Ecological Indicators 29 (2013) 7992

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

A tool to assess the ecological condition of tropical high Andean streams in

Ecuador and Peru: The IMEERA index
Christian Villamarn a, , Maria Rieradevall a , Michael J. Paul b , Michael T. Barbour b , Narcs Prat a
a
Grup de Recerca F.E.M. (Freshwater Ecology and Management), Departament dEcologia, Universitat de Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain
b
Center for Ecological Sciences, Tetra Tech, Inc., 400 Red Brook Blvd, Suite 200, Owings Mills, MD 21117, USA

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

Article history: The main objective of this study was to develop a highland Andean streams ecological assessment tool
Received 27 April 2012 for managers to determine the biological quality in this broad area of South America. Sampling was con-
Received in revised form 4 December 2012 ducted during the dry season at 123 sites in eight watersheds of high Andean streams from south of
Accepted 6 December 2012
Peru to North of Ecuador. The sites were at elevations above 2000 m a.s.l., and ranged in anthropogenic
disturbance from none or little (reference) to highly disturbed. Using the physicochemical, hydromor-
Keywords:
phological and aquatic macroinvertebrate assemblage attributes of the reference sites, two different
Andean highland rivers
elevation bioregions were identied (from 2000 to 3500 m a.s.l. and those sites at altitudes higher than
Multi-metric index
Ecological status
3500 m a.s.l.). Differences between these two bioregions were related to the change in altitude of the
Vegetation types most relevant environmental factors, i.e., temperature, oxygen content of the water and the extent of
Riparian forest forested vegetation in the basin and in the riparian zone. These features were paramount to having dif-
Habitat heterogeneity ferent macroinvertebrate assemblages as demonstrated by an MDS analysis of our data. Two versions
Bioregions of the multi-metric index IMEERA were developed (the acronym comes from the Spanish name ndice
Bioassessment Multimtrico del Estado Ecolgico para Ros Altoandinos) that corresponded to the two bioregions. In
the lower altitude bioregion (Bosque river type, IMEERA-B index), the pressure gradient was driven by
the organic pollution and the hydromorphological degradation. While in the higher elevation bioregion
(Pramo and Puna river types; IMEERA-P river type), the gradient was driven by the organic pollution and
the habitat heterogeneity. The IMEERA B index includes six macroinvertebrate metrics using its richness,
habit characteristics and tolerance/intolerance to disturbances (EPT taxa, % clingers, % climbers, intoler-
ant taxa, ABI and % tolerant taxa). The IMEERA P index was calculated using four metrics corresponding
to macroinvertebrate richness and its tolerance/intolerance to disturbances (total taxa, intolerant taxa,
ABI and % tolerant taxa). The index was validated with a set of independent data from the headwaters of
Guayllabamba River in Ecuador.
2012 Elsevier Ltd. All rights reserved.

1. Introduction equatorial and tropical zones have been identied as important

The ecological and economic importance of the high moun-
tain areas is increasingly recognized (Mittermeier et al., 1998;
Carrera & Gunkel, 2003; Meyer et al., 2003; Buytaert et al., 2006,
2007; Jacobsen, 2008), and in particular the aquatic ecosystems,
such as mountain Andean streams, for their roles as reservoirs as
well as other ecological services that they provide. These services
can include ood mitigation, maintenance of good water quality
and quantity, groundwater recharge, sediment retention, nutrient
recycling, habitat availability for the biota and the provision of food
resources both for ecological communities and for human popula-
tions (Meyer et al., 2003; Jacobsen, 2008). On the other hand, the
Corresponding author at: Universitat de Barcelona, Diagonal 643, 08028
Barcelona, Spain. Tel.: +34 93 403 1377; fax: +34 93 411 1438.
E-mail address: cvillamarinf@ub.edu (C. Villamarn).
reservoirs of biodiversity (Mittermeier et al., 1998; Myers et al.,
2000). In this context, the tropical Andes are one of the priority
areas to be preserved as biodiversity hotspot.
As are many headwaters in the world, high Andean streams are
coming under strong pressure due to human activities (Roldn,
1999; Sarmiento and Frolich, 2002; Carrera and Gunkel, 2003;
Jacobsen et al., 2007), and this pressure has steadily increased since
pre-Inca times (Buytaert et al., 2006; Mena & Hofstede, 2006). The
activities that most often affect high Andean streams are agricul-
ture, livestock, deforestation, road construction and pollution from
urban and industrial areas (Sarmiento and Frolich, 2002; Carrera
and Gunkel, 2003; Segnini and Chacn, 2005; Mena & Hofstede,
2006; Prat et al., 2009). These streams in the tropics are poorly
studied (Jacobsen, 2008); setting conservation priorities in this
area require that effective scientic tools are available to know
the ecological status of these rivers. Recently, tools used by water
resource agencies to assess water quality in the Andes were mostly

