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P R I M A R Y R E S E A R C H P A P E R

A fish-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 fish-based biotic integrity index to assess

lowland streams in a highly deforested region of the

Upper Parana River basin. Fifty-six first-order seg-

ments were randomly selected for environmental and

fish evaluation. Because previous analysis had identi-

fied the main type of effect on the streams of the region

as physical habitat degradation, 22 qualitatively bio-

logical attributes were selected and tested over a

physical condition gradient between reference and

degraded sites. Sensitivity and redundancy of eachattribute revealed that five metrics were adequate for

discriminating higher quality from degraded sites. Of

the fifty-six streams assessed, one (2%) was classified

as good, four (7%) as fair, ten (18%) as poor, and forty-

one (73%) as very poor, indicating that, on a regional

scale, many aspects of biological integrity are altered,

indicative of serious degradation. Considering that

first-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, indica-

tive 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 inte-

grate the behavior of elements and biological

processes at various levels of organization expressing

anthropogenic interference with aquatic communi-

ties. 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, definedas 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 fish 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. LangeaniDepartamento de Zoologia e Botanica, UNESP-Universidade Estadual Paulista, Laboratorio de Ictiologia,IBILCE, Rua Cristovao Colombo, 2265, 15054-000 SaoJose do Rio Preto, SP, Brazile-mail: lcasatti@ibilce.unesp.br

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DOI 10.1007/s10750-008-9656-x

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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

modifications, not reflecting environmental impacts

(Tejerina-Garro et al., 2006).

In continental Brazilian aquatic environments, the

IBI based on fish assemblages has been adapted toevaluate segments of a large river (Pinto & Araujo,

2007), reservoirs (Petesse et al., 2007), and streams in

the southern (Bozzetti & Schulz, 2004) and southeast-

ern 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 fish fauna diversity combined with the poor

knowledge of many systematic (Buckup et al., 2007)

and ecological aspects, and the difficulty of finding

water courses entirely conserved to serve as refer-ences, 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

Sao Paulo State, which has only 4% of its native

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 thestreamsmainly of first 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 fish species dependent

on rocky substrates and species that exploit the water

column (Casatti et al., 2006). Therefore, the devel-

opment 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

lowland streams of the Upper Parana River basin, in

southeastern Brazil.

Methods

Study area

Several environmental factors affect the structure of

fish 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

rocks of the Cauia and Bauru groups (IPT, 2001),

including drainage of the Sao Jose dos Dourados,

Turvo, and Grande rivers, in the northwest of the Sao

Paulo State. Native vegetation was mostly repre-

sented 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 rainyseason 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 min-

imum (13C) in July (IPT, 2001).

Reference sites, sampling sites, and fish collection

The concept of regional reference was adopted to test

biological attributes, because it is considered the mostappropriate 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 first-order streams (sensu

Strahler, scale 1:50.000) located in relatively less

degraded regions of the Upper Parana River system,

and previously studied in the states of Sao Paulo and

Parana (Casatti, 2002, 2005; Castro et al., 2003,

2004), were used as references (Fig. 1, Table 1).

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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 besampled 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.

The number of segments sampledper basin (Sao Jose

dos Dourados, Turvo, and Grande) was proportional

to the number of first-order kilometers in each basin.

Using a 1:50.000 topographic map base, the total extent

of first-order sections in each basin was calculated for a

further random selection of a stream approximately

every 100 km (modified from Rothet al., 1999). Within

each randomly selected stream, sites chosen for sam-pling 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 field conditions (Roth et al.,

1999). Following Kasyak (2001), a 75-m reach with

greater variability of available mesohabitats was

Fig. 1 Map showing the limits of the study area ( dark line), reference streams (R1R4, larger circles) and 56 sampled streams (156,small circles) in the northwestern region of Sao Paulo State, Brazil

Table 1 Location and general characterization of the reference streams used to calibrate candidate metrics

