Australian Journal of Basic and Applied Sciences, 7(8): 991-1003, 2013 ISSN 1991-8178

Lotic Meiofauna Communities as Bioindicators of Aquatic Pollution in the State Park, Minas Gerais State, Brazil
1,2

Juliana R. de Meira, 1Filipe R. Moura and 1Andr R.S. Garraffoni

Laboratory of Zoology, Department of Biological Sciences, Federal University of the Jequitinhonha and Mucuri Campus JK, highway BR-367, CEP: 39100-000, Diamantina, MG, Brazil. 2 Graduate Program in vegetable production.
Abstract: Aim: This study aims to evaluate the quality of water based on physical-chemical conditions and in the zoobenthos assemblages in a stream called gua Limpa, located in the Biribi State Park, Diamantina-MG. Method: On a stream of about 4 km, it was chosen four collect points, in that the variable physico-chemical and microbiological parameters. The characterization in the different sampling points was conducted in accordance with the limits established by CONAMA Resolution 357 of March 17, 2005. For the collection of aquatic organisms, each of the four points was sampled in three subareas replicated at three different points, totalizing 144 samples. Two collections were carried out in the wet season - March 2009 - and two in dry season - in August 2009. The zoobenthos organisms were sorted and identified with the aid of optical microscope in the lowest possible taxonomic level. The differences in mean values of the physical, chemical and microbiological and zoobenthonics organisms obtained between points and sampling dates were statistically tested using analysis of variance (ANOVA).When ANOVA showed significant differences at 5%, Tukey test was applied. Results: It was noted that points 1, 2 and 3 are presented as similar to physical-chemical conditions, however, as fecal coliforms, only the point 1 framed within the limits allowed. The most significant taxa such points were Ephemeroptera, Plecoptera and Trichoptera, which are more demanding about the environmental quality. But point 4 stood out with high average fecal coliform, phosphorus and turbidity and low dissolved oxygen in water. Conclusion: Points 4 have contributed to the quality decline of stream water and exacerbate eutrophication processes, species extinction and propagation of aquatic diseases. The zoobenthos assemblages were effective to indicate levels of pollution occurring in the studied stretch and subsidize future studies of biomonitoring. Key words: water quality, environmental bioindicator, water pollution, zoobenthos. INTRODUCTION

An accurate prediction of antropogenic impacts in the environment would be achieved with an a priori census of a proposed human development plus a detailed knowledge of the ecological system and a clear understanding of both interactions (Kennedy and Jacoby, 1999). In an ecological system the distribution and abundance of organisms are influenced by biogeographical factors and environmental characteristics, such as, sediment type, organic matter content, depth, physical and chemical water variables, and presence or not of macrophytes (Carvalho and Uieda 2004; Smith et al., 2003; Vidal-Abarca et al., 2004). Thus, the relationship between environmental monitoring and benthic organisms occur due to the important role that they play in the regeneration of nutrients and energy transfer in the food webs. Zooenthonic organisms have generalist diet that affect the population growth rates of bacteria and fungi involved in the remineralization of nutrients and convert them to a form usable by higher trophic levels. Besides, as the water availability depends on the degree of contamination, it will be only possible to estimate its total amount if reliable monitoring networks show success in generating data about this resource (Buss et al., 2003; Knig et al., 2008). Thus, those organisms have been used in the evaluation of anthropic impacts as biological indicators of water quality due to represent number of distinct species; they can be found in practically all kinds of aquatic environments; they have slow movements in the sediments; they can be used in experimental manipulations (Bicudo and Bicudo, 2004). The term Meiofauna was coined by Mare (1942) to characterize the metazoan associated with sediment that pass through a 0.5 sieve but are retained on 0.042 sieve. This size range separates group of organism whose morphology, feeding and life history have evolved to exploit the interstial sediments (Kennedy & Jacoby, 1999). Meiofauna organisms occurs in freshwater and marine habitats, from intertidal to deep oceans or from small stream to large rivers and lagoon (Vincx, 1996; Coull, 1988). Despite this functional definition, the taxa
Corresponding Author: Juliana R. de Meira, Laboratory of Zoology, Department of Biological Sciences, Federal University of the Jequitinhonha and Mucuri Campus JK , highway BR-367, CEP: 39100-000, Diamantina, MG, Brazil. E-mail: ju_demeira@yahoo.com.br.