1470-160X/$ see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecolind.2012.12.006
80 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
physicochemical measurements, while the study of the ecologi-
cal condition of streams has been lacking. Some recent attempts
to produce biological methods suitable for the area (Acosta et al.,
2009) have become available. However, this study provides a new
robust method to assess the biologial condition of the Andean rives
similar to methods developed in other regions for the purpose of
bioassessment (Bonada et al., 2006).
Ecological assessment tools for streams have been mostly devel-
oped and applied to the streams of North America and Europe
(Prat et al., 2009), with the macroinvertebrate assemblage being
the group most frequently used in these applications (Bonada
et al., 2006). Many investigators have shown the macroinver-
tebrate assemblage to have the capacity of detecting various
alterations and multiple pollutants, owing to their sensitivity to
environmental change (Allan, 2004; Prat et al., 2009). The macroin-
vertebrate assemblage reects the biological condition of a water
body through alteration to specic composition, diversity and the
natural functional organization for a known region (Barbour et al.,
1996; Karr, 1999; Allan, 2004; Prat et al., 2009).
Although the literature on the Andean highland macroinverte-
brate assemblage is not extensive, there are some country-based
studies (Colombia, Ecuador, Peru, Bolivia and Chile) that describe
the environmental characteristics typical of the Andean high-
lands, as well as the effects of increased organic matter pollution
from cities on the composition of benthic assemblages (Jacobsen
and Encalada, 1998; Roldn, 1999; Carrera and Gunkel, 2003;
Figueroa et al., 2003; Moya et al., 2007; Acosta et al., 2009;
Prat et al., 2009). Knowledge of Andean aquatic ecosystems has
allowed development of some ecological assessment endpoints
using aquatic macroinvertebrate assemblages as in the case of the
Andean biotic index (ABI) proposed in the Calidad Ecolgica de
los Ros Altoandinos (CERA) protocol in Ecuador (Acosta et al.,
2009), and the Biological Monitoring Working Party adapted to
Colombia (BMWP-Col) (Roldn, 1999) together with some other
ones summarized in Segnini (2003) and Prat et al. (2009). How-
ever, none of these locally calibrated indices are sufcient to
adequately manage water resources throughout the Andes area.
Therefore, it is important to develop biological assessment indi-
cators that may be used for the entire region (Acosta et al., 2009;
Prat et al., 2009), which would provide consistency and broader
application.
One of the most effective methods for evaluating biologi-
cal condition of freshwaters are multi-metric indexes using the
macroinvertebrate assemblages (Karr and Chu, 1997; Karr, 1999).
Each metric composing the multi-metric index, measures a dif-
ferent component of the assemblage such as taxonomic richness,
taxonomic composition, trophic groups, habit, and its toler-
ance/intolerance to pollution; together they give a comprehensive
measure of ecological river health (Gerritsen et al., 2000; Baptista
et al., 2006; Barbour et al., 1999, 2006; Bonada et al., 2006; Prat
et al., 2009). The lack of ecological data and knowledge of regional
species traits has precluded the application of these indices in South
America prior to this study. Nonetheless, the Serra dos rgos
Multi-metric Index (SOMI) (Baptista et al., 2006) in Brazil, and one
for the Isiboro-Secure stream basin in Bolivia (Moya et al., 2007)
were designed for lowland tropical areas, but were not relevant to
the Andean highlands. In this study, the development of a multi-
metric bioassessment tool applicable to the Andean highlands was
undertaken to afford the ability for managers to implement a bet-
ter regional water resources management to a broad geographical
region.
Our research was performed in eight Andean highland basins
(between 2000 and 4800 m a.s.l.) in Ecuador and Peru. Our main
objective was to propose and test a multi-metric index for assessing
the biological condition of Andean highlands streams that could be
applied to a broad geographical range.
2. Materials and methods
2.1. Spatial and temporal scope of the study
Samples were collected in the northern and central Andes region
between October 2007 and November 2008 during the dry season.
This sampling season was chosen for several reasons: (1) ease of
accessibility, (2) the concentration of pollutants was presumably
higher due to reduced ow, and (3) community stability due to the
reduction of natural disturbances such as oods (Jacobsen et al.,
1997; Jacobsen and Marn, 2007; Maldonado et al., 2011). One hun-
dred twenty three sites were sampled, which were located between
2000 and 4800 m a.s.l. and distributed across four basins in Ecuador
and four in Peru (Fig. 1), with 14 to 16 sites per basin.
Given broad altitudinal and latitudinal gradients, different types
of vegetation were found in the studied area. Lower elevation zones
(between 2000 and 3500 m a.s.l.) are characterized by the presence
of riparian vegetation and forests in the basin. Precipitation in this
zone was highly variable, averaging between 1000 and 1800 mm
per year, depending on the basin and slope. Temperature varied
from 16 C during the day to 10 C at night, and relative humidity
was 80% (Winckell et al., 1997).
Higher elevation zones (between 3500 and 4800 m a.s.l.) were
characterized by steppe vegetation (called pramo in the north and
puna in the south) without any woodland. The natural vegetation
of this ecosystem was a herbaceous perennial with a few small
shrubs or trees, such as Polylepis (Yarupait and Albn, 2003; Garca
and Beck, 2006; Mena and Hofstede, 2006) close to the rivers. Pre-
cipitation was highly variable: it was higher in pramo zones (in
the north section of the studied area), where the average annual
rainfall was 1000 mm (Mena and Hofstede, 2006); while lower in
the puna (in the south section of the studied area), with an average
annual rainfall of 700 mm (Yarupait and Albn, 2003; Garca and
Beck, 2006). The temperature was very similar in both the pramo
and puna, with uctuations between 10 C during the day and 0 C
at night and an average annual temperature of 6 C (Garca and
Beck, 2006; Mena and Hofstede, 2006).
In the study area, some differences in the hydromorphological
and physicochemical characteristics were identied. Argollo (2006)
noted that the Andes can be grouped into three regions (North
Andes, Central Andes and South Andes) by their climatic, vege-
tal and geological characteristics. In our study, the sampled basins
are located in North and Central Andes. The climatology tends to
be slightly different in seasonality and less humidity at study area
high latitudes and both of these characteristics will inuence the
vegetation types (Aramayo et al., 2004; Emck et al., 2006). Based
on lithology data in the north of the study area (Mira, Aguarico,
Guayas, Pastaza, Santa and Mosna catchments), the geological com-
position was predominantly granite, andesite, and hard rock that
are erosion resistant (Toro et al., 2002; Segnini and Chacn, 2005;
Argollo, 2006). While in the south study area (Colca and Urubamba
catchments), the carbonates are the predominant geological com-
position, which are more soluble and increase the conductivity
values (Segnini and Chacn, 2005; Argollo, 2006).
2.2. Site selection and establishment of reference conditions
Of the 1416 locations sampled in each basin, 46 sites were
considered to be reference sites, i.e., with little or no human
interference. Multiple sites are needed to establish the biological
reference conditions (EPA, 1990; Barbour et al., 1999). Reference
sites were selected using the methods proposed by Acosta et al.
(2009) for high Andean streams. This method considers 24 param-
eters relating to the environmental conditions of different scales,
including basin, hydrology, reach and mesohabitat (Acosta et al.,
2009). Basin and hydrological aspects were rated using tools such
 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
Fig. 1. Geographical location of sampling sites located in the basins studied in Ecuador (MI: Mira 1:500.000, AG: Aguarico 1:100.000, GU: Guayas and PA: Pastaza 1:1.000.000)
and Peru (SA: Santa and MO: Mosna 1:750.000, CO: Colca 1:500.000, VS: Urubamba 1:500.000).
as cartographic maps and GIS tools. All other aspects (reach and
mesohabitat) were assessed in the eld. This method proposes that
the sites with a qualication score below 100 points will be con-
sidered unlike reference and the locations above 100 points will be
considered to be reference sites (Acosta et al., 2009).
In each basin, both unaffected sites and sites with different
amounts of anthropogenic disturbance were selected. The affected
sites are inuenced by the agricultural practices, livestock graz-
ing, urbanization and pollution from urban areas (Sarmiento and
Frolich, 2002; Carrera and Gunkel, 2003; Segnini and Chacn, 2005;
Mena and Hofstede, 2006; Prat et al., 2009). These are the principal
and frequent human activities in Ecuador and Peru. While mining
activities were considered, the inaccessibility to sampling the min-
ing efuents and the low heavy metals concentration in our streams
were inconclusive as to the impact of this activity on the ecologi-
cal condition. We used the proportion of the land use in each basin
(Andean reference condition: basin parameters, Acosta et al., 2009)
in determining the reference conditions.
2.3. Sampling of the aquatic macroinvertebrate assemblage
The aquatic macroinvertebrate assemblage was sampled using
the quantitative method protocol MIQU (from the Catalan pro-
tocol MacroInvertebrats QUantitatiu, Nnez and Prat, 2009),
adapted from the AFNOR protocol (Qualit cologique des milieux
