Science of the Total Environment 409 (2011) 612–624

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Science of the Total Environment

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Assessing land-use effects on water quality, in-stream habitat, riparian ecosystems

and biodiversity in Patagonian northwest streams
María Laura Miserendino a,⁎, Ricardo Casaux a, Miguel Archangelsky a, Cecilia Yanina Di Prinzio a,
Cecilia Brand a, Adriana Mabel Kutschker b
a
CONICET Laboratorio de Investigaciones en Ecología y Sistemática Animal-Universidad Nacional de la Patagonia San Juan Bosco, Argentina
b
Cátedra de Ecología-Facultad de Ciencias Naturales - Universidad Nacional de la Patagonia San Juan Bosco, Argentina

a r t i c l e i n f o a b s t r a c t

Article history: Changes in land-use practices have affected the integrity and quality of water resources worldwide. In
Received 15 April 2010 Patagonia there is a strong concern about the ecological status of surface waters because these changes are
Received in revised form 14 October 2010 rapidly occurring in the region. To test the hypothesis that greater intensity of land-use will have negative
Accepted 16 October 2010
effects on water quality, stream habitat and biodiversity we assessed benthic macroinvertebrates, riparian/
Available online 20 November 2010
littoral invertebrates, fish and birds from the riparian corridor and environmental variables of 15 rivers
(Patagonia) subjected to a gradient of land-use practices (non-managed native forest, managed native forest,
Keywords:
Water quality
pine plantations, pasture, urbanization). A total of 158 macroinvertebrate taxa, 105 riparian/littoral
Macroinvertebrates invertebrate taxa, 5 fish species, 34 bird species, and 15 aquatic plant species, were recorded considering
Fish all sites. Urban land-use produced the most significant changes in streams including physical features,
Bird conductivity, nutrients, habitat condition, riparian quality and invertebrate metrics. Pasture and managed
Pastures native forest sites appeared in an intermediate situation. The highest values of fish and bird abundance and
Forest management diversity were observed at disturbed sites; this might be explained by the opportunistic behavior displayed by
these communities which let them take advantage of increased trophic resources in these environments. As
expected, non-managed native forest sites showed the highest integrity of ecological conditions and also great
biodiversity of benthic communities. Macroinvertebrate metrics that reflected good water quality were
positively related to forest land cover and negatively related to urban and pasture land cover. However, by
offering stream edge areas, pasture sites still supported rich communities of riparian/littoral invertebrates,
increasing overall biodiversity. Macroinvertebrates were good indicators of land-use impact and water quality
conditions and resulted useful tools to early alert of disturbances in streams. Fish and birds having a greater
ability of dispersion and capacity to move quickly from disturbances would reflect changes at a higher scale.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction
All over the world the ecological integrity of river systems is being
endangered by land-use changes. This widespread and ever-increasing
phenomenon involving urbanization, agriculture, pasture conversion,
deforestation, and the replacement of native species by exotic ones with
commercial value, represents a real and pervasive threat to the
biodiversity and conservation of lotic ecosystems (Allan 2004; Morley
and Karr, 2001; Paul and Meyer, 2001; Scrimgeour and Kendall, 2003).
However, the relationship between land-use change and alteration of
stream physical characteristics can be complex and influenced by many
factors acting from different spatial scales ranging from local (e.g.,
adjacent to the stream) to basin level or to ecoregional scales (Goldstein
⁎ Corresponding author. CONICET Laboratorio de Investigaciones en Ecología y
Sistemática Animal FCN-Universidad Nacional de la Patagonia-Sede Esquel Sarmiento
849-9200 Esquel-Chubut-Argentina. Tel.: + 54 2945 451165; fax: + 54 2945 452271.
E-mail address: mlau@ar.inter.net (M.L. Miserendino).
et al., 2007). In this sense, current threats to global biodiversity require
understanding of how progressively or locally human activities might
scale up to affect regional biotas (Manel et al., 2000). This phenomenon
has captured the attention of scientists dedicated to the study of
communities living in aquatic ecosystems and those associated with
their riparian corridors (Danger and Robson, 2004; Diamond et al.,
2002; Meador and Goldstein, 2003; Saunders et al., 2002; Thompson
and Townsend, 2004).
Widespread removal of basin vegetation has been shown to alter
flow characteristics, to change the amount of sediment introduced to
stream systems (Walling and Fang, 2003), to decrease infiltration and
increase surface runoff. Frequently, stream concentrations of many
chemical constituents such as nitrate concentration and phosphorus
compounds are affected both directly and indirectly by human land-
use (Bahar et al., 2008; Quinn et al., 1997). In turn, increases in
nutrients can result in overgrowth of algae and aquatic plants, which
potentially alter habitat suitability for endemic fauna (Hall et al.,
2001).

0048-9697/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2010.10.034
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624
Channelization and realignment of rivers are also common
practices in urban or agricultural areas, which can produce substrate
modification and disruption of the riffle/pool sequences that provide a
diversity of habitats for aquatic species such as fish and invertebrates
(Jones et al., 1999; Nolan and Guthrie, 1998). The clearing of riparian
areas alongside rivers, as modification and/or extirpation of stream-
side vegetation, can also alter the functioning of river ecosystems and
disrupt fluxes of organic matter and energy (McCord et al., 2007).
Moreover this can affect directly or indirectly the river biota. For
example, the loss of oviposition sites and habitat for aerial stages of
insects with aquatic larvae can be critical to preserve “in stream”
macroinvertebrate diversity (Bojsen and Jacobsen, 2003).
There is ample evidence that landscape factors influence aquatic
vertebrate fauna, as for instance landscape characteristics can be
linked to fish species assemblages (Walters et al., 2003). Allan (2004)
has shown significant relationships between some landscape metrics
such as amount of agricultural, forest or urban land cover, and some
biological metrics for fish. At a more local scale, habitat conditions can
affect fish distribution as has been observed by Wohl (2000), who
reported that some native species in highland stream systems may be
particularly vulnerable to replacement by generalist species in
response to increased sediment input.
Fragmentation of continuous habitats (e.g. riparian corridors and
native forest) results in habitat loss and an increase in isolation, which
might affect birds by decreasing colonization, increasing mortality
and extinction, and reducing biodiversity, among other potential
effects (Saunders et al., 1991; Wilcox and Murphy, 1985). Changes in
agricultural practices also continue to have a wide range of effects on
terrestrial and aquatic birds species (Duncan et al., 1999; Henderson
et al., 2000), whereas urbanization is considered one of the leading
drivers of native bird species extirpation at the continental and
regional scales (Czech et al., 2000).
Biodiversity in Patagonian mountains, is globally significant due to
pronounced endemism, habitat heterogeneity and biogeographic
location (Morrone 2006; Paruelo et al., 1998). Presently there is a
strong concern because land-use practices are changing rapidly the
landscape in the region, being the most widespread activities the
conversion of native forest to pasture, forest exploitation (wood
collection for fuel, carpentry, etc.), and the substitution of native
forest for pine plantations. These human activities have gained
attention in recent studies: analyses of water quality and macro-
invertebrate response to impairment (Miserendino and Pizzolón,
2000; Miserendino et al., 2008); land-use changes (Miserendino,
2004; Miserendino and Pizzolón 2004); effect on fish (Di Prinzio et al.,
2009; Lara et al., 2009) and bird communities (Lantschner and Rusch,
2007; Willson et al., 1994).
Assessing the impact of land-use activities on river catchments is
an important subject faced by resource managers. Although stream
ecologists traditionally have tried to address how land-use changes
affect aquatic environments, integrated approaches examining dis-
turbance through environmental features and biological communities
(including aquatic plants, macroinvertebrates, riparian and littoral
invertebrates, fish and birds) are not frequent. It is also crucial to
regionally calibrate and test existing stream assessment protocols.
To test the hypothesis that greater intensity of land-use will have
negative effects on water quality, stream habitat and biodiversity, in
this work we assess 18 stream sites (north-western Chubut province)
subjected to a gradient of land-use practices (non-managed native
forest, managed native forest, pine plantations, pasture, urbaniza-
tion). We also evaluate the quality of riparian ecosystems and in
stream habitat conditions using two indexes adapted to Patagonian
environments and assess the values of these indexes as predictors of
the biotic assemblages. Finally, we attempt to identify which
communities are more responsive to local and large scale changes in
Patagonian mountain streams in order to suggest better management
practices.
613
2. Materials and methods
2.1. Study area and site selection
The study area belongs to the Andean-Humid and Sub-Andean
Sub-Humid regions (Del Valle et al., 1998; Paruelo et al., 1998) and is
located in a transitional mountain and piedmont area in the
Northwest of Chubut province, Argentina between the Chilean border
and the city of Esquel in Northern Patagonia (Fig. 1). Studied basins
are similar in size, gradient and geology. From a phytogeographic
perspective, the study area is located in the ecotone between the
Subantarctic Forest and the Patagonian steppe, and exhibits a marked
altitudinal gradient. The Subantarctic Forest is constituted by
perennial (Austrocedrus chilensis, Nothofagus dombeyi and Maitenus
boaria) and deciduous tree species (N. pumilio, N. antarctica), whereas
the shrub and herbaceous strata are composed mainly by Chusquea
culeou, Berberis buxifolia, Fuchsia magellanica, Aristotelia chilensis,
Oenothera odorata, Fragaria chiloensis and Geranium sp. The valleys are
dominated by the herbaceous, shrub-like steppe vegetation, Mulinum
spinosum, Stipa speciosa, S. humilis, Corynabutilon bicolor, Verbena
tridens, Nassauvia glomerulosa and Berberis heterophylla (Tell et al.,
1997).
The exotic vegetation is composed mainly by forests of Pseudot-
suga menziesii, Pinus ponderosa, P. radiata and P. lambertiana; in many
cases these species occupy the riparian corridor replacing most of the
native species.
Across our study region, we sampled streams impacted by four
different land-uses: selective harvest of native forests (HNF: managed
native forest), plantations of non-native commercially-harvest conifers
(Pn: pine plantations), grazed pasture (Pas: pasture), and urbanization
(Ur: urban). We also sampled two types of reference streams: non-
managed native forests (NF) and reference urban streams (R-ur).
Within each of these six categories, we collected samples from three
streams. A sampling site was a 100-m reach of the selected stream, for
bird censuses this area was extended to accomplish the protocol (see
biological sampling).
Sites on non-managed native Nothofagus forest (NF: Chiquito, Loro
and Comisario) were considered as reference sites to test for the
following impacts: conversion of forest to pasture, pine plantation and
wood extraction. Three sites on streams with native N. antarctica and
N. pumilio managed forest were selected (HNF: Glyn, Cabeza de Vaca
and Pipo). At these sites the harvest was achieved during the spring
and summer seasons previous to the study. The logging operations
implied a selective cut of young to mature trees (dead and live
specimens), which affected no more than 50% of the studied area/
parcel. Exploitation should exclude specimens from the river corridor
and operators also have to keep the streams free of debris and
branches once the tree is logged. However during the survey we
observed some river corridors having logged trees, and some water-
courses obstructed with debris. Most of the properties having wood
collection permission have a mixed management, thus areas are used
for extensive livestock which is sustained by the herbaceous stratum.
To assess pasture impact we selected sites (Pas: Nant y Fall,
Manguera and Los Ñires) that had been cleared from the native
Nothofagus forest (~60–70 years ago) and had been intensively grazed.
Pasture sites sustain livestock, mainly cows and sheep. The pine
plantations sites corresponded to streams running (950–1200 m)
through plantations of the exotics P. menziesii, P. ponderosa, P. radiata
and P. lambertiana (Pn: Golondrinas, Patriada and Ifona) that were
mainly established between 1954 and 1970. Three urban rivers, (Ur: Las
Minas, Carbón and Esquel) plus their respective reference sites (R-ur:
Las Minas ref, Carbón ref and Esquel ref) were included in order to assess
specifically the urban impact and make sites comparable in terms of
environmental features (Fig. 1).
For stream selection we looked at similitude among streams
within a geographical range, but also evaluated the accessibility to the
614 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624

