Hydrobiologia (2009) 623:173189 DOI 10.

1007/s10750-008-9656-x

PRIMARY RESEARCH PAPER

A sh-based biotic integrity index for assessment of lowland streams in southeastern Brazil
Lilian Casatti Cristiane P. Ferreira Francisco Langeani

Received: 4 August 2008 / Revised: 10 November 2008 / Accepted: 17 November 2008 / Published online: 24 December 2008 Springer Science+Business Media B.V. 2008

Abstract This study was carried out to develop and apply a sh-based biotic integrity index to assess lowland streams in a highly deforested region of the River basin. Fifty-six rst-order segUpper Parana ments were randomly selected for environmental and sh evaluation. Because previous analysis had identied the main type of effect on the streams of the region as physical habitat degradation, 22 qualitatively biological attributes were selected and tested over a physical condition gradient between reference and degraded sites. Sensitivity and redundancy of each attribute revealed that ve metrics were adequate for discriminating higher quality from degraded sites. Of the fty-six streams assessed, one (2%) was classied as good, four (7%) as fair, ten (18%) as poor, and fortyone (73%) as very poor, indicating that, on a regional scale, many aspects of biological integrity are altered, indicative of serious degradation. Considering that rst-order segments amount to 11,000 km in total, it is noticeable that 10,000 km of the stream segments have

no more than half of the expected conditions, indicative of poor or very poor biotic integrity conditions. Possible strategies of mitigating this scenario are discussed. Keywords Ichthyofauna Habitat quality Conservation IBI Biological monitoring

Introduction Analysis of the quality of the aquatic environments should, ideally, incorporate attributes able to integrate the behavior of elements and biological processes at various levels of organization expressing anthropogenic interference with aquatic communities. The most recent approaches to assessing the integrity of environments are multimetric, aiming to combine attributes that represent the broad existing ecological diversity at different levels of biological organization, always having the characteristic of comparing them with a reference condition, dened as the one with the minimum possible anthropogenic impact (Hughes, 1995). This is true for the index of biotic integrity (IBI), originally developed by Karr (1981) based on sh fauna attributes. This index has been considered adequate for identifying the ability of an environment to withstand and maintain a diverse community with a functional organization comparable with that of a natural regional habitat (Karr & Dudley, 1981).

Handling editor: S. M. Thomaz L. Casatti (&) C. P. Ferreira F. Langeani nica, UNESPDepartamento de Zoologia e Bota rio de Ictiologia, Universidade Estadual Paulista, Laborato va o Colombo, 2265, 15054-000 Sa o IBILCE, Rua Cristo do Rio Preto, SP, Brazil Jose e-mail: lcasatti@ibilce.unesp.br

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The IBI and its variants have been the paradigm of biotic integrity assessments of streams and rivers of North America (Karr, 1981; Angermeier & Karr, 1986; Miller et al., 1988), Europe (Oberdorff & Hughes, 1992; Angermeier & Davideanu, 2004), Central America (Lyons et al., 1995), Asia (Ganasan & Hughes, 1998), Africa (Kamdem Toham & Teugels, 1999), and New Zealand (Joy & Death, 2004). The IBI has also been shown to be especially sensitive when used in combination with physical and chemical data to isolate possible causes of stress in aquatic biota (Karr et al., 1985), considering that changes in physical and chemical properties can vary regularly with time or suffer induced natural seasonal modications, not reecting environmental impacts (Tejerina-Garro et al., 2006). In continental Brazilian aquatic environments, the IBI based on sh assemblages has been adapted to jo, evaluate segments of a large river (Pinto & Arau 2007), reservoirs (Petesse et al., 2007), and streams in the southern (Bozzetti & Schulz, 2004) and southeastern regions (Ferreira & Casatti, 2006), though it is still a little known tool for assessing the biological integrity of freshwater ecosystems. Factors limiting application of the IBI in several of these Brazilian ecosystems are the high sh fauna diversity combined with the poor knowledge of many systematic (Buckup et al., 2007) and ecological aspects, and the difculty of nding water courses entirely conserved to serve as references, especially in non-Amazonian areas. In Brazil, the largest water demand is recorded in the southeastern region, totaling approximately 15 km3/year, where numerous human activities have affected the quality of its waters (Tundisi, 2003). To illustrate the magnitude of this impact, one of the most critical situations is recorded in the northwest of o Paulo State, which has only 4% of its native Sa vegetation left (SMA/IF, 2005). Recent studies (Casatti et al., 2006; Silva et al., 2007) suggest that this area has high erosive potential and that the streamsmainly of rst and second orderare seriously affected by the loss of physical quality of the habitat. Impairment of the physical quality of the habitat adversely affects both sh species dependent on rocky substrates and species that exploit the water column (Casatti et al., 2006). Therefore, the development of tools able to diagnose the current state of the streams is urgently needed, so that future measures for the conservation and sustainable use

of aquatic resources of the region can be conducted. Because of this need, this study was carried out to develop and apply the index of biotic integrity to River basin, in lowland streams of the Upper Parana southeastern Brazil.