aquatiques- Prlvement des macro-invertbrs aquatiques en riv-
ires peu profondes) (Mondy et al., 2012). The adaptation differed
from the original only in stream reach length sampled, due to
the topographic features of the Andes region and the difculty in
81
accessing some of the sites. In this study, the length of these samp-
ling sites was between 25 m and 50 m (instead of the 100 m used
in the original protocol).
The protocol calls for sampling different microhabitats at each
site using a Surber net with a sampling area of 0.1023 m2 and a
250 mesh size. For the sampling of different microhabitats, sub-
strates were categorized and separated into dominant substrates
(occupying > 5% of the sample site) and marginal substrates (5%)
(Nnez and Prat, 2009; Mondy et al., 2012), and samples were pre-
served in different containers. At each site, a total of 12 Surber
samples were taken: four from dominant habitats and four from
marginal habitats were sampled in the order of microhabitats pro-
posed by Mondy et al. (2012) protocol according to a table of
substrate denition, which prioritizes their habitability and taxa
richness (Appendix A). Finally, four Surber samples were also taken
from dominant habitats according to their representativeness (%
of cover) in the stream section. Samples of marginal and domi-
nant habitats were pooled in one container and preserved in 4%
formalin.
In the laboratory, macroinvertebrates were separated and pre-
served in 70% ethanol. Subsequently, aquatic macroinvertebrates
were identied and counted. The identication of macroinverte-
brates was conducted using the literature suitable for each group
(Holzenthal, 1988; Angrisano, 1995; Merrit and Cummins, 1996;
Roldn, 1996; Domnguez and Fernndez, 2009). Genus was the
lowest taxonomic resolution, with the exception of some Diptera
(e.g., Chironomidae, Ephydridae and Limoniidae) and beetles (e.g.,
Elmidae), which were identied at family level, and Hydracarina,
nematodes and oligochaetes, that were identied at order level.
82 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
2.4. Using physicochemical characteristics and aquatic
macroinvertebrate assemblage to dene stream types
The composition and diversity of biota largely reects the char-
acteristics of the local environment (Towsend and Hildrew, 1994;
Newson et al., 1998; Barbour et al., 1999; Gerritsen et al., 2000).
This variability of the macroinvertebrate assemblages compared
with the natural characteristics of the environment allows its use
in classifying streams in different types (Bailey et al., 1998; Barbour
et al., 1999; Hawkins et al., 2000a, 2000b; Reynoldson et al., 2001).
The characterization of aquatic ecosystems is an important step
prior to aquatic resource management and for the assessment of
the ecological condition of streams for which the use of reference
sites is necessary (Bonada et al., 2004). This classication (den-
ing types) helps in better interpreting the natural variance in the
metrics.
The characterization of the high Andean streams was conducted
using the physicochemical and hydromorphological variables of
the reference sites, through a multidimensional scaling (MDSphy)
analysis on a Euclidean distance matrix constructed with standard-
ized matrix. On the other hand, to validate the results of MDSphy a
MDS analysis using the macroinvertebrate abundances (MDSbiol)
was conducted on a Bray Curtis similarity matrix constructed with a
transformed log (x + 1) matrix. Both MDS analyses were conducted
employing the PRIMER6 program (Clarke and Warwick, 1994). The
MDS ordination method has proved more robust and produces
better separation than other methods (Barbour et al., 1996). In addi-
tion, an analysis of similarities (ANOSIM) was performed between
reference site groups to determine whether differences between
the variables of the sites in the higher and lower bioregions are
signicant with the statistic R. The global R is a distance absolute
measure between groups. The R positive value and higher shows
a low similitude between groups; while the lower values show a
high similitude between groups.
2.5. Environmental variables and stressor gradient
25 environmental variables were measured at each site, includ-
ing physicochemical, hydromorphological and habitat variables
(Appendix B). These were used to dene the stressor gradient that
affects high Andean stream macroinvertebrate assemblages (note
that all sites were used for such analysis, not only the reference
sites). Some variables were taken in situ, the velocity was mea-
sured with a mini air ow meter, and subsequently the width and
depth were measured in transects to calculate the ow. The pH
and the conductivity were measured with a multimetric sensor
YSI-63, while the dissolved oxygen (mg/l and % saturation) and the
temperature were measured with an oximeter YSI-550.
At each site 500 ml of water were sampled and kept on ice.
Ammonia, phosphates, nitrites and nitrates concentration were
measured to identify possible water impairments due to urban
or agricultural inputs. Copper, silver, lead, zinc and iron were
measured to characterize impact from mining activities. All the
measurements were performed within 48 h of collection with a
portable spectrophotometer Hach Lange DR2800. To assess the
quality of the riparian vegetation, the Andes riparian vegetation
index was used (QBR-And) (Acosta, 2009), which provides a rapid
assessment of the overall condition of Andean riparian vegeta-
tion by using four aspects (degree of cover in the stream zone,
cover structure, cover quality and the degree of naturalness of the
stream channel). The QBR-And index is an adaptation of the QBR
index (Munn et al., 2003). The QBR-And differs from the origi-
nal in the cover quality aspect, which was adapted to neo-tropical
high Andean vegetation (Acosta et al., 2009). In study sites located
above 3500 m a.s.l., the cover quality aspect was excluded because
the riparian zone has no tree cover (pramo and puna streams);
thus, the QBR-And index would only have a maximum value of
75 points in these locations. To compare the values of QBR-And
from the higher zone with those of the lower zone (maximum 100
points), the values were normalized from 0 to 1. The total score
and the partial scores for each part of the QBR were used in the
statistical analysis.
The stream habitat assessment index (IHF) was applied to deter-
mine the quality of habitats existing in the sampled sites and
to determine how they inuenced the assemblage composition
(Pardo et al., 2002). This index uses seven aspects (embeddedness,
presence and frequency of rapids, substrate composition, veloc-
ity/depth relationship, percentage of shade, habitat heterogeneity
and aquatic vegetation coverage) to evaluate the habitat conditions
for macroinvertebrates, and has also been adapted to the particular
characteristics of the Andean highlands (Acosta, 2009). The index
ranges between 11 and 100 and this score as well as the individual
scores for each of the 7 parts of the index were used in the analysis.
To determine the stressor gradient affecting high Andean
streams, a principal component analysis (PCA) was conducted for
each zone (Bosque and Pramo-Puna) using the Ginkgo program
(Cceres et al., 2003) and employing all the environmental vari-
ables. Previously, the variables were standardized subtracting the
mean and dividing by standard deviation to achieve normal distri-
butions of each variable. A Spearman correlation was performed
to identify highly-correlated variables (>0.8), which were removed
to eliminate redundant data in the analysis. The rst and second
axes were selected as stressor gradients. The location values of the
sites in the PCA were normalized to a 01 range (Cceres et al.,
2003; Snchez-Montoya et al., 2010) and these values were used
as stressor gradients, with values closer to 1 indicating greater dis-
turbance.
2.6. Development of the multi-metric index
The data obtained from the analysis of aquatic macroinverte-
brate assemblages were used to calculate 69 biological metrics
(Appendix C) that should indicate the assemblages response to
changes caused by human activity (Carter et al., 1996; Barbour et al.,
1999; Wiseman, 2003; Boonsoong et al., 2009). These metrics were
grouped into different categories that relate to different attributes
of the macroinvertebrate assemblages (Gerritsen et al., 2000). The
categories of metrics included in this study were as follows: tax-
onomic richness, taxonomic composition, functional group, habit
preference and values of tolerance/intolerance to increased pol-
lution. To determine the biological metrics that best correlated
to the stressor gradient, a Spearman correlation was performed
among the 69 calculated metrics and the stressor gradient. Metrics
were selected that showed a correlation (Spearman r 0.4) to the
stressor gradient as determined by the environmental parameters.
Correlation coefcient was calculated among the biological
metrics exhibiting signicant response to the environmental
stressor gradient. This calculation was performed to minimize
redundancy and to simplify the information. Highly correlated
metrics (Spearman 0.8) were excluded from subsequent analyses.
Furthermore, the discriminative efciency (DE) (Barbour et al.,
1996; Gerritsen et al., 2000) of the metrics that showed low
redundancy and higher correlation with the stressor gradient was
determined and tested. With this analysis, nal metrics were
selected for the multi-metric index. Discriminative efciency is an
important value for the selection of metrics because it is the ability
of a metric to discriminate between reference sites and non refer-
ence sites (Barbour et al., 1996; Gerritsen et al., 2000). The DE is
calculated using the following formula:
  a 
DE = 100 (Formula 1)
b
 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992 83

