lake Caçó, MA, Brazil. Braz. J. Biol. 70:593-600. http://dx.doi.org/10.1590/S1519-69842010000300016
• MANDAVILLE, S.M. 2002. Benthic macroinvertebrates in freshwaters taxa tolerance values, metrics and protocols. (Project H-1) Soil; water conservation society of Metro Halifax.
• MARTINS, R.T., STEPHAN, N.N.C & ALVES, R.G. 2008. Tubificidae (Annelida:Oligochaeta) as indicator of water quality in an urban stream in southeast Brazil. Acta Limnol. Brazil. 20:221-226.
• MISERENDINO, M.L., CASAUX, R., ARCHANGELSKY, M., DI PRINZIO, C.Y., BRAND, C. & KUTSCHKER, A.M. 2011. Assessing land-use effects on water quality, in-stream habitat, riparian ecosystems and biodiversity in Patagonian northwest streams. Sci. Total Environ. 409:612-624. http://dx.doi.org/10.1016/j.scitotenv.2010.10.034
• MORENO, P. & CALLISTO, M. 2006. Benthic macroinvertebrates in the watershed of an urban reservoir in southeastern Brazil. Hydrobiologia. 560:311-321, 2006. http://dx.doi.org/10.1007/s10750-005-0869-y
• NUSH, E. 1980, Comparison of differents methods for chlorophilla and phaeropigments determination. Arch. Hydrobiol. 4:14-36.
• PADIAL, A.A. & THOMAZ, S.M. 2008. Prediction of the light attenuation coefficient through the Secchi disk depth: empirical modeling in two large Neotropical ecosystems. Limnology. 9:143-151. http://dx.doi.org/10.1007/s10201-008-0246-4
• PAMPLIN, P.A.Z., ALMEIDA, T.C.M. & ROCHA, O. 2006. Composition and distribution of benthic macroinvertebrates in Americana Reservoir (SP, Brazil). Acta Limnol. Bras. 18:121-132.
• PINHO, L.C. 2008, Diptera. In Guia on-line: Identificação de larvas de Insetos Aquáticos do Estado de São Paulo (C.G. Froehlich, org.). http://sites.ffclrp.usp.br/aguadoce/guiaonline (último acesso em 11/01/2012).
• ROSENBERG, D.M. 1998. A National Aquatic Ecosystem Health Program for Canada: We should go against the flow. Bull. Entomol. Soc. Can. 30:144-152.
• SAETHER, O.A. 1980. Glossary of chironomid morphology terminology (Diptera, Chironomidae). Entomologica Scandinavica. Supplement no 14. Sweden: Borgströms Tryckeri AB.
• SALLES, M.H.D., CONCEIÇÃO, F.T., ANGELUCCI, V.A., SIA, R., PEDRAZZI, F.J.M. CARRA, T.A., MONTEIRO, G., SARDINHA, D.S. & NAVARRO, G.R.B. 2008. Avaliação simplificada de impactos ambientais na Bacia do Alto Sorocaba (SP). Rev. Estud. Ambient. 10(1):6-20.
• SIMIÃO-FERREIRA, J., DEMARCO JUNIOR, P., MAZÃO, G.R. & CARVALHO, A.R. 2009. Chironomidae community structure in relation to organic enrichment of an aquatic environment. Neotrop. Entomol. 38:464-471. http://dx.doi.org/10.1590/S1519-566X2009000400004
• SHARMA, R.C. & RAWAT, J.S. 2009. Monitoring of aquatic macroinvertebrates as bioindicator for assessing the health of wetlands: A case study in the Central Himalayas, India. Ecol. Indic. 9:118-128. http://dx.doi.org/10.1016/j.ecolind.2008.02.004
• SHOSTELL, J.M. & WILLIAMS, B.S. 2007. Habitat complexity as a determinate of benthic macroinvertebrate community structure in cypress tree reservoirs. Hydrobiologia. 575:389-399. http://dx.doi.org/10.1007/s10750-006-0385-8
• SURIANI, A.L., FRANÇA, R.S., PAMPLIN, P.A.Z., MARCHESE, M., LUCCA, J.V. & ROCHA, O. 2007. Species richness and distribution of oligochaetes in six reservoirs on Middle and Low Tietê River (SP, Brazil). Acta Limnol. Bras. 19:415-426.
• TERRA, B.F., ARAÚJO, F.G. 2011. A preliminary fish assemblage index for a transitional riverreservoir system in southeastern Brazil. Ecol. Indic. 11:874-881. http://dx.doi.org/10.1016/j.ecolind.2010.11.006
• TRIVINHO-STRIXINO, S. 2011. Larvas de Chironomidae: guia de identificação. Universidade Federal de São Carlos, São Carlos.
• VERDONSCHOT, P.F.M. 1989. The role of oligochaetes in the management of waters. Hydrobiologia. 180:213-227. http://dx.doi.org/10.1007/BF00027554
• VODOPICH, D.S. & COWELL, B.C. 1984. Interaction of factors governing the distributioin of a predatory aquatic insect. Ecology. 65:39-52. http://dx.doi.org/10.2307/1939456
• VOTORANRIM. Secretaria do Meio Ambiente - SEMA. Represa de Itupararanga. http://www.votorantim.sp.gov.br/pmv/arq/sema/bancodedados/represadeitupararanga.doc (último acesso em 11/01/2012.
• WETZEL, R.G. & LIKENS, G.E. 2000, Limnological analyses. New York: Springer Science+Business Media, Inc.

Publication Dates

• Publication in this collection
  01 Feb 2013
• Date of issue
  Dec 2012

History

• Received
  29 Mar 2012
• Accepted
  04 Dec 2012
• Reviewed
  03 Dec 2012