Methods Study area Several environmental factors affect the structure of sh assemblages on different spatial scales and may compromise the quality of generated multimetric indexes based on information from the ichthyofauna (Tejerina-Garro et al., 2005). In order to minimize such affects, a geographically homogeneous area subjected to similar kinds of effects was selected. The study area is located in the Upper Parana River basin (Fig. 1), having basaltic and sedimentary and Bauru groups (IPT, 2001), rocks of the Cauia dos Dourados, o Jose including drainage of the Sa o Turvo, and Grande rivers, in the northwest of the Sa Paulo State. Native vegetation was mostly represented by semi-deciduous forest, currently restricted to 4% of its original area (SMA/IF, 2005). At the end of the sampling periods, from 70 to 75% of the land was being used for grazing (Silva et al., 2007). Climate is hot tropical (Nimer, 1989) with a rainy season from October to March (January and February are the most rainy months, having approximately 54% of the total annual rainfall) and a dry season, from April to September; the maximum average temperature (31C) occurs in January and the minimum (13C) in July (IPT, 2001). Reference sites, sampling sites, and sh collection The concept of regional reference was adopted to test biological attributes, because it is considered the most appropriate strategy to be applied in homogeneous geographical regions, where the causes of effects are little known (Barbour et al., 1999; Karr & Chu, 1999). In this context, four rst-order streams (sensu Strahler, scale 1:50.000) located in relatively less degraded regions of the Upper Parana River system, o Paulo and and previously studied in the states of Sa (Casatti, 2002, 2005; Castro et al., 2003, Parana 2004), were used as references (Fig. 1, Table 1).

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Fig. 1 Map showing the limits of the study area (dark line), reference streams (R1R4, larger circles) and 56 sampled streams (156, o Paulo State, Brazil small circles) in the northwestern region of Sa Table 1 Location and general characterization of the reference streams used to calibrate candidate metrics Streams Mean width Mean depth Dissolved oxygen (m) (m) (mg l-1) 0.9 0.7 0.4 0.5 10.3 11.3 9.5 8.2 Conductivity (lS cm-1) 16 30 151 22 pH

rrego Sa o Carlos 22360 23.800 S 52150 08.600 W 1. Co 2.6 0 00 0 00 rrego Santa Clara 2245 54.2 S 5225 19.0 W 2. Co 1.6 gua do Macaco 22390 46.900 S 50490 39.500 W 1.7 rrego A 3. Co 4. Unnamed stream, tributary of Rio Sapuca 2.7 21000 40.700 S 47130 11.500 W

7.9 7.6 7.4 8.6

Reference information for trophic attributes was collected from the studies of Uieda et al. (1997) and Casatti (2002). Random sampling of sites was chosen as the sampling design because of the wide area to be sampled and the impossibility of sampling all the water bodies of the region (Karr & Chu, 1999). This design was also adopted to avoid selection of sites on a basis of known sources of degradation and because the region was experiencing strong pressure to convert the pastures to sugarcane cultivation. o Jose The number of segments sampled per basin (Sa dos Dourados, Turvo, and Grande) was proportional to the number of rst-order kilometers in each basin.

Using a 1:50.000 topographic map base, the total extent of rst-order sections in each basin was calculated for a further random selection of a stream approximately every 100 km (modied from Roth et al., 1999). Within each randomly selected stream, sites chosen for sampling were located in the lower third segments to avoid unsampleable conditions in the shallow stretches of the headwaters. In all basins, about 10% of extra segments were selected as a contingency against loss of sampling sites because of restricted access to selected streams or because streams were dry, too deep, or otherwise unsampleable owing to eld conditions (Roth et al., 1999). Following Kasyak (2001), a 75-m reach with greater variability of available mesohabitats was

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selected in each segment and a block net was placed across the upstream and downstream boundaries. The streams were sampled in the dry seasons of 2003 (streams 1 to 22), 2004 (streams 23 to 38), and 2005 (streams 39 to 56), seeking to minimize seasonal effects on the composition and structure of assemblages. Fishing efforts were standardized across all collecting sites, with each section of blocked stream using 5-mm mesh stop nets up and downstream, and afterwards submitted to two electro-shing passes according to methods reported by Mazzoni et al. (2000). Captured specimens were xed in a 10% formalin solution and, after 48 h, transferred to a 70% EtOH solution. Fishes were identied by species, counted, and weighed. All specimens were incorporated in the sh collection at the Departamento de nica da Universidade Estadual PauliZoologia e Bota do Rio Preto, Sa o Jose o Paulo sta (DZSJRP), Sa State, Brazil.