Table 1
Variables with the greatest inuence in the PCA. Respective weights, axes and river types to which they belong.

Factor PCA Bosque PCA Pramo/Puna

pc-1 pc-2 pc-1 pc-2

Physical-chemical Oxygen 0.35

Temperature 0.30 0.26
Ammonia 0.30
Phosphates 0.26
Nitrates 0.28 0.25
Copper 0.38
Lead 0.37
Hidromorphology Degree of cover in the stream zone (QBR 1) 0.34
Cover structure (QBR 2) 0.35
Cover quality (QBR 3) 0.29
Naturalness of the stream channel (QBR4) 0.25
QBR total score 0.38
Habitat Rapids embeddednes (IHF 1) 0.39
Rapids frequency (IHF 2) 0.31
Velocity/depth relationship (IHF 4) 0.29
Percentage of shade (IHF 5) 0.35 0.41
Elements of heterogeneity (IHF 6) 0.36
Aquatic vegetation coverage (IHF 7) 0.31
IHF total score 0.43

where b is the total number of non reference sites (Acosta et al.,
2009). The value of a represents metrics that decrease in response
to stressors (e.g., EPT, total taxa) and corresponds to the number
of non reference sites with values below the 25th percentile of the
distribution of reference sites. For metrics that increase with expo-
sure to stressors (e.g., % Diptera and tolerant taxa), the value of a
corresponds to the number of non reference sites with values above
the 75th percentile of the distribution of reference sites.
The criteria to select the nal biological metrics were: (i) a Spear-
man correlation above 0.4, and (ii) a discriminative efciency above
50. To select the metrics and to avoid redundancy when high corre-
lation existed between two of them (Spearman 0.8); metrics that
are more generally accepted (e.g.: number of taxa) or widely used
in other indices (e.g. EPT) were given preference to be included
in the index compared to other more specic ones. Finally, the
selected metrics were normalized (0100) (Gerritsen et al., 2000)
from which they would be aggregated to obtain the nal value of the
index. For metrics that are expected to decrease with the stressor
gradient (Formula 2), the following formula was used:
 X
 sites was calculated (EDref) together with that of the affected sites
score = 100 (Formula 2)
X95 Xmin
where X = metric value, X95 = 95th percentile of reference sites val-
ues and Xmin = minimum possible value.
In contrast, for metrics that are expected to increase with the
stressor gradient (Formula 3), the following formula was used:
X X
 affected sites, (EDimp), a is the number of affected sites with a
max
score = 100 (Formula 3)
Xmax X5
where X = metric value, X5 = 5th percentile of reference sites values
and Xmax = maximum possible value.
Lastly, to construct a nal index, the average of the normalized
values of the nal metrics was calculated for each site (Formula 4),
giving a nal index value between 0 and 100 (Barbour et al., 1999,
2006; Gerritsen et al., 2000), with 0 indicating poor quality (bio-
logical impairment) and 100 indicating good quality (unimpaired).
 score 1 + score 2&score n 
index value = (Formula 4)
N
where score 1, 2, . . ., n = the value obtained for each metric in the
score from 0 to 100, and N = number of calculated metrics.
To determine the discriminating capacity of the nal multi-
metric index between reference sites and affected sites, the DE was
calculated using the same formula as above (Formula 1).
Index validation was conducted on a different database from the
original dataset used to develop the index. The database used for
validation of the index was based on twenty streams sampled in
Ecuador, ten of which are located in the higher elevation bioregion
(pramo) and the remaining ten in the lower elevation bioregion,
between 2000 and 3500 m a.s.l. (Ordnez, 2011). For this dataset,
the sampling of physicochemical data, the application of indices of
habitat quality, the establishment of reference sites and the assess-
ment of riparian vegetation were made according to the protocol
proposed by Acosta et al. (2009), the same protocol used in the
calibration dataset.
The validation consisted of applying the multi-metric index to
the independent database. The normalization formulas obtained
for each metric were used, and the nal index value was calcu-
lated for each site in the independent database. To determine if
the index was applicable or not, the DE value of the reference
(EDimp) (Gerritsen et al., 2000). The DE calculation of the valida-
tion uses the same equation (Formula 1) but with the following
criteria: for reference sites (EDref), a is the number of reference
sites in the independent database that show a nal index value
above the 25th percentile of the original data, and b is the total
number of reference sites in the independent database. For the
nal index value lower than the 25th percentile of the original
data, and b is the total number of affected sites in the independent
database.
Having validated the index and conrmed its effectiveness,
ve biological quality groups were established (very good, good,
moderate, poor, poorest), as recommended by the European Water
Framework Directive (Wallin et al., 2003). The threshold between
good and moderate was established using the 25th percentile
of reference sites (Barbour et al., 1999). The threshold between
very good and good was set using the 75th percentile of refer-
ence sites. Subsequently, a range of values was determined using
the value of the 25th percentile of reference sites and the min-
imum value of the affected sites. This range was divided into
three groups to determine the categories of moderate, poor and
poorest.
84 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
Fig. 2. MDS analysis of physicochemical and hydromorphological variables (a:
MDSphy) and MDS analysis of aquatic macroinvertebrate assemblages (b: MDS-
biol) of reference sites in high Andean streams in Ecuador and Peru. In gray dots,
the stream of the Andean higher river type P: (3500 to 4800 m a.s.l.) while lower
elevation bioregions river type B:(2000 to 3500 m a.s.l.) are in black dots.
3. Results
3.1. The typology of high elevation Andean streams
Multidimensional scaling analysis with physicochemical and
hydromorphological data (MDSphy) from reference sites showed
important differences between higher altitude sites (3500 to
4800 m a.s.l.) and those in lower elevation bioregions (2000 to
3500 m a.s.l.) (Fig. 2a). Similar results are obtained using the
macroinvertebrate assemblages with the same methods. The MDS-
biol (Fig. 2b) conducted with macroinvertebrate community data
have the same response, showing discrimination between higher
and lower altitude of reference sites. Although the differences look
gradual in both the MDSphy and MDSbiol, the analysis of similari-
ties (ANOSIM) shows that differences between the higher and lower
altitude assemblages are signicant using the physicochemical and
Fig. 3. PCA vectors and primary stressor gradient of the river type B.
hydromorphological data (global R 0.025, p 0.001), as well as with
the macroinvertebrate assemblage (global R 0.029, p 0.02).
For these reasons it was therefore decided to group the sites into
two sets (river type B for lower altitude bioregions and river type P
for higher altitude bioregions) and to carry out the stressor gradient
separately because these differences could mask changes caused
by human activities. Thus, indices were developed independently
for each of the two areas (representing two different river types)
identied in the MDS. These two types will be qualied until now
as P (form Pramo or Puna) the sites at higher altitudes and B (from
Bosque) for the sites at lower altitudes.
3.2. Determination of pressure gradients
Given the previous results, the determination of pressure gradi-
ents was performed using the PCA of the environmental variables
for each type of stream independently (P and B). In the lower ele-
vation bioregion (river type B) (2000 to 3500 m a.s.l.), the rst
two axes of the PCA explained 38% of the total variance, and two
pressure gradients were determined: hydromorphological degra-
dation and organic pollution (Fig. 3). The rst PCA axis is directly
related to the quality of the riparian woodland and hydromorpho-
logical degradation. Thus, the degree of cover, the cover structure
and the quality of riparian vegetation cover, along with the natu-
ralness of the stream channel and the nal value of the QBR, are
the variables with greatest weight in the rst axis of the analysis
(>0.25) (Table 1). The second axis of the PCA shows the variables of
temperature, ammonia, nitrites and copper as having the greatest
weight (>0.25) (Table 1). We associate a loss of riparian vegeta-
tion quality with an increase in agricultural or populated areas,
which also causes the increase of organic pollutants in the envi-
ronment.
In highland streams of river type P (pramo and puna > 3500 m
a.s.l.), the rst two PCA axes explain 32% of the total variance, with
two pressure gradients different from those of the lower altitude
bioregion: change in habitat heterogeneity and organic pollution
(Fig. 4). The sites in the higher elevation bioregion are arranged
along the rst PCA axis by the stream habitat heterogeneity, so
that in the right side shows the sites that have a greater number
of habitats, such as rocks, round stones, aquatic vegetation, leaf
litter and exposed roots. Sites were arranged along the second axis
according to phosphate concentrations (Table 1).
Table 2
Candidate measures to develop the multi-metric index for each bioregion with its respective discriminative efciency value (ED). Measures that were selected for the nal index for the river type Bosque (B) and/or river type
Pramo-Puna (P) are indicated.