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included in the meiofauna do not represent a homogeneous ecological group, because the great number of distinct microhabitats that held to different local adaptation. Besides, the total number of individuals that present in meiofauna is extremely high (on average, 1-10 million individuals in 1m2 of sediment), although the biomass is only a few grams (Vincx, 1996). From the taxonomic point of view, more than 20 higher taxon of 33 metazoan phyla have some meiobenthonic representatives, and over 10 (p. ex. Gastrotricha, Rotifera, Gnathostomulida, Kinorhyncha, Loricifera, and Tardigrada) are exclusive of this environment (Vincx, 1996; Higgins & Thiel, 1988). Studies that aimed study the biology and ecology of meiofauna organisms initiated to be routinely from the decade 70, and the main interest of these studies was understand the effects of pollution on the community, and the possible use of the meiofauna as tool to better understand the human impacts on aquatic environment caused by different sources. That deflection happens due to the fact of meiofauna organisms play several parts in benthic ecosystem of continental waters, such as food for juvenile and fish larvae and higher trophic levels, facilitation of biomineralization of organic matter and nutrient regeneration (Hicks and Coull, 1983; Fleeger, 1985; Coull, 1988; 1999). Due to great abundance, short life cycle and holobenthic, the intimate association with the sediment and great sensibility to entrance of anthropogenic material, the meiofauna is becoming a very useful tool for biomonitoring studies in aquatic ecosystems (Murolo, 2005). However, most ecological studies on meiofauna in biomonitoring studies have been performed in marine environment (Vincx, 1996; Coull, 1988). In order to associate the biomonitoring with physical-chemical and microbiological analysis to evaluate the distinct impact levels suffered by aquatic ecosystems in Biribiri State Park, this study aimed to: (a) assess the meiofauna fauna of gua Limpa Stream; (b) investigate the possible influence of physical-chemical and microbiological conditions of water from this stream on those meiofunal organism. The results of this research can prove a cohesive discussion of the future use of biomonitoring using lotic meiofauna as a mechanism for improving public health in Brazil. MATERIAL AND METHODS Study Site and Sampling Design: The Biribiri State Park was created by the State Decree # 39.909 of September 22, 1998 and supplies protection to 16.998,66 hectares near Diamantina city, in Minas Gerais State, Brazil (IEF, 2005). The implementation of this conservation unit can be a successful conservation strategy in order to maintaining the integrity of the cerrado ecosystem observed in Minas Gerais State. This biome exhibits a number of characteristics that are unique compared to other tropical savannah regions in the world, which make it especially worth of protection. In Biribiri State Park, it can be found most of the waterfalls of the district which tourists visit a lot. Thus, this stream water quality in this State Park has great importance for ecotourism, because these watercourses are frequently visited for leisure activities and bathing. gua limpa stream belongs to the headwaters of the Jequitinhonha river basin (between parallels 15 30 and 18 30 S and the meridians 38 50 and 43 50 W) and is located in the southern Espinhao Mountain Range (Southeastern Brazil), a water divisor of the Brazilian basins of So Francisco and Doce rivers. The hierarchical model was used as sample design model, in order to understand the distribution patterns of the organisms in different spatial scales, as centimeters, meters, dozens of meters to hundreds of meters. This kind of sample design can maximize the representative of the organisms in each sample, mainly in meiofauna where the patch distribution is evident (Merrit and Cummins 1988). Thus, sampling was carried out at four different sample sites (Point 1: 645137 / 7987876; Point 2: 646261 / 7985574, Point 3: 646485 / 7985554 and Point 4: 648140 / 7985305; coordinates in UTM - Zone: 23K) with average distances of 1km among each point, in a longitudinal gradient. This longitudinal gradient was established base on distinct anthropogenic influences. The first sample point was close to the stream source. The two subsequent points, 2 and 3, were chosen because in this part of the stream the riparian vegetation is in good condition, but it is used for visitors to recreation. In point 4, a tributary flows to the gua limpa stream discharging domestic waste originating primarily from inadequate occupation on the border of the park. Altogether four collections were accomplished, two ones during the wet season (10 and 21/03/2009) and two ones in the dry periods (11/07 and 10/08/2009). In each four sampling points, three sampling sites were chosen with at least ten meters among each one. To avoid the occurrence of pseudo-replication, in each of these three sites, three sub-areas were sampled using a PVC tube of 3.5cm diameter and 5cm height. Meiofauna: The samples were collected and placed into plastic litter adding 500ml of formaldehyde at 4% and 125 g of sucrose, labeled according to each sample sites. For quantitative analyses and to extract the microinvertebrates from the sediment, samples were washed and meiofauna retained with a sieve of 0.062mm mesh size. In the laboratory, the samples were washed using 0,062 mm sieves, sorted and, under stereomicroscope. The 992

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specimens were counted and identied to the lowest taxonomic level following the relevant literature (Prez, 1988; Merritt & Cummins 1988; Cummins, 1973; Koste, 1978; Nogrady et al., 1993, 1995; Segers, 1995; Kisielewski, 1987; 1991; Balsamo & Todaro, 2002; Todaro & Rocha, 2004; 2005; Todaro & Hummon, 2008). The specimens sorted were fixed in slides or keep in microtubes and deposited in the collection of the Laboratory of Invertebrate Zoology in UFVJM. Physical, Chemical and Microbiological Analysis: Samplings of the physical, chemical and microbiological parameters were performed during the transition of the wet to dry periods in 2009. Monthly samples were done from 31/03/2009 to 03/08/2009 in the four sample sites. Water samples were collected in glass flasks, previously sterilized, and kept in an icebox for two hours (Freire and Paulino, 2001). The temperature was determined with a thermometer buried in the sediment during the sampling. The measurement of the pH and turbidity were done, respectively, by the pHmeter AT-300 and Turbidimeter Microprocessor Plus. Nitrite, Nitrate, Iron, Phosphorus and Ammonia, were analysed by Spectrophotometer AT-100PB following the methodologies presented in table 1. The concentration of dissolved oxygen was analysed using the Compact Kit with oxide-reduction titration. For quantitative fecal coliforms analysis the Microbiological Kit for detection of E.Coli, Coliforms and Salmonellas was used. All these kits and equipments were assayed according to the Standard Methods for the Examination of Water and Wastewater from American Public Health Association (APHA, 1992).
Table 1: Parameters, analytical methodologies and references. METHODOLOGY VARIABLES Colorimetric method (thioglycolic acid) Iron (mg L-1) Colorimetric method (molybdovanadate) Total Phosphorus (mg L-1) Colorimetric method (Indotest) Ammonia (mg L-1) Colorimetric method (Alfanaftilamina) Nitrite (mg L-1) Colorimetric method (Brucine) Nitrate (mg L-1) Titration by the Winkler Dissolved Oxygen (mg L-1) Nephelometric method Turbidity (NTU*) Potenciometric pH Thermometry Temperature (C) Microbiological Kit Coliforms (UFC*/100mL) * NTU = Nephelometric unit total, CFU= Colony forming unit =, pH = hydrogen potential REFERENCE FRIES (1977) DAVINO (1976) APHA (2005) FRIES (1971) FRIES (1977)