representative nature (recorded in 95% of the sampled streams). Frequency of occurrence and dominance were calculated for each feeding item to identify the most important items of the sh diet (Bennemann et al., 2006). Fish metrics test and IBI development Previous analysis (Casatti et al., 2006) identied physical habitat degradation as the main threat to the integrity of sh assemblages, especially as a result of the riparian vegetation removal and habitat simplication. Approximately 88% of the 56 studied streams have poor or very poor physical habitat integrity conditions (according to the Physical Habitat Index, PHI, regionally adapted by Casatti et al., 2006). PHIevaluated metrics were substrate stability, velocity and depth variability, ow stability, bottom deposition, combinations of pool-rifes-runs, channel alteration, streamside cover, bank vegetative stability, and bank stability (Casatti et al., 2006). Thus, the biological attributes were tested by comparing the medians with the rst and third quartiles over a gradient between reference (PHI good) and degraded (PHI regular, poor, or very poor) sites. The IBI as proposed by Karr (1981) includes 12 metrics that were adjusted worldwide depending on habitat features, bio-geographical regions, and several environmental factors (Karr & Chu, 1999). Following Hughes & Oberdorff (1998), qualitative analysis of attributes listed in the literature was conducted and 16 metrics were selected. Some metrics widely used in studies of integrity of sh communities were excluded. For example, the proportion of piscivores (Oberdorff & Hughes, 1992) was eliminated in this assessment because, in small streams of the region, exclusively piscivore shes do not occur. Reproductive metrics were also eliminated because there is no information of this nature that makes it possible to infer, for example, the importance of substrate integrity in the reproduction of the recorded sh species. In addition to 16 selected metrics, four were proposed herein and tested. To test the sensitivity of each metric we adopted procedures detailed in Baptista et al. (2007), judging according to the degree of interquartile overlap in Box-and-Whisker plots (Barbour et al., 1999) and conrmed by the MannWhitney test (alpha = 0.05). A redundancy analysis was performed using the

Analysis For each stream the species richness, abundance, and biomass were obtained; these were later used for calculation of biological metrics. The abundance and biomass was divided by the sampled area of each stream. Dominance was calculated using two indices (BergerParker and Simpson) with the computational software PAST (Hammer et al., 2001) and values close to zero indicate low dominance. Based on literature data and personal experience, each species was classied according to its origin in hydrographic system (Langeani the Upper Parana et al., 2007), its position in the water column (Casatti et al., 2001; Casatti, 2002), its tolerance to hypoxia (Kramer & Mehegan, 1981; Araujo & Garutti, 2003; Bozzetti & Schulz, 2004), and its trophic group (Andrian et al., 1994; Castro & Casatti, 1997; Uieda et al., 1997; Gibran et al., 2001; Casatti, 2002; Ferreira & Casatti, 2006; Ceneviva-Bastos & Casatti, 2007). In view of the trophic plasticity of teleost species, particularly tropical ones, it is not easy to establish feeding patterns within a particular group of species (Abelha et al., 2001). As a way of minimizing this limitation and to complement literature data, stomach contents of 2,171 Characidae individuals were examined. Trophic information was collected from Characidae specimens because of their highly

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Spearman correlation test with pairs of metrics regarded as sensitive. This was done to simplify the index, reduce the cost of analyses, and avoid redundant information; when one or more metrics showed redundancy by being highly correlated (Spearman r [ 0.75, P \ 0.05), only one was chosen to represent that information in the index (Baptista et al., 2007). After dening the set of metrics that best discriminated affected streams from reference streams, individual metrics for the IBI were scored as 1, 3, or 5, on the basis of comparisons with the distribution of metric values at reference sites. Calculations of metric scoring thresholds were based on the distribution of values at reference sites, with the lower threshold established at the 25th percentile and the upper threshold at the 75th percentile (Schleiger, 2000). The rst case would score 1, the second case would score 5, and intermediate conditions, i.e. between the 75th and 25th percentiles of the reference sites, would score 3. For dominance and frequency of detritus in the diet, thresholds were established by comparison with fair sites, because detritus was a rare item in the gastric contents of specimens from reference sites. Scores for IBI were calculated as the mean of the individual metric scores and, therefore, ranged from 1 to 5 (Roth et al., 1999).

decision to keep the number of rheophilic species instead of the number of benthic species was because the term benthic does not always distinguish tolerant species from those intolerant of siltation, as discussed below. Eight metrics enabled sensitive discrimination of higher-quality from degraded sites (Table 5). Trophic metrics were excluded from this analysis because missing data resulted in low representativeness of specimens in some stretches. Thus, nal IBI composition comprised ve metrics of species richness, dominance, habitat use, and tolerance. Detailed descriptions of stream biological integrity associated with each of the IBI categories are given in Table 6. Thus, of the 56 streams analyzed, one (2%) was classied as good, four (7%) as fair, ten (18%) as poor, and 41 (73%) as very poor (Table 6), indicating that, on a regional scale, many aspects of biological integrity are altered, indicative of serious degradation. Considering that rst-order reaches contribute a distance of 11,000 km to the entire watershed, it is noteworthy that 10,000 km of the stream segments have no more than a half of the expected conditions, indicative of poor or very poor biotic integrity.