Metric Assemblage Gradient Spearman Discriminative Selected metrics to Gradient Spearman Discriminative Selected metrics to Reason for include or exclude
response correlation B efciency (DE) B river type B correlation P efciency (DE) P river type P the metric in the nal index

Taxonomic richness
Coleoptera taxa ? 0.2 0.6 Unknown response
Diptera taxa ? 0.2 0.5 Unknown response
Ephemeroptera taxa Decrease 0.4 50 0.5 77.7 Included in EPT
Plecoptera taxa Decrease 0.4 73 0.1 61.1 Included in EPT
Trichoptera taxa Decrease 0.5 51.6 0.3 33.3 Included in EPT

C. Villamarn et al. / Ecological Indicators 29 (2013) 7992

EPT taxa Decrease 0.4 51.6 0.2 22 Correlated with gradient and
DE acceptable
Total taxa Decrease 0.4 0.7 88.8 Correlated with gradient and
DE acceptable

Taxonomic composition
% Baetidae/Ephemeroptera Increase 0.2 40 0.5 22.2 Without a good response
% Trichoptera Decrease 0.4 0.1 Without a good response
% Amphipoda Decrease 0.1 0.1 Without a good response
Evenness Decrease 0.2 0.3 Without a good response

Functional group
% Filterers Increase 0.1 0.2 Without a good response
% Scrapers Decrease 0.1 40 0.2 55.5 Without a good response

Habit/behavior designations
% Climbers Decrease 0.5 51.6 0.3 33.3 Correlated with gradient and
DE acceptable
% Clingers Decrease 0.5 75 0.1 22.2 Correlated with gradient and
DE acceptable

Tolerance
Intolerant taxa Increase 0.4 80 0.4 66.6 Correlated with gradient and
DE acceptable
% tolerant taxa Decrease 0.5 93.3 0.6 72.2 Correlated with gradient and
DE acceptable

Indexes
Margalefs diversity Decrease 0.5 0.7 High correlation with ABI
BMWP Decrease 0.4 0.5 High correlation with ABI
ABI Decrease 0.5 90 0.5 83.3 Correlated with gradient and
DE acceptable

85
86 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992

Table 3
Metrics for the river type Bosque (IMEERA B) with their respective 5th or 95th per-
centiles, maximum or minimum value and the formula applied for the multi-metric
index.

Metrics that decrease 95th percentil Min Standardization formula

with the gradient

EPT taxa 6 0 Score = (100 (X/6))

% Climbers 22.03 0 Score = (100 (X/22.03))
% Clingers 35.68 0 Score = (100 (X/35.68))
Intolerant taxa 7 0 Score = (100 (X/7))
ABI 120 14 Score = (100 (X/106))

Metrics that increase 5th Max Standardization formula

with the gradient percentil

% Tolerant taxa 12.5 71.4 Score = (100 (71.4 X)/(58.9))

Fig. 4. PCA vectors and primary stressor gradient of the river type P.

3.3. Selection of biological metrics

Of the 69 biological metrics calculated for the sites in each zone

(Appendix C), 20 metrics correlated (Spearman > 0.4) to stressor
gradients determined by streams from the two bioregions (Table 2).
The combination of the graphical and statistical methods used
for the evaluation of the metrics helped to determine the metrics
that give greatest stressor signal. The logic of including or excluding
different metrics in the nal multi-metric index was considering
the Spearman correlation among stressor gradient and biologi-
cal metrics and, for other hand, discriminative efciency among
impaired and reference sites (Table 2). Thus, from the 20 responsive,
uncorrelated metrics, 6 were selected for the sites in the river type B
(number of EPT taxa, % climbers, % clingers, number of tolerant fam-
ily taxa, % of intolerant families and the ABI index) and 4 for the sites
in the river type P (total number of taxa, number of tolerant fam-
ily taxa, % of intolerant families and the ABI index). These metrics
showed good discrimination of reference sites from affected sites.
In both river types B and P, the Andean Biotic Index (ABI) (Acosta
et al., 2009) was selected as highly correlated with the stressor gra-
dient. This index proposes revised tolerance/sensitivity values for
some macroinvertebrate families, based on literature focused on
the Andean region (Acosta et al., 2009). This is of interest, because
the tolerance information of the families was not included in other
indexes, such as BMWP-Col.
3.4. Performance of the high elevation Andean stream
multi-metric index (IMEERA)
3.4.1. High elevation Andean stream multi-metric index of the
bioregion between 2000 and 3500 m a.s.l. (IMEERA B)
Using the six selected metrics for the lower elevation biore-
gion and after values were normalized, the nal index value was
obtained, giving the same weight to the six metrics (Table 3). The
index is called IMEERA (from the Spanish, ndice Multimtrico
de Estado Ecolgico para Ros Altoandinos) with a B indicating
that sites are in basins covered by forests (Bosque in Spanish). The
box plot shows a good discrimination between reference sites and
affected sites, and the index has a DE of 72.97, which is applicable
to high altitude Andean streams between 2000 and 3500 m a.s.l.
Fig. 5. Discriminative efciency expressed as the percentage of sites showing values
less than the 25th percentile of reference sites for metrics that decrease with the
stress gradient and above the 75th percentile for metrics that increase with stress.
Box plot of the multi-metric index and classication of reference and affected sites
of the high elevation Andean streams in the river type B.
3.4.2. High elevation Andean stream multi-metric index of the
bioregion between 3500 and 4800 m a.s.l. (IMEERA P)
To develop the index for high Andean streams in the Pramo and
Puna bioregions, four metrics were selected, the values were nor-
malized and then the nal index value was determined (Table 4).
IMMERA P refers to the usefulness of this index in the Pramo and
Puna, areas where no forests are present in the basin neither in the
riparian zone. The DE of the reference sites from the affected sites
and the categorization of the index are shown in the box plot. The
index developed for the higher elevation bioregion in the Andes
shows a DE of 66.66 (Fig. 6). The threshold value between good
and moderate class boundaries was the 73, while 99 was the one
between good and very good classes. The rest of the values vary
among 7248 (Table 5).
Table 4
Metrics for the river type Pramo-Puna (IMEERA P) with their respective 95th per-
centile, maximum or minimum value and the formula applied for the multi-metric
index.
Metrics that decrease 95th Min Standardization formula
with the gradient percentil
Total taxa 23 3 Score = (100 (X/20))
Intolerant taxa 5 0 Score = (100 (X/5))
ABI 91.8 9 Score = (100 (X/82.8))