ALFAKIT (2007)

Statistical Analysis: The analysis of the zoobenthic assemblages structure was calculated using Shannon-Wiener diversity index, and the Pielou Evenness. In order to compare the species richness and distribution in dry and wet season it was used the statistical program DivEs (Rodrigues, 2005). The differences among the averages estimates of the taxa found in each collection point were statistically estimated by F-tested from the variance analysis (ANOVA). Furthermore, it was used a model for hierarchical classification: Yijk = M + Ti + Pj + ICTY + k / ij where M = overall average; Ti = taxon effect; Pj = sample effect; TPij = interaction effect between Ti and Pj, and k / ij = variation effect between repetitions inside of each combination TiPj. This model was used both in the dry and wet seasons. Data were transformed for the logarithmic scale according to the expression log (x + 2). Tukey Test was applied when ANOVA showed 0.05 significant level and Correlation analyses were used to measure the degree of relationship between the physicalchemical and microbiological variables and the taxa collected at 0.1 significance level by bilateral T-test. Results: Meiofauna Taxa: A total of 4371 specimens were identified into 10 major taxa and 15 insect larvae families in the wet season and 8439 specimens were identified into 7 major taxa and 15 insect families were identified in the dry season (Tables 2 and 3). The benthic meiofuna of the Biribiri State Park mainly consisted of Oligochaeta, Copepoda, and Chironomidae larvae (85.6% total number of individuals) in the wet season and Oligochaeta, Copepoda, Cladocera and Chironomidae larvae in the dry season (96.3%). Other organisms, such as Rotifera, Tardigrada, Gastrotricha, Hirundinea, Turbellaria and other insect larvae families were found sporadically and in insignificant amount (Tables 2 and 3). Although there were common taxa sampled across the two seasons, an exception was Hirudinea much higher in dry season than wet. The low species richness and dominance of few species leads to very low species diversity, as expressed by the Shannon-Wiener index (Table 4), although this index increases in each sample site from wet to dry season. On the other hand, comparing the wet and dry season, The Pielou Evenness index increased in sample sites 1 (0.47 to 0.508) and 2 (0.514 to 0.523) and decreased in sample sites 3 (0.6429 to 0.5049) and 4 (0.563 to 0.3542). The higher evenness value was reached in sample site 3 during the wet season and the lower was in sample site 4 in the dry season (0.3542). 993

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The Tukey's test of all comparisons among each samples sites in wet season (table 5), showed a low significantly different at the 5% level, as only Copepods in point 3 (2.403) and Baetidae in point 1 (0.625) and 3 (1.298) had significant difference. Notwithstanding, for the dry season (table 6) the significant was much more evident and the following taxa significant difference: Oligochaeta, Copepod, Cladocera, Hirudinea, Chironomidae, Psephenidae, Elmidae, Hydroscaphidae, Perlidae, Leptophlebiidae and Baetidae. In the dry season, (Table 3), the mean test was significantlly with lower value in sample site 1 to Elmidae (0,434) and higher value in sample site 2 to Cladocera (1.839), Psephenidae (0.852) e Perlidae (1.341). In sample site 4 Hirudinea (1.108), Chironomidae (2.552) and Oligochaeta (2.761) showed the higher value and Leptophlebiidae (0.301) and Baetidae (0.492) the lower value. Environmental Variables: The results of physico-chemical and microbiological (Table 7), temperature was uniformly in the four sample sites during the wet season and lightly increases in the dry season. The nitrite values reported in samples sites 1, 2 and 3 were almost similar and close to 0.0 mgL-1 in March and reached 0.0 mg L-1August. During the wet season, nitrate was not found in sample sites 1 and 2 and ammonia was not found in sample site 1. The highest values of most of the appraised parameters occur in the sample site 4 in both seasons. However, for the dissolved oxygen the latter sample site presented the lowest values in both analyzed periods. Relationships Between Meiofauna and Environmental Variables: The significant correlations between taxa and physical-chemical and microbiological parameters during wet and dry season are shown in tables 8 and 9. In March, there were significant correlations between the following taxa and physical-chemical and microbiological parameters: Hirudinea with total phosphorus (0.95), Hydropsychidae with nitrite (0.99); Copepod, Acari, Tabanidae and Baetidae with nitrate; Cladocera with ammonia (respectively, -0.91, -0.98, 0.94, -0.96); Acari, Tabanidae with dissolved oxygen (0.93), being that Acari presented positive correlation and Tabanidae negative correlation with this variable; Hirudinea and Chironomidae with fecal coliforms (0.94). In August, the significant correlations were: Psychodidae with total phosphorus (-0.91), Oligochaeta, Hirudinea, Chironomidae Simulidae with nitrate (respectively, 0.97, 1.00, 0.94 and 1.00); Copepod and Hydropsychidae with ammonia, Oligochaeta, Copepod and Chironomidae with iron; Hirudinea, Empididae, Culicidae and Simulidae presented, with oxygen, negative correlation (respectively -0.95, -0.94, -0.94, 0.93) and Leptophlebiidae positive correlation with this variable; Copepod and Hydropsychidae with turbidity, Hirudinea, Chironomidae, Empididae, Culicidae and Simulidae showed positive correlation with fecal coliform, however, Ceratopogonidae showed negative correlation with the latter parameter; Acari and Ceratopogonidae presented negative correlation with temperature (-0.97); Leptophlebiidae and Baetidae with pH (0.97 and 0.92) (table 9).
Table 2: Zoobentonic organisms found in samples collected in the wet season. TAXONS SITE 1 SITE 2 Subareas Subareas A B C TOTAL A B Rotifera 2 8 2 12 10 4 Tardigrada 0 0 5 5 0 0 Gastrotricha 0 0 0 0 0 0 Oligochaeta 62 164 68 294 142 45 Copepoda 22 17 14 53 90 42 Ostracoda 4 0 1 5 0 1 Cladocera 8 20 13 41 86 1 Hirudinea 0 0 0 0 0 0 Acari 0 0 2 2 3 0 Turbellaria 1 1 0 2 0 0 Chironomidae 28 16 28 72 119 27 Empididae 0 0 0 0 0 0 Culicidae 0 0 0 0 0 0 Ceratopogonidae 0 0 0 0 0 0 Psychodidae 0 0 0 0 0 0 Simuliidae 0 0 0 0 0 0 Tabanidae 1 0 0 1 0 0 Tipulidae 0 0 1 1 0 0 Glossomatidae 0 0 0 0 0 0 Hydroptilidae 0 1 1 2 0 0 Hydropsychidae 0 0 0 0 0 0 Psephenidae 5 0 1 6 3 5 Elmidae 5 2 0 7 10 7 Hydroscaphidae 1 0 3 4 0 0 Perlidae 3 1 0 4 0 0 Libellulidae 0 0 0 0 0 0 Leptohyphidae 0 0 0 0 0 0 Leptophlebiidae 1 10 2 13 3 0 Baetidae 1 3 3 7 28 8 Naucoride 0 0 0 0 0 0 Total 144 243 144 531 494 140 SITE 3 Subareas B C 12 8 10 1 1 4 98 92 562 133 21 0 3 11 0 0 4 4 0 2 56 37 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 1 1 0 1 0 6 1 0 0 0 0 0 0 0 0 0 0 27 3 1 0 805 297 SITE 4 Subareas B 9 1 0 257 49 0 4 2 0 0 357 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 2 0 683

