Influence of taxonomic resolution of stream macroinvertebrate
communities on the evaluation of different land uses.
CORBI1, J . J . & T R I V I N H O - S T R I X I N O1, S .
1 Laboratório de Entomologia Aquática, Departamento de Hidrobiologia, Universidade Federal de
São Carlos, C. Postal 676, São Carlos, SP, Brasil. e-mail: julianocorbi@yahoo.com.br
ABSTRACT: Influence of taxonomic resolution of stream macroinvertebrate communities on the evaluation of different land uses. Stream macroinvertebrate communities have been widely used as i n d i c a t o r s o f w a t e r q u a l i t y. The knowledge of the stream macroinvertebrates structure provides fundamental information about the response of this fauna to impacts of chemical a n d / o r p h y s i c a l p e r t u r b a t i o n s r e s u l t i n g f r o m d i f f e r e n t l a n d u s e s , a s d e f o r e s t a t i o n f o r agricultural activity or input of domestic and industrial effluents. In Brazil, many studies h a v e b e e n c o n d u c t e d u s i n g t h e m a c r o i n v e r t e b r a t e f a u n a a s b i o i n d i c a t o r o f l a n d u s e . However, there is a little information about which is the more adequate taxonomic resolution level for the best biological evaluation of these impacts. In this study we analyze the influence of sugar cane cultivation, pasture and presence of riparian vegetation on the aquatic macroinvertebrate communities of 9 streams located on Cerrado areas of the State of São Paulo (Brazil). This fauna was analyzed using two taxonomic levels: macroinvertebrates families and chironomid species. The community indices applied to these two taxonomic levels show, in general, similarity of results, that is, higher values of richness and diversity, and lower dominance for the communities living on streams protected by the riparian vegetation. These results allow concluding that for streams of the studied region, the family level of taxonomic resolution was enough to evaluate the effect of the agricultural land use.
Key-words: stream macroinvertebrates, land uses, taxonomic resolution, bioindicators. RESUMO: Influência da resolução taxonômica das comunidades de macroinvertebrados de córregos na avaliação de diferentes usos do solo. Os macroinvertebrados aquáticos têm sido amplamente utilizados como indicadores de qualidade da água. A estrutura dessa comunidade pode f o r n e c e r i n f o r m a ç õ e s a r e s p e i t o d e p e r t u r b a ç õ e s q u í m i c a s e / o u f í s i c a s r e s u l t a n t e s d e diferentes usos do solo, como por exemplo, o desmatamento para atividade agrícola ou despejos de efluentes domésticos e industriais. No Brasil, vários estudos têm sido condu-zidos utilizando os macroinvertebrados aquáticos como bioindicadores de qualidade da á g u a . N o e n t a n t o , p o u c a i n f o r m a ç ã o s e t e m a r e s p e i t o d e q u a l o n í v e l d e r e s o l u ç ã o taxonômica é mais adequado para se ter uma melhor avaliação biológica desses impactos. Neste estudo, foi analisada a influência do cultivo de cana-de-açúcar, da pastagem e da presença de vegetação ripária sobre a comunidade de macroinvertebrados aquáticos de 9 córregos de baixa ordem localizados em uma área de Cerrado do Estado de São Paulo (Brasil). Essa fauna foi analisada utilizando dois níveis de resolução taxonômica: famílias de macroinvertebrados e espécies de Chironomidae (Diptera). Os índices comunitários aplicados aos dois níveis taxonômicos mostraram, no geral, semelhança de resultados, ou seja, valores de riqueza e diversidade mais elevados, e de dominância mais baixos para as comunidades dos córregos protegidos por mata ripária. Estes resultados permitem concluir que, para os córregos da região, a resolução taxonômica em nível de famílias de macroinvertebrados foi suficiente para avaliar os efeitos dos usos do solo.
Palavras-chave: m a c r o i n v e r t e b r a d o s d e c ó r r e g o s , u s o s d o s o l o , r e s o l u ç ã o t a x o n ô m i c a , bioindicadores.