(Fig. 5). The IMEERA B rating values establishes the value 43 as a

Metrics that increase 5th Max Standardization formula
score that separate the good and moderate, while, 73 is the thresh- with the gradient percentil
old between good and very good, the rest of values vary among 42
% Tolerant taxa 14.6 66.6 Score = (100 (66.6 X)/(52))
to 22 (Table 5).
 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
Table 5
Rating values and class boundaries for high Andean streams for each river type.
Class boundaries Rating values
IMEERA B IMEERA P
Very good 73 99
Good 7243 9873
Moderate 4235 7259
Poor 3423 5849
Poorest <22 <48
Fig. 6. Discriminative efciency expressed as the percentage of sites showing values
less than the 25th percentile of reference sites for metrics that decrease with the
stress gradient and above the 75th percentile for metrics that increase with stress.
Box plot of multi-metric index values and the classication of reference and affected
sites of high elevation Andean streams in the river type P.
3.5. Validation of the multi-metric index
As outlined in the methodology, the validation of the multi-
metric index IMEERA was conducted using an independent
database of aquatic macroinvertebrate assemblages in the trib-
utaries of the micro-basin of the Chiche stream (Guayllabamba
Stream Basin) located in Ecuador (Ordnez, 2011). This study had
sites located in both the higher and lower elevation bioregions. The
sites of the lower elevation bioregion had an EDref of 100 and an
EDimp of 77.7. While the sites in the higher elevation bioregion
show an EDref of 100 and an EDimp of 80. The validation pro-
cess also shows a good discrimination between reference and non
reference sites in both river types (Fig. 7).
4. Discussion
The composition and diversity of aquatic macroinvertebrate
faunal assemblages show great variability, depending on the phys-
ical, climatic and geomorphological characteristics in which it is
located (Barbour et al., 1999; Gerritsen et al., 2000). In the high
elevation Andean streams studied, two different river types were
found with different macroinvertebrate assemblages and different
hydromorphological conditions. Those of the highest altitude areas
(Pramo and Puna area, river type P, above 3500 m a.s.l.), and those
at less altitude (between 2000 m and 3500 m a.s.l.), which have a
well dened riparian area and a more forested basin (river type B).
The natural variability of streams complicates the process of set-
ting and classifying reference sites (Barbour et al., 1996), which
is important and essential in the development of multi-metric
indices. Therefore, the method used to develop the index was aimed
at minimizing this variability, thus ensuring the development,
applicability and replication of the index (Smith et al., 2005). Our
87
Fig. 7. Box plots for the reference sites and affected sites of high elevation Andean
streams in the river type B (a) and the river type P (b). Which were performed with
independent data set from the Chiche River in the upper part of the Guayllabamba
basin in Ecuador.
study showed differences in the composition of physicochemical,
hydromorphological and aquatic macroinvertebrate assemblages
in reference sites of the Andean highlands that were especially cor-
related to the altitudinal gradient in natural conditions. This change
with the altitudinal gradient has been described by several authors
(Vannote et al., 1980; Jacobsen et al., 1997, 2003; Jacobsen, 2003).
These differences are also evident in the habitat characteristics
and quality of riparian vegetation. Therefore, the differences in the
ecosystems of the lower elevation bioregion (2000 to 3500 m a.s.l.)
and higher elevation bioregion (3500 to 4800 m a.s.l.) identied in
our study were used in the denition of the multimetric indices. In
the lower elevation bioregion, the absence of riparian vegetation
may be associated with the impact of human activities; in contrast,
in the higher elevation bioregion, it is the natural condition of the
Andean pramos and punas (Sarmiento and Frolich, 2002; Garca
and Beck, 2006; Mena and Hofstede, 2006). In the case of the lower
elevation bioregion, it was important to take into account the qual-
ity of vegetation and naturalness of the riparian zone, criteria which
are included in the index QBR. For all these reasons, the develop-
ment and application of the IMEERA has been made independently
for each bioregion: IMEERA P for river types of Pramo and Puna
zone and IMEERA B for the lower altitude bioregion with clear and
well developed riparian area.
The establishment of a river typology may lead in many cases to
a great number of river types, as is the case of GUADALMED project
with 9 river types established (Bonada et al., 2004). The number
88 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992
of river types depends mostly on the physicochemical or biological
available data from reference sites (Gerritsen et al., 2000; Bonada
et al., 2004). In our study, the available information allowed us to
determine only two river types as statistically signicant, which
is very convenient for managers to dene and establish monitor-
ing programs. In addition, the GUADALMED biomonitoring system,
for example, has many sites, in a smaller geographic area than the
Andes, Moreover, we interpret the reduction in river types in the
Andes because the intense inuence of altitude not only to the
macroinvertebrate assemblage but also to the physicochemical and
river forest features, as has been demonstrated in other studies
in Andean rivers (Jacobsen, 1998, 2003, 2004, 2008; Carrera and
Gunkel, 2003; Jacobsen et al., 2003; Jacobsen and Marn, 2007).
Acosta et al. (2009) proposed one ecological quality assess-
ment protocol for high Andean streams (CERA), which considers
the differences in the characteristics of the higher Andean zone.
They demonstrated the importance of using methods of assessing
habitat conditions of the stream bed (IHF index) or the riparian
vegetation (QBR-And index), because of its inuence on the struc-
ture and composition of the macroinvertebrate assemblages (Pardo
et al., 2002; Munn et al., 2003; Boonsoong et al., 2009) and for
characterizing disturbances in the aquatic ecosystem. Thus, sev-
eral studies have demonstrated the relationship between habitat
assessment and the outcomes of the bio-assessment of the aquatic
macroinvertebrate assemblage (Rabeni, 2000; Munn et al., 2003;
Acosta et al., 2009). The quality of the habitat of the riparian zone
and tree cover can inuence EPT taxa richness, total richness and
diversity (Bailey et al., 1998; Rios and Bailey, 2006). Regardless of
differences in natural character, the increase in urban areas, agri-
cultural practices and industry have intensied pressure on tropical
streams (Jacobsen and Encalada, 1998). Loss of riparian vegetation,
increase in organic matter and loss of habitat have been estab-
lished as common issues for the conservation of Andean aquatic
ecosystems (Carrera and Gunkel, 2003; Moya et al., 2007; Jacobsen,
2008; Acosta et al., 2009; Ordnez, 2011). These pressures pro-
duce changes in all attributes of the macroinvertebrate assemblage,
including composition, species richness and abundance or relative
density of individuals (Cao et al., 1997). Alterations of the ripar-
ian areas are prevalent around the world (Jacobsen, 1998; Allan,
2004; Buytaert et al., 2006, 2007) and should be addressed in any
biological assessment. For this reason integrating the hydromor-
phological conditions in the setting up of an index provides an
added dimension to only using physicochemical conditions. Varia-
tions in the natural vegetation cover of the instream habitat were
an important component of the stressor gradient, indicating that
the IMEERA index is not only sensitive to organic pollution but
to habitat degradation. As human population becomes more dis-
persed in the area and rivers have a considerable ow, the extent
and importance of organic pollution is diminished compared to the
hydromorphological degradation due to agriculture and livestock.
Before this study, most ecological assessment methods using
aquatic macroinvertebrate assemblages applied to the high altitude
Andean streams have been designed using qualitative or semi-
quantitative data, as in the case of ABI, proposed in the CERA
protocol (Acosta et al., 2009), or BMWP-Col (Roldn, 1999). In addi-
tion, the previous indices, such as ABI and BMWP-Col, require
to set the reference values for each specic basin where is the
index was applied (Acosta et al., 2009). The implementation of
an index developed from a quantitative database arising from
extensive sampling in a large area and using regional reference
conditions, as in the case of the IMEERA, provides a more prac-
tical tool in assessing the ecological quality of Andean streams
(Figueroa et al., 2005, 2007; Acosta et al., 2009; Prat et al., 2009).
This assessment tool is applicable to a broad geographical area
without having to establish specic tresholds of quality status for
each basin. The IMEERA index respond to environmental pressures
in both the higher and lower elevation bioregions. The resulting
multimetric indices were capable of evaluating the ecological con-
dition when applied to other areas (validation data subset). Note
that the ABI index is used as a metric in both IMEERA indexes,
which indicates the usefulness of these previous and more restric-
tive measures of disturbance pressure. The integration of ABI with
other metrics made the value of the index more independent of the
maximum values that may be achieved by ABI depending on the
reference value of each particular basin or river type (Acosta et al.,
2009).
The development of IMEERA has taken all the precedent con-
siderations and using descriptive statistics and graphical analyses
to select the metrics that compose the multi-metric index. The
effectiveness of this method has been demonstrated in studies
using the biological attributes of the benthic assemblage to evalu-
ate the ecological condition of streams (Barbour et al., 1996, 2006;
Gerritsen et al., 2000; Baptista et al., 2006; Boonsoong et al., 2009).
The IMEERA, in addition to meeting this requirement, give greater
information on the various aspects of structure, composition and
environmental health of streams (Karr, 1999; Gerritsen et al., 2000;
Baptista et al., 2006; Barbour et al., 2006; Solimini et al., 2008;
Barbour and Paul, 2010). The six metrics selected for the lower
elevation bioregion (IMEERA B) and the four metrics selected for
the higher elevation bioregion (IMEERA P), representing richness,
habitat and tolerance to pollution originated by agriculture, live-
stock, urbanization and pollution from urban areas; were both
validated on an independent set of sites. This validation demon-
strated the effectiveness of the multi-metric method and that it
could be applied to high Andean streams as a tool for evaluating
biological integrity.
The IMEERA is an assessment tool restricted to the streams
located above 2000 m a.s.l.; but has broad latitudinal application in
both the Northern and Central Andes. Both IMEERA B and IMEERA
P can be used from North of Ecuador to South of Peru and both
in the Pacic or Atlantic basins. The differences between the two
indices, as indicated previously, are due to differences in vegetation
type and the habitats that this vegetation provides, in addition to
variability in physical and chemical characteristics of these streams
(Omernik, 1995). In fact, the absence of metrics related to riparian
zone (QBR values) in the index for high elevation bioregion (IMEERA
P) is determined by the natural absence of riparian vegetation. Thus,
one of the most signicant contributions of this study compared
with other studies in the Andean highlands is the broad geograph-
ical range of the sampled area, from northern Ecuador to southern
Peru. It is expected that the IMEERA could and would be applied
to other countries with altitudes over 2000 m a.s.l. in the northern
and central Andes. The use of the same assessment tool across large
areas, simplies the task of water managers in the way to improve
water resource management with the objective to preserve and
restore the ecological integrity of streams and rivers. An on-line tool
has been developped to calculate the IMMERA index and is available
at: http://www4.ub.edu/riosandes/index.php/cabira.html.
5. Conclusions
The results obtained in this work show that the IMEERA is a
suitable evaluation tool for determining the ecological quality of
Andean highland rivers. The IMEERA index is sensitive not only to
the water physico-chemistry but also to the hydromorphological
conditions, and therefore it is a good indicator of general eco-
logical stream conditions. Given the importance for the aquatic
macroinvertebrate assemblages of the altitude in the studied range
(between 2500 and 5500 m a.s.l.), and of the presence or absence
of the vegetation cover in the basin and in the riparian zone, the
IMEERA index has two different formulations according to the
 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992 89

