Hindawi Publishing Corporation

International Journal of Ecology

Volume 2014, Article ID 253134, 11 pages
http://dx.doi.org/10.1155/2014/253134

Research Article
Macroinvertebrate Richness Importance in Coastal Tropical
Streams of Esmeraldas (Ecuador) and Its Use and Implications
in Environmental Management Procedures

Carlos Martínez-Sanz,1 Sara María Puente-García,2

Eduardo Rodolfo Rebolledo,1 and Pedro Jiménez-Prado1
1
Faculty of Environmental Science, Pontifical University Catholic of Ecuador in Esmeraldas (PUCESE),
C/ Espejo y Santa Cruz S/N, 080150 Esmeraldas, Ecuador
2
Area of Ecology, Faculty of Biology and Environmental Science, University of León, Campus de Vegazana, S/N, 24071 León, Spain

Correspondence should be addressed to Carlos Martı́nez-Sanz; [email protected]

Received 18 July 2013; Revised 5 December 2013; Accepted 8 December 2013; Published 8 January 2014

Academic Editor: Ram C. Sihag

Copyright © 2014 Carlos Martı́nez-Sanz et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.

This study was aimed at determining the performance of some indices and community attributes frequently used to assess river
quality and test the role of macroinvertebrate taxa richness as element of bioindication in several coastal tropical streams of western
Esmeraldas (Ecuador). In addition, a macroinvertebrate taxon list of this region was provided for the first time. Thirteen sampled
points distributed across nine streams were selected for this study and nineteen parameters and attributes of bioindication were
tested. The differences between nonimpact and impact places were evaluated mainly using one-way analysis of variance. Jackknife 2
and Clench were used to estimate the regional richness and the quality of the inventory, respectively. Seventy taxa (principally genus
and family) of the main groups of macroinvertebrates were collected. Measured richness and family richness were the best metric
followed by Biological Monitoring Working Party/Colombia (BMWP/Col), Odonata richness, Shannon-Weiner, and EPT richness
(Ephemeroptera + Plecoptera + Trichoptera) indices. Only a slight right trend (Ephemeroptera, Trichoptera, and Chironomidae
attributes) or incorrect performances (Average Score Per Taxon (ASPT) and % EPT) were showed by frequently used metrics.
Finally, several recommendations were made about taxonomic level used, the ranks of quality of taxa richness, and the effort-results
relationship in the field of bioindication.

1. Introduction activity [3]. The causes and effects of pollution in tropical

rivers have been studied by several researchers, mainly with
Global change, population growth, and industrial devel- respect to particulate and suspended matter, the chemical
opment are currently exerting great impacts on natural dynamics in waters connected with organic matter content,
ecosystems, especially on aquatic systems [1]. Agricultural nutrient loading, and pH [4]. In Latin America, such rivers
practices, livestock and domestic discharges, the felling of pass through a strong water quality degradation gradient due
trees, exotic species introductions, and direct erosion have to increasing exploitation of the resources and the excessive
caused increase in the organic matter and suspended solids water pollution [5], especially in Ecuador where only 5% of
in water, resulting in strong alterations in the ecological the wastewater in the region is subjected to some type of
functioning of aquatic systems [2]. Coastal river basins are treatment. This is surprising since the water law establishes
among the most dynamic aquatic ecosystems on earth, with the prohibition of sewage discharges in rivers and lakes (in
enormous spatial and temporal complexity, but they are often Title II of the Conservation and Water Pollution Chapter
influenced by continental run-off waters which are rich in II Article 22). The province of Esmeraldas (Ecuador) is not
nutrients derived from urban, agricultural, and industrial exempted from these impacts. In recent decades, its rivers
2 International Journal of Ecology