Introduction
I n B r a z i l i a n h i s t o r y , d u r i n g t h e c o l o n i z a t i o n , t h e n a t i v e l a n d c o v e r vegetation was removed, and substituted
b y a g r i c u l t u r e , m a i n l y o f s u g a r c a n e a n d p a s t u r e s . T h e s e p r o c e s s e s r e s u l t e d i n d e f o r e s t a t i o n , e s p e c i a l l y i n t h e B r a z i l i a n s o u t h e a s t r e g i o n ( M a r t i n s , 2 0 0 1 ) . T h e s e
mosaics of land uses, especially agriculture and pasture, in addition to the deforestation of riparian vegetation, have caused impacts o n t h e h y d r i c r e s o u r c e s o f t h e a d j a c e n t areas (Dudgeon, 1989; Nery, 2000; Martins, 2001; Angelotti-Netto et al., 2004; Corbi et al., 2006).
As the aquatic organisms may integrate effects of perturbations, numerous studies h a v e b e e n p r o p o s e d t o u s e t h e s t r e a m m a c r o i n v e r t e b r a t e f a u n a t o a n a l y z e t h e e f f e c t s o f d i f f e r e n t l a n d u s e s . I n s t u d i e s using this fauna as indicators for monitoring r i v e r s a n d s t r e a m s , s p e c i e s l e v e l i d e n t i f i c a t i o n s i n c o m p a r i s o n w i t h h i g h resolution identifications can have greater i n f o r m a t i o n c o n t e n t a n d r e s u l t i n m o r e r e l i a b l e s i t e c l a s s i f i c a t i o n s a n d b e t t e r capacity to discriminate between sites, yet many of such monitoring programs identify s p e c i m e n s t o f a m i l y l e v e l r a t h e r t h a n species. This is often because it is cheaper to obtain family level data than species level data. The choice of appropriate taxonomic r e s o l u t i o n i s a c o m p r o m i s e b e t w e e n t h e c o s t o f o b t a i n i n g d a t a a t h i g h t a x o n o m i c resolutions and the loss of information at lower resolutions. The optimum taxonomic r e s o l u t i o n s h o u l d b e d e t e r m i n e d b y t h e information required to address objective programs. In this perspective, some studies using stream macroinvertebrates have been c o n d u c t e d a r o u n d t h e w o r l d t o t e s t t h e implications of taxonomic resolution and its i n f l u e n c e a s b i o i n d i c a t o r s o f s o m e e n v i r o n m e n t a l c o n d i t i o n s ( H e w l e t t , 2 0 0 0 ; T h o m p s o n & T o w n s e n d , 2 0 0 0 ; G u e r o l d , 2000; Gabriels et al., 2005; Nahmani, et al., 2 0 0 6 ) .
In Brazil, many studies have attempted t o r e l a t e t h e a n t h r o p i c i m p a c t s o n t h e stream macroinvertebrates. These studies h a v e c o n s i d e r e d d i f f e r e n t e n v i r o n m e n t a l s i t u a t i o n s , s u c h a s : d e f o r e s t a t i o n s a n d impacts of agriculture (Roque et al., 2000; Ometo et al., 2000; Corbi et al., 2000; Cleto-Filho & Walker, 2001; Corbi, 2006), mining ( C a l l i s t o & E s t e v e s , 1 9 9 8 ) , o r g a n i c enrichment and metals (Guereschi & Melão, 1 9 9 7 ; C o r b i e t a l ., 2 0 0 6 ) a n d i m p a c t s o f reservoirs (Brandimarte, 1997; Anaya, 1997). I n t h e s e s t u d i e s d i s t i n c t m e t h o d o l o g i e s were used with different levels of taxonomic r e s o l u t i o n , w h i c h m a k e d i f f i c u l t t h e e s t a b l i s h m e n t o f p o s s i b l e c o m p a r a t i v e a n a l y s e s . T h e r e a r e a f e w s t u d i e s t h a t i n f e r r e d t h e i d e n t i f i c a t i o n o f t h e p o s s i b l e effects of taxonomic resolution of stream macroinvertebrates as bioindicators of land
uses. These points bring up the question of determining which is the more adequate t a x o n o m i c a l r e s o l u t i o n l e v e l f o r t h e b e s t biological evaluation of these impacts. In t h i s c o n t e x t , t h e a i m o f t h i s s t u d y i s t o v e r i f y i f t h e c h a n g e s i n t h e t a x o n o m i c r e s o l u t i o n a r e a b l e t o a l t e r t h e v a l u e o f stream macroinvertebrates as bioindicators of land use.