Discussion Results A total of 8,660 shes of 50 species were collected (Table 2). Among the 22 metrics (Table 3), 11 were able to discriminate among reference and degraded streams (Fig. 2, Table 4). Of these, three pairs of metrics were tested to assess redundancy, which showed signicant correlations (P \ 0.05): number of species versus number of native species, number of rheophilic species versus percentage abundance of rheophilic species, and number of benthic species versus number of rheophilic species. We decided to include the number of native species in the IBI nal composition, because the presence of non-native species is often associated, to some extent, with anthropogenic interference. The number of rheophilic species was adopted in the IBI nal composition, instead of the abundance percentage of rheophilic species, to keep a more conservative position with regard to sampling limitations which may result in underestimation of the abundance of this guild. The Metrics reecting sh species richness, composition, and dominance The concept of species richness has been extensively used to infer the quality of ecological systems (Roth et al., 2000). The number of native species, as originally proposed by Karr (1981), indicates that some species can be lost due to habitat degradation (Karr et al., 1986). Either the number of species or the number of native species (Fig. 2) discriminates sites with good physical condition from those with worse condition. However, because the presence of exotic species is often associated with some extent of anthropogenic interference, we believe that the number of native species is a more reliable metric indicating relatively human-free condition. The predominance of species belonging to the orders Characiformes and Siluriformes in preserved continental waters of the neotropical region is well known (Castro et al., 2003, 2004), but in degraded conditions the environment may be dominated by

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178 Table 2 Classication of sampled species according to their river system (NAT, natives; ALO, origin in the Upper Parana allochthonous; EXO, exotics), position in the water column (BEN/RIF, benthics associated with rifes; BEN, benthics; NEK, nektonics; NEK/BAN, nektonics associated with stream banks; SUR, close to the surface of the water; BEN/LEA, benthics associated with leaves), hypoxia tolerance (TOL, Order and species Characiformes Apareiodon piracicabae (Eigenmann, 1907) Parodon nasus Kner, 1858 ndez-Ye pez, 1948) Cyphocharax modestus (Ferna Cyphocharax vanderi (Britski, 1980) ndez-Ye pez, 1948) Steindachnerina insculpta (Ferna Leporinus friderici (Bloch, 1794) Leporinus lacustris Campos, 1945 Leporinus paranensis Garavello & Britski, 1987 Characidium aff. lagosantense Travassos, 1947 Characidium zebra Eigenmann, 1909 Astyanax altiparanae Garutti & Britski, 2000 Astyanax bockmanni Castro & Vari, 2007 Astyanax fasciatus (Cuvier, 1819) Astyanax paranae Eigenmann, 1914 Hemigrammus marginatus Ellis, 1911 Hyphessobrycon eques (Steindachner, 1882) Knodus moenkhausii (Eigenmann & Kennedy, 1903) Moenkhausia sanctaelomenae (Steindachner, 1907) Oligosarcus pintoi Campos, 1945 Piabina argentea Reinhardt, 1867 Serrapinnus heterodon (Eigenmann, 1915) Serrapinnus notomelas (Eigenmann, 1915) tken, 1875) Acestrorhynchus lacustris (Lu Erythrinus erythrinus (Bloch & Schneider, 1801) Hoplias malabaricus (Bloch, 1794) Pyrrhulina australis Eigenmann & Kennedy, 1903 Siluriformes cker, 1976 Aspidoras fuscoguttatus Nijssen & Isbru Corydoras aeneus (Gill, 1858) Callichthys callichthys (Linnaeus, 1758) Hoplosternum littorale (Hancock, 1828) Hisonotus francirochai (Ihering, 1928) Hypostomus ancistroides (Ihering, 1911) Hypostomus sp. Imparnis mirini Haseman, 1911 Imparnis schubarti (Gomes, 1956) Pimelodella avanhandavae Eigenmann, 1917 Rhamdia quelen (Quoy & Gaimard, 1824) NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT BEN BEN BEN BEN BEN/LEA BEN BEN/RIF BEN/RIF BEN BEN BEN NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT NAT ALO NAT NAT NAT NAT NAT NAT NAT NAT NAT BEN/RIF BEN/RIF BEN BEN BEN BEN BEN BEN BEN BEN/RIF NEK NEK NEK NEK NEK NEK NEK NEK NEK/BAN NEK SUR SUR NEK/BAN NEK/BAN NEK/BAN SUR

Hydrobiologia (2009) 623:173189 tolerant; INT, intolerant), and trophic group (PER, periphytivores; DET, detritivores; AQUINS, insectivores with predominance of aquatic forms; ONI, onivores; TERINS, insectivores with predominance of terrestrial forms; ALG, algivores; CAR, carnivores with predominance of invertebrates and shes) Origina Positionb Tolerancec Trophicd