presence (Bosque, IMEERA-B) or the absence (Pramo, IMEERA-P) Appendix A ( Continued ).

of riparian and watershed wooded vegetation. This increases the Substrate denition Habitability Observations
positive discrimination of the index between reference and non- Particulate organic matter 9 Includes the surface layer of
reference sites in these two very different bioregions. sediment
Submerged roots 8 Sample only de root
Acknowledgements Stones and pebbles 7 Includes different types of
(25250 mm) sediment grain size
Blocks (>250 mm) includes 6 Includes the sediment and
We thank the FUCARA Project (AECID-D/011294/07) and Veron- the pebbles and rock fauna associated with block
ica Ordnez that provided the database used for the validation matrix (25250 mm)
process of the IMEERA index. Moreover, we thank Nria Snchez, Gravel (225 mm). 5 Includes different types of
sediment grain size
Ral Acosta, Manuel Anda, Carolina Arroyo, Fernanda Gonzles,
Emerging spermatophytes 4 Includes the surface layer of
Karla Jimnez and Mauricio Herrera for assisting in the laboratory (helophytes) sediment
and the eld. To Clorinda Vergara of the Museo de Entomologa of Fine sediment (<0.1 mm) 3 Sediment surface layer (<3 cm)
the Universidad Nacional Agraria La Molina and to Andrea Encal- with ne organic matter
ada of the Laboratorio de Ecologa Acutica of the Universidad San Sands and silts (<2 mm) 2 Sediment surface layer (<3 cm)
Algae 1 Includes support mineral
Francisco de Quito by providing laboratory facilities. This work was
elements
nanced by Ministerio de Educacin y Ciencia de Espana (AECID: Hard smooth surfaces 0 Scraped urface
CGL2006-04333). Two anonymous reviewers helped to enhance natural and articial
the manuscript.
Appendix B
Appendix A
Descriptive statistics of the environmental variables in each
Denition and sampling order of the aquatic substrates (Nnez basin used to determine the pressure gradient that affects high
and Prat, 2009). The substrates are in order from higher habitability Andean streams. QBR1: degree of cover of riparian vegetation in
to lower habitability; some observations are indicated to taking streamside zones. QBR2: cover structure of the riparian forest.
account in the sampled moment. QBR3: cover quality of the riparian vegetation. QBR4: degree of
Substrate denition Habitability Observations naturalness of the stream channel. QBR: quality index of ripar-
Bryophytes 11 Liverworts, mosses and ian vegetation. IHF1: rapids embeddedness. IHF2: frequency of
hornworts on blocks or stones rapids. IHF3: substrate composition. IHF4: velocity/depth relation-
Submerged spermatophytes 10 Includes the plant and surface ship. IHF5: percentage of shade. IHF6: heterogeneity elements. IHF
(hydrophytes) aquatic layer of sediment
7: aquatic vegetation coverage.
plants
 90
Variables ECUADOR PERU