Fig. 1. Location of sampling sites (site codes in Table 1), Chubut Province, Patagonia, Argentina. Symbols are: ■: urban sites, △: managed native forest, ○: pasture, □: reference urban
sites, ●: non-managed native forest and ▲: pine plantations.

study reach. We also revised existing data sources in different
governmental administration offices (DPByP Dirección Provincial de
Bosques y Parques, INTA Instituto Nacional de Tecnología Agrope-
cuaria). We conducted this study on 18 sites on 15 mountain and
piedmont streams. Sites were visited in May (autumn), September
(winter) and December (spring) 2005 and in February (summer)
2006, under normal hydrological conditions (avoiding rainstorms or
extremely high discharge events).
2.2. Site characterization
In order to identify basin features, vegetation types and coverage, a
set of LandSat images ETM (2000 and 2001, mapping resolution 15 m)
were classified and processed using a geographical information
system (GIS) (Arc VIEW 3.3 package) by the DPByP. For each surveyed
site we obtained sub-basin area above to the sampling site, and the
percent coverage of native and exotic vegetation, pasture and urban
settlements.
At each site, percentages of boulder, cobble, gravel, pebble, and
sand in the reach were estimated using a 1-m2 grid. Current speed
was measured in mid channel (average of three trials) by timing a
float as it moved over a distance of 10 m (Gordon et al., 1994).
Average depth was estimated from five measurements with a
calibrated stick along one transverse profile across the channel. Wet
and dry widths (from bank to bank) of the channel were also
determined. Discharge was obtained by combining depth, wet width
and current velocity as in Gordon et al. (1994). At each site, air and
water temperature were measured with a mercury thermometer.
At each occasion and in the mid channel section of the reach,
specific conductance, pH, turbidity and dissolved oxygen were
measured with a Horiba U2-probe. For nutrients analyses water
samples were collected below the water surface, kept at 4 °C and
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624
transported to the laboratory for analysis. Total suspended solids
(TSS) were measured from separate water samples. Total nitrogen
(TN) and total phosphorus (TP) were determined on unfiltered
samples digested with persulphate, whereas nitrate plus nitrite
nitrogen (NO3 + NO2), ammonia (NH4), and soluble reactive phos-
phate (SRP) were analyzed using standard methods (APHA, 1994).
Attributes of the riparian vegetation were examined at each site
using an adaptation of the QBR index (Riparian corridor quality index,
Munné et al., 1998) for Patagonian streams: the QBRp (Kutschker et
al., 2009). This index combines information from total cover,
structure, complexity and naturalness of vegetation, and the degree
of channel alteration (e.g. bank modifications, dredging, etc.). The
total QBRp score ranges from 0 points (extreme degradation) to 100
points (excellent quality, natural riparian forest).
We evaluated habitat quality (HCI: habitat condition index) using
the assessment procedure for high gradient streams of Barbour et al.
(1999). This method ranks 10 river channel features (e.g. epifaunal
substrate availability, frequency of riffles, etc.) from 0 to 20. A score of
200 points indicates that the river is natural and pristine and in its best
possible condition (range: 150–200). This index evaluates the ability
of the stream's physical habitat to support a given fauna, and then is a
measure of the spatial heterogeneity of the stream (Castela et al.,
2008).
A vegetation sampling was conducted in February of 2006. We
collected and made vouchers of 60 plants. Species were identified in
the laboratory using the keys in Correa (1978, 1999). At each reach
coverage of aquatic plants and also filamentous algae (eg. Cladophora
sp.) were assessed visually as in Hauer and Lamberti (1996).
2.3. Biological sampling
Quantitative macroinvertebrate samples were taken with a
Surber sampler (0.09 m2; 250 μm pore size). On each reach, three
samples from riffles and three from pools (n = 6) were taken.
Samples were fixed in situ with 4% formaldehyde, and sorted in the
laboratory under at least 5x magnification. Macroinvertebrate
species were identified to the lowest possible taxonomic level
using regional keys (Archangelsky and Manzo, 2007; Fernández
and Domínguez, 2001; Manzo, 2005) and counted.
We calculated a set of macroinvertebrate community descriptors
for each site and sampling date, including richness measures: taxa
richness (SR) and Ephemeroptera, Plecoptera and Trichoptera (EPT)
richness; enumerations measures: total density (TD) (Barbour et al.,
1999; Resh et al., 1995) and diversity measures: Shannon-Weaver
diversity index (H'). A biotic index previously adapted for use in the
Patagonian region, BMPS (Biotic Monitoring Patagonian Streams) was
calculated (Miserendino and Pizzolón, 1999). The BMPS is an
adaptation of the BMWP (Biological Monitoring Working Party
index; Armitage et al., 1983) and is obtained from a table of 95
families with different degrees of pollution sensitivity (scores 1–10)
present in Patagonia. The total BMPS score ranges from 0 to N150.
Riparian and littoral insects were collected using an array of
different techniques. Littoral species are aquatic species associated to
the aquatic vegetation, or found underneath rocks or wood within the
water; these species usually do not appear in Surber samples. Riparian
species are those species that live close to the water, or that can be
associated to the marginal vegetation, but are terrestrial. The samples
were qualitative, and the material was fixed in 80% ethyl alcohol.
Littoral species were collected by passing a D-frame net (Merritt and
Cummins, 1996) through the aquatic vegetation and also by removing
the substrate (rocks, branches, algae, etc.). The content of the net was
placed in a white pan and inspected visually and the insects caught
were pulled out with featherweight forceps. Riparian species were
sampled by washing the substrate in white pans, and also by direct
observation. Flying adults of some orders were collected with a
sweeping net used through the vegetation on the margins, and also by
615
visual inspection over rocks, trees and bushes. Riparian and littoral
species were identified to the lowest taxonomic level and treated
together in the analyses. Sampling of these communities aimed at
increasing the diversity of taxa sampled in the watercourses; they will
also be used for additional studies not included in this paper (e.g.
insects available as prey for fish communities).
Fish sampling was carried out by electro-fishing with a powered
backpack machine and a hand net. Stream reaches were blocked off
with a downstream net. Each reach was sampled three times;
downstream passes of equal effort were done in a slow zigzag
pattern. Specimens were identified to species following López et al.
(2003) and counted. Given that an intensive sampling program may
affect the fish populations under study (see Casaux and Barrera-Oro,
2002), up to 30 individuals per species (selected randomly) were
preserved for posterior analyses; the remaining specimens were
returned alive to the stream. Individuals carried to the laboratory
were weighed (W, accuracy 0.01 g). Considering the total of the
individuals caught, mean density (ind. m2) and biomass (g. m2) were
estimated for each species at each sampling site. For the biomass
estimation, the mass of the individuals returned to the stream was
assumed to be similar to the mean mass of the individuals carried to
the laboratory.
Taking advantage of the overall sampling effort, we opportunis-
tically performed exploratory avian censuses aimed to estimate bird
abundance (number of individuals per point count), richness and
diversity (Simpson Index) and to look for correlations between these
and the remaining parameters measured throughout the study (see
previous discussion). At each stream and during each sampling period
we censused birds at three stations located within the riparian
corridor and separated by at least 200 m, using 30 m fixed-radius
point counts (0.28 ha) of 10 min duration (the censuses started two
minutes after arrival at the station). Due to the overall sampling
protocol, censuses were not performed according to the standard
methodology (observations within the three hours after the sunrise or
before the sunset). The individuals observed were identified following
the descriptions in Narosky and Yzurieta (1987).
2.4. Statistical analysis
One way ANOVA analyses with land-use as categorical variable in
the treatments followed by post hoc test when significant (Tukey test
p b 0.05), or non-parametric ANOVA models (Kruskal–Wallis) were
used to assess differences in environmental variables among land-
uses. Rivers subjected to certain land-use (pastures, urban, etc.) were
cases in the models (n = 3). Additionally sampling dates were used as
cases to improve significance in comparisons, which is acceptable in
order to contrast multiple independent samples (Kruskal–Wallis)
(Sokal and Rohlf, 1995). This included physico-chemical parameters
(geomorphological measurements, nutrients, etc.), the QBRp and the
HCI. The same analysis was performed for community descriptors and
metrics. Differences in SR, TD, H´, EPT richness and BMPS were
assessed for the benthic community, species richness for riparian and
littoral invertebrates, fish density and total biomass for the fish
community, and species richness and total density for the bird
community.
Prior to analysis data were checked for normality and homogeneity
of variances using Kolmogorov–Smirnov and Levene's test, respectively,
and log (x+ 1)-transformed when appropriate (Gotelli and Ellison,
2004).
Redundancy Analysis (RDA) was run using CANOCO (ter Braak and
Smilauer, 1999) to assess relationships between main community
attributes (riparian and littoral invertebrate richness, macroinverte-
brate metrics, density and biomass of fish and bird) and environ-
mental variables. RDA was chosen because previous inspection of the
data revealed a linear mode rather than a unimodal response in the
biotic variables (ter Braak and Smilauer, 1998). All environmental
616 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624