Material and methods
Study sites
The study was performed in 9 low order s t r e a m s l o c a t e d o n J a c a r é - G u a ç u R i v e r Basin, State of São Paulo, Brazil (Fig. 1). All streams are located in low altitude (500m t o 7 0 0 m ) a r e a o f C e r r a d o v e g e t a t i o n a n d present low flow in predominant sand bed (Tab. I). The average annual precipitation in the Jacaré-Guaçu River basin is about 1400 m m . T h e w e t s e a s o n o c c u r s b e t w e e n October and March, while dry season occurs from April to September. Streams Água Su-m i d a , S ã o J o ã o , O u r o a n d C h i b a r r o a r e located in extensive areas with sugar cane cultivation. Streams Fazzari, Espraiado and Monjolinho (reference sites) are located on forested areas, while Água Preta and An-des are located in pasture areas, without riparian vegetation.
Stream macroinvertebrate communities
M a c r o i n v e r t e b r a t e s w e r e s u r v e y e d i n three periods: March/April, 2002; June/July/ August, 2002; November/December, 2002. Twenty seven samples were collected: 12 i n s t r e a m s w i t h s u g a r c a n e c u l t u r e , 9 i n streams with riparian vegetation and 6 in p a s t u r e a r e a s . T h e f a u n a w a s c o l l e c t e d using a D-frame (Merritt & Cummins, 1996)
aquatic net (250 µm) including riffle and pool
areas, during 5 minutes, as recommended by Fontoura (1985). Three collections were combined into a single sample in each site. S a m p l e s w e r e t a k e n t o t h e l a b o r a t o r y , w a s h e d i n a s i e v e o f 0 . 2 1 m m o f m e s h , selected on an illuminated tray and fixed with 70% alcohol. Insects were dominant a n d t h e t a x o n o m i c i d e n t i f i c a t i o n w a s achieved at family level for most of them, on the basis of the available published data ( B r i n k h u r s t & M a r c h e s e , 1 9 9 1 ; M e r r i t t & Cummins, 1996). Because the Chironomidae (Diptera) family dominated all streams, the l a r v a e o f t h i s g r o u p w e r e a n a l y z e d t o
Figure 1: Location of the Jacaré-Guaçu River basin and the 9 stream sampling sites, State of São Paulo, B r a z i l .
Table I: Streams localization and general information about land uses.
species level (Trivinho-Strixino & Strixino, 1 9 9 5 ) .
Data analysis
S t r e a m m a c r o i n v e r t e b r a t e s w e r e identified and analyzed in two taxonomic resolutions: (I) family of macroinvertebrates
and (II) species of chironomids. The list of t h e m a c r o i n v e r t e b r a t e f a m i l i e s a n d chironomid species may be seen in Corbi ( 2 0 0 6 ) .
In the State of São Paulo there is no i n d e x c o r r e l a t i n g t h e m a c r o i n v e r t e b r a t e
Legend
Stream
City
Land use
Coordinates
S1 Água Sumida Araraquara Sugar cane 21º56’ (S) 48º16’ (W)
S2 São João Guarapiranga Sugar cane 21º57’(S) 48º15’(W)
S3 Água Preta Ribeirão Bonito Pasture 22º00’ (S) 48º12’(W)
S4 Andes Araraquara Pasture 21º55’ (S) 48º11’(W)
S5 Ouro Araraquara Sugar cane 21º47’(S) 48º0.7’(W)
S6 Chibarro Araraquara e Ibaté Sugar cane 21º52’(S) 48º0.5’(W)
S7 Fazzari São Carlos Riparian vegetation 21º59’ (S) 47º54’ (W)
S8 Monjolinho São Carlos Riparian vegetation 22º00’ (S) 47º50’ (W)
communities and the local environment, or a n y w a t e r - q u a l i t y i n d e x u s i n g s t r e a m benthic fauna. Moreover, many assessment t e c h n i q u e s a d o p t a m u l t i m e t r i c a p p r o a c h using a suite of simple metrics to assess environmental degradation. The strength of this approach lies in its ability to integrate information from the various features of a community to give an overall classification o f d e g r a d a t i o n w i t h o u t l o s i n g t h e information provided by individual metrics (Thorne & Williams, 1997). So, in order to evaluate the influence of the two taxonomic r e s o l u t i o n s o n u s e s t r e a m m a c r o -invertebrates to assess the impacts of the land uses, and the integrity of each stream, t h e c o m m u n i t y c h a r a c t e r i s t i c s w e r e determined by the 6 following metrics: Taxa r i c h n e s s , D o m i n a n c e i n d e x , S h a n n o n ’ s diversity index, Simpson’s diversity index, M a r g a l e f ’ s r i c h n e s s i n d e x a n d C o e f f i c i e n t of Community Loss (Courtemanch & Davies, 1987). The diversity/dominance indices were calculated using the Past Statistic Program (version 1.47). Data were analyzed by linear regressions, comparing the family taxonomic resolution versus chironomid species taxonomic resolution between the streams. Because of the high number of families, we used the preserved streams (S7, S8 and S9) as reference to make these analyses.
Results
Macroinvertebrate communities
I n t h i s s t u d y , 2 6 2 2 s p e c i m e n s o f 3 5
families of stream macroinvertebrates were i d e n t i f i e d . I n a l l s t r e a m s , t h e l a r v a e o f Chironomidae (Diptera) dominated, with 70% o f t h e t o t a l m a c r o i n v e r t e b r a t e s c o l l e c t e d . O t h e r t a x o n o m i c g r o u p s l i k e L i b e l l u l i d a e , D y t i s c i d a e , C e r a t o p o g o n i d a e a n d P o l y c e n t r o p o d i d a e w e r e a l s o f r e q u e n t l y o b s e r v e d i n m a n y o f t h e s t r e a m s . I n t h e streams without vegetation cover, especially in those located near to the area with su-g a r c a n e c u l t i v a t i o n , a su-g r e a t a m o u n t o f O d o n a t a ( L i b e l l u l i d a e f a m i l y ) a n d o f Annelida, including the families Tubicidae, Naididae and Lumbricidae (Oligochaeta) and Glossiphoniidae (Hirudinea) were observed. T h e s t r e a m s p r o t e c t e d b y r i p a r i a n v e g e t a t i o n s h o w e d a g r e a t e r v a r i e t y o f g r o u p s s u c h a s t h e E p h e m e r o p t e r a , P l e c o p t e r a a n d T r i c h o p t e r a f a m i l i e s , a n d other Insecta.
At the two taxonomic levels analyzed, the values of the diversity indices (richness indices and diversity indices) were high in streams with riparian vegetation (reference sites). In contrast, the dominance indices s h o w e d s m a l l e r v a l u e s i n t h e r e f e r e n c e streams. The analysis of the coefficient of the community loss showed high values in streams located in open areas (Tab. II).
T h e p r e s e n t s t u d y s h o w e d a s t r i n g c o r r e l a t i o n b e t w e e n f a m i l y l e v e l o f t a x o n o m i c r e s o l u t i o n v e r s u s c h i r o n o m i d species level applied to the six community i n d i c e s s h o w i n g t h a t t h e t w o t a x o n o m i c resolutions are correspondent (Fig. 2). Table II: Values of the six community indices applied to the two taxonomic resolutions of the 9 streams.
Legends as table I.
Indices/Streams
S1 S2 S3 S4 S5 S6 S7 S8 S9
Family taxa richness 3.0 6.0 9.0 7.0 12 11 18 23 23 Chironomid taxa richness 2.0 10 8.0 7.5 15 19 23 24 28 Family dominance 0.9 0.5 0.5 0.6 0.5 0.6 0.4 0.4 0.3 Chironomid dominance 0.9 0.5 0.7 0.6 0.4 0.3 0.2 0.2 0.1 Family diversity (Shannon) 0.2 1.1 1.0 0.8 1.1 0.9 1.6 1.6 1.8 Chironomid diversity (Shannon) 0.1 0.9 0.5 0.7 1.6 2.1 2.4 2.4 3.0 Family diversity (Simpson) 0.1 0.4 0.5 0.4 0.4 0.3 0.6 0.6 0.6 Chironomid diversity (Simpson) 0.1 0.4 0.2 0.3 0.6 0.8 0.8 0.8 0.9 Family richness (Margalef) 0.5 1.1 1.2 1.1 2.1 1.9 2.8 3.8 3.8 Chironomid richness (Margalef) 0.1 1.7 1.1 1.2 2.8 3.2 4.0 4.4 5.1 Coefficient of community loss (Family) 10 3.0 2.8 3.0 1.7 1.8 0.4 0.0 0.0 Coefficient of community loss (Chironomid) 22 3.6 4.0 4.0 1.5 1.0 0.6 0.2 0.0
0 2 4 6 8 10 0 2 4 6 8 10 12 14 16 18 20 22 24
Coefficient of community loss p<0.0001 r=0.979 chironomid species Macroinvertebrates family 0 5 10 15 20 25 0 5 10 15 20 25 30 Taxa richness p=0.0001 r=0.945 chironomid species Macroinvertebrates family 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 p=0.011 r=0.787 Dominance chironomid species Macroinvertebrates family 0.3 0.6 0.9 1.2 1.5 1.8 2.1 0.0 0.3 0.6 0.9 1.2 1.5 1.8 2.1 2.4 2.7 3.0 3.3 Shannon's diversity p=0.002 r=0.874 chironomid species Macroinvertebrates family 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 Simpson's diversity p=0.013 r=0.790 chironomid species Macroinvertebrates family 0 1 2 3 4 0 1 2 3 4 5 6 Margalef's richness p<0.0001 r=0.967 chironomid species Macroinvertebrates family
Figure 2: Linear regressions between family taxonomic resolution versus chironomid species applied to six community indices of the 9 streams.
Discussion
The appropriate taxonomic resolution for a particular study should be determined by the information required to address its objectives. As demonstrate by Resh et al. (1995) the choice of taxonomic resolution f o r m o n i t o r i n g i s a c o m p r o m i s e b e t w e e n the cost of obtaining data at high taxonomic resolutions and the loss of information at l o w e r r e s o l u t i o n s . A s p o i n t e d o u t b y
N a h m a n i e t a l . , ( 2 0 0 6 ) , t h e s c a l e o f t h e taxonomical resolution to be used depends o n t h e g o a l s o f t h e s t u d y. F o r s o m e conservation purposes, the use of species level is required (Nahmani et al. 2006).
In Brazil, especially in the State of São Paulo, many streams are located in areas of Cerrado vegetation at low altitudes, low d e c l i v i t y a n d w i t h p r e d o m i n a n c e o f s a n d substrates. As the result, a dominance of the Chironomidae fauna is observed (Corbi
et al., 2000; Roque & Trivinho-Strixino, 2001; Freire & Gessner, 2002; Kleine & Trivinho-Strixino, 2005). This fact was also observed in all streams of the present study. So, the use of lower taxonomic resolution using that family, as bioindicator of impacts of land uses can be considered, but costs/benefits and operational time required efforts should b e e x a m i n e d ( M a r s h a l l e t a l . , 2 0 0 6 ) . H o w e v e r , i n t h e C h i r o n o m i d a e , s e v e r a l s p e c i e s p r o v e d t o b e g o o d i n d i c a t o r s o f open areas (without land cover) as pastures and agriculture, whereas other species were v e r y s e n s i t i v e t o t h e s e i m p a c t s ( C o r b i , 2006). Clearly, gathering these species into a s i n g l e t a x o n o m i c u n i t l e a d s t o l o s s o f interesting information like, for example, the shredder species of Chironomidae (Guerold, 2000). To work out about this problem, we s u g g e s t e d t h a t t h e u s e t h i s o f f a m i l y a s bioindicator of land uses can be good, but l o w t a x o n o m i c r e s o l u t i o n i s n e e d e d . Although, our results also point that the use of stream macroinvertebrates identified in level of family offered a good indicative of t h e i m p a c t s o f l a n d u s e s . M o r e o v e r , a l t h o u g h d o m i n a n t i n t h e s t r e a m s , t h e results showed that Chironomidae species i d e n t i f i c a t i o n s o f f e r e d n o s u b s t a n t i a l advantage over macroinvertebrate family-l e v e family-l i d e n t i f i c a t i o n s t o d i s c r i m i n a t e t h e impacts of land uses. Simultaneously, time and cost savings may also be available for studies that require the detail provided by species-level data. Our results showed that all 9 streams data sets were similar when t h e t w o t a x o n o m i c r e s o l u t i o n s ( s t r e a m macroinvertebrates family or Chironomidae species) were used.
Overall, family identification appeared t o b e g o o d f o r m o n i t o r i n g t h e e f f e c t s o f l a n d u s e s o n s t r e a m m a c r o i n v e r t e b r a t e s c o m m u n i t y i n l o w o r d e r s t r e a m s o f t h e C e r r a d o ’ s s t r e a m a n d c o u l d r e d u c e taxonomic effort.
Acknowledgements
We would like to thanks to Dr. Pedro. P. Corbi, Dra. Vanessa Colombo-Corbi, Dr. Irineu Bianchini and Dr. Marcel Okamoto Tanaka for the suggestions. Financial support CA-PES and BIOTA-FACA-PESP.
References
A n a y a , M . 1 9 9 7 . I m p a c t o d e u m r e p r e -s a m e n t o -s o b r e a c o m u n i d a d e d e
i n v e r t e b r a d o s b e n t ô n i c o s d o r i o M o g i -Guaçu e de seu tributário, Rio do Peixe (SP, Brasil). São Carlos, USP, 140p (Master T h e s i s ) .
Angelotti-Netto, A., Crestana, S., De Olivei-ra, S.C. & Barbosa, R.V.R. 2004. Metais pesados provenientes de atividade agrí-cola: formas, prevenção e controle. In: Espíndola, E.L.G & Wendland, E. (eds.) Ba-cia hidrográfica. Rima, São Carlos. p.1-14. B r a n d i m a r t e , A . L . 1 9 9 7 . I m p a c t o s limnológicos da construção do reserva-tório de aproveitamento múltiplo do rio Mogi-Guaçu (SP, Brasil). São Carlos, USP, 97p (PhD Thesis).
Brinckhurst, R.O. & Marchese, M.R. 1991. Guía p a r a l a i d e n t i f i c a c i ó n d e o l i g o q u e t o s a c u a t i c o s c o n t i n e n t a l e s d e s u d y c e n t r o a m e r i c a . A s s o c i a c i ó n C i e n c i a s Naturales del Litoral J. Maciá, Argentina. 2 0 7 p .
C a l l i s t o , M . & E s t e v e s , F. A . 1 9 9 8 . B i o -monitoramento da macrofauna bentônica d e C h i r o n o m i d a e ( D i p t e r a ) e m d o i s igarapés amazônicos sob influência das atividades de uma mineração de bauxita. In: Nessimian, J.L. & Carvalho, A.L. (eds). E c o l o g i a d e i n s e t o s a q u á t i c o s . P P G E -UFRJ, Rio de Janeiro. p.299-309. (Series Oecologia Brasiliensis, 5).
Cleto-Filho, S.E.N. & Walker, I. 2001. Efeitos da ocupação urbana sobre a macrofauna d e i n v e r t e b r a d o s a q u á t i c o s d e u m Igarapé da cidade de Manaus/AM – Ama-zônia Central. Acta Amazônica, 31:69-89. Corbi, J.J. 2006. Influência de práticas de m a n e j o d e s o l o s o b r e o s m a c r o i n v e r t e b r a d o s a q u á t i c o s d e córregos: ênfase para o cultivo de cana-d e - a ç ú c a r e m á r e a s a cana-d j a c e n t e s . S ã o Carlos, UFSCar, 92p (PhD Thesis).
Corbi, J.J., Trivinho-Strixino, S., Dos Santos, A. & Del Grande, M. 2006. Environmental diagnostic of metals and organochlorated compounds in streams near sugar cane plantations activity (state of São Paulo, Brazil). Quím. Nova, 29:61-65.
Corbi, J.J., Sampaio, E.V., De Ribeiro, V.R., Domingos, M.D., Ferraz Freire, C., Ferreira, P.S., Pelaez Rodríguez, M., Rojas, N.T. & Strixino, S.T. 2000. Levantamento preli-minar da entomofauna aquática do Cen-tro Nacional de Pesquisa de Peixes Tro-picais (CEPTA). Bol. Téc. Cepta, (13):71-8 3 .
C o u r t e m a n c h , D . L . & D a v i e s , S . P. 1987. A coefficient of community loss to assess d e t r i m e n t a l c h a n g e s i n a q u a t i c communities. Water Res., 21:217-222.
Dudgeon, D. 1989. The influence of riparian vegetation on the functional organization of four Hong Kong stream communities. Hydrobiologia, 179:183-194.
Fontoura, A.P. 1985. Manual de vigilância da qualidade das águas superficiais. Avalia-ção biológica da qualidade da água. Ins-tituto de zoologia. Faculdade de Ciênci-as, Universidade do Porto, Porto. 38p. Freire, C.F. & Fonseca-Gessner, A.A. 2002.
L a r v a s d e C h i r o n o m i d a e ( D i p t e r a ) n a m i c r o b a c i a d o R i b e i r ã o C a n c h i m , S ã o C a r l o s , S P, B r a s i l . E n t o m o l . Ve c t o r e s , 8 : 4 1 7 - 4 2 9 .
Gabriels, W., Goethals, P.L.M. & De Pauw, N. 2 0 0 5 . I m p l i c a t i o n s o f t a x o n o m i c m o d i f i c a t i o n s a n d a l i e n s p e c i e s o n biological water quality assessment as e x e m p l i f i e d b y B e l g i a n B i o t i c I n d e x method. Hydrobiologia, 542:137-150. G u e r e s c h i , R . M . & M e l ã o , M . G . G . 1 9 9 7 .
M o n i t o r a m e n t o b i o l ó g i c o d a b a c i a hidrográfica do Rio Monjolinho pelo uso d e m a c r o i n v e r t e b r a d o s b e n t ô n i c o s . I n : Anais do VIII Seminário Regional de Eco-logia. São Carlos. v.1, p.61-76.
G u e r o l d , F. 2 0 0 0 . I n f l u e n c e o f t a x o n o m i c d e t e r m i n a t i o n l e v e l o n s e v e r a l community indices. Water Res., 34:487-4 9 2 .
Hewlett, R. 2000. Implications of taxonomic resolution and sample habitat for stream classification at a broad geographic scale. J. North Am. Benthol. Soc., 19:352-361. K l e i n e , P. & T r i v i n h o - S t r i x i n o , S . 2 0 0 5 .
C h i r o n o m i d a e a n d o t h e r a q u a t i c m a c r o i n v e r t e b r a t e s o f a f i r s t o r d e r stream: community response after habitat fragmentation. Acta Limnol. Bras., 17:81-9 0 .
Marshall, J.C., Steward, A.L. & Harch, B.D. 2 0 0 6 . T a x o n o m i c r e s o l u t i o n a n d q u a n t i f i c a t i o n o f f r e s h w a t e r m a c r o i n v e r t e b r a t e s a m p l e s f r o m a n Australian dryland river: the benefits and costs of using species abundance data. Hydrobiologia, 572:171-194.
Martins, S.J. 2001. Recuperação de matas ciliares. Aprenda Fácil, Viçosa. 90p. M e r r i t t , R . W. & C u m m i n s , K . W. 1 9 9 6 . A n
i n t r o d u c t i o n t o t h e a q u a t i c i n s e c t s o f N o r t h A m e r i c a . 3a e d . K e n d a l l - H u n t ,
Dubuque. 862p.
Nahmani, J. Lavelle, P. & Rossi, J.P. 2006. D o e s c h a n g i n g t h e t a x o n o m i c a l r e s o l u t i o n a l t e r t h e v a l u e o f s o i l m a c r o i n v e r t e b r a t e s a s b i o i n d i c a t o r s o f m e t a l p o l l u t i o n ? S o i l B i o l . B i o c h e m . , 3 8 : 3 8 5 - 3 9 6 .
Nery, M.S. 2000. Desempenhos operacional e econômico de uma colhedora em cana crua. ESALQ, Piracicaba. 108p.
Ometo, J.P.H.B., Martinelli, L.A., Ballister, M.V., Gessner, A., Krische, A.V. & Victoria, R.L. 2000. The effects of land use on water chemistry and macroinvertebrates rates i n t w o s t r e a m s o f t h e P i r a c i c a b a r i v e r basin South-east Brazil. Freshwater Biol., 4 4 : 3 2 7 - 3 3 7 .
Resh, V.H., Norris, R.H. & Barbour, M.T. 1995. D e s i g n a n d i m p l e m e n t a t i o n o f r a p i d a s s e s s m e n t a p p r o a c h e s f o r w a t e r r e s o u r c e m o n i t o r i n g u s i n g macroinvertebrates. Aust. J. Ecol., 20:108-121.
R o q u e , F. O . & T r i v i n h o - S t r i x i n o , S . 2 0 0 1 . B e n t h i c m a c r o i n v e r t e b r a t e s i n m e s o h a b i t a t s o f d i f f e r e n t s p a t i a l dimensions in a first order stream (São Carlos-SP). Acta Limnol. Bras., 13:69-77. Roque F.O., Corbi, J.J. & Trivinho-Strixino, S.
2000. Considerações sobre a utilização de larvas de Chironomidae (Diptera) na a v a l i a ç ã o d a q u a l i d a d e d a á g u a d e C ó r r e g o s d o E s t a d o d e S ã o P a u l o . I n : Espíndola, E.L.G., Paschoal, C.M.R.B., Ro-cha, O., Bohrer, M.B.C. & Neto, A.L.O. (eds.) Ecotoxicologia perspectivas para o sé-culo XXI. Rima, São Carlos. p.115-126. Thompson, R.M. & Townsend, C.R. 2000. Is
r e s o l u t i o n t h e s o l u t i o n ? T h e e f f e c t o f taxonomic resolution on the calculated p r o p e r t i e s o f t h r e e s t r e a m f o o d w e b s . Freshwater Biol., 44:413-422.
T h o r n e , R . J . & W i l l i a m s , W. P. 1 9 9 7 . T h e response of benthic macroinvertebrates t o p o l l u t i o n i n d e v e l o p i n g c o u n t r i e s : a m u l t i m e t r i c s y s t e m o f b i o a s s e s s m e n t . Freshwater Biol., 37:671-686.
Trivinho-Strixino, S. & Strixino, G. 1995. Lar-vas de Chironomidae (Diptera) do Esta-do de São Paulo: Guia de identificação e diagnose de gêneros. PPG-ERN/UFSCar, São Carlos. 227p.
Received: 02 December 2006 Accepted: 22 February 2007