have been severely altered by numerous human activities,

such as oil and fuel spills, sewage and industrial waste
disposals, introduction of alien species, and illegal extractive
activities [6]. In addition, there is no consistent wastewater
treatment system in the region. 1
2
It is, therefore, necessary to use tools that can reveal the 3
4
5
7 6
overall effect of human impact on the aquatic ecosystem [7]. 9 8
Benthic macroinvertebrates have been considered as excel- 11 10
12
lent indicators of water quality. Their study is a key to the work Esmeraldas
of bioindication and evaluation of the aquatic ecosystem [8] 50 km
13
and they constitute the most suitable group of organisms for
evaluating river water quality for organic contamination [9].
There are several studies that have used macroinvertebrate
communities to assess the effect of organic waste on the Ecuador
Ecuado
coastal streams of South American countries. Most of them
have been carried out in Colombia [10], Chile [9], Argentina Figure 1: Area of study and sample points. 1: Rı́o Verde (RV), 2:
[11], Uruguay [12], Peru [13], Brazil [14], and Bolivia [15] Estero Camarones (Ca), 3: Estero Tachina I (T-I), 4: Estero Tachina
but still few in Ecuador [5, 16] and none on its tropical II (T-II), 5: Estero Tachina III (T-III), 6: Estero Tachina IV (T-IV),
coastal streams. There are two large groups of techniques 7: Estero Tabiazo (Tbz), 8: Estero Chipa (Ch), 9: Estero Plátano Bajo
used to assess the biological quality using macroinvertebrates: (EPb), 10: Estero Plátano Alto (EPa), 11: Estero Quinge (Q), 12: San
community attributes and biological indices [17]. The use of Francisco (SF), and 13: Estero Mompiche (M).
simple metrics based on several community attributes, such
as taxa richness or number of taxa of some selected groups of
organisms, is a widely adopted technique in South America relating to the community structure, such as taxa richness,
(e.g., [13, 18]), but its performance must still be tested in these should also have good performance.
regions due to the latitudinal and longitudinal patterns of
taxa [19] and their wide distribution range [20]. On the other 2. Materials and Methods
hand, among all the biological indices developed to measure
the river quality, the most commonly used are those based 2.1. Study Area. Thirteen sampling points distributed across
on the Biological Monitoring Working Party (BMWP) [21]. nine streams were selected for this study (Figure 1). All of
The BMWP has been adopted in many countries such as them are located in the province of Esmeraldas, Ecuador
Spain (IBMWP [22]) or Australia (SIGNAL [23]). In South (South America). The area is located in the dry tropical forest
America also, there are several examples of its application life zone [29] on the west pacific coast, where shallow and
in biomonitoring [24], for example, in Patagonian Andes short streams with variable seasonal flow are predominant
region (IAP and BMPS [25]), Argentina [26], Colombia [30]. Table 1 shows some characteristics of these streams and
(BMWP/Col [10]), Brazil [27], and Andean region of Peru, the presence or absence of human impact.
and Ecuador [16]. However, in Ecuador for its coastal tropical
rivers, neither these indices have been adopted nor any study 2.2. Macroinvertebrate Sampling. Sampling at all the points
has been made on its performance. Despite this, these are was done once in October 2012 to coincide it with the dry
widely used by environmental technician and auditors in season, the recommended period to carry out bioindication
several studies, even though these versions were developed studies in this region [31]. Benthic macroinvertebrate sam-
for Europe [28]. ples were collected with a pond net (FBA standard, mesh
The aim of this study was to test the performance of some size 500 𝜇m) following a multihabitat time-limited sampling
of the most commonly used macroinvertebrate indices and [32]. Each point, proportionally distributed among the main
community attributes to assess the water quality of coastal habitats in the river, was sampled during three minutes’ time
tropical streams of western Ecuador. In addition, for the first [33], although in all cases the predominant substrate was of
time, a macroinvertebrate taxon list of these systems will be gravel, stones, and rock (hard substrate). Macroinvertebrates
provided for the above-mentioned fluvial systems and region. were separated and counted under a binocular microscope
The main purpose of this paper is to establish more adequate (10x) and identified to genus (60%) and family (40%) levels.
techniques and recommendations using macroinvertebrate The principal guides and books used were by Fernández and
to devise a suitable management strategy for the aquatic Domı́nguez [34] and Holzenthal et al. [35].
resources (when the Ecuadorian legislation is applied). At the
same time, there is also an interest in directly verifying the 2.3. Metric Selection. We compared the performance
role of biodiversity as an environmental assessment measure. of 19 parameters frequently used to assess river quality
The majority of these evaluation techniques are based on the (Table 2). We calculated the total abundance and
sensitivity and tolerance of macroinvertebrates to pollution. richness of the macroinvertebrate community as well
But we think and predict that in Ecuador, one of the areas as the percentage of abundance and richness of the
with the greatest biodiversity in the world, other attributes most relevant taxa used for bioindication [17]. Diversity
International Journal of Ecology 3

Table 1: Some characteristics of the streams included in the study.

Temp. Human
Study area∗ UTM∗∗ Altitude (m) pH Depth (cm) Width (m) Substrate type
(∘ C) impact∗∗∗
RV 674195/103203 25 25 7.3 90 6 Stony and sandy IMP
Ca 659722/107374 80 25.3 7 40 5 Stony IMP
T-I 657039/103944 75 27 6.8 32 6.5 Stony IMP
T-II 657299/103546 81 26.5 7 30 6 Stony IMP
T-III 659162/099949 164 28 6.9 31 5 Stony Non-IMP
T-IV 659730/099523 195 28.2 7.2 30 4 Stony Non-IMP
Tbz 644956/087091 40 27 7.1 90 9 Stony Non-IMP
Ch 605058/082185 90 26 7 32 4.3 Stony Non-IMP
EPb 601471/083773 30 26 7.3 27 5.2 Stony IMP
EPa 602116/082477 49 25 7.2 31 4.1 Stony Non-IMP
Q 602108/079216 28 25 6.7 40 3.7 Stony and sandy Non-IMP
SF 609060/077145 45 25.8 7 42 7.9 Stony Non-IMP
M 609754/055039 25 24.7 6.8 28 4.4 Stony IMP
∗
Rı́o Verde (RV), Estero Camarones (Ca), Estero Tachina I (T-I), Estero Tachina II (T-II), Estero Tachina III (T-III), Estero Tachina IV (T-IV), Estero Tabiazo
(Tbz), Estero Chipa (Ch), Estero Plátano Bajo (EPb), Estero Plátano Alto (EPa), Estero Quinge (Q), San Francisco (SF), and Estero Mompiche (M). ∗∗ Universal
Transverse Mercator Geographic Coordinate System. ∗∗∗ IMP: human impact present; Non-IMP: human impact not present.

Table 2: Values of the metrics measured in each stream.

Attribute (RV) (Ca) (T-I) (T-II) (T-III) (T-IV) (Tbz) (Ch) (EPb) (EPa) (Q) (SF) (M)
Measured richness 19 14 20 16 28 32 30 25 17 32 28 32 23
Family richness 15 13 16 13 22 24 22 19 15 26 21 22 20
Total abundance 156 196 640 156 263 385 445 142 108 597 220 791 269
Shannon-Wiener 4 2 3 3 4 4 4 4 3 4 4 3 4
BMWP/Col 104 84 115 78 159 179 153 134 91 183 130 145 141
ASPT 5 6 6 5 6 6 5 5 5 6 5 5 6
EPT richness 13 8 9 11 9 11 10 7 10 9 4 5 10
EPT (%) 7 4 9 8 9 11 13 11 5 10 9 10 10
Richness of Ephemeroptera 6 3 6 7 6 5 9 6 3 5 8 8 6
Richness of Trichoptera 1 1 3 1 2 5 4 4 2 5 1 2 4
Richness of Plecoptera 0 0 0 0 1 1 0 1 0 0 0 0 0
Richness of Odonata 2 3 1 1 2 4 3 3 3 4 4 3 2
Richness of Coleoptera 1 1 3 1 4 4 1 3 1 3 2 2 2
Percentage of Ephemeroptera 25 4 68 51 29 25 34 32 9 14 60 60 53
Percentage of Trichoptera 4 1 10 1 2 8 7 18 5 14 1 7 11
Percentage of Chironomidae 20 1 13 4 34 25 36 15 11 12 5 4 5
Percentage of Odonata 2 3 1 2 2 8 2 13 5 5 4 1 9
Percentage of Coleoptera 6 26 2 9 15 19 6 14 44 9 5 6 10
Percentage of Plecoptera 0 0 0 0 0 1 0 2 0 0 0 0 0
∗
% R-Jack 2 20 15 22 17 30 34 32 27 18 34 30 34 25
∗
% R-Jack 2 is the percentage of richness measured in relation to the regional richness estimation (Jack 2 = 93 taxa).
Abbreviations for study areas are as in Table 1.

was estimated using the Shannon-Wiener index. In types of impact, and their degree. We chose river points
addition, we calculated BMWP/Col [10], Average distant from large populations and the effect of industrial
Score Per Taxon (ASPT) [22], and EPT (richness activity, considering only the impact of little urban-domestic
and percentage of Ephemeroptera + Plecoptera + activities and livestock-agricultural at small scale, all of them
Trichoptera) indices, also widely used in South America to without wastewater treatment system [6]. Assigning a level of
assess the rivers quality. On the other hand, a cornerstone impact in these rivers basin is almost impossible; therefore,
was to assign the locations with and without impacts, the we established two realistic and more practical situations:
4 International Journal of Ecology

Table 3: Macroinvertebrate taxa and total number of individuals collected in the study area.

Class/order Family Genus Number

Cl. Gastropoda F. Thiaridae 420
F. Hydrobiidae 29
F. Neritidae 53
F. Planorbidae 4
Cl. Bivalvia F. Sphaeriidae 5
F. Corbiculidae 19
O. Decapoda F. Palaemonidae Macrobrachium 85
F. Atyidae Caridina 2
O. Ephemeroptera F. Leptophlebiidae Farrodes 630
Hagenulopsis 80
Traverella 2
Thraulodes 11
Atopophlebia 5
F. Leptohyphidae Leptohyphes 101
Tricorythodes 608
Traverhyphes 141
F. Caenidae Caenis 6
F. Baetidae Callibaetis 4
Guajirolus 34
Camalobaetidus 10
Harpagobaetis 62
Fallceon 86
O. Plecoptera F. Perlidae Anacroneuria 8
O. Odonata F. Protoneuridae 3
F. Platystictidae Palaemnema 12
F. Megapodagrionidae 1
F. Calopterygidae 3
F. Coenagrionidae Argia 73
F. Gomphidae Epigomphus 4
F. Libellulidae Perithemis 41
Brachymesia 1
Otros n.i. 16
O. Heteroptera F. Naucoridae 45
F. Corixidae 9
F. Gerridae Trepobates 71
Brachymetra 7
Gerris 3
F. Veliidae Velia 77
Microvelia 5
Rhagovelia 34
F. Hebridae 6
O. Megaloptera F. Corydalidae 2
O. Lepidoptera F. Pyralidae 15
O. Coleoptera F. Psephenidae 53
F. Elmidae 323
F. Hydrophilidae 8
F. Ptilodactilidae 7
F. Dryopidae 37
International Journal of Ecology 5

Table 3: Continued.
Class/order Family Genus Number
O. Trichoptera F. Calamoceratidae Phylloicus 5
F. Philopotamidae Chimarra 13
F. Hydropsichidae Smicridea 188
Leptonema 7
F. Polycentropodidae Polycentropus 9
F. Glossosomatidae Protoptila 31
F. Hydroptilidae Metrichia 3
Hydroptila 74
F. Leptoceridae 12
O. Diptera F. Chironomidae Tanypodinae 264
Orthocladiinae 179
Chironominae 194
F. Ceratopogonidae 13
F. Limoniidae Hexatomini 47
Eriopterini 35
F. Empididae 9
F. Sciomycidae 1
F. Simulidae 1
F. Stratiomyidae 12
F. Psychodidae 3
F. Dixidae 3
F. Culicidae 1

without impact (Non-IMP) (without any influence of human significant Pearson and Spearman’s correlation (𝑃 = 0.05) to
impact) and with impact (IMP) (with some degree of very test the degree of relationship between variables.
slight human impact, e.g., discharge of isolated farms and
presence of sparse cattle or people frequently doing little
domestic cleaning in the littoral waters).
3. Results
3.1. Macroinvertebrate Community. We collected 70 taxa
from the 13 sampled points, finding high total abundance
2.4. Richness Estimation. In addition to observed richness (4365 organisms). Table 3 includes a list of the taxa collected
of macroinvertebrate, measures of estimated richness were in the study area; it is the first report on the aquatic benthic
calculated using nonparametric methods [36, 37]. In the invertebrates in this region.
present study, Jack 2 [38] was used to estimate the regional
richness of a number of samples (13 rivers point) to obtain
real percentages of the fauna collected in each of the streams 3.2. Response of the Metrics. Figure 2 shows the differences
(Table 2). It was calculated over 100 randomized iterations in the responses of the studied metrics between impact
of the species accumulation using EstimateS ver. 8 [39]. (IMP) and nonimpact (Non-IMP) river points. Only the taxa
In addition, we used the asymptotic accumulation function and index significantly differing from these two situations
of Clench to obtain information about the quality of our are represented. In addition, attributes classically used and
inventory [38]. relevant for the aims of this study have also been included
in order to keep useful information. The values of all
indices and attributes in each sampled point are presented
2.5. Data Analysis. The responses of the several metrics and in Table 2. Measured richness and family richness were the
indices to assess the streams quality were graphically explored best metrics to discriminate between impact and nonimpact
by means of box plots, showing mean value, standard error, places showing strong significant differences (𝑃 = 0.000023
and standard deviation of the metrics within each river and 𝑃 = 0.00028, resp.). BMWP/Col and S-W indices also
category (IMP and Non-IMP). One-way analysis of variance showed significant differences, although less powerful than
(ANOVA) was applied to detect significant differences (𝑃 < the previous (𝑃 = 0.0012 and 0.025, resp.).
0.01). The assumptions of normality and variance homogene-
ity were tested using the Kolmogorov-Smirnov and Levene’s 3.3. Richness Estimation. The nonparametric estimator Jack
tests, respectively. The statistical processing was performed 2 predicted a high value of regional richness for the study
with the STATISTICA 6.0 package. In addition, we used area (93 taxa) (Figure 3). We assume that this value could be
6 International Journal of Ecology

36 28
32 P = 0.00028
24
28 P = 0.000023
Measured richness

20

Family richness
24
20 16
16 12
12
8
8
4
4
0 0
Non-IMP IMP Non-IMP IMP

7
220
200 6
P = 0.0012
180 P = 0.017
5
160

S Odonata
BMWP/col

4
140
120 3
100
2
80
60 1

40 0
Non-IMP IMP Non-IMP IMP

6 14

P = 0.025 P = 0.009
5 12
Shannon-Wiener

4 10
EPT richness

3 8

2 6

1 4

0 2
Non-IMP IMP Non-IMP IMP

120

100 Mean + SD

80 Mean + SE
60
EPT (%)

40 Mean

20
Mean − SE
0
Mean − SD
−20

−40
Non-IMP IMP
(a)

Figure 2: Continued.
International Journal of Ecology 7

1000
7
800

6
600

Total abundance
ASPT

400
5

200
4
0

3 −200
Non-IMP IMP Non-IMP IMP

10
14

12 8
S Ephemeroptera

10 6

S Trichoptera
8
4
6
2
4
0
2

0 −2
Non-IMP IMP Non-IMP IMP

100 22

80 18

60 14
Ephemeroptera (%)

Trichoptera (%)

40 10

20 6

0 2

−20 −2

−40 −6
Non-IMP IMP Non-IMP IMP

50

40 Mean + SD

Mean + SE
Chironomidae (%)

30

20 Mean

10 Mean − SE

0 Mean − SD

−10
Non-IMP IMP
(b)

Figure 2: Response of several analyzed metrics to human impact on the studied streams. S: richness; %: percentage of abundance.
8 International Journal of Ecology

100 is, in South America [16], North America [44], Africa [45],
93 and Europe [46]. Why does richness perform adequately
80 here? Ecuador has the highest biotic diversity per unit area
among the South American countries [47]. In particular,
70
western Ecuador harbors an exceptionally rich biota and
60
consequently is listed by Conservation International as one
Richness

of 25 global biodiversity hotspots [48]; this is made evident

40 by the high number of taxa found in this study (70 taxa in
only 53 minutes of sampling). The greatest biotic richness is
20
frequently found in small and medium sized streams, as the
ones in our study, where environmental variability, mainly
in temperature, might be large, consequently creating a high
0 number of niches [49]. Not intense human disturbances
0 2 4 6 8 10 12 14 could affect more hardly the quality and integrity of several
Points of rivers functional niches than in other lotic system types. Moreover,
Jack 2
in temperate regions where most studies that reflect the
Observed richness uncertain performance of richness in bioindication have been
carried out (see [50]), it is possible that a slight disturbance
Figure 3: Observed and estimated regional richness in the study only lowers abundance but not necessarily richness [51]. Cau-
area. The nonparametric estimation was obtained by the nonpara- tious analysis will be needed after, since tropical streams differ
metric estimator Jackknife 2 (Jack 2).
from their temperate counterparts in many characteristics,
including evolutionary history, precipitation patterns, and
water temperature, indicating that theories developed mainly
used as a reference to calculate the percentage of real fauna for the temperate region may not apply to tropical regions
collected in each river (Table 2), due to the fact that the [52]. Regardless of the possible causes and conjectures for
distance between sampling points is not very high (Figure 1) this subject and according to the results of this study, we
and the orographic is very smooth. Only the nonimpact recommend taxa richness as the principal tool considered to
places presented values higher than 25%. On the other hand, reflect human impact, even in front of the classical indices
the parametric estimator Clench estimated a value of regional used for this purpose. Furthermore, the same substratum
richness slightly larger than the observed richness (84 taxa) type of the rivers included in this study (Table 2) minimized
and we tