Science of The Total Environment
Science of The Total Environment
Science of The Total Environment
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 et al., 2007). In this sense, current threats to global biodiversity require
understanding of how progressively or locally human activities might
All over the world the ecological integrity of river systems is being scale up to affect regional biotas (Manel et al., 2000). This phenomenon
endangered by land-use changes. This widespread and ever-increasing has captured the attention of scientists dedicated to the study of
phenomenon involving urbanization, agriculture, pasture conversion, communities living in aquatic ecosystems and those associated with
deforestation, and the replacement of native species by exotic ones with their riparian corridors (Danger and Robson, 2004; Diamond et al.,
commercial value, represents a real and pervasive threat to the 2002; Meador and Goldstein, 2003; Saunders et al., 2002; Thompson
biodiversity and conservation of lotic ecosystems (Allan 2004; Morley and Townsend, 2004).
and Karr, 2001; Paul and Meyer, 2001; Scrimgeour and Kendall, 2003). Widespread removal of basin vegetation has been shown to alter
However, the relationship between land-use change and alteration of flow characteristics, to change the amount of sediment introduced to
stream physical characteristics can be complex and influenced by many stream systems (Walling and Fang, 2003), to decrease infiltration and
factors acting from different spatial scales ranging from local (e.g., increase surface runoff. Frequently, stream concentrations of many
adjacent to the stream) to basin level or to ecoregional scales (Goldstein 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
⁎ Corresponding author. CONICET Laboratorio de Investigaciones en Ecología y
Sistemática Animal FCN-Universidad Nacional de la Patagonia-Sede Esquel Sarmiento
nutrients can result in overgrowth of algae and aquatic plants, which
849-9200 Esquel-Chubut-Argentina. Tel.: + 54 2945 451165; fax: + 54 2945 452271. potentially alter habitat suitability for endemic fauna (Hall et al.,
E-mail address: [email protected] (M.L. Miserendino). 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) 612–624 613
Channelization and realignment of rivers are also common 2. Materials and methods
practices in urban or agricultural areas, which can produce substrate
modification and disruption of the riffle/pool sequences that provide a 2.1. Study area and site selection
diversity of habitats for aquatic species such as fish and invertebrates
(Jones et al., 1999; Nolan and Guthrie, 1998). The clearing of riparian The study area belongs to the Andean-Humid and Sub-Andean
areas alongside rivers, as modification and/or extirpation of stream- Sub-Humid regions (Del Valle et al., 1998; Paruelo et al., 1998) and is
side vegetation, can also alter the functioning of river ecosystems and located in a transitional mountain and piedmont area in the
disrupt fluxes of organic matter and energy (McCord et al., 2007). Northwest of Chubut province, Argentina between the Chilean border
Moreover this can affect directly or indirectly the river biota. For and the city of Esquel in Northern Patagonia (Fig. 1). Studied basins
example, the loss of oviposition sites and habitat for aerial stages of are similar in size, gradient and geology. From a phytogeographic
insects with aquatic larvae can be critical to preserve “in stream” perspective, the study area is located in the ecotone between the
macroinvertebrate diversity (Bojsen and Jacobsen, 2003). Subantarctic Forest and the Patagonian steppe, and exhibits a marked
There is ample evidence that landscape factors influence aquatic altitudinal gradient. The Subantarctic Forest is constituted by
vertebrate fauna, as for instance landscape characteristics can be perennial (Austrocedrus chilensis, Nothofagus dombeyi and Maitenus
linked to fish species assemblages (Walters et al., 2003). Allan (2004) boaria) and deciduous tree species (N. pumilio, N. antarctica), whereas
has shown significant relationships between some landscape metrics the shrub and herbaceous strata are composed mainly by Chusquea
such as amount of agricultural, forest or urban land cover, and some culeou, Berberis buxifolia, Fuchsia magellanica, Aristotelia chilensis,
biological metrics for fish. At a more local scale, habitat conditions can Oenothera odorata, Fragaria chiloensis and Geranium sp. The valleys are
affect fish distribution as has been observed by Wohl (2000), who dominated by the herbaceous, shrub-like steppe vegetation, Mulinum
reported that some native species in highland stream systems may be spinosum, Stipa speciosa, S. humilis, Corynabutilon bicolor, Verbena
particularly vulnerable to replacement by generalist species in tridens, Nassauvia glomerulosa and Berberis heterophylla (Tell et al.,
response to increased sediment input. 1997).
Fragmentation of continuous habitats (e.g. riparian corridors and The exotic vegetation is composed mainly by forests of Pseudot-
native forest) results in habitat loss and an increase in isolation, which suga menziesii, Pinus ponderosa, P. radiata and P. lambertiana; in many
might affect birds by decreasing colonization, increasing mortality cases these species occupy the riparian corridor replacing most of the
and extinction, and reducing biodiversity, among other potential native species.
effects (Saunders et al., 1991; Wilcox and Murphy, 1985). Changes in Across our study region, we sampled streams impacted by four
agricultural practices also continue to have a wide range of effects on different land-uses: selective harvest of native forests (HNF: managed
terrestrial and aquatic birds species (Duncan et al., 1999; Henderson native forest), plantations of non-native commercially-harvest conifers
et al., 2000), whereas urbanization is considered one of the leading (Pn: pine plantations), grazed pasture (Pas: pasture), and urbanization
drivers of native bird species extirpation at the continental and (Ur: urban). We also sampled two types of reference streams: non-
regional scales (Czech et al., 2000). managed native forests (NF) and reference urban streams (R-ur).
Biodiversity in Patagonian mountains, is globally significant due to Within each of these six categories, we collected samples from three
pronounced endemism, habitat heterogeneity and biogeographic streams. A sampling site was a 100-m reach of the selected stream, for
location (Morrone 2006; Paruelo et al., 1998). Presently there is a bird censuses this area was extended to accomplish the protocol (see
strong concern because land-use practices are changing rapidly the biological sampling).
landscape in the region, being the most widespread activities the Sites on non-managed native Nothofagus forest (NF: Chiquito, Loro
conversion of native forest to pasture, forest exploitation (wood and Comisario) were considered as reference sites to test for the
collection for fuel, carpentry, etc.), and the substitution of native following impacts: conversion of forest to pasture, pine plantation and
forest for pine plantations. These human activities have gained wood extraction. Three sites on streams with native N. antarctica and
attention in recent studies: analyses of water quality and macro- N. pumilio managed forest were selected (HNF: Glyn, Cabeza de Vaca
invertebrate response to impairment (Miserendino and Pizzolón, and Pipo). At these sites the harvest was achieved during the spring
2000; Miserendino et al., 2008); land-use changes (Miserendino, and summer seasons previous to the study. The logging operations
2004; Miserendino and Pizzolón 2004); effect on fish (Di Prinzio et al., implied a selective cut of young to mature trees (dead and live
2009; Lara et al., 2009) and bird communities (Lantschner and Rusch, specimens), which affected no more than 50% of the studied area/
2007; Willson et al., 1994). parcel. Exploitation should exclude specimens from the river corridor
Assessing the impact of land-use activities on river catchments is and operators also have to keep the streams free of debris and
an important subject faced by resource managers. Although stream branches once the tree is logged. However during the survey we
ecologists traditionally have tried to address how land-use changes observed some river corridors having logged trees, and some water-
affect aquatic environments, integrated approaches examining dis- courses obstructed with debris. Most of the properties having wood
turbance through environmental features and biological communities collection permission have a mixed management, thus areas are used
(including aquatic plants, macroinvertebrates, riparian and littoral for extensive livestock which is sustained by the herbaceous stratum.
invertebrates, fish and birds) are not frequent. It is also crucial to To assess pasture impact we selected sites (Pas: Nant y Fall,
regionally calibrate and test existing stream assessment protocols. Manguera and Los Ñires) that had been cleared from the native
To test the hypothesis that greater intensity of land-use will have Nothofagus forest (~60–70 years ago) and had been intensively grazed.
negative effects on water quality, stream habitat and biodiversity, in Pasture sites sustain livestock, mainly cows and sheep. The pine
this work we assess 18 stream sites (north-western Chubut province) plantations sites corresponded to streams running (950–1200 m)
subjected to a gradient of land-use practices (non-managed native through plantations of the exotics P. menziesii, P. ponderosa, P. radiata
forest, managed native forest, pine plantations, pasture, urbaniza- and P. lambertiana (Pn: Golondrinas, Patriada and Ifona) that were
tion). We also evaluate the quality of riparian ecosystems and in mainly established between 1954 and 1970. Three urban rivers, (Ur: Las
stream habitat conditions using two indexes adapted to Patagonian Minas, Carbón and Esquel) plus their respective reference sites (R-ur:
environments and assess the values of these indexes as predictors of Las Minas ref, Carbón ref and Esquel ref) were included in order to assess
the biotic assemblages. Finally, we attempt to identify which specifically the urban impact and make sites comparable in terms of
communities are more responsive to local and large scale changes in environmental features (Fig. 1).
Patagonian mountain streams in order to suggest better management For stream selection we looked at similitude among streams
practices. 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 percent coverage of native and exotic vegetation, pasture and urban
governmental administration offices (DPByP Dirección Provincial de settlements.
Bosques y Parques, INTA Instituto Nacional de Tecnología Agrope- At each site, percentages of boulder, cobble, gravel, pebble, and
cuaria). We conducted this study on 18 sites on 15 mountain and sand in the reach were estimated using a 1-m2 grid. Current speed
piedmont streams. Sites were visited in May (autumn), September was measured in mid channel (average of three trials) by timing a
(winter) and December (spring) 2005 and in February (summer) float as it moved over a distance of 10 m (Gordon et al., 1994).
2006, under normal hydrological conditions (avoiding rainstorms or Average depth was estimated from five measurements with a
extremely high discharge events). calibrated stick along one transverse profile across the channel. Wet
and dry widths (from bank to bank) of the channel were also
2.2. Site characterization determined. Discharge was obtained by combining depth, wet width
and current velocity as in Gordon et al. (1994). At each site, air and
In order to identify basin features, vegetation types and coverage, a water temperature were measured with a mercury thermometer.
set of LandSat images ETM (2000 and 2001, mapping resolution 15 m) At each occasion and in the mid channel section of the reach,
were classified and processed using a geographical information specific conductance, pH, turbidity and dissolved oxygen were
system (GIS) (Arc VIEW 3.3 package) by the DPByP. For each surveyed measured with a Horiba U2-probe. For nutrients analyses water
site we obtained sub-basin area above to the sampling site, and the samples were collected below the water surface, kept at 4 °C and
M.L. Miserendino et al. / Science of the Total Environment 409 (2011) 612–624 615
transported to the laboratory for analysis. Total suspended solids visual inspection over rocks, trees and bushes. Riparian and littoral
(TSS) were measured from separate water samples. Total nitrogen species were identified to the lowest taxonomic level and treated
(TN) and total phosphorus (TP) were determined on unfiltered together in the analyses. Sampling of these communities aimed at
samples digested with persulphate, whereas nitrate plus nitrite increasing the diversity of taxa sampled in the watercourses; they will
nitrogen (NO3 + NO2), ammonia (NH4), and soluble reactive phos- also be used for additional studies not included in this paper (e.g.
phate (SRP) were analyzed using standard methods (APHA, 1994). insects available as prey for fish communities).
Attributes of the riparian vegetation were examined at each site Fish sampling was carried out by electro-fishing with a powered
using an adaptation of the QBR index (Riparian corridor quality index, backpack machine and a hand net. Stream reaches were blocked off
Munné et al., 1998) for Patagonian streams: the QBRp (Kutschker et with a downstream net. Each reach was sampled three times;
al., 2009). This index combines information from total cover, downstream passes of equal effort were done in a slow zigzag
structure, complexity and naturalness of vegetation, and the degree pattern. Specimens were identified to species following López et al.
of channel alteration (e.g. bank modifications, dredging, etc.). The (2003) and counted. Given that an intensive sampling program may
total QBRp score ranges from 0 points (extreme degradation) to 100 affect the fish populations under study (see Casaux and Barrera-Oro,
points (excellent quality, natural riparian forest). 2002), up to 30 individuals per species (selected randomly) were
We evaluated habitat quality (HCI: habitat condition index) using preserved for posterior analyses; the remaining specimens were
the assessment procedure for high gradient streams of Barbour et al. returned alive to the stream. Individuals carried to the laboratory
(1999). This method ranks 10 river channel features (e.g. epifaunal were weighed (W, accuracy 0.01 g). Considering the total of the
substrate availability, frequency of riffles, etc.) from 0 to 20. A score of individuals caught, mean density (ind. m2) and biomass (g. m2) were
200 points indicates that the river is natural and pristine and in its best estimated for each species at each sampling site. For the biomass
possible condition (range: 150–200). This index evaluates the ability estimation, the mass of the individuals returned to the stream was
of the stream's physical habitat to support a given fauna, and then is a assumed to be similar to the mean mass of the individuals carried to
measure of the spatial heterogeneity of the stream (Castela et al., the laboratory.
2008). Taking advantage of the overall sampling effort, we opportunis-
A vegetation sampling was conducted in February of 2006. We tically performed exploratory avian censuses aimed to estimate bird
collected and made vouchers of 60 plants. Species were identified in abundance (number of individuals per point count), richness and
the laboratory using the keys in Correa (1978, 1999). At each reach diversity (Simpson Index) and to look for correlations between these
coverage of aquatic plants and also filamentous algae (eg. Cladophora and the remaining parameters measured throughout the study (see
sp.) were assessed visually as in Hauer and Lamberti (1996). previous discussion). At each stream and during each sampling period
we censused birds at three stations located within the riparian
2.3. Biological sampling 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
Quantitative macroinvertebrate samples were taken with a minutes after arrival at the station). Due to the overall sampling
Surber sampler (0.09 m2; 250 μm pore size). On each reach, three protocol, censuses were not performed according to the standard
samples from riffles and three from pools (n = 6) were taken. methodology (observations within the three hours after the sunrise or
Samples were fixed in situ with 4% formaldehyde, and sorted in the before the sunset). The individuals observed were identified following
laboratory under at least 5x magnification. Macroinvertebrate the descriptions in Narosky and Yzurieta (1987).
species were identified to the lowest possible taxonomic level
using regional keys (Archangelsky and Manzo, 2007; Fernández 2.4. Statistical analysis
and Domínguez, 2001; Manzo, 2005) and counted.
We calculated a set of macroinvertebrate community descriptors One way ANOVA analyses with land-use as categorical variable in
for each site and sampling date, including richness measures: taxa the treatments followed by post hoc test when significant (Tukey test
richness (SR) and Ephemeroptera, Plecoptera and Trichoptera (EPT) p b 0.05), or non-parametric ANOVA models (Kruskal–Wallis) were
richness; enumerations measures: total density (TD) (Barbour et al., used to assess differences in environmental variables among land-
1999; Resh et al., 1995) and diversity measures: Shannon-Weaver uses. Rivers subjected to certain land-use (pastures, urban, etc.) were
diversity index (H'). A biotic index previously adapted for use in the cases in the models (n = 3). Additionally sampling dates were used as
Patagonian region, BMPS (Biotic Monitoring Patagonian Streams) was cases to improve significance in comparisons, which is acceptable in
calculated (Miserendino and Pizzolón, 1999). The BMPS is an order to contrast multiple independent samples (Kruskal–Wallis)
adaptation of the BMWP (Biological Monitoring Working Party (Sokal and Rohlf, 1995). This included physico-chemical parameters
index; Armitage et al., 1983) and is obtained from a table of 95 (geomorphological measurements, nutrients, etc.), the QBRp and the
families with different degrees of pollution sensitivity (scores 1–10) HCI. The same analysis was performed for community descriptors and
present in Patagonia. The total BMPS score ranges from 0 to N150. metrics. Differences in SR, TD, H´, EPT richness and BMPS were
Riparian and littoral insects were collected using an array of assessed for the benthic community, species richness for riparian and
different techniques. Littoral species are aquatic species associated to littoral invertebrates, fish density and total biomass for the fish
the aquatic vegetation, or found underneath rocks or wood within the community, and species richness and total density for the bird
water; these species usually do not appear in Surber samples. Riparian community.
species are those species that live close to the water, or that can be Prior to analysis data were checked for normality and homogeneity
associated to the marginal vegetation, but are terrestrial. The samples of variances using Kolmogorov–Smirnov and Levene's test, respectively,
were qualitative, and the material was fixed in 80% ethyl alcohol. and log (x+ 1)-transformed when appropriate (Gotelli and Ellison,
Littoral species were collected by passing a D-frame net (Merritt and 2004).
Cummins, 1996) through the aquatic vegetation and also by removing Redundancy Analysis (RDA) was run using CANOCO (ter Braak and
the substrate (rocks, branches, algae, etc.). The content of the net was Smilauer, 1999) to assess relationships between main community
placed in a white pan and inspected visually and the insects caught attributes (riparian and littoral invertebrate richness, macroinverte-
were pulled out with featherweight forceps. Riparian species were brate metrics, density and biomass of fish and bird) and environ-
sampled by washing the substrate in white pans, and also by direct mental variables. RDA was chosen because previous inspection of the
observation. Flying adults of some orders were collected with a data revealed a linear mode rather than a unimodal response in the
sweeping net used through the vegetation on the margins, and also by 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 3.2. Aquatic plants
response of community descriptors and sites to environmental
gradients. Variables (except pH) and community attributes (except A total of 15 species of aquatic plants were recorded, with pasture
H´) were transformed (log x + 1), prior to analysis. Variables that and urban sites supporting more species than the rest (Table 4). In
were strongly intercorrelated with others (those with an inflation contrast pine and non-managed native forest sites had fewer species
factor N10) in the initial analysis, were removed and a further analysis mostly represented by Veronica anagallis-aquatica, Juncus balticus and
was carried out with the remaining environmental variables. A Monte Ranunculus sp. Bryophytes were well represented at both managed
Carlo permutation test (9999 permutations) was used to verify the and non-managed native forest sites. Aquatic plant coverage ranged
significance of the models (ter Braak and Smilauer, 1998). between 0 to N50% (Table 1).
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
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
richness, BMPS, EPTr and macroinvertebrate richness increased conductivity, nutrients and oxygen. On the other hand, stream-bank
significantly with percentage of native cover and better habitat erosion was an obvious feature in managed native sites as well as in
conditions. Instead, macroinvertebrate density augmented with urban some pasture sites with an extreme situation at Los Ñires; changes in
land cover percentage, whereas fish biomass, bird density and bird the riparian vegetation, together with the direct effects of stock
richness were positively correlated with the percentage of pasture trampling, probably accounted for an increase of fine material in the
cover. 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).
4. Discussion
We detected significant increases in water temperature and
conductivity values in harvested forest sites when compared with
4.1. Environmental variables and land-use
non-harvested sites, meaning that wood collection is affecting the
environmental features. Baillie et al. (2005) documented marked
A considerable number of physical, chemical, and environmental
increases in stream light levels and maximum monthly water
changes associated with different land-use practices were documen-
temperatures in streams draining through 25% clear-cut forests in
ted in this study. A reduction of the riparian canopy resulted in an
New Zealand watersheds and Kedzierski and Smock (2001) reported
increase of the water temperature and sedimentation symptoms,
important differences in incident light reaching streambeds when
which diminished the quality of the stream habitat. As reported in
compared with unlogged and logged sections in a lowland creek.
other studies (Collier, 1995; Miserendino et al., 2008) water quality
variables showed that urban sites were the most affected in terms of
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
4.3. Macroinvertebrate environmental relationships percentage of urban cover are fully consistent with those reported by
Strayer et al. (2003) and Morley and Karr (2001) who documented a
We found several significant relationships among macroinverte- significant relationship between macroinvertebrate species richness
brate attributes and water quality variables, land-use coverage types, and urban land cover for North American watersheds.
and riparian and habitat condition indexes. Most metrics (SR, EPT Regarding water quality parameters, the strong relationships
richness and BMPS) were positively correlated with native forest observed between macroinvertebrate metrics with dissolved oxygen,
coverage and negatively correlated with urban and pasture land nitrate and TSS confirmed the ability of benthos community to detect
cover. These observations are in agreement with Collier (1995, 2008) stream impairment. Nitrate and ammonia are strong indicators of
findings for New Zealand streams and with Roy et al. (2003) for organic pollution (Hall et al., 2001; Paul and Meyer, 2001),
streams in Georgia (USA). They reported positive relationship consequently significant reductions in SR, EPT richness, H, BMPS
between total richness, EPT richness and the percentage of indigenous occurred with increases of nitrogen concentrations at urban sites. We
forest, but also a negative correlation with the increase of pasture can conclude that these metrics are useful to detect impairment
cover. The relationships between the metrics considered and the especially at urban reaches in Patagonia.
20 3,0
NF>all Ur< R-ur, Pn, NF
RIP./LIT. INVERT. RICHNESS
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
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 heterogeneity of the stream (Castela et al., 2008) and macroinverte-
using the BMPS biotic index, this revealed that several sensitive brates diversity (H´) was also evidenced in the ordination. Subsequently,
families (e.g. Ameletopsidae, Diamphipnoidea, Nesameletidae, Ecno- native forest sites having the best ecological conditions (highest QBRp
midae, etc.), well represented in native forest and pine sites, were and HCI scores) supported the most diverse communities whereas sites
practically absent at pasture, harvested native and urban sites. As with incipient problems of sedimentation had less diverse communities
anticipated by Miserendino and Pizzolón (1999) BMPS appears composed by tolerant taxa. Physical disturbances such as dredging,
promising to assess disturbances involving sedimentation processes realignment of the channel and vegetation removal probably accounted
and habitat impoverishment. for the high TSS values and low HCI scores at sites with extreme positions
As indicated by Roy et al. (2003), the present paper highlights the role in RDA (Las Minas down, Los Ñires, Pipo).
of the riparian buffers in preserving water quality. This was evidenced in In our study, the reduction in H' and EPT richness was marked and
the RDA analysis performed, where a clear gradient in riparian significant (pair wise comparisons) when contrasting harvested
ecosystem conditions, habitat quality, NO3−NO2 and TSS contents was native forest with native forest. Bojsen and Jacobsen (2003) found
shown. A high relationship between HCI which is a measure of the spatial 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.
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- some large epibenthic taxa (Molineri, 2008), reducing individuals
brate diversity in pasture streams. Baillie et al. (2005) mentioned that body size and modifying the functional structure (Buria et al. 2007).
harvesting effects can vary depending on stream type and harvesting Thus, it is possible that some of the changes detected in benthic
practices, particularly post-harvesting wood treatment, but usually communities in our study can be related to some extent with trout
there is a decrease in relative abundance of sensitive taxa (EPT) as is impact on receiving ecosystems.
reported here. A combination of environmental modifications such as
higher temperatures, more sediment in the bottom channel, and 4.4. Usefulness of habitat assessment and riparian conditions indexes
changes in the organic material supply, could account for the changes
observed in these sensitive insect communities (Richardson, 2008). In relation to the QBRp index, site conditions varied from poor to
Introduced salmonids, which were present at most of the sampling very good. The lower QBRp values were registered at urban and
sites, usually affect benthic communities by diminishing the density of 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
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