variables included in Table 1 and 2 were used, initially, to evaluate the
response of community descriptors and sites to environmental
gradients. Variables (except pH) and community attributes (except
H´) were transformed (log x + 1), prior to analysis. Variables that
were strongly intercorrelated with others (those with an inflation
factor N10) in the initial analysis, were removed and a further analysis
was carried out with the remaining environmental variables. A Monte
Carlo permutation test (9999 permutations) was used to verify the
significance of the models (ter Braak and Smilauer, 1998).
3.2. Aquatic plants
A total of 15 species of aquatic plants were recorded, with pasture
and urban sites supporting more species than the rest (Table 4). In
contrast pine and non-managed native forest sites had fewer species
mostly represented by Veronica anagallis-aquatica, Juncus balticus and
Ranunculus sp. Bryophytes were well represented at both managed
and non-managed native forest sites. Aquatic plant coverage ranged
between 0 to N50% (Table 1).

3.3. Habitat condition and riparian quality

3. Results
3.1. Environmental characteristics and land-use
Elevation of sampling sites ranged between 361 and 820 m.a.s.l.
(Table 1). Stream shade was higher at non-managed native forest sites
(Table 2), which resulted in significantly lower mean values of water
temperature than the rest (ANOVA, p b 0.002, Table 3). Wet channel
width (range 1.1–25 m) varied considerably between sites, with
pasture and urban sites having the widest channels. However
differences were only significant when comparing urban and pasture
wet width with all types of forested channels (ANOVA, p b 0.02,
Table 3). At most sites the substrate particle size was mainly boulder,
cobble and pebble; however a higher proportion of soft sediments
(N30%) was observed on some sites (Table 1), having managed native
significantly higher sand percentage than non-managed native sites
(Table 3).
Mean conductivity values ranged between 35 and 160.7 μS cm− 1
(Table 2), having urban and pasture sites significantly higher
conductivity values than native forest (with and without manage-
ment) (Kruskal–Wallis, p = 0.02).
Except for managed native forest and reference stations for urban
sites, dissolved oxygen contents were significantly higher at non-
managed native forest sites (Kruskal–Wallis p b 0.02, Table 3) than at
the rest. Most chemical variables including SRP, TP, NO3–NO2 and NH4
showed higher mean values at urban use than at the rest of the sites
(Table 2). Except for reference stations in urban sites, NO3–NO2 values
were significantly higher at urban sites than at the rest (Kruskal–
Wallis p b0.027, Table 3). However NH4 and SRP values were highly
variable, which might be explained by extreme values at Esquel down
urban site.
QBRp mean scores showed that urban sites had strong riparian
ecosystem alteration whereas pasture and pine plantations sites
showed a moderate disturbance (Fig. 2). Sites Manguera (Pas) and
Carbón down (Ur) showed the lowest values of riparian vegetation
coverage, having simplified and poor quality communities mostly
represented by; Plantago laneolata, Rumex acestosella, Artemisia
absinthium and Trifolium repens. Other urban sites showed dominance
of exotics such as Cytisus scoparia, Rosa rubiginosa and Conium
maculatum. Non-managed native forest sites showed significantly
higher values of QBRp than the rest (Kruskal–Wallis, p = 0.017, Table 3).
HCI index mean values ranged between 111.3 and 182 (Fig. 2).
Urban and pasture sites showed suboptimal habitat quality, possibly
as consequence of channel realignment and dredging which was a
regular practice at these particular sites. When comparing all values,
scores were significantly higher at non-managed native forest, pine
plantation and reference urban sites than at the rest (Kruskal–Wallis,
p = 0.013).
3.4. Riparian and littoral invertebrates
We collected and identified 105 riparian and littoral taxa from all
sites, being Trichoptera (24%), Plecoptera (19%), Ephemeroptera
(18%), Diptera (16%) and Coleoptera (16%) the most diverse orders.
Riparian and littoral invertebrate richness ranged from 0 to 25 taxa
when taking into account absolute values, whereas mean values per
site ranged from 0 to 15 taxa. Significant differences on taxa richness
were found among land-uses (Kruskal–Wallis p b 0.008, Fig. 3a)
having urban sites significantly lower richness than the rest, and
pasture sites significantly higher richness than pine, and managed
native forest. This pattern was mostly explained by the presence of

Table 1
Physical characteristics of 18 sampled sites of streams in Patagonia, Argentina. Land-use codes: R-ur: reference for urban site; Ur: urban site; Pas: pasture; Pn: pine plantation; HNF:
managed native forest; NF: non-managed native forest. Bo: boulder, Co: cobble, Pe: pebble, Gra: gravel, Sa: sand.

Site Site Land- Elevation Catchment size % Native % Pasture % Exotic % Urban % Timberline Substrate % % Aquatic plant
Code use (m.a.s.l) (km2) forest wetlands forest areas and lakes size Sand coverage

Esquel EU R-ur 721 22.9 11.3 0 0.7 0 88.0 Bo/co 10 b5

Las Minas LMU R-ur 573 35 93.1 1.3 0 0 5.6 Bo/co 10 b5
Carbón CU R-ur 384 80.9 97.0 1.4 1.4 0.2 0 Bo/co 10 b5
Esquel ED Ur 491 299 11.0 18.7 5.6 9.0 55.7 Pe/gra 20 N50
Las Minas LMD Ur 555 35.5 92.3 1.3 0 0.7 5.7 Co/pe 5 b5
Carbón CD Ur 403 110 96.6 1.5 1.1 0.4 0.4 Bo/co 10 b5
Nant y Fall NyF Pas 690 161.8 69.7 4.4 0.2 0 25.7 Gra/co 15 25
E. Los Ñires LÑ Pas 667 102.9 81 8 0 0 11 Sa/gra 40 b5
Manguera MG Pas 699 20.6 76 b1 0 0 23 Bo/co 5 b5
Golondrinas GOL Pn 361 5.7 63 0 5.3 0 31.7 Co/sa 30 0
Patriada PAT Pn 495 1.8 79.1 0 7.3 0 13.6 Gra/sa 35 0
IFONA IFO Pn 368 35.5 69.5 0 3.1 0 27.4 Bo/co 5 0
Cab. de vaca CVA HNF 699 88.7 90.4 2.8 0 0 6.8 Co/gra 15 15
Pipo PIP HNF 728 2.2 99.0 0 0 0 1.0 Gra/sa 35 20
Glyn GLY HNF 615 21.7 98.8 0 0 0 1.2 Pe/co 15 20
Comisario COM NF 770 21.8 62.8 0 0 0 37.2 Bo/co 5 15
Loro LO NF 820 8.2 43.7 0 0 0 56.3 Bo/co 5 35
Chiquito CHI NF 670 11.1 97.1 0 0 0 2.9 Co/pe 10 15
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624 617

Table 2
Means and ranges (in brackets) of environmental quality variables in the study streams during the one-year study period (n = 12).

Land-use: Ref. urban Urban Pine plantation Pasture Managed native Non-managed
forest native forest
Variable:

Physicochemical variables
Water temp. (°C) 8.6 (5.1–10.2) 10 (5.7–11.9) 8.1 (7.1–11.5) 8.2 (3.4–13.6) 7.1 (4–10.6) 4.5 (1.7–7.4)
Wet width (m) 5.3 (2.1–9.1) 11.5 (3.8–23.5) 4.1 (1.1–9.2) 11.3 (5–25) 4.3 (1.3–11) 4.7 (1.5–8.9)
Depth (cm) 21 (9.2–31.5) 23 (7–38.2) 22 (7.8–41.3) 30 (13.5–33.7) 18 (5.2–28) 25 (10.4–34.3)
W. velocity (m s− 1) 0.84 (0.33–1.36) 0.91 (0.33–1.81) 0.59 (0.20–1.07) 0.94 (0.66–1.11) 0.81 (0.10–1.66) 0.92 (0.10–1.66)
Discharge (m3 s− 1) 1.02 (0.12–2.83) 2.83 (0.15–8.97) 1.09 (0.02–3.8) 3.60 (0.45–8) 1.03 (0.01–3.08) 1.36 (0.02–4.7)
pH 7.33 (6.7–7.7) 7.23 (6.7–7.7) 7.16 (6.8–7.5) 7.38 (6.6–7.9) 7.28 (7–7.6) 7.28 (7–7.6)
Conductivity 20 ºC (μS. cm−¹) 97.6 (44–186) 160.7 (52–390) 79.8 (29–137) 87.3 (61–118) 61.3 (38–97) 35 (9–92)
Dis. oxygen (mg l−¹) 11.5 (9.2–18) 10.5 (7.9–17.1) 11.6 (8.6–15.7) 11.1 (7.7–14.9) 12.7 (8.9–18.8) 14.1 (11–20)
Turbidity (NTU) 25.1 (0–158) 48.2 (1–287) 33.7 (0–240) 9.7 (2–32) 7.6 (0–37) 30.5 (0–192)
TSS (mg l−¹) 7.56 (0.1–52.3) 14.75 (0.7–102.7) 2.15 (0.27–5.59) 5.29 (1.08–16.1) 4.24 (0.67–33.9) 1.97 (0.1–6.1)
SRP (ug l−¹) 0.62 (0.36–1.17) 4.88 (0.29–20.96) 0.50 (0.19–1.24) 0.72 (0.32–1.79) 0.72 (0.21–2.65) 0.56 (0.16–1.88)
Nitrate/nitrite (ug l−¹) 2.34 (0–17.44) 16.47 (0.03–69) 0.42 (0–1.61) 0.16 (0–0.60) 0.22 (0.07–0.62) 0.20 (0–1.55)
Ammonia (ug l−¹) 1.23 (0–3.26) 35.51 (0.49–271.5) 0.96 (0.08–1.58) 1.15 (0.38–2.49) 1.28 (0.14–4) 1.20 (0.17–3.89)

Sigara sp., Notonecta sp., Belostoma sp. (Hemiptera, Heteroptera), 3.6. Fish communities and land-use
Rionaeschna sp. and Cyanallagma interruptum (Odonata), Rhantus
signatus, Liodessus patagonicus and Gymnochthebius sp. (Coleoptera), Five fish species were represented in the samples. Three of them
which were frequently recorded at these sites. (Oncorhynchus mykiss, Salmo trutta and Salvelinus fontinalis) were
exotic species (99.1% of the individuals caught) and the remaining
(Hatcheria macraei and Odontesthes hatcheri) were native ones
3.5. Benthic macroinvertebrates and land-use relationships (Table 5). Whereas exotic species were represented at all of the
land-uses, native fish only occurred in reference urban, pastures and
A total of 158 taxa were recorded in the study; macroinvertebrate managed native sites. Overall, fish density ranged between 0 and 2.69
density and number of taxa ranged from 298 to 38,831 individuals ind. m− 2 (Table 5). Total fish density did not vary in a systematic
m− 2 and from 11 to 54 taxa site− 1 respectively (Fig. 3c and d). manner among land-uses (Kruskal–Wallis test, p = 0.55, Fig. 3g). Fish
Number of taxa differed among land-uses having non-managed native biomass ranged between 0 and 54.0 g m− 2 (Table 5). Total biomass
forest sites higher richness than the rest with the exception of was significantly higher at urban than at pine sites (Tukey test
managed native forest sites (p = 0.002, Fig. 3c); an identical pattern p b 0.05, Fig. 3h).
was displayed by EPT richness (p = 0.003, Fig. 3e). Mean macro-
invertebrate density was significantly higher at urban sites except for 3.7. Bird community and land-use
managed native sites (p = 0.001, Fig. 3d). Non-managed native forest
sites had significantly more macroinvertebrate diversity than the rest A total of 34 species were identified throughout the study, but only
of land-uses, and as expected urban sites showed the lowest diversity, 8 of them (23.5%) were observed actively interacting with the streams
being significantly lower than reference urban and pine sites (Table 6). The highest number of species (26) and mean annual
(p b 0.001). Analysis of BMPS showed that only urban sites fall into diversity (1.46) were observed at urban sites. Maximum density (4.96
lower categories of water quality (Mean score = 84.9). Non-managed individuals per point count) was observed at pasture sites (Table 6).
native sites (Mean score = 163) showed very clean waters, whereas Differences observed in bird diversity and density among land-uses
pine sites (Mean score = 135) displayed clean waters (Fig. 3f). were not statistically significant (Kruskal–Wallis p = 0.16 and
Managed native sites showed clean waters though BMPS values p = 0.13 Fig. 3i and j).
were significantly lower than reference sites (p b 0.0001).
3.8. Ordination analysis
Table 3
Results of the Kruskal–Wallis ANOVA by rank analyses (non-parametric) among First two axes of RDA analysis accounted for 56.1 of the total
environmental variables and land-use classes. n = 3 for QBRp and HCI, n = 12 for the variance in the community data (Fig. 4). The 1st axis was significant
rest of variables. ns: non significant. Land-use codes: R-ur: reference for urban site; Ur: (p b 0.005), and represented an environmental gradient mainly
urban site; Pas: pasture; Pn: pine plantation; HNF: managed native forest; NF: non- defined by land-use coverage and water quality conditions whereas
managed native forest.
the 2nd axis was associated to pasture land cover and oxygen contents
Variable p Relationship observed (Table 7). According to the model landscape variables such as urban
Water temperature 0.002 Ur N HNF,NF Pas, Pn, R-ur, HNF N NF percentage and pasture land cover decreased from the positive to the
Wet width 0.0052 Pas,Ur N rest negative end of the RDA1, whereas percent of native forest cover,
Depth ns increased to the negative end of same axis. Urban sites were
Current velocity ns
positioned in the lower right quadrant whereas non-managed native
Discharge ns
% Sand 0.04 HNF N NF forested sites were in the lower left quadrant (Fig. 4 and Table 7). A
Dissolved oxygen 0.04 NF N Ur,Pas,Pn gradient in water quality conditions including dissolved oxygen,
pH ns nitrate and TSS contents was also highlighted in the model and
Turbidity ns associated with RDA1 (Fig. 4 and Table 7). Sites having better water
TSS ns
Conductivity 0.004 Pas,Ur N HNF N NF
quality conditions were positioned at the negative extreme of RDA1
NH4 ns and polluted sites at the positive extreme of RDA1. Sites having
NO3 0.026 Ur N Pas, HNF, NF, Pn physical disturbances such as dredging, realignment of the channel
SRP ns and vegetation removal (which in turn produced high TSS levels)
QBRp 0.017 NF N rest HNF N Pn N Ur
were positioned in the lower right quadrant. Community descriptors
HCI 0.013 NF,Pn,R-ur N Pas,HNF,Ur
were located along the same gradients, thus H´, invertebrate riparian
618 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624

Table 4
Aquatic vegetation present in 18 sampling sites in Patagonian streams (Chubut, Argentina) according to selected land-use during the study (2005–2006). Nf: no found.

Reference urban Urban Pine plantations Pasture Managed native forest Non-managed native forest

Veronica anagallis-aquatica V. anagallis-aquatica Nf V. anagallis-aquatica V. serpyllifolia J. arcticus

Juncus microcephalus V. serpyllifolia V. anagallis-aquatica Ranunculus sp.
J. arcticus J. arcticus M. glabratus Bryophytes
Myriophyllum quitense J. burkartii R. hydrophilus
Callitriche lechleri J. diemii C. lechleri
Ranunculus sp. J. microcephalus E. pseudoalbibracteata
Mimulus glabratus Eleocharis albibracteata Bryophytes
Eleocharis sp. E. melanostachys
Cladophora sp. C. lechleri
Ranunculus flagelliformis
Limosella australis
Lilaeopsis macloviana
M. glabratus
Cladophora sp.

richness, BMPS, EPTr and macroinvertebrate richness increased
significantly with percentage of native cover and better habitat
conditions. Instead, macroinvertebrate density augmented with urban
land cover percentage, whereas fish biomass, bird density and bird
richness were positively correlated with the percentage of pasture
cover.
4. Discussion
4.1. Environmental variables and land-use
A considerable number of physical, chemical, and environmental
changes associated with different land-use practices were documen-
ted in this study. A reduction of the riparian canopy resulted in an
increase of the water temperature and sedimentation symptoms,
which diminished the quality of the stream habitat. As reported in
other studies (Collier, 1995; Miserendino et al., 2008) water quality
variables showed that urban sites were the most affected in terms of
conductivity, nutrients and oxygen. On the other hand, stream-bank
erosion was an obvious feature in managed native sites as well as in
some pasture sites with an extreme situation at Los Ñires; changes in
the riparian vegetation, together with the direct effects of stock
trampling, probably accounted for an increase of fine material in the
streambed. Stocking with sheep or cattle in the absence of streamside
fences or riparian strips can lead to bank erosion, bed disturbance, and
increased supply of fine sediment (Quinn et al., 1997).
We detected significant increases in water temperature and
conductivity values in harvested forest sites when compared with
non-harvested sites, meaning that wood collection is affecting the
environmental features. Baillie et al. (2005) documented marked
increases in stream light levels and maximum monthly water
temperatures in streams draining through 25% clear-cut forests in
New Zealand watersheds and Kedzierski and Smock (2001) reported
important differences in incident light reaching streambeds when
compared with unlogged and logged sections in a lowland creek.
4.2. Riparian and littoral invertebrate richness pattern

100 Very good quality Our results suggest that urban sites showed lower richness than
the remaining uses; human impacts observed in urban sites include
75 Good quality afforestation, river canalization and pollution, mostly by domestic
QBRp score

Riparian ecosystem sewage. These impacts help to reduce taxonomic diversity (Maitland
alteration and Morgan, 1997). Our observations are in agreement with what
50
was showed by Subramanian et al. (2005). These authors reported
Strong riparian
ecosystem that generic richness of insects was higher in the streams with
25 alteration natural riparian vegetation than in those modified by humans; they
Extreme degradation also found that the diversity of riparian grasslands is comparable to
of riparian ecosystem
that of streams with riparian paddy fields. Our forested sites had an
0
intermediate richness of riparian and littoral invertebrates; this
R-ur Ur Pas Pn HNF NF
could probably be explained by the absence of marginal areas with
200 slow moving water with macrophytes and algae, which harbor an
important number of species. Instead, our pasture sites supported
Optimal
more species of riparian and littoral invertebrates than other uses.
150
HABITAT score

The taxa occurring at these sites were characteristic of marginal

Suboptimal pools (Merritt and Cummins, 1996), sometimes with poor or slow
100 flow and with macrophytes and algae, biotopes that were present
mostly at our pasture sites. Some of the species in these marginal
Marginal
areas are also opportunistic (e.g. Tropisternus setiger and Rhantus
50
signatus colonize all kind of stagnant or slow moving waters). The
Poor species assemblages of riparian and littoral invertebrates at pasture
0 sites seem to be more diverse because they also incorporate adult
R-ur Ur Pas Pn HNF NF stages of aquatic insects, for example many of the aquatic beetles
and bugs collected in pastures have both larval and adult stages
Fig. 2. Habitat condition index (upper) and riparian ecosystem condition score (lower)
per land-use during the study. R-ur: reference for urban sites; Ur: urban; Pas: pastures;
aquatic (e.g. Tropisternus setiger, Enochrus sp., Rhantus signatus,
Pn: Pine plantation; HNF: managed native forest; NF: non-managed native forest Liodessus patagonicus, Gymnochthebius sp., Notonecta sp., Sigara sp.,
(n = 3). etc.).
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624 619

4.3. Macroinvertebrate environmental relationships
We found several significant relationships among macroinverte-
brate attributes and water quality variables, land-use coverage types,
and riparian and habitat condition indexes. Most metrics (SR, EPT
richness and BMPS) were positively correlated with native forest
coverage and negatively correlated with urban and pasture land
cover. These observations are in agreement with Collier (1995, 2008)
findings for New Zealand streams and with Roy et al. (2003) for
streams in Georgia (USA). They reported positive relationship
between total richness, EPT richness and the percentage of indigenous
forest, but also a negative correlation with the increase of pasture
cover. The relationships between the metrics considered and the
percentage of urban cover are fully consistent with those reported by
Strayer et al. (2003) and Morley and Karr (2001) who documented a
significant relationship between macroinvertebrate species richness
and urban land cover for North American watersheds.
Regarding water quality parameters, the strong relationships
observed between macroinvertebrate metrics with dissolved oxygen,
nitrate and TSS confirmed the ability of benthos community to detect
stream impairment. Nitrate and ammonia are strong indicators of
organic pollution (Hall et al., 2001; Paul and Meyer, 2001),
consequently significant reductions in SR, EPT richness, H, BMPS
occurred with increases of nitrogen concentrations at urban sites. We
can conclude that these metrics are useful to detect impairment
especially at urban reaches in Patagonia.

20 3,0
NF>all Ur< R-ur, Pn, NF
RIP./LIT. INVERT. RICHNESS

BENTHOS DIVERSITY (H)

Pas> Pn, HNF, Ur p=0.001
15 Ur<all
p=0.008 2,5

10

2,0
5

0 a 1,5
b
R-ur Ur Pn Pas HNF NF R-ur Ur Pn Pas HNF NF
LAND USE LAND USE

50 20000
NF> R-ur, Ur, Pn, Pas Ur>R-ur, Pn, Pas, NF
HNF> Ur p=0.001
BENTHOS S. RICHNESS

BENTHOS DENSITY

p=0.002 15000
40

10000

30
5000

c d
20 0
R-ur Ur Pn Pas HNF NF R-ur Ur Pn Pas HNF NF
LAND USE LAND USE

25
NF>R-ur, Ur, Pn, Pas NF>R-ur, Ur, Pas, HNF Very
HNF>Ur Pn>R-ur, Ur, Pas p=0.0001 clean
p=0.003 150 water
20
EPT RICHNESS

BMPS

15 Clean
water
100
Incipient pollution or other
10
kinds of perturbation

e f
5 50
R-ur Ur Pn Pas HNF NF R-ur Ur Pn Pas HNF NF
LAND USE LAND USE

Fig. 3. Distribution values of selected metrics for a) riparian and littoral invertebrate richness, b) benthic diversity (Shannon-Weaver), c) macroinvertebrate species
richness, d) macroinvertebrate total density (ind.m− 2 ), e) EPT richness, f) BMPS quality index, g) fish density (ind.m− 2 ), h) fish biomass (g.m− 2 ), i) bird diversity
(S: Simpson index) and j) bird density per land-use (ind. per point count). Range bars show maxima and minima, boxes are interquartile ranges (25–75%), small
squares are medians. Significant relationships (ANOVA Kruskal–Wallis, Tukey test) are shown in bold. Land-uses: R-ur: reference for urban sites; Ur: urban; Pas:
pastures; Pn: Pine plantation; HNF: managed native forest; NF: non-managed native forest. Sample size was n = 12 except for item a) n = 9.
620 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624

1,2 1,2
Ur>Pn
p=0.55 p=0.039

FISH BIOMASS (log x+1)

FISH DENSITY

0,6 0,6

g h
0,0 0,0
R-ur Ur Pn Pas HNF NF R-ur Ur Pn Pas HNF NF
LAND USE LAND USE
3 8

p=61.0 p=31.0
BIRD DIVERSITY (S)

BIRD DENSITY
2

1
2

i j
0
R-ur Ur Pn Pas HNF NF R-ur Ur Pn Pas HNF NF
LAND USE LAND USE

Fig. 3 (continued).

Even though impairment was only evident at urban sites when
using the BMPS biotic index, this revealed that several sensitive
families (e.g. Ameletopsidae, Diamphipnoidea, Nesameletidae, Ecno-
midae, etc.), well represented in native forest and pine sites, were
practically absent at pasture, harvested native and urban sites. As
anticipated by Miserendino and Pizzolón (1999) BMPS appears
promising to assess disturbances involving sedimentation processes
and habitat impoverishment.
As indicated by Roy et al. (2003), the present paper highlights the role
of the riparian buffers in preserving water quality. This was evidenced in
the RDA analysis performed, where a clear gradient in riparian
ecosystem conditions, habitat quality, NO3−NO2 and TSS contents was
shown. A high relationship between HCI which is a measure of the spatial
heterogeneity of the stream (Castela et al., 2008) and macroinverte-
brates diversity (H´) was also evidenced in the ordination. Subsequently,
native forest sites having the best ecological conditions (highest QBRp
and HCI scores) supported the most diverse communities whereas sites
with incipient problems of sedimentation had less diverse communities
composed by tolerant taxa. Physical disturbances such as dredging,
realignment of the channel and vegetation removal probably accounted
for the high TSS values and low HCI scores at sites with extreme positions
in RDA (Las Minas down, Los Ñires, Pipo).
In our study, the reduction in H' and EPT richness was marked and
significant (pair wise comparisons) when contrasting harvested
native forest with native forest. Bojsen and Jacobsen (2003) found
that diversity index values were greater in forested sites compared to

Table 5
Mean annual values (± SD) of fish species density (ind. m− 2) and biomass (g. m− 2) per land-use in the study streams during the one-year study period (n = 12). Empty cells indicate
that the species was not recorded. N: cumulative number of individuals in the entire study. D: density B: biomass.

Land-use: Reference urban Urban Pine plantation Pasture Managed native forest Non-managed native forest N

Salmonidae:
Oncorhynchus mykiss D 2.34 ± 2.45 1.64 ± 2.05 0.13 ± 0.22 0.37 ± 0.19 0.63 ± 0.58 0.97 ± 1.22 2113
B 17.01 ± 17.83 32.67 ± 35.82 0.44 ± 0.76 15.86 ±16.31 9.37 ± 9.19 18.99 ± 25.58
Salmo trutta D 0.13 ± 0.22 0.20 ± 0.35 0.02 ± 0.04 0.25 ± 0.43 247
B 1.29 ± 1.74 2.62 ± 4.54 0.33 ± 0.58 2.89 ± 5.00
Salvelinus fontinalis D 0.25 ± 0.43 31
B 6.38 ± 11.05
Trichomycteridae
Hatcheria macraei D 0.01 ± 0.02 0.02 ± 0.02 0.02 ± 0.02 31
B 0.01 ± 0.02 0.08 ± 0.09 0.12 ± 0.11
Atherinidae
Odontesthes hatcheri D 0.002 ± 0.002 4
B 0.003 ± 0.01
Total density (min–max) TD 0.01–2.69 0.02–2.63 0–0.28 0.01–0.54 0–0.69 0–1.17
Total biomass (min–max) TB 0.13–21.83 1.42–54.00 0–8.37 0.06–31.14 0–13.86 0–20.85
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624 621

Table 6
Mean annual diversity (± SD) and density (overall and by species; individuals per point count ± SD) per land-use of the bird species observed in the studied streams during the one-
year study period (n = 12). The species with (*) corresponds to those observed actively interacting with the streams. S: Simpson index. Code of uses in Table 1.

R-ur Ur Pn Pas HNF NF

Diversity (S) 1.20 ± 0.7 1.46 ± 1.1 0.91 ± 0.8 1.39 ± 1.1 1.31 ± 0.7 0.58 ± 0.5

Density 2.01 ± 1.2 4.94 ± 4.3 1.67 ± 1.7 4.96 ± 5.8 2.37 ± 1.4 0.91 ± 0.9

Threskiornithidae
Theristicus caudatus (Black-faced Ibis) – 0.03 ± 0.1 – 0.03 ± 0.1 – –
Anatidae
Chloephaga picta * (Upland Goose) – – – 0.11 ± 0.4 – –
Anas flavirostris * (Speckled Teal) 0.06 ± 0.2 – – 0.17 ± 0.6 0.11 ± 0.3 –
Accipitridae
Circus cinereus (Cinereous Harrier) – 0.03 ± 0.1 – – – –
Falconidae
Milvago chimango (Chimango Caracara) – 0.03 ± 0.1 0.03 ± 0.1 0.08 ± 0.2 0.03 ± 0.1 –
Falco sparverius (American Kestrel) – 0.03 ± 0.1 – 0.03 ± 0.10 – –
Charadriidae
Vanellus chilensis (Southern Lapwing) 0.06 ± 0.2 0.06 ± 0.1 – 0.33 ± 0.6 – –
Scolopacidae
Gallinago gallinago (Common Snipe) – 0.03 ± 0.1 – 0.03 ± 0.1 – –
Columbidae
Zenaida auriculata (Eared Dove) 0.03 ± 0.1 – – 0.06 ± 0.2 – –
Trochilidae
Sephanoides galeritus (Green-backed Firecrown) – 0.03 ± 0.1 – – – –
Alcedinidae
Ceryle torquata * (Ringed Kingfisher) 0.03 ± 0.1 0.06 ± 0.1 – – 0.14 ± 0.2 –
Picidae
Colaptes pitius (Chilean Flicker) 0.06 ± 0.2 – – 0.06 ± 0.2 – 0.03 ± 0.1
Picoides lignarius (Striped Woodpecker) – – – – 0.03 ± 0.1 –
Furnariidae
Cinclodes patagonicus * (Dark-bellied Cinclodes) 0.11 ± 0.3 0.17 ± 0.6 – 0.08 ± 0.29 0.03 ± 0.1 –
Cinclodes fuscus * (Bar-winged Cinclodes) – 0.03 ± 0.1 – – 0.03 ± 0.1 –
Cinclodes oustaleti * (Grey-flanked Cinclodes) – 0.14 ± 0.4 – – – –
Aphrastura spinicauda (Thorn-tailed Rayadito) – 0.11 ± 0.4 0.50 ± 0.9 0.03 ± 0.1 0.42 ± 0.5 0.11 ± 0.3
Rhinocryptidae
Scelorchilus rubecula (Chucao Tapaculo) 0.06 ± 0.2 – 0.14 ± 0.2 – 0.03 ± 0.1 –
Tyrannidae
Xolmis pyrope (Fired-eyed Diucon) 0.03 ± 0.1 0.17 ± 0.3 – 0.03 ± 0.1 0.06 ± 0.1 –
Lessonia rufa (Rufous-backed Negrito) – 0.06 ± 0.2 – 0.28 ± 0.5 – –
Anairetes parulus (Tufted Tit-tyrant) 0.08 ± 0.3 0.06 ± 0.2 0.03 ± 0.1 – – 0.03 ± 0.1
Elaenia albiceps (White-crested Elaenia) 0.25 ± 0.5 0.19 ± 0.5 0.17 ± 0.4 0.17 ± 0.5 0.33 ± 0.6 0.11 ± 0.3
Hirundinidae
Tachycineta leucopyga * (Chilean Swallow) 0.17 ± 0.6 1.61 ± 3.8 – 1.94 ± 4.3 0.17 ± 0.6 0.03 ± 0.1
Notiochelidon cyanoleuca * (Blue-and-White Swallow) – 0.42 ± 1.4 – – – –
Troglodytidae
Troglodytes aedon (House Wren) 0.17 ± 0.2 0.08 ± 0.3 0.17 ± 0.3 0.11 ± 0.2 0.19 ± 0.5 0.42 ± 0.6
Turdidae
Turdus falcklandii (Austral Thrush) 0.14 ± 0.3 0.50 ± 0.9 0.03 ± 0.1 – 0.09 ± 0.1 0.08 ± 0.3
Motacillidae
Anthus correndera (Correndera Pipit) – – – 0.08 ± 0.3 – –
Vireonidae
Passer domesticus (House sparrow) 0.03 ± 0.1 0.06 ± 0.2 – – – –
Emberizidae
Diuca diuca (Common Diuca-Finch) 0.06 ± 0.2 – – – 0.03 ± 0.1 –
Phrygilus patagonicus (Patagonian Sierra-Finch) 0.08 ± 0.2 0.11 ± 0.4 – – – –
Zonotrichia capensis (Rufous-collared Sparrow) – – – 0.06 ± 0.2 – –
Fringilidae
Carduelis barbata (Black–chinned Siskin) 0.17 ± 0.6 0.36 ± 0.8 0.12 ± 0.4 – – –
Icteridae
Molothrus bonariensis (Shiny Cowbird) – – – – 0.11 ± 0.3 –
Sturnella loyca (Long-tailed Meadowlark) – 0.08 ± 0.3 – 0.03 ± 0.1 – –
Passer. Unidentified * 0.03 ± 0.1 0.11 ± 0.4 – – – 0.03 ± 0.1

deforested sites, and Hall et al. (2001) reported lower macroinverte-
brate diversity in pasture streams. Baillie et al. (2005) mentioned that
harvesting effects can vary depending on stream type and harvesting
practices, particularly post-harvesting wood treatment, but usually
there is a decrease in relative abundance of sensitive taxa (EPT) as is
reported here. A combination of environmental modifications such as
higher temperatures, more sediment in the bottom channel, and
changes in the organic material supply, could account for the changes
observed in these sensitive insect communities (Richardson, 2008).
Introduced salmonids, which were present at most of the sampling
sites, usually affect benthic communities by diminishing the density of
some large epibenthic taxa (Molineri, 2008), reducing individuals
body size and modifying the functional structure (Buria et al. 2007).
Thus, it is possible that some of the changes detected in benthic
communities in our study can be related to some extent with trout
impact on receiving ecosystems.
4.4. Usefulness of habitat assessment and riparian conditions indexes
In relation to the QBRp index, site conditions varied from poor to
very good. The lower QBRp values were registered at urban and
pasture sites, confirming that these land-uses negatively impact rivers
622 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624

successful expansion of salmonids in Patagonia which, at least for

Argentina, is supported by a continuous stocking. Oncorhynchus
mykiss was the most abundant fish both in density and biomass. Its
highest values of density and biomass where observed at reference
urban and urban sites respectively. This agrees with studies reporting
that salmonids can occupy and compete against other species in
altered ecosystems (Boët et al., 1999; McKinney, 2002) and the ability
of O. mykiss to grow faster and to larger sizes at urban sites,
presumably due to higher water temperatures and food availability
(Paul and Meyer, 2001).
Differently to the observed in salmonids, native species were
restricted to high altitude sites located in the ecotone region between
the Andes and the steppe. This scenario seems to be evidencing a
process of geographical segregation between exotic and native
species (Di Prinzio et al., 2009; Soto et al., 2006). However, given
Fig. 4. Triplot of the sampling sites and community descriptors in relation to the first
ordination axes of RDA based on land cover percentages, water quality parameters and
that the sampling sites located in the ecotone region were affected by
reach scale variables as environmental variables. Symbols are described in Fig. 1. two of the less aggressive land-uses considered in this study (pasture
and managed native forest) whereas most of the sites where native
fish were absent were associated to more disturbing land-uses (urban
in Northwest Chubut. The QBRp allowed us to assess not only the and pine plantations), both processes (i.e. changes in land-uses and
ecological integrity of riparian buffer zones, but also to identify strong competence between native and exotic fish) seem to be interacting
relationships between the status of those zones and some biotic and more studies are required to better understand their real effects
elements (macroinvertebrate metrics). By using the QBR index and on fish communities (Di Prinzio et al., 2009).
the fluvial habitat index Castela et al. (2008) detected that the benthic
community responded negatively to increases in nutrient concentra- 4.6. Bird patterns
tion, changes in the riparian vegetation and to the reduction of habitat
quality. Riparian plant cover can control local processes such as Only 23.5% of the species represented in the censuses interacted
shading, loading of leaf litter and wood into the channel, provision of actively (feeding or swimming while looking for food) with the water
egg-laying or adult emergence sites (Danger and Robson, 2004; Hall courses, which might be explained by the low order of the streams
et al., 2001; Richardson, 2008). studied. Consequently, overall bird density and diversity were not
In our work, the HCI did not show the same picture as the QBRp; directly correlated with the stream physical and chemical variables
when using HCI exotic pine plantations did not differ from non- considered. Bird density and diversity only responded in a significant
managed native forest sites. The presence of riparian forest, whether way to the percentage of pasture cover in the riparian corridor. Birds
native or exotic, would help to structure the in-stream habitat. display a high dispersal capacity thus their communities at the study
However, the quality of the litter supply (Pinus vs Nothofagus) can lead streams seem to be structured by environmental characteristics at a
to changes in the functional attributes of macroinvertebrate commu- scale larger than the one here considered.
nities as for example the shredder richness (Miserendino and Masi, The density and diversity were higher in urban and pasture sites
2010). where the riparian forest was strongly altered and almost absent, and
lower at pine and non-managed native forest sites where the riparian
4.5. Fish patterns corridor was densely forested. This might be explained by the space
available to transit within the sites given that this parameter
Exotic fish dominated in density and biomass at all the sampling positively interacts with bird abundance. This pattern is also explained
sites. This is in line with the reports for Patagonia, both in Chile (Soto by an increase in the presence of steppe and ecotone birds as the
et al., 2006) and Argentina (Pascual et al., 2002) and reflects the disturbance in the riparian forest increases, a phenomenon also
observed by Lantschner and Rusch (2007) in North Patagonian forests.
In this sense, studies carried out elsewhere reported that bird species
Table 7
Eigenvalues and correlation of standardized environmental variables with the first two
richness and diversity are strongly and positively correlated with the
RDA axes. The species-environmental correlations scale the strength of the relationship structural complexity of vegetation (MacArthur, 1964; Pearson and
between community descriptors and environment for the axes. F-ratio statistics are Ralph, 1978). However, our results are fully in line with those obtained
listed for the first axis and for all the axes combined. at Northern Patagonia where the species diversity and richness was
Axis RDA1 RDA 2 higher at structurally simple environments (Christie et al., 2004; Ralph,
1985; Vuilleumier, 1972).
Eigenvalue 0.463 0.098
Species-environmental correlations 0.95 0.77 The overall bird abundance, richness and diversity do not help to
Cumulative percentage variance assess land-use effects on stream systems at the study area. For such
Of species data 46.3 56.1 purposes, future studies should identify specific indicator species,
Of species-environmental relation 67.6 81.9 something not possible with our sampling protocol.
Correlations
% Urban 0.87 − 0.15
% Native − 0.37 0.29 5. Conclusions
% Pasture 0.78 0.43
Habitat condition − 0.57 0.10 According to our integrated approach urban land-use produced
QBRp − 0.46 0.21
the most significant changes in aquatic ecosystems including physical
TSS 0.69 − 0.16
NO3 0.80 − 0.05 features, nutrients, habitat conditions, riparian quality, riparian and
Dissolved oxygen − 0.74 − 0.36 littoral invertebrate and macroinvertebrate communities. This is
F-value and significance, Montecarlo test.
significant considering that percentage of urban areas found in this
First axis: 7.768 p b 0.005. study was very low. In an intermediate situation were pasture, pine
All axis: 2.451, p b 0.001. plantations and managed native forest land-uses. As expected, native
 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624
forest sites showed the highest integrity of ecological conditions,
which in turn resulted in higher values of QBRp and HCI, and also in a
greater biodiversity of the local benthic communities (richness, EPT
richness). However, by offering stream edge areas, pasture sites still
supported richer communities of riparian and littoral invertebrates,
which increased overall biodiversity.
Of all the biological communities used to evaluate the impact of
different land-uses, aquatic macroinvertebrates showed the most
obvious and significant responses. This was also the only community
that allowed detection of differences between managed native and
non-managed native forest sites. On the other hand, fish and birds
having a greater ability of dispersion and capacity to move quickly
from disturbances would reflect changes at a higher scale.
Pine plantations affected in different ways the communities
considered. Exotic plantations produced an intermediate impact on
benthic communities whereas this use resulted in impoverished fish
and bird communities both in diversity and abundance. The analysis
of different variables (environmental, biotic) with the percentage of
exotic cover did not show any consistent pattern.
Changes in land-use practices are emerging issues concerning the
integrity and conservation of water resources in Patagonia, and this
paper proves that stream ecosystems are particularly vulnerable;
moreover it expands understanding to a poorly researched part of the
world with distinctive assemblages of species.
Acknowledgements
This paper was supported by the CONICET (PIP 5733), the PADI
Foundation (Grant 19/2006), and Project A.W.A.R.E. Foundation
(P-001036). We also thank Estancia Tecka for the loan of the electro
fishing equipment, and the staffs of estancias Los Ñires and Río Frío,
and Mr. Cirilo Ñancual who facilitated the access to some of the
sampling sites. We greatly appreciate the reviews of Dr. John
Richardson for his thoughtful and constructive suggestions. Thanks
to anonymous reviewers for valuable comments that greatly
improved the manuscript. This is Scientific Contribution No. 52 from
LIESA.
References
Allan JD. Landscapes and riverscapes: the influence of land-use on stream ecosystems.
Annu Rev Ecol Evol Syst 2004;35:257–84.
APHA. Standard Methods for the Examination of Water and Wastewater. Hanover,
Maryland, USA: American Public Health Association; 1994.
Archangelsky M, Manzo V. Descripción de las larvas maduras de los géneros Stethelmis
Hinton y Luchoelmis Spangler and Staines (Insecta: Coleoptera, Elmidae). Rev Mus
Argent Cienc Nat 2007;9:79–87.
Armitage PD, Moss D, Wright JF, Furse MT. The performance of a new biological water
quality score system based on macroinvertebrates over a range of unpolluted
running water sites. Water Res 1983;17:333–47.
Bahar MM, Ohmori H, Yamamuro M. Relationship between river water quality and
land-use in a small river basin running through the urbanizing area of Central
Japan. Limnology 2008;9:19–26.
Baillie BB, Collier KJ, Nagels J. Effects of forest harvesting and woody debris removal on
two Northland streams, New Zealand. NZ J Mar Fresh 2005;39:1-15.
Barbour MT, Gerritsen J, Snyder BD, Stribling JB. Rapid Bioassessment Protocols for Use
in Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and Fish.
second edition. Washinton. D.C.: U.S. Environmental Protection Agency; 1999. 841-
b-99-002.
Boët P, Duvoux B, Allardi J, Belliard J. Incidence des orages estivaux sur les peuplements
piscicoles de la Seine á l´aval de l´agglomération parisiense (bief Andrésy-
Méricourt). Houille Blanche 1999;1–2:141–7.
Bojsen BH, Jacobsen D. Effects of deforestation on macroinvertebrate diversity and
assemblage structure in Ecuadorian Amazon streams. Arch Hydrobiol 2003;158:
317–42.
Buria L, Albariño R, Díaz Villanueva V, Modenutti B, Balseiro E. Impact of exotic rainbow
trout on the benthic macroinvertebrate community from Andean–Patagonian
headwater streams. Arch Hydrobiol 2007;168:145–54.
Casaux R, Barrera-Oro E. Effect of a shore-based sampling program on Notothenia
coriiceps populations. Antarct Sci 2002;14:221–4.
Castela J, Ferreira V, Graça M. Evaluation of stream ecological integrity using litter
decomposition and benthic invertebrates. Environ Pollut 2008;153:440–9.
623
Christie M, Ramilo E, Bettinelli M. Aves del Noroeste Patagónico: Atlas y Guía. Buenos
Aires: L.O.L.A; 2004.
Collier KJ. Environmental factors affecting the taxonomic composition of aquatic
macroinvertebrate communities in lowland waterways of Northland, New Zealand.
N Z J Mar Fresh 1995;29:453–65.
Collier K. Temporal patterns in the stability, persistence and condition of stream
macroinvertebrate communities: relationships with catchment land-use and
regional climate. Freshwater Biol 2008;53:603–16.
Correa MN. Flora Patagónica, Tomo VIII, parte III: Gramineae. Buenos Aires: INTA; 1978.
Correa MN. Flora Patagónica, Tomo VIII, parte VI: Dicotiledóneas Gamopétalas
(Ericaceae a Calyceraceae). Buenos Aires: INTA; 1999.
Czech B, Krausman P, Devers P. Economic associations among causes of species
enlargement in the United States. Bioscience 2000;50:593–601.
Danger AR, Robson BJ. The effects of land-use on leaf-litter processing by macro-
invertebrates in an Australian temperate coastal stream. Aquat Sci 2004;66:1–9.
del Valle HF, Elissalde NO, Gagliardini DA, Milovich J. Status of desertification in the
Patagonian region: assessment and mapping from satellite imagery. Arid Soil Res
Rehabil 1998;12:1-27.
Diamond JM, Dressier DW, Serveiss VB. Assessing relationships between human land-
uses and the decline of native mussels, fish, and macroinvertebrates in the Clinch
and Powell river watershed, USA. Environ Toxicol Chem 2002;21:1147–55.
Di Prinzio CY, Casaux RJ, Miserendino ML. Effects of land-use on fish assemblages in
Patagonian low order streams. Ann Limnol 2009;45:267–77.
Duncan P, Hewison AJM, Houte S, Rosoux R, Tournebize T, Dubs F, et al. Long term
changes in agricultural practices and wildfowling in an internationally important
wetland, and their effects on the guild of wintering ducks. J Appl Ecol 1999;36:
11–23.
Fernández HR, Domínguez E. Guía para la determinación de los Artrópodos bentónicos
sudamericanos. Tucumán, Argentina: EUDET; 2001.
Goldstein RM, Carlisle DM, Meador MR, Short TM. Can basin land-use effects on physical
characteristics of streams be determined at broad geographic scales? Environ
Monit Assess 2007;130:495–510.
Gordon ND, McMahon TA, Finlayson BL. Stream hydrology, an introduction for
ecologists. New York: Wiley and Sons; 1994.
Gotelli NJ, Ellison AM. A primer of ecological statistics. Sunderland, Massachusetts, U.S.
A: Sinauer Associates Inc. Publishers; 2004.
Hall MJ, Closs P, Riley RH. Relationships between land-use and stream invertebrate
community structure in a South Island, New Zealand, coastal stream catchment. N Z
J Mar Fresh 2001;35:591–603.
Hauer FR, Lamberti GA. Methods in Stream Ecology. San Diego, California: Academic
press; 1996.
Henderson IG, Cooper J, Fuller RJ, Vickery J. The relative abundance of birds on set-aside
and neighbouring fields in summer. J Appl Ecol 2000;37:335–47.
Jones EBD, Helfman GS, Harper JO, Bolstad PV. Effects of riparian forest removal on fish
assemblages in southern Appalachian streams. Conserv Biol 1999;13:1454–65.
Kedzierski WM, Smock LA. Effects of logging on macroinvertebrate production in a
sand-bottomed, low gradient stream. Freshwater Biol 2001;46:821–33.
Kutschker AM, Brand C, Miserendino ML. Un índice de calidad de ribera para ambientes
lóticos de cordillera patagónica sometidos a diferentes usos de la tierra. Ecologia
Aust 2009;19:19–34.
Lara A, Little C, Urrutia R, McPhee J, Alvarez-Garretón C, Oyarzún C, et al. Assessment of
ecosystem services as an opportunity for the conservation and management of
native forests in Chile. For Ecol Manage 2009;258:415–24.
Lantschner V, Rusch V. Impacto de diferentes disturbios antrópicos sobre las
comunidades de aves de bosques y matorrales de Nothofagus antarctica en el NO
Patagónico. Ecología Aust 2007;17:99-112.
López HL, Miquelarena AM, Menni RC. Lista comentada de los peces continentales de la
Argentina. La Plata. División Zoología de Vertebrados. Museo de La Plata. 2003.
MacArthur R. Environmental factors affecting species diversity. Am Nat 1964;98:387–97.
McCord S, Grippo RS, Eagle DM. Effects of silviculture using best management practices
on stream macroinvertebrate communities in three ecoregions of Arkansas, USA.
Water Air Soil Pollut 2007;184:299–311.
McKinney ML. Urbanization, biodiversity, and conservation. Bioscience 2002;52:883–90.
Maitland PS, Morgan NC. Conservation Management of Freshwater Habitats. London:
Chapman and Hall; 1997.
Manel S, Buckton ST, Ormerod SJ. Testing large-scale hypotheses using surveys: the
effects of land-use on the habitat, invertebrates and birds of Himalayan rivers. J
Appl Ecol 2000;37:756–70.
Manzo MV. Key to the South American genera of Elmidae (Insecta: Coleoptera) with
distributional data. Stud Neotrop Fauna Environ 2005;40:201–8.
Meador MR, Goldstein RM. Assessing water quality at large geographic scales: relations
among land-use, water physicochemistry, riparian condition, and fish community
structure. J Environ Manage 2003;31:504–17.
Merritt RW, Cummins KW. An Introduction to the Aquatic Insects of North America.
Dubuque, Iowa: Kendall-Hunt; 1996.
Miserendino ML. Effects of landscape and desertification on the macroinvertebrate
assemblages of rivers in Andean Patagonia. Arch Hydrobiol 2004;159:185–209.
Miserendino ML, Brand C, Di Prinzio C. Assessing urban impacts on water quality,
benthic communities and fish in streams of the Andes Mountains, Patagonia
(Argentina). Water Air Soil Pollut 2008;194:91-110.
Miserendino ML, Masi CI. The effects of land-use on environmental features and
functional organization of macroinvertebrate communities in Patagonian low order
streams. Ecolog Ind 2010;10:311–9.
Miserendino ML, Pizzolón LA. Rapid assessment of river water quality using
macroinvertebrates: a family level biotic index for the Patagonic Andean zone.
Acta Limnol Bras 1999;11:137–48.
624 M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624
Miserendino ML, Pizzolón LA. Macroinvertebrates of a fluvial system in Patagonia:
altitudinal zonation and functional structure. Arch Hydrobiol 2000;150:55–83.
Miserendino ML, Pizzolón LA. Interactive effects of basin features and land-use change
on macroinvertebrate communities of headwater streams in the Patagonian Andes.
River Res Appl 2004;20:967–83.
Molineri C. Impact of rainbow trout on aquatic invertebrate communities in subtropical
mountain streams of northwest Argentina. Ecol Aust 2008;18:101–17.
Morley SA, Karr JR. Assessing and restoring the health of urban streams in the Puget
Sound Basin. Conserv Biol 2001;16:1498–509.
Morrone JJ. Biogeographic areas and transition zones of Latin America and the
Caribbean Islands based on Panbiogeographic and Cladistic analyses of the
entomofauna. Annu Rev Entomol 2006;51:467–94.
Munné A, Solá C, Prat N. QBR Un índice rápido para la evaluación de la calidad de los
ecosistemas de ribera. Tecnol Agua 1998;175:20–37.
Narosky T, Yzurieta D. Guía para la identificación de las aves de Argentina y Uruguay.
Buenos Aires: Asociación Ornitológica del Plata; 1987.
Nolan PA, Guthrie N. River rehabilitation in an urban environment: examples from the
Mersey basin, North West England. Aquat Conserv 1998;8:685–700.
Paul MJ, Meyer JL. Streams in the urban landscape. Annu Rev Ecol Evol 2001;32:333–65.
Pascual M, Macchi P, Urbanski J, Marcos F, Riva Rossi C, Novara M, et al. Evaluating
potential effects of exotic freshwater fish from incomplete species presence
absence data. Biol Invasions 2002;4:101–13.
Paruelo JM, Jobbagy EG, Sala OE. Biozones of Patagonia (Argentina). Ecol Aust 1998;8:
170–8.
Pearson O, Ralph C. The diversity and abundance of vertebrates along an altitudinal
gradient in Peru. Mem Mus Hist Nat “Javier Prado”, Nº 18. ; 1978. Lima, Perú.
Quinn JM, Cooper AB, Davies-Colliey RJ, Rutherford JC, Williamson RB. Land-use effects
on habitat, water quality, periphyton, and benthic invertebrates in Waikato, New
Zealand, hill-country streams. N Z J Mar Fresh 1997;31:579–97.
Ralph C. Habitat association patterns of forest and steppe birds of Northern Patagonia,
Argentina. Condor 1985;87:471–83.
Resh VH, Norris R, Barbour M. Design and implementation of rapid assessment
approaches for water resource monitoring using benthic macroinvertebrates. Aust J
Ecol 1995;20:108–21.
Richardson JS. Aquatic arthropods and forestry: effects of large-scale land-use on
aquatic systems in Nearctic temperate regions. Can Entomol 2008;140:495–509.
Roy AH, Rosemond AD, Paul MJ, Length DS, Wallace B. Stream macroinvertebrate
response to catchment urbanization (Georgia, USA). Freshwater Biol 2003;48:
329–46.
Saunders D, Hobbs R, Margules C. Biological consequences of ecosystem fragmentation:
a review. Conserv Biol 1991;5:18–32.
Saunders DL, Meeuwig JJ, Vincent CJ. Freshwater protected areas: strategies for
conservation. Conserv Biol 2002;16:30–41.
Scrimgeour GJ, Kendall S. Effects of livestock grazing on benthic invertebrates from a
native grassland ecosystem. Freshwater Biol 2003;48:347–62.
Sokal RR, Rohlf FJ. Biometry. 3rd edition. New York: W.H. Freeman and Company; 1995.
Soto D, Arismendi I, Gonzalez J, Sanzana J, Jara F, Jara C, et al. Southern Chile, trout and
salmon country: invasion patterns and threats for native species. Rev Chil Hist Nat
2006;79:97-117.
Strayer DL, Beighley RE, Thompson LC, Brooks S, Nilsson Ch, Pinay G, et al. Effects of land
cover on stream ecosystems: roles of empirical models and scaling issues.
Ecosystems 2003;6:407–23.
Subramanian KA, Sivaramaskrishnan KG, Gadgil M. Impact of riparian land-use on
stream insects of Kudremukh National Park, Karnataka State, India. J Insect Sci
2005;49:1-10.
Tell G, Izaguirre I, Quintana R. Flora y Fauna Patagónicas. Bariloche, Argentina:
Ediciones Caleuche; 1997.
ter Braak CJF, Smilauer P. CANOCO Reference Manual and User's guide to Canoco for
Windows: Software for Canonical Community Ordination (version 4). Microcom-
puter power; 1998. (Ithaca, NY, USA).
ter Braak CJF, Smilauer P. CANOCO for Windows (version 4.02) a FORTRAN program for
canonical community ordination. Centre for biometry, Wageningen, The Netherlands.
1999.
Thompson RM, Townsend CR. Land-use influences on New Zealand stream commu-
nities effects on species composition, functional organization, and food-web
structure. N Z J Mar Fresh 2004;38:595–608.
Vuilleumier F. Bird species diversity in Patagonia (temperate South America). Am Nat
1972;106:266–71.
Walling DE, Fang D. Recent trends in the suspended sediment loads of the world's
rivers. Global Planet Change 2003;39:111–26.
Walters DM, Leigh DS, Bearden AB. Urbanization, sedimentation, and the homogenization
of fish assemblages in the Etowah River Basin, USA. Hydrobiologia 2003;494:5-10.
Wilcox B, Murphy D. Conservation strategy: the effects of fragmentation on extinction.
Am Nat 1985;125:879–87.
Willson MF, De Santo T, Sabag C, Armesto JJ. Avian communities of fragmented South
temperate rainforest in Chile. Conserv Biol 1994;8:508–20.
Wohl E. Mountain Rivers, Water Resources Monograph 14. Washington, D.C.: American
Geophysical Union; 2000.