C 6 1 0 13 107 0 2 1 7 0 35 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 3 3 0 179

TOTAL 20 1 0 200 239 1 89 1 10 0 181 0 0 0 0 0 0 0 0 0 0 9 17 0 0 0 0 6 39 0 813

A 6 1 0 473 210 1 10 0 8 0 147 0 0 1 0 2 0 0 1 0 1 3 33 0 0 0 0 2 52 0 951

TOTAL 26 12 5 663 905 22 24 0 16 2 240 0 0 1 0 4 0 0 1 1 2 4 40 0 0 0 0 2 82 1 2053

A 2 0 0 47 16 0 4 0 0 0 11 0 0 0 0 0 0 0 0 0 0 0 7 0 0 0 0 1 3 0 91

C 11 0 0 89 22 5 0 0 0 0 50 0 0 0 0 1 0 0 0 0 3 0 7 0 0 0 0 1 11 0 200

TOTAL 22 1 0 393 87 5 8 2 0 0 418 0 0 0 0 1 1 0 0 0 3 0 14 0 0 0 0 3 16 0 974

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Table 3: Zoobentonics organisms found in samples collected in the dry season. TAXONS SITE 1 SITE 2 Subareas Subareas A B C TOTAL A B Rotifera 0 0 0 0 0 0 Tardigrada 0 0 0 0 2 0 Gastrotricha 0 0 0 0 0 0 Oligochaeta 52 43 18 113 135 218 Copepoda 25 3 11 39 182 250 Ostracoda 0 0 0 0 0 0 Cladocera 3 3 12 18 76 18 Hirudinea 0 1 0 1 0 0 Acari 5 0 3 8 0 2 Turbellaria 0 0 0 0 0 7 Chironomidae 83 30 37 150 118 164 Empididae 0 0 0 0 0 0 Culicidae 0 0 0 0 0 0 Ceratopogonidae 7 0 3 10 1 2 Psychodidae 1 0 0 1 0 0 Simuliidae 0 0 0 0 0 0 Tabanidae 0 0 0 0 0 0 Tipulidae 0 0 0 0 0 0 Glossomatidae 0 0 0 0 1 0 Hydroptilidae 0 0 0 0 0 0 Hydropsychidae 0 0 1 1 5 2 Psephenidae 2 1 0 3 4 8 Elmidae 3 0 0 3 14 33 Hydroscaphidae 5 1 0 6 0 0 Perlidae 0 0 0 0 25 21 Libellulidae 0 0 0 0 0 0 Leptohyphidae 1 0 0 1 0 0 Leptophlebiidae 10 3 1 14 18 4 Baetidae 8 5 6 19 40 68 Naucoride 0 0 0 0 0 0 Total 205 90 92 387 621 797

C 0 0 0 264 362 0 209 0 8 1 193 0 0 7 0 0 0 0 1 0 0 4 27 0 15 0 0 6 36 0 1133

TOTAL 0 2 0 617 794 0 303 0 10 8 475 0 0 10 0 0 0 0 2 0 7 16 74 0 61 0 0 28 144 0 2551

A 0 0 0 59 142 0 9 1 2 0 40 0 0 1 0 0 0 0 0 0 0 2 6 1 0 1 0 19 6 0 289

SITE 3 Subareas B 0 0 10 91 138 0 37 1 0 1 122 0 0 2 0 0 0 0 0 0 0 0 16 0 0 0 0 6 41 0 465

C 0 0 0 52 96 0 47 0 1 0 51 0 0 5 0 0 0 0 0 0 0 0 3 2 0 0 0 1 10 0 268

TOTAL 0 0 10 202 376 0 93 2 3 1 213 0 0 8 0 0 0 0 0 0 0 2 25 3 0 1 0 26 57 0 1022

A 0 0 0 195 95 0 2 3 1 0 309 2 1 3 1 0 0 0 0 0 5 0 10 0 0 0 0 0 0 0 627

SITE 4 Subareas B C 0 0 0 0 0 0 1171 826 564 385 0 0 34 22 45 7 0 1 0 0 430 336 0 0 0 0 2 1 0 0 0 1 0 0 0 0 0 0 0 0 2 4 0 0 12 4 1 0 0 0 0 0 0 0 0 0 3 1 0 0 2264 1588

TOTAL 0 0 0 2192 1044 0 58 55 2 0 1075 2 1 6 1 1 0 0 0 0 11 0 26 1 0 0 0 0 4 0 4479

Table 4: Shannon Diversity Indices (H ') and Pielou evenness (J) in wet and dry season. SITE 1 SITE 2 SITE 3 wet H' J 0.702 0.47 dry 0.758 0.508 wet 0.766 0.514 dry 0.7805 0.5233 wet 0.4311 0.6429 dry 0.753 0.5049 wet

SITE 4 dry 0.5282 0.3542

0.377 0.563

Table 5: Means of taxon found at each collection site in the wet season. TAXON Rotifera Tardigrada Gastrotricha Oligochaeta Copepoda Ostracoda Cladocera Hirudinea Acari Turbellaria Chironomidae Empididae Culicidae Ceratopogonidae Psychodidae Simuliidae Tabanidae Tipulidae Glossomatidae Hydrobiosidae Hydroptilidae Hydropsychidae Psephenidae SITE 1 0.735 0.482 0.301 1.957 1.288 0.519 1.173 0.301 0.401 0.418 1.403 0.301 0.301 0.301 0.301 0.301 0.360 0.360 0.301 0.301 0.418 0.301 0.541 a a a a c a a a b a b a a a a a a a a a a a a SITE 2 0.920 0.360 0.301 1.669 1.882 0.360 1.008 0.360 0.651 0.301 1.704 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.674 a a a b b a a a a a a a a a a a a a a a a a a SITE 3 1.016 0.678 0.519 2.217 2.403 0.713 0.964 0.301 0.852 0.401 1.843 0.301 0.301 0.360 0.301 0.502 0.301 0.301 0.360 0.301 0.360 0.418 0.492 a a a a a a a a a a a a a a a a a a a a a a a SITE 4 0.919 0360 0.301 2.021 1448 0.482 0.619 0.401 0.301 0.301 1.795 0.301 0.301 0.301 0.301 0.360 0.360 0.301 0.301 0.301 0.301 0.434 0.301 a a a a bc a b a b a a a a a a a a a a a a a a

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Elmidae Hydroscaphidae Perlidae Libellulidae Leptohyphidae Leptophlebiidae Baetidae Naucoride

0.583 0.492 0.492 0.301 0.301 0.719 0.625 0.301

a a a a a a b a

0.778 0.301 0.301 0.301 0.301 0.566 1.059 0.301

a a a a a a ab a

0.975 0.301 0.301 0.301 0.301 0.401 1.298 0.360

a a a a a a a a

0.737 0.301 0.301 0.301 0.301 0.477 0.805 0.301

a a a a a a b a

Means followed by same letter in same row not significantly different at 5% by Tukey test. Transformed data log (x +2). Table 6: Means of taxon found at each collection site in the dry season. TAXON Rotifera Tardigrada Gastrotricha Oligochaeta Copepoda Ostracoda Cladocera Hirudinea Acari Turbellaria Chironomidae Empididae Culicidae Ceratopogonidae Psychodidae Simuliidae Tabanidae Tipulidae Glossomatidae Hydrobiosidae Hydroptilidae Hydropsychidae Psephenidae Elmidae Hydroscaphidae Perlidae Libellulidae Leptohyphidae Leptophlebiidae Baetidae Naucoride SITE 1 0.301 0.301 0.301 1.562 1.081 0.301 0.848 0.360 0.615 0.301 1.675 0.301 0.301 0.651 0.360 0.301 0.301 0.301 0.301 0.301 0.301 0.360 0.460 0.434 0.541 0.301 0.301 0.360 0.752 0.916 0.301 a a a c b a c b a a b a a a a a a a a a a b b c a b a a a b a SITE 2 0.301 0.401 0.301 2.301 2.409 0.301 1.839 0.301 0.634 0.577 2.196 0.301 0.301 0.678 0.301 0.301 0.301 0.301 0.418 0.301 0.301 0.583 0.852 1.404 0.301 1.341 0.301 0.301 0.994 1.683 0.301 a a a b a a a b a a a a a a a a a a a a a a a a b a a a a a a SITE 3 0.301 0.301 0.560 1.829 2.099 0.301 1.441 0.418 0.460 0.360 1.814 0.301 0.301 0.641 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.301 0.401 0.952 0.460 0.301 0.360 0.301 0.901 1.205 0.301 a a a c a a b b a a b a a a a a a a a a a b b b a b a a a b a SITE 4 0.301 0.301 0.301 2.761 2.442 0.301 1.180 1.108 0.418 0.301 2.552 0.401 0.360 0.593 0.360 0.360 0.301 0.301 0.301 0.301 0.301 0.742 0.301 1.001 0.742 0.301 0.301 0.301 0.301 0.492 0.301 a a a a a a bc a a a a a a a a a a a a a a a b b a b a a b c a

Means followed by same letter in same row not significantly different at 5% by Tukey test. Transformed data log (x +2).

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Table 7: Results of physico-chemical and microbiological tests performed during wet (03/31/2009) and dry (08/03/2009) seasons. WET SEASON PARAMETERS Total Phosphorusrus (mg L-1) Nitrite (mg L-1) Nitrate (mg L ) Ammonia (mg L-1) Iron (mg L-1) Dissolved Oxygen (mg L -1) pH
1 -1

SITE 1 0.69400 0.00900 1.73000 3.39600 0.98800 9.8000 6.42 0.62000 21.0 0

SITE 2 0.83600 0.01000 1.00000 3.26400 0.00000 12.5000 6.07 0.31000 21.0 420 DRY SEASON

SITE 3 0.51500 0.02000 0.49000 3.40000 0.47500 12.6000 6.20 0.46000 21.0 300

SITE 4 1.52200 0.02000 1.80000 3.53200 1.93900 8.2000 6.92 3.85000 21.0 1500

Turbidity1 (NTU) Temperature (C) Fecal Coliforms1 (UFC)

PARAMETERS Total Phosphorusrus (mg L ) Nitrite (mg L ) Nitrate (mg L-1) Ammonia (mg L ) Iron (mg L-1) Dissolved Oxygen (mg L ) pH1 Turbidity (NTU) Temperature (C) Fecal Coliforms (CFU)
1 1 -1 -1 -1 -1

SITE 1 0.83800 0.00000 0.00000 0.00000 0.02300 8.00000 6.90 0.00000 19.0 60

SITE 2 1.26700 0.00000 0.00000 0.28700 0.87800 9.40000 7.11 1.75000 19.0 540

SITE 3 1.62400 0.00000 0.09000 0.00900 0.64300 8.10000 7.00 0.00000 20.5 840

SITE 4 0.93400 0.29800 5.18500 0.30000 1.83600 4.80000 6.76 1.97000 21.0 5580

1: Unit of measurement for pH-unit pH; Turbidity-Unit Nephelometric Turbidity (NTU); Fecal coliforms -Colony-forming unit (CFU).
Table 8: Estimates of coefficients correlation between taxon and physico- chemical and microbiological variables in the wet season and their significance by t test bilaterally. TAXON Phosphorus Nitrite Nitrate Ammonia Iron Dis. Oxyg. Turb. Fecal col. Temperature Copepoda r -0.59 0.52 -0.91 -0.14 -0.44 0.70 -0.41 -0.27 0.00 P(t) bilateral 0.41 48.01% 0.09 0.86 0.55 0.30 0.59 73.06% 0.00 Cladocera r -0.37 -0.77 -0.26 -0.95 -0.81 0.60 -0.66 -0.48 0.00 P(t) bilateral 0.63 0.23 0.74 0.05 0.19 0.39 0.34 0.51 0.00 Hirudinea r 0.95 0.32 0.46 0.43 0.56 -0.55 0.84 0.94 0.00 P(t) bilateral 0.05 0.67 0.53 0.57 0.44 0.44 0.16 0.07 0.00 Acari r -0.71 0.18 -0.98 -0.54 -0.77 0.93 -0.66 -0.45 0.00 P(t) bilateral 0.28 0.81 0.02 0.46 0.23 0.07 0.34 0.55 0.00 Chironomidae r 0.78 0.83 0.12 0.67 0.61 -0.42 0.85 0.95 0.00 P(t) bilateral 0.22 0.17 0.88 0.32 0.39 0.57 0.15 0.05 0.00 Tabanidae r 0.57 -0.05 0.94 0.70 0.85 -0.95 0.63 0.34 0.00 P(t) bilateral 0.43 0.95 0.06 0.30 0.15 0.05 0.37 0.65 0.00 Hydropsychidae r 0.33 0.99 -0.20 0.72 0.49 -0.20 0.57 0.61 0.00 P(t) bilateral 0.68 0.02 0.80 0.28 0.50 0.80 0.42 0.39 0.00 Psephenidae r -0.64 -0.82 -0.35 -0.98 -0.89 0.70 -0.86 -0.75 0.00 P(t) bilateral 0.36 0.18 0.65 0.02 0.11 0.30 0.14 0.25 0.00 Baetidae r -0.55 0,47 -0.96 -0.27 -0.55 0.78 -0.43 -0.23 0.00 P(t) bilateral 0.45 0,53 0.03 0.73 0.45 0.22 0.57 0.77 0.00 The shaded cells highlight the values with 10% significance by t test (bilateral). Table 9: Estimates of coefficients correlation between taxon and physico- chemical and microbiological variables in the dry season and their significance by t test bilaterally. TAXON Phosphorus Nitrite Nitrate Amonnia Iron Dis. Oxyg. Turb. Fecal col. Temperature Oligochaeta r -0.38 0.97 0.97 0.77 0.94 -0.85 0.80 0.97 0.65 P(t) bilateral 0.62 0.03 0.03 0.23 0.06 0.15 0.20 0.02 0.35 Copepoda r -0.00 0.72 0.72 0.94 0.95 -0.47 0.94 0.76 0.49 P(t) bilateral 0.99 0.28 0.28 0.06 0.05 0.53 0.06 0.24 0.50 Hirudinea r -0.42 1.00 1.00 0.58 0.87 -0.95 0.62 0.99 0.74 P(t) bilateral 0.58 0.00 0.00 0.42 0.13 0.05 0.38 0.01 0.25 Acari r -0.17 -0.65 -0.66 0.04 -0.56 0.78 0.00 -0.70 -0.97 P(t) bilateral 0.83 0.35 0.34 0.96 0.44 0.22 0.99 0.30 0.03 Chironomidae r -0.34 0.94 0.94 0.83 0.96 -0.78 0.86 0.95 0.61 P(t) bilateral 0.66 0.06 0.06 0.16 0.04 0.22 0.14 0.05 0.39 Empididae r -0.43 1.00 1.00 0.60 0.88 -0.94 0.64 0.99 0.73 P(t) bilateral 0.57 0.00 0.00 0.40 0.12 0.05 0.36 0.01 0.27 Culicidae r -0.43 1.00 1.00 0.60 0.88 -0.94 0.64 0.99 0.73 P(t) bilateral 0.57 0.00 0.00 0.40 0.12 0.05 0.36 0.01 0.27 Ceratopogonidae r 0.01 -0.87 -0.88 -0.34 -0.82 0.89 -0.37 -0.91 -0.97 P(t) bilateral 0.99 0.13 0.12 0.66 0.18 0.11 0.63 0.88 0.03 Psychodidae r -0.91 0.58 0.57 0.01 0.13 -0.69 0.06 0.48 0.14 P(t) bilateral 0.09 0.42 0.43 0.99 0.87 0.31 0.94 0.52 0.86 Simulidae r -0.43 1.00 0.99 0.60 0.88 -0.94 0.64 0.99 0.73 P(t) bilateral 0.57 0.00 0.01 0.40 0.12 0.05 0.36 0.01 0.27 Hydropsychidae r -0.39 0.80 0.80 0.95 0.88 -0.57 0.97 0.80 0.33 pH -0.48 0.51 -0.75 0.25 0.65 0.35 -0.79 0.21 0.67 0.34 0.82 0.17 0.49 0.51 -0.87 0.13 -0.56 0.44

pH -0.67 0.33 -0.19 0.81 -0.83 0.17 0.66 0.34 -0.59 0.41 -0.82 0.18 -0.82 0.18 0.72 0.28 -0.87 0.13 -0.82 0.18 -0.38

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P(t) bilateral 0.61 0.20 0.20 r 0.73 -0.87 -0.87 P(t) bilateral 0.26 0.12 0.12 Baetidae r 0.50 -0.55 -0.55 P(t) bilateral 0.50 0.45 0.44 The shaded cells highlight the values with 10% significance by t test (bilateral) Leptophlebiidae

0.05 -0.29 0.71 0.31 0.69

0.12 -0.54 0.46 -0.13 0.87

0.43 0.93 0.07 0.79 0.21

0.03 -0.34 0.66 0.25 0.74

0.20 -0.82 0.18 -0.50 0.49

0.66 -0.51 0.49 -0.53 0.47

0.62 0.97 0.03 0.92 0.08

Discussion: High diversity indexes at the stream were commonly associated with unimpacted or unpolluted conditions, while a lower species biodiversity often signified environmental stress due to human activities (Callisto et al., 2001; Azrina et al., 2006). The higher Shannon-Wiener indices were recorded in the aquatic habitats with good integrity (sample site 2) and the lower indices (sample site 4) were recorded in the poor quality water (Marques et al., 1999; Moreno & Callisto, 2004; Paz et al., 2008). The highest degree of environmental preservation and the largest vegetal covering upstream of sampled fields produces a high quantity of leaf litter, which serves as food and shelter for many insects larval. Thus, the roles of leaf litter during the dry period shows the importance of the presence of riparian vegetation and the flow speed in the distribution of invertebrates (Uieda & Gajardo, 1996). Through the downslope movement of water its velocity increase, the sediment is transported and the benthic fauna can not attach in the substratum, although most of these animals bears pedal glands that secrets a sticky cement. It can explain the evenness decrease at the nearest points to the spring (Thorp and Covich, 2001). Different results might be obtained on flat surfaces, where the biggest water volume provides sediment ripping and favors distribution and remain of benthic organisms for several microhabitats, which increased equitability in points 3 and 4. The velocity of water also can create micro habits that can work as roost against predation, influencing the distribution and abundance of species (Hart and Merz, 1998), besides affecting food resources availability, such as plants and perifiton (Brooks et al., 2005). Nevertheless, the unequal distribution of the zoobentonic community was indicated by the lowest evenness rate, during dry period, in point 4. Low values of Pielou rate indicate water quality decrease (Corra and Uieda, 2008). More stable conditions of water, during drought, provide better condition for bottom colonization by benthic communities. On the other hand, during wet season, increase of water flow caused the drag of organisms down the stream, which determined less significance related to these organisms average, in drought. (Oliveira et al., 1997; Kikuchi and Uieda, 1998; Huamantico and Nessimian, 1999). The taxons Copepoda and Cladocera are either tolerant or intolerant for pollution condition and canlive in oligo or eutrophic waters. The Copepoda feed on algae or they can be feed of a lot of species that demands environment quality for live, being considered more sensitive to waters pollution (Gntzel, 2000; Moretto, 2001). However, several morphotypes of copepodas occur, often, in aquatic eutrophic systems and the capacity to survive in such environments is due to the to select food (Matsumura-Tundisi and Rocha, 1983; Tundisi et al., 1988). High means of Copepoda occurred, both seasons, not only in environments with better physical-chemical and micobiological conditions of water but also in environments with condition of eutrophication quite advanced. The literature mentions cladocerans as one of the most abundant groups in continental waters, containing some species found in oligotroph environments (Gntzel, 2000 e Moretto, 2001) and others that tolerate pollution (Blancher, 1984; Wong et al., 1992). However, in this study, cladocerans was sampled in preserved environments due to the higher significance of their means at points of collection with less environment impact. Rotifera has been mentioned in literature as indicator of organic pollution and associated to waters of low transparency (Souza & Neumann-Leito, 1998; Branco and Cacalcanti, 1999). The direct relation of Rotifera with high trophic levels is related with the group feeding, which includes ingestion of bacteria and suspended organic detritus (Nogrady et al., 1993; Esteves, 1998). It explains a higher quantity of them in March, period of higher turbidity caused by particles entrainment to the streams. Regarding taxon Ostracoda, the literature seems quite poor of data, what is inherent to difficulties related to identification of these organisms (Martens, 1985; 1995; Higuti, 2006). The ostracods have tolerance to great environmental variation strips and capacity to resist desiccation or recolonize flooded habitats, therefore, they are characteristically cosmopolitan (klkyluglu and Dgel, 2004). Important variables to the survival and reproduction of these organisms are the content of dissolved oxygen, which must be elevated, and high temperatures kept (Delorme, 2001). This information goes with the higher quantity of these organisms in the samples collected in March, when oxygen rates were high. Assemblages of Trichoptera, Ephemeroptera e Plecoptera are associated to undisturbed aquatic habitats because there are considered to be very sensitive to water pollution, therefore the presence of these organisms are indicators of good water quality sites (Oliveira and Froehlich, 1997; Bispo et al., 2001; Boyle and Fraleigh Jr., 2003; Fontanella et al., 2009). Low oxygen value is common in sources that were not affected by anthropogenic impacts on water quality, because they have low water volume and the water table in the ground moves slowly to percolate through pore spaces without contact with the atmosphere (Almeida et al., 2004). These characteristics can lead to a low frequency of bioindicators of good water quality, as Baetidae, and Leptophlebiidae in sample site 1. However, in the intermediated samples sites (2 and 3), where low 998

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concentration of eutrophication related water quality parameters and higher oxygen value were observed, the mean results individuals of Baetidae (Ephemeroptera) Trichoptera and Perlidae (Plecoptera) were significative. Specimens of the family Psephenidae (order Coleoptera) have been considered to be indicator of environments with good water quality, well oxygenized and moderate to rapid current (Prez, 1988; Callisto et al., 2001; Goulart and Callisto, 2003). Lower occurrence of samples from this order at the last point of collection, again, indicates that, at this point, there are unsuitable conditions for life of more demanding organisms for environment quality. Specimens of Elmidae (order Coleoptera), different from Psephenidae, are pointed as tolerant of pollution, with considerable part of scavengers species (Moreno and Callisto, 2004; Prez, 1988). Less quantity of Elmidae at the headwater corroborates the literature since at this place there was a lack of availability of food to them. The taxons Oligochaeta, Hirudinea and Chironomidae are benthic invertebrates resistant to pollution and the high abundance of these groups can be a strong indicative of aquatic pollution and high levels of organic matter (Kazanci and Girgin, 1998; Esteves, 1998; Boulton and Jenkins, 1998; Matsumura-Tundisi, 1999; Bubinas and Jaminien, 2001). In many Chironomidae species the presence of high amounts of hemoglobin in their hemolymph (Wilps and Zebe, 1976; Weber, 1980; Frank, 1983) or the typical burrow architecture and their burrowing behavior can be very important under hypoxic conditions to support aerobic metabolism (Leuchs, 1996; Heins & Crommentuijn 1992; Callisto & Esteves, 1996). In the field sample 4, those three taxa reported below were significantly high and this result can indicate degradation in the water quality downstream. The eutrophication state of the site is observed due to the high value of organic matter and low-dissolved oxygen. The high number of microorganisms can contribute to the high rates of oxygen uptake during the degradation of organic matter. Thus, the dissolved oxygen level becomes too low that sensitive species were not survival to this new environmental condition and only the resistant will be found (CALLISTO, 2004). Furthermore, these species known to prefer pollution condition will have positive correlation to phosphorus, nitrogen, and fecal coliform (Goulart & Callisto, 2003; Mccormick et al., 2004; Azrima et al., 2006). Conclusion: The present study highlighted the effect of habitat degradation by anthropic influence in the gua Limpa Stream based on the aquatic invertebrate biodiversity. Taxa, such as, Perlidae, Leptophlebiidae and Baetidae are considered to be sensitive to environmental stress and can potentially indicate good quality waters of the sample sites 1, 2 and 3. On the other hand, Oligochaeta, Hirudinea and Chironomidae, that tolerate unfavorable conditions, indicated that the sample site 4 as a place of larger risk to resilience incapacity, due to the high levels of organic contamination evidencing human activities. Thus, this last sample site contributed for the lower level of water quality of gua Limpa Stream, which can lead to an eutrophization process, aquatic species extinction and transmission of diseases. Furthermore, the dry period showed more significant results for the assessment of biomonitoring studies than the wet period, due to the maintenance of stable water conditions in the former period. The results suggest that groups of meiofauna as Rotifera, Copepod, Ostracoda and Cladocera can be used in biomonitoring studies since we are able to obtaining accurate taxonomic resolution that ensure accurate assessments of ecosystem health. The identification at the specific or generic levels of those groups is still incipient, and, currently, this misidentification turns unreliable the use of those taxa as a bioindicators. Finally, we hope that our studies can serve as a baseline for biomonitoring studies in adjacent State Parks in Minas Gerais State in order to offer a better management of the lotic environments. The use of a more systemic investigation model, indicating variations of biotic and abiotic factors, will help to better detect changes in environment and the water quality. ACKNOWLEDGMENTS We would like to express our gratitude to Paulo Henrique Grazziotti, at Universidade Federal dos Vales do Jequitinhonha Mucuri, for the use of laboratory space and equipment ; Maryana F. Fonseca for technical support in the physical-chemical; Institute Estadual de Floresta (IEF) for field support; Jos Sebastio Fernandes Cunha, for the clarifications and help in the statistical calculations; Marcos Callisto Laboratory of Ecology of Benthos / Project Manuelzo/ UFMG, for the reception, assistance and bibliographic material microscopy required to identify the benthic macrofauna; Juliana France, by explanations related to the collection methodology; Wander Ribeiro Ferreira and Lurdemar Tavares de Paiva, by teaching followed monitoring the key identification of benthics. REFERENCES Almeida, R.M.A., G.J. Hussar and M.R. Peres, 2004. Qualidade microbiolgica do crrego Ribeiro dos Porcos no municpio de Esprito Santo do Pinhal. Engenharia Ambiental, 1(1): 51-56.

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