INT INT INT INT INT INT INT INT INT INT INT INT INT INT INT INT TOL INT INT INT TOL TOL INT TOL TOL TOL TOL TOL TOL TOL INT TOL INT INT INT INT TOL

PER PER DET DET DET ONI HER ONI AQUINS AQUINS ONI ONI TERINS TERINS TERINS TERINS ONI TERINS TERINS AQUINS ALG ALG CAR CAR CAR ALG AQUINS AQUINS ONI ONI DET DET PER AQUINS AQUINS AQUINS AQUINS

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Hydrobiologia (2009) 623:173189 Table 2 continued Order and species Gymnotiformes Gymnotus carapo Linnaeus, 1758 Gymnotus inaequilabiatus (Valenciennes, 1839) Eigenmannia virescens (Valenciennes, 1842) Cyprinodontiformes Rivulus pictus Costa, 1989 Phalloceros harpagos Lucinda, 2008 Poecilia reticulata Peters, 1859 Synbranchiformes Synbranchus marmoratus Bloch, 1795 Perciformes Cichlasoma paranaense Kullander, 1983 Crenicichla britskii Kullander, 1982 Geophagus brasiliensis (Quoy & Gaimard, 1824) Laetacara aff. dorsigera (Heckel, 1840) Oreochromis niloticus (Linnaeus, 1758) Satanoperca pappaterra (Heckel, 1840) Taxonomic classication follows Buckup et al. (2007)
a b c d

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Origina

Positionb

Tolerancec

Trophicd

NAT NAT NAT NAT NAT EXO NAT NAT NAT NAT NAT EXO ALO

NEK/BAN NEK/BAN BEN/LEA SUR SUR SUR NEK/BAN BEN NEK/BAN BEN BEN BEN BEN

TOL TOL INT INT INT TOL TOL TOL INT TOL TOL TOL TOL

AQUINS AQUINS AQUINS ONI ONI DET CAR ONI AQUINS ONI ONI ONI ONI

Langeani et al. (2007) Casatti et al. (2001), personal observations; Casatti (2002) Kramer & Mehegan (1981), Araujo & Garutti (2003), Bozzetti & Schulz (2004), personal observations

Andrian et al. (1994), Castro & Casatti (1997), Uieda et al. (1997), Gibran et al. (2001), Casatti (2002), Ferreira & Casatti (2006), Ceneviva-Bastos & Casatti (2007)

more tolerant Perciformes and Cyprinodontiformes species, modifying the original proportions. In this study, however, neither species richness nor relative abundance of Characiformes and Siluriformes could separate higher quality from degraded streams. It is expected that in slightly degraded streams few dominant species and many rare species would be recorded (Ferreira & Casatti, 2006). The dominance of a few species with low species richness is typical of degraded environments. Often, (the few) dominant species are also those most tolerant of changes in both limnological and structural conditions. Of the two dominance indices calculated, the Simpson index enabled more sensitive discrimination between higher quality and degraded streams. Metrics reecting habitat use Habitat use is potentially one of the most informative, but few data sets are available enabling assessment of the integrity of aquatic ecosystems. This is because

information about habitat use is very reliable only if it is obtained from direct observations in the environment, and there are practical limitations to conducting studies of this nature (Sabino, 1999). A number of regional adjustments in the metrics originally proposed by Karr (1981) were made; however, few were actually tested. Among metrics reecting habitat use which were tested, only the number of nektonic species (Karr, 1981) and the number of rheophilic species (Harris, 1995) enabled sensitive discrimination between high quality and degraded streams. According to the denition of Lincoln et al. (1995), nektonics are active swimmers in the water column and, therefore, they have great maneuverability between habitat patches of better quality. This metric was originally proposed as the number of water column species and its increase would be an indicator of conservation (Karr, 1981). By studying streams in southern Brazil, Bozzetti & Schulz (2004) considered that this guild would be more indicative of

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180 Table 3 Metrics (n = 22) qualitatively selected to be combined in the sh index of biotic integrity for lowland streams in southeastern Brazil

Hydrobiologia (2009) 623:173189

Metric Fish richness, composition, and dominance Number of species Number of native species Percentage of Characiformes and Siluriformes richness Percentage abundance of Characiformes and Siluriformes Dominance (BergerParker index) Dominance (Simpson index) Habitat use Number of nektonic species Percentage abundance of nektonic species Number of benthic species Percentage abundance of benthic species Number of rheophilic species Percentage abundance of rheophilic species Trophic structure Frequency of occurrence of detritus in the diet of nektonic Characidae Number of feeding categories in the diet of nektonic Characidae Frequency of occurrence of Trichoptera larvae in the diet of nektonic Characidae Physical condition of sh and tolerance Percentage of individuals with pathologies Percentage of individuals tolerant of hypoxia Percentage abundance of Poecilia reticulata Abundance and biomass Abundance by square meter Native abundance by square meter Biomass by square meter Native biomass by square meter

Ref.

Karr (1981) Lyons et al. (1995) Ferreira & Casatti (2006) Present study Present study Ferreira & Casatti (2006) Karr (1981) Ferreira & Casatti (2006) Karr (1981) Lyons et al. (1995) (adapted) Harris (1995) Ferreira & Casatti (2006) Present study Present study Present study

Karr (1981) Karr (1981) (adapted) Ferreira & Casatti (2006) Karr (1981) Present study Karr (1981) Present study

degradation, because of habitat complexity losses caused by the input of ne sediment in the water bodies, making the environment less favorable to benthic species and more favorable to nektonics. Our results demonstrate that, in extremely silted streams, not even the nektonic species are able to establish themselves, because habitat volume reduction compromises their swimming performance along the water column. In temperate regions the number of stream benthic species seems to indicate the quality of the substrate (Roth et al., 1999). In this study, this metric and also the number of rheophilic species were able to discriminate pristine from very poor habitat conditions, in contrast with benthic abundances (Fig. 2).

However, benthic species such as Aspidoras fuscoguttatus and Corydoras aeneus are often abundant in silted streams (Araujo & Garutti, 2003; Casatti, 2004), demonstrating that the term benthic does not always distinguish tolerant species from those intolerant of siltation. For this reason we decided to exclude the number of benthic species from the nal IBI calculation, following Harriss (1995) recommendation to consider only the number of rheophilic species. Roth et al. (2000) used the percentage of litophilous individuals (the number of individuals of a community belonging to a species that use rocky substrates for reproduction) for calculation of the IBI of streams in the USA. As such species generally use

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Hydrobiologia (2009) 623:173189 Fig. 2 Graphic representations of median (squares), 1st and 3rd quartiles (boxes), standard deviations (lines) and outliers (circles) of 22 biological attributes tested as a function of habitat integrity categories. Good conditions refer to those observed in reference rstorder stretches in lowland streams of the Upper Rio system Parana

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interstitial spaces between rocks on the river bed during reproductive events, this guild is often susceptible to siltation and tends to diminish in sites impacted by sediment input. Nevertheless, knowledge of reproductive biology of the sh fauna in the Upper Parana River system is not enough to compile a safe list of litophilous species, so that information was not incorporated into the IBI composition.

Metrics reecting trophic structure The trophic metrics in the composition of the IBI reect the extent of change in food chains. The main metrics tested in the literature are restricted to examining the representativeness of a particular guild, both in terms of number of individuals and/or species. The rst version of the IBI (Karr, 1981) contained an

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182 Fig. 2 continued

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abundance of omnivores, insectivores, and top predators, all of which were common in streams of pristine temperate regions. The abundance of insectivores refers to species of Cyprinidae which feed exclusively on terrestrial insects. In degraded environments, cyprinids are expected to be represented by few individuals or to be missing (Karr, 1981).

As already mentioned, trophic specialization in tropical freshwater shes is rare (Abelha et al., 2001) and therefore, when only insectivores species are recorded, this may be more because of food availability than trophic specialization. Furthermore, the contribution of Formicidae in tropical streams is remarkable and this item is abundant even in those

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Hydrobiologia (2009) 623:173189 Fig. 2 continued

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most degraded (personal observation), making it impracticable to incorporate the insectivores guild into the IBI. In pristine streams of tropical regions, a reasonable variety of food resources (testate amoebas, algae, plants, mollusks, microcrustaceans, spiders, mites, aquatic insects, terrestrial insects, and periphyton), with frequent record of some guilds such as omnivores, aquatic insectivores, and periphytivores, are expected to be found (Uieda et al., 1997; Casatti, 2002). Representatives of aquatic insectivore and periphytivore species are small catsh of the family Heptapteridae and armored catshes of the family Loricariidae, respectively. When the extent of human interference is from moderate to severe, these taxa are generally at a disadvantage because they are dependent on preserved substrates for shelter and foraging sites.

On the other hand, omnivores are mainly represented by small nektonic Characidae (mainly from the genera Astyanax, Piabina, Moenkhausia, and Hemigrammus) which depend on a reasonable portion of the water column to capture items brought in by the current; they are, therefore, at a disadvantage in cases of water column reduction. As human interference increases, the number of food categories decreases, being substituted, in extreme cases, almost exclusively by detritus (Oliveira & Bennemann, 2005). So, because of the ability to capture food items offered in various strata of the water column, nektonic species may provide a more reliable picture of the availability of food resources, making it possible to infer the quality of the local food supply. In higher-quality streams, detritus is restricted to river beds in depositional areas and, because of this,

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184 Table 4 Responses of metric comparison between reference and very poor habitat quality sites

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Metric Number of species Number of native species Percentage of Characiformes and Siluriformes richness Percentage abundance of Characiformes and Siluriformes Dominance (BergerParker index) Dominance (Simpson index) Number of nektonic species Percentage abundance of nektonic species Number of benthic species Percentage abundance of benthic species Number of rheophilic species Percentage abundance of rheophilic species Frequency of occurrence of detritus in the diet of nektonic Characidae Number of feeding categories in the diet of nektonic Characidae Frequency of occurrence of Trichoptera larvae in the diet of nektonic Characidae Percentage of individuals with pathologies Percentage of individuals tolerant of hypoxia Percentage abundance of Poecilia reticulata Abundance by square meter

Sensitivity 3 3 1 1 0a 3 3 0b 3 0b 3 3 3 3 3 0b 3 0b 0a 3 3 0a

U 0.5 0.5 12.0 11.0 19.0 5.0 1.0 24.0 3.0 21.0 0.5 4.0 0 2 0 22.0 4.0 14.0 18.0 8.0 11.0 12.0

U P-level 0.004* 0.004* 0.146 0.115 0.544 0.008* 0.005* 1.000 0.011* 0.716 0.004* 0.015* 0.008* 0.017* 0.007* 0.808 0.015* 0.223 0.467 0.052 0.115 0.146

*Valid metrics based on sensitivity with MannWhitney (U) results (P \ 0.05) Table 5 Predicted response and criteria used for scoring IBI metrics adapted for this study

Native abundance by square meter Biomass by square meter Native biomass by square meter

Metric

Predicted response Decrease Increase Decrease Decrease Increase Decrease Decrease Increase

Scoring criteria 5 x C 14 x \ 12 xC3 x[2 x \ 58 xC9 x C 12 x \ 32 3 x = 13 12 B x \ 20 x=2 x=2 58 B x \ 88 x=8 12 \ x B 9 32 B x \ 58 1 x \ 13 x C 20 xB1 xB1 x C 88 x\8 x\9 x C 58

1. Number of native species 2. Dominance (Simpson index) 3. Number of nektonic species 4. Number of rheophilic species 5. Frequency of occurrence of detritus in the diet of nektonic Characidaea 6. Number of feeding categories in the diet of nektonic Characidaea
a

Metrics excluded from this analysis because of low representativeness of specimens

7. Frequency of occurrence of Trichoptera larvae in the diet of nektonic Characidaea 8. Percentage of individuals tolerant of hypoxia

this item is usually absent in the diet of species that forage in the water column. In contrast, in degraded streams, detritus may be one of the most abundant items (Oliveira & Bennemann, 2005) available all along the water column, and its presence in the diet of

nektonic sh species may be indicative of some impairment. The frequency of Trichoptera larvae in the nektonic Characidae diet is, in contrast, not indicative of severely affected sites because most of these larvae live in clear, well oxygenated water,

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185

Table 6 Detailed descriptions of stream biological integrity associated with each of the IBI categories (adapted from Roth et al., 2000) and summary of the IBI scores calculated for the 56 rst-order streams (mean standard deviation) Categories Good Values 4.05.0 Descriptions Comparable with reference streams and regarded as minimally affected. On average, biological metrics fall within the upper 75% of the reference conditions Comparable with reference streams, but with some aspects of biological integrity compromised. On average, biological metrics are within the 75 and 50% of the reference conditions Signicant deviation from reference conditions, with many aspects of biological integrity not resembling the quality of minimally impacted streams. On average, biological metrics are within 50 and 25% of the reference conditions Strong deviation from reference conditions, with many aspects of biological integrity endangered, indicating severe degradation. Most biological metrics fall below 25% of the reference conditions Mean SD 4.2 (n = 1)

Fair

3.03.9

3.1 0.2 (n = 4)

Poor

2.02.9

2.4 0.2 (n = 10)

Very poor

01.9

1.3 0.3 (n = 41)

under rocks, trunks, or woody debris (Callisto et al., 2001); the presence of these larvae in the diet of shes is, therefore, a trophic metric indicative of good conditions. Metrics reecting physical condition and tolerance of sh The percentage of individuals with pathologies (Karr, 1981) reects the physical integrity of individuals in the community, and is a metric used in several versions of the IBI, especially in locations where the incidence of toxic compounds is high (Hughes & Oberdorff, 1998). In the set of streams studied, besides the absence of deformed sh, toxic compounds with a potential to cause such abnormalities are unlikely to be released into the waters, because the region was predominantly used for grazing (Silva et al., 2007). On the other hand, it is also well known that environmental stress can affect the physiological status of sh, affecting their immune system and making them more susceptible to parasite infestations (Pavanelli et al., 2002). Ectoparasites were detected in six streams, with 97% prevalence of Clinostomidae larvae, recorded in sh belonging to the genera Astyanax, Cyphocharax, and Steindachnerina. The intensity of the infection caused by these parasites is documented to be higher under less polluted conditions (Azevedo et al., 2007). In fact, sites classied as very poor had no record of these parasites (Fig. 2)

but, because of the few records and the absence of studies linking parasitic diseases to environmental degradation, this metric was provisionally excluded from the composition of the regional IBI. Tolerant species are those having adapted to low levels of dissolved oxygen, as Bozzetti & Schulz (2004) observed for two air-breathing armored catshes which may be abundant in both pristine (Casatti, 2002) and degraded sites (Casatti et al., 2006). Sites where unique or dominant species are also tolerant may exhibit severe degradation, as recorded for the guppy Poecilia reticulata in several streams. However, despite its importance as an alien species and a pioneer (Schleiger, 2000) and its absence from pristine streams, Poecilia reticulata cannot be included in the IBI composition, because its sensitivity was not sufcient to enable discrimination between higher quality and degraded sites. Metrics associated with abundance and biomass Neither the abundance and biomass metrics nor the native abundance and native biomass discriminated higher quality from impacted streams. This is probably because of the large contribution of abundance and biomass to degradation of other less susceptible native species (e.g., Serrapinnus spp., Gymnotus carapo, Laetacara aff. dorsigera), compromising the predictive power of these metrics.

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Hydrobiologia (2009) 623:173189

Biotic integrity In the study region, riparian zonesconsidered to be 30-m-wide strips along the water bodiesoccupy approximately 1,000 km2, of which 61 to 78% are occupied by grazing (Silva et al., 2007). Occupation of riparian zones promotes a decrease in the physical habitat quality of streams, especially headwaters, which are fragile environments regarded as poorly resilient. Among the non-trophic metrics, the lowest scores were obtained for dominance, number of rheophilic species, and number of native species. The last two are closely related to the simplication of the internal structure of the streams, which is a consequence from the increased ne sediment inputs to streams, and burying rapids. The loss of native species is a result of a long history of environmental degradation in the region and is the most serious and clear signal indicating a need for ecological restoration. The observation that many aspects of biological integrity of the sh fauna are altered, indicating serious degradation, reinforces the low quality of the physical habitat in the set of streams studied (Casatti et al., 2006). It is important to note that loss of biotic integrity does not always follow physical degradation of habitat, because losses of biotic integrity can result from a number of other factors (e.g., chemical pollution, introduction of alien species) which must be considered together with physical degradation. There is, moreover, a historic land-use component which must be taken into account (Harding et al., 1998), because sometimes it may mask contemporary ecological patterns. In a historical analysis, Harding et al. (1998) found that land use of drainages in the USA in the 1950s, particularly in agriculture, is the factor that best explains the present-day diversity in streams. In addition, past land use may cause such profound changes in aquatic diversity that even the reforestation of riparian zones is insufcient to restore and maintain stream biodiversity; to do this it would be necessary to recover and protect most or all of the watershed (Harding et al., 1998). The benets to water bodies of the presence of riparian vegetation are numerous (Pusey & Arthington, 2003, and authors cited therein) and may yet represent a great opportunity to increase connectivity between terrestrial habitats (Becker et al., 2004). The current cost of restoring one hectare of riparian forest o Paulo, for in the Rio Piracicaba basin in State of Sa

example, was estimated to be approximately US$3,350 (Silva et al., 2007). Assuming that this value is valid for other basins in the state, it is estimated that to restore the 700 km2 of degraded riparian zones in the region studied (corresponding to an average of 70% of riparian zones used for grazing, as mentioned by Silva et al., 2007) US$234 million would be necessary. We agree with the assumption that only restoration of the land strips adjacent to the streams is not enough to improve stream integrity as a way of maintaining natural diversity (Harding et al., 1998; Teels et al., 2006 and authors listed therein; ve que et al., 2008). Notwithstanding, restoration of Le the entire watershed in developing countries (especially those experiencing strong pressure for the production of biofuels) is not on the list of priorities, and we must nd alternatives to reduce stress and mitigate the impact on aquatic biota at lower cost. Finally, given the main impact on stream ecosystems of the study areaphysical degradation of the habitatisolation of riparian zones along the drainage, preventing their use for other activities, despite its limitation, must be investigated as a strategy for starting preservation of the streams and their biota. Some studies have reported the efciency and limitations of certain restorative methods, providing good examples of lower-cost actions (Holl et al., 2000; Bianconi et al., 2007).
rio de Ictiologia Acknowledgments We thank the Laborato colleagues for their help during eld work and the Departamento nica IBILCE-UNESP for facilities, IBAMA de Zoologia e Bota for obtaining a license (001/2003), landowners for permission to conduct research on their properties, Ricardo M. C. Castro for information about reference sites, Sirlei T. Bennemann and Oscar A. Shibatta for suggestions, Francisco L. Tejerina-Garro lio F. Baptista for comments, and David R. Mercer for and Darc language revision. This study was made possible by funding from FAPESP in the BIOTA/FAPESP Program (www.biota. org/br). LC receives grants from CNPq (141028/2007-6) and CPF from FAPESP (06/01479-4).

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