MIRA (n = 16) AGUARICO (n = 14) GUAYAS (n = 15) PASTAZA (n = 16) SANTA (n = 16) MOSNA (n = 16) COLCA (n = 15) URUBAMBA (n = 15)
Average (min max) Average (min max) Average (min max) Average (min max) Average (min max) Average (min max) Average (min max) Average (min max)

Oxygen 76.74 79.31 81.55 79.29 74.88 77.21 78.22 82.45

(%) (71.6 81.5) (77 82.6) (68.7 87) (69.3 86.6) (66.2 81.5) (57.8 85.1) (0.24 116.4) (70.7 116.9)
Temperature 11.37 10.62 12.19 10.83 11.70 11.23 14.52 16.26
( c) (7.7 17.3) (8 12.6) (8.6 16.2) (6.1 16.6) (6.6 18.10) (7.4 15) (2 20.8) (10.1 22.9)
pH 8.40 7.80 8.06 7.90 7.13 7.51 6.93 7.69
(7.35 9.5) (6.54 8.72) (7.3 8.5) (6.9 8.5) (3.2 8.43) (4.5 8.3) (5 9) (6 9)
Ammonia 0.20 0.00 0.07 0.19 0.07 0.31 0.34 0.42
(mg/l) (0 1.42) (0 0) (0 0.23) (01.07) (0 23) (0 1.4) (0 3.76) (0 1.34)
Phosphates 0.94 0.17 0.51 0.32 0.01 0.02 0.21 0.41
(mg/l) (0.01 2.31) (00.58) (0 3.7) (0. 2.4) (0 0.04) (0 0.09) (0 0.8) (0 4.06)
Nitrites 0.01 0.01 0.01 0.00 0.01 0.00 0.01 0.02
(mg/l) (0 0.15) (0 0.1) (0 0.03) (0 0.03) (0 0.02) (0 0.01) (0 0.03) (0 0.23)
Nitrates 0.24 0.10 0.22 0.22 0.18 0.19 0.19 0.51
(mg/l) (0.1 0.6) (0 0.2) (0 0.8) (0 0.7) (0 0.4) (0 0.6) (0.1 0.7) (0 3.3)

C. Villamarn et al. / Ecological Indicators 29 (2013) 7992

Copper 0.07 0.07 0.05 0.06 0.04 0.07 0.10 1.48
(mg/l) (0 0.23) (0 0.13) (0 0.4) (00.34) (0 0.15) (0 0.14) (00.9) (0.04 4.7)
Silver 0.00 0.00 0.00 0.04 0.03 0.08 0.00 0.00
(mg/l) (0 0.01) (0 0) (00) (0 0.28) (0 0.11) (0 0.52) (0 0.02) (0 0)
Lead 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.00
(mg/l) (0 0.03) (0 0.3) (0 0.01) (0 0.03) (0 0.01) (0 0.02) (0 0) (0 0.03)
Zinc 0.07 0.11 0.18 0.20 0.12 0.06 0.06 0.03
(mg/l) (0 0.15) (0.03 0.2) (0.06 0.4) (0.01 0.9) (0 0.3) (0 0.14) (0 0.21) (0 0.09)
Iron 0.44 0.32 0.30 0.48 0.26 0.29 0.07 0.04
(mg/l) (0.03 1.47) (0.14 0.8) (0.01 1.02) (0.11 2.14) (0 1.05) (0.03 1.2) (0.01 0.23) (0 0.11)
QBR 1 0.11 0.13 0.10 0.11 0.11 0.18 0.21 0.15
(0 0.27) (0 0.25) (0 0.33) (0 0.33) (0 0.33) (0 0.33) (0 0.33) (0 0.25)
QBR 2 0.07 0.14 0.09 0.04 0.10 0.12 0.04 0.14
(0 0.25) (0 0.25) (0 0.25) (0 0.25) (0 0.25) (0 0.25) (0 0.2) (0 0.25)
QBR 3 0.16 0.23 0.09 0.12 0.18 0.18 0.27 0.17
(0 0.33) (0.05 0.25) (0 0.33) (0 0.33) (0 0.33) (0 0.33) (0.1 0.33) (0 0.25)
QBR 4 0.19 0.23 0.21 0.17 0.26 0.26 0.29 0.21
(0.0.33) (0.15 0.25) (0 0.33) (0 0.33) (0.15 0.33) (0.1 0.33) (0.2 0.3) (0 0.25)
QBR 0.53 0.73 0.49 0.44 0.65 0.73 0.81 0.67
(0 1) (0.3 1) (0.15 1) (0.05 1) (0.25 1) (0.45 1) (0.5 1) (0.25 0.95)
IHF 1 5.94 5.36 5.67 4.94 5.94 4.06 7.00 6.00
(0 10) (0 10) (0 10) (4 5) (0 10) (0 10) (5 10) (0 10)
IHF 2 9.63 9.86 9.60 9.63 9.75 10.00 8.80 9.60
(6 10) (8 10) (6 10) (6 10) (8 10) (10 10) (4 10) (8 10)
IHF 3 13.31 14.64 15.33 16.50 12.69 11.56 11.73 11.80
(5 17) (11 17) (12 20) (11 20) (10 14) (11 14) (7 14) (5 15)
IHF 4 8.75 10.00 9.47 9.63 8.25 8.88 7.87 8.13
(6 10) (10 10) (6 10) (8 10) (6 10) (6 10) (4 10) (6 10)
IHF 5 6.00 6.71 4.80 4.13 5.69 4.94 3.27 5.80
(3 10) (3 10) (3 10) (3 10) (3 10) (3 10) (3 5) (3 10)
IHF 6 5.75 8.43 6.13 3.50 6.50 5.69 2.13 3.87
(2 10) (4 10) (2 10) (2 8) (2 8) (4 11) (0 6) (0 8)
IHF 7 11.88 6.79 6.33 9.38 10.00 5.63 12.00 6.67
(0 20) (0 20) (0 15) (0 20) (0 25 (0 15) (5 20) (0 20)
IHF 61.25 61.79 57.33 57.69 58.81 50.75 52.80 51.87
(47 82) (48 87) (35 80) (43 73) (39 85) (38 67) (33 67) (35 73)
 C. Villamarn et al. / Ecological Indicators 29 (2013) 7992 91

Appendix C Appendix C (Continued)

Category Metric name Expected
Metrics used to build the multi-metric index and the expected response
response to the stressor gradient. The expected response was Tolerant/intolerant Andean biotic Decrease
determined considering information reported in specialized bib- index relationship
liography (Holzenthal, 1988; Merrit and Cummins, 1996; Roldn, Diversity indexes Simpson index Decrease
Taxonomic evenness Decrease
1996; Barbour et al., 1999; Domnguez and Fernndez, 2009).
Pielou Index Decrease
Margalef index Decrease
ShannonWiener index (log e) Decrease
Category Metric name Expected ShannonWiener index (log 2) Decrease
response ShannonWiener index (log 10) Decrease

Taxonomic Amphipoda taxa Decrease

richness
Gasteropoda taxa Decrease
Coleoptera taxa Decrease References
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