Streams Mean width(m)

Mean depth(m)

Dissolved oxygen(mg l-1)

Conductivity(lS cm-1)

pH

1. Corrego Sao Carlos 2236023.800S 5215008.600W 2.6 0.9 10.3 16 7.9

2. Corrego Santa Clara 2245054.200S 5225019.000W 1.6 0.7 11.3 30 7.6

3. Corrego Agua do Macaco 2239046.900S 5049039.500W 1.7 0.4 9.5 151 7.4

4. Unnamed stream, tributary of Rio Sapuca2100040.700S 4713011.500W

2.7 0.5 8.2 22 8.6

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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 col-lecting sites, with each section of blocked stream

using 5-mm mesh stop nets up and downstream, and

afterwards submitted to two electro-fishing passes

according to methods reported by Mazzoni et al.

(2000). Captured specimens were fixed in a 10%

formalin solution and, after 48 h, transferred to a 70%

EtOH solution. Fishes were identified by species,

counted, and weighed. All specimens were incorpo-

rated in the fish collection at the Departamento de

Zoologia e Botanica da Universidade Estadual Pauli-

sta (DZSJRP), Sao Jose do Rio Preto, Sao PauloState, Brazil.

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 computationalsoftware PAST (Hammer et al., 2001) and values

close to zero indicate low dominance.

Based on literature data and personal experience,

each species was classified according to its origin in

the Upper Parana hydrographic system (Langeani

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

representative nature (recorded in 95% of the sam-

pled streams). Frequency of occurrence and

dominance were calculated for each feeding item to

identify the most important items of the fish diet

(Bennemann et al., 2006).

Fish metrics test and IBI development

Previous analysis (Casatti et al., 2006) identified

physical habitat degradation as the main threat to the

integrity of fish assemblages, especially as a result of

the riparian vegetation removal and habitat simplifi-

cation. 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). PHI-

evaluated metrics were substrate stability, velocity

and depth variability, flow stability, bottom deposi-tion, combinations of pool-riffles-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 first 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 sev-

eral 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 fish

communities were excluded. For example, the pro-

portion of piscivores (Oberdorff & Hughes, 1992)

was eliminated in this assessment because, in small

streams of the region, exclusively piscivore fishes 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 impor-tance of substrate integrity in the reproduction of the

recorded fish 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

confirmed by the MannWhitney test (alpha = 0.05).

A redundancy analysis was performed using the

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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 redun-

dant 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 defining the set of metrics that best discrim-

inated 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 distri-

bution 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 first case would score 1, the second case

would score 5, and intermediate conditions, i.e.between the 75th and 25th percentiles of the refer-

ence 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).

Results

A total of 8,660 fishes 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 significant 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 toinclude the number of native species in the IBI final

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 final 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

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). Trophicmetrics were excluded from this analysis because

missing data resulted in low representativeness of

specimens in some stretches. Thus, final IBI compo-

sition comprised five 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 classified 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 biologicalintegrity are altered, indicative of serious degrada-

tion. Considering that first-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

Metrics reflecting fish 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 ofexotic 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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Table 2 Classification of sampled species according to theirorigin in the Upper Parana river system (NAT, natives; ALO,allochthonous; EXO, exotics), position in the water column(BEN/RIF, benthics associated with riffles; BEN, benthics;NEK, nektonics; NEK/BAN, nektonics associated with streambanks; SUR, close to the surface of the water; BEN/LEA,benthics associated with leaves), hypoxia tolerance (TOL,

tolerant; INT, intolerant), and trophic group (PER, periphyti-vores; DET, detritivores; AQUINS, insectivores withpredominance of aquatic forms; ONI, onivores; TERINS,insectivores with predominance of terrestrial forms; ALG,algivores; CAR, carnivores with predominance of invertebratesand fishes)

Order and species Origina Positionb Tolerancec Trophicd

Characiformes

Apareiodon piracicabae (Eigenmann, 1907) NAT BEN/RIF INT PER

Parodon nasus Kner, 1858 NAT BEN/RIF INT PER

Cyphocharax modestus (Fernandez-Yepez, 1948) NAT BEN INT DET

Cyphocharax vanderi (Britski, 1980) NAT BEN INT DET

Steindachnerina insculpta (Fernandez-Yepez, 1948) NAT BEN INT DET

Leporinus friderici (Bloch, 1794) NAT BEN INT ONI

Leporinus lacustris Campos, 1945 NAT BEN INT HER

Leporinus paranensis Garavello & Britski, 1987 NAT BEN INT ONI

Characidium aff. lagosantense Travassos, 1947 NAT BEN INT AQUINSCharacidium zebra Eigenmann, 1909 NAT BEN/RIF INT AQUINS

Astyanax altiparanae Garutti & Britski, 2000 NAT NEK INT ONI

Astyanax bockmanni Castro & Vari, 2007 NAT NEK INT ONI

Astyanax fasciatus (Cuvier, 1819) NAT NEK INT TERINS

Astyanax paranae Eigenmann, 1914 NAT NEK INT TERINS

Hemigrammus marginatus Ellis, 1911 NAT NEK INT TERINS

Hyphessobrycon eques (Steindachner, 1882) NAT NEK INT TERINS

Knodus moenkhausii (Eigenmann & Kennedy, 1903) ALO NEK TOL ONI

Moenkhausia sanctaefilomenae (Steindachner, 1907) NAT NEK INT TERINS

Oligosarcus pintoi Campos, 1945 NAT NEK/BAN INT TERINS

Piabina argentea Reinhardt, 1867 NAT NEK INT AQUINS

Serrapinnus heterodon (Eigenmann, 1915) NAT SUR TOL ALG

Serrapinnus notomelas (Eigenmann, 1915) NAT SUR TOL ALG

Acestrorhynchus lacustris (Lutken, 1875) NAT NEK/BAN INT CAR

Erythrinus erythrinus (Bloch & Schneider, 1801) NAT NEK/BAN TOL CAR

Hoplias malabaricus (Bloch, 1794) NAT NEK/BAN TOL CAR

Pyrrhulina australis Eigenmann & Kennedy, 1903 NAT SUR TOL ALG

Siluriformes

Aspidoras fuscoguttatus Nijssen & Isbrucker, 1976 NAT BEN TOL AQUINS

Corydoras aeneus (Gill, 1858) NAT BEN TOL AQUINS

Callichthys callichthys (Linnaeus, 1758) NAT BEN TOL ONI

Hoplosternum littorale (Hancock, 1828) NAT BEN TOL ONI

Hisonotus francirochai (Ihering, 1928) NAT BEN/LEA INT DET

Hypostomus ancistroides (Ihering, 1911) NAT BEN TOL DET

Hypostomus sp. NAT BEN/RIF INT PER

Imparfinis mirini Haseman, 1911 NAT BEN/RIF INT AQUINS

Imparfinis schubarti (Gomes, 1956) NAT BEN INT AQUINS

Pimelodella avanhandavae Eigenmann, 1917 NAT BEN INT AQUINS

Rhamdia quelen (Quoy & Gaimard, 1824) NAT BEN TOL AQUINS

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more tolerant Perciformes and Cyprinodontiformesspecies, 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 thetwo dominance indices calculated, the Simpson index

enabled more sensitive discrimination between higher

quality and degraded streams.

Metrics reflecting 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 itis obtained from direct observations in the environ-

ment, 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

reflecting 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 definition of Lincoln et al.

(1995), nektonics are active swimmers in the water

column and, therefore, they have great maneuver-

ability 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

Table 2 continued

Order and species Origina Positionb Tolerancec Trophicd

Gymnotiformes

Gymnotus carapo Linnaeus, 1758 NAT NEK/BAN TOL AQUINS

Gymnotus inaequilabiatus (Valenciennes, 1839) NAT NEK/BAN TOL AQUINS

Eigenmannia virescens (Valenciennes, 1842) NAT BEN/LEA INT AQUINSCyprinodontiformes

Rivulus pictus Costa, 1989 NAT SUR INT ONI

Phalloceros harpagos Lucinda, 2008 NAT SUR INT ONI

Poecilia reticulata Peters, 1859 EXO SUR TOL DET

Synbranchiformes

Synbranchus marmoratus Bloch, 1795 NAT NEK/BAN TOL CAR

Perciformes

Cichlasoma paranaense Kullander, 1983 NAT BEN TOL ONI

Crenicichla britskii Kullander, 1982 NAT NEK/BAN INT AQUINS

Geophagus brasiliensis (Quoy & Gaimard, 1824) NAT BEN TOL ONI

Laetacara aff. dorsigera (Heckel, 1840) NAT BEN TOL ONI

Oreochromis niloticus (Linnaeus, 1758) EXO BEN TOL ONI

Satanoperca pappaterra (Heckel, 1840) ALO BEN TOL ONI

Taxonomic classification follows Buckup et al. (2007)a Langeani et al. (2007)b Casatti et al. (2001), personal observations; Casatti (2002)c Kramer & Mehegan (1981), Araujo & Garutti (2003), Bozzetti & Schulz (2004), personal observationsd Andrian et al. (1994), Castro & Casatti (1997), Uieda et al. (1997), Gibran et al. (2001), Casatti (2002), Ferreira & Casatti (2006),Ceneviva-Bastos & Casatti (2007)

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degradation, because of habitat complexity losses

caused by the input of fine 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 establishthemselves, because habitat volume reduction com-

promises 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 condi-

tions, in contrast with benthic abundances (Fig. 2).

However, benthic species such as Aspidoras fusco-

guttatus 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 toexclude the number of benthic species from the final

IBI calculation, following Harriss (1995) recom-

mendation to consider only the number of rheophilic

species.

Roth et al. (2000) used the percentage of litoph-

ilous 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

Table 3 Metrics (n = 22)qualitatively selected to becombined in the fish indexof biotic integrity forlowland streams insoutheastern Brazil

Metric Ref.

Fish richness, composition, and dominance

Number of species Karr (1981)

Number of native species Lyons et al. (1995)

Percentage of Characiformes and Siluriformes richness Ferreira & Casatti (2006)

Percentage abundance of Characiformes and Siluriformes Present studyDominance (BergerParker index) Present study

Dominance (Simpson index) Ferreira & Casatti (2006)

Habitat use

Number of nektonic species Karr (1981)

Percentage abundance of nektonic species Ferreira & Casatti (2006)

Number of benthic species Karr (1981)

Percentage abundance of benthic species Lyons et al. (1995) (adapted)

Number of rheophilic species Harris (1995)

Percentage abundance of rheophilic species Ferreira & Casatti (2006)

Trophic structure

Frequency of occurrence of detritus in the diet of nektonicCharacidae

Present study

Number of feeding categories in the diet of nektonicCharacidae

Present study

Frequency of occurrence of Trichoptera larvae in the dietof nektonic Characidae

Present study

Physical condition of fish and tolerance

Percentage of individuals with pathologies Karr (1981)

Percentage of individuals tolerant of hypoxia Karr (1981) (adapted)

Percentage abundance of Poecilia reticulata Ferreira & Casatti (2006)

Abundance and biomass

Abundance by square meter Karr (1981)Native abundance by square meter Present study

Biomass by square meter Karr (1981)

Native biomass by square meter Present study

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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, knowl-

edge of reproductive biology of the fish 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 reflecting trophic structure

The trophic metrics in the composition of the IBI

reflect the extent of change in food chains. The main

metrics tested in the literature are restricted to exam-

ining the representativeness of a particular guild, both

in terms of number of individuals and/or species.

The first version of the IBI (Karr, 1981) contained an

Fig. 2 Graphicrepresentations of median(squares), 1st and 3rdquartiles (boxes), standarddeviations (lines) andoutliers (circles) of 22biological attributes tested

as a function of habitatintegrity categories. Goodconditions refer to thoseobserved in reference first-order stretches in lowlandstreams of the Upper RioParana system

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abundance of omnivores, insectivores, and top preda-

tors, 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, cyp-

rinids are expected to be represented by few

individuals or to be missing (Karr, 1981).

As already mentioned, trophic specialization in

tropical freshwater fishes is rare (Abelha et al., 2001)

and therefore, when only insectivores species are

recorded, this may be more because of food avail-

ability than trophic specialization. Furthermore, the

contribution of Formicidae in tropical streams is

remarkable and this item is abundant even in those

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 amoe-

bas, algae, plants, mollusks, microcrustaceans,

spiders, mites, aquatic insects, terrestrial insects,

and periphyton), with frequent record of some guilds

such as omnivores, aquatic insectivores, and periph-ytivores, are expected to be found (Uieda et al., 1997;

Casatti, 2002). Representatives of aquatic insectivore

and periphytivore species are small catfish of the

family Heptapteridae and armored catfishes 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 repre-

sented 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 disadvan-

tage in cases of water column reduction. As human

interference increases, the number of food categoriesdecreases, 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,

Fig. 2 continued

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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 fish 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,

Table 4 Responses ofmetric comparison betweenreference and very poorhabitat quality sites

*Valid metrics based onsensitivity with Mann-Whitney (U) results(P\0.05)

Metric Sensitivity U U P-level

Number of species 3 0.5 0.004*

Number of native species 3 0.5 0.004*

Percentage of Characiformes and Siluriformes richness 1 12.0 0.146

Percentage abundance of Characiformes and Siluriformes 1 11.0 0.115

Dominance (BergerParker index) 0a 19.0 0.544Dominance (Simpson index) 3 5.0 0.008*

Number of nektonic species 3 1.0 0.005*

Percentage abundance of nektonic species 0b 24.0 1.000

Number of benthic species 3 3.0 0.011*

Percentage abundance of benthic species 0b 21.0 0.716

Number of rheophilic species 3 0.5 0.004*

Percentage abundance of rheophilic species 3 4.0 0.015*

Frequency of occurrence of detritus in the diet of nektonicCharacidae

3 0 0.008*

Number of feeding categories in the diet of nektonic

Characidae

3 2 0.017*

Frequency of occurrence of Trichoptera larvae in thediet of nektonic Characidae

3 0 0.007*

Percentage of individuals with pathologies 0b 22.0 0.808

Percentage of individuals tolerant of hypoxia 3 4.0 0.015*

Percentage abundance of Poecilia reticulata 0b 14.0 0.223

Abundance by square meter 0a 18.0 0.467

Native abundance by square meter 3 8.0 0.052

Biomass by square meter 3 11.0 0.115

Native biomass by square meter 0a 12.0 0.146

Table 5 Predictedresponse and criteria usedfor scoring IBI metricsadapted for this study

a Metrics excluded fromthis analysis because of lowrepresentativeness ofspecimens

Metric Predictedresponse

Scoring criteria

5 3 1

1. Number of native species Decrease x C 14 x = 13 x\13

2. Dominance (Simpson index) Increase x\ 12 12 B x\ 20 x C 20

3. Number of nektonic species Decrease x C 3 x = 2 x B 1

4. Number of rheophilic species Decrease x[ 2 x = 2 x B 1

5. Frequency of occurrence of detritusin the diet of nektonic Characidaea

Increase x\ 58 58 B x\ 88 x C 88

6. Number of feeding categories

in the diet of nektonic Characidae

a

Decrease x C 9 x = 8 x\8

7. Frequency of occurrence of Trichopteralarvae in the diet of nektonic Characidaea

Decrease x C 12 12\x B 9 x\9

8. Percentage of individuals tolerant of hypoxia Increase x\ 32 32 B x\ 58 x C 58

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under rocks, trunks, or woody debris (Callisto et al.,

2001); the presence of these larvae in the diet of

fishes is, therefore, a trophic metric indicative of

good conditions.

Metrics reflecting physical condition and

tolerance of fish

The percentage of individuals with pathologies (Karr,

1981) reflects the physical integrity of individuals inthe 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 fish, toxic com-

pounds 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 fish, affecting their immune system andmaking them more susceptible to parasite infestations

(Pavanelli et al., 2002). Ectoparasites were detected

in six streams, with 97% prevalence of Clinostomidae

larvae, recorded in fish 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 condi-

tions (Azevedo et al., 2007). In fact, sites classified 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

catfishes which may be abundant in both pristine

(Casatti, 2002) and degraded sites (Casatti et al.,

2006). Sites where unique or dominant species arealso 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 composi-

tion, because its sensitivity was not sufficient 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 prob-

ably 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.

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 first-order streams (mean standard deviation)

Categories Values Descriptions Mean SD

Good 4.05.0 Comparable with reference streams and regarded as minimallyaffected. On average, biological metrics fall within the upper75% of the reference conditions

4.2 (n = 1)

Fair 3.03.9 Comparable with reference streams, but with some aspects of biological integrity compromised. On average, biologicalmetrics are within the 75 and 50% of the referenceconditions

3.1 0.2 (n = 4)

Poor 2.02.9 Significant deviation from reference conditions, with manyaspects of biological integrity not resembling the quality ofminimally impacted streams. On average, biological metricsare within 50 and 25% of the reference conditions

2.4 0.2 (n = 10)

Very poor 01.9 Strong deviation from reference conditions, with many aspectsof biological integrity endangered, indicating severedegradation. Most biological metrics fall below 25% of thereference conditions

1.3 0.3 (n = 41)

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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 physicalhabitat 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 simplification of

the internal structure of the streams, which is a

consequence from the increased fine 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 andclear signal indicating a need for ecological restoration.

The observation that many aspects of biological

integrity of the fish 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 insufficient to

restore and maintain stream biodiversity; to do thisit would be necessary to recover and protect most or

all of the watershed (Harding et al., 1998).

The benefits to water bodies of the presence of

riparian vegetation are numerous (Pusey & Arthing-

ton, 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

in the Rio Piracicaba basin in State of Sao Paulo, for

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 millionwould 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;

Leveque et al., 2008). Notwithstanding, restoration of

the entire watershed in developing countries (espe-

cially those experiencing strong pressure for the

production of biofuels) is not on the list of priorities,

and we must find alternatives to reduce stress and

mitigate the impact on aquatic biota at lower cost.Finally, given the main impact on stream ecosys-

tems of the study areaphysical degradation of the

habitatisolation of riparian zones along the drain-

age, 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 efficiency and

limitations of certain restorative methods, providing

good examples of lower-cost actions (Holl et al.,

2000; Bianconi et al., 2007).

Acknowledgments We thank the Laboratorio de Ictiologiacolleagues for their help during field work and the Departamentode Zoologia e Botanica IBILCE-UNESP for facilities, IBAMAfor obtaining a license (001/2003), landowners for permission toconduct research on their properties, Ricardo M. C. Castro forinformation about reference sites, Sirlei T. Bennemann andOscar A. Shibatta for suggestions, Francisco L. Tejerina-Garroand Darclio F. Baptista for comments, and David R. Mercer forlanguage revision. This study was made possible by fundingfrom FAPESP in the BIOTA/FAPESP Program (www.biota.org/br). LC receives grants from CNPq (141028/2007-6) andCPF from FAPESP (06/01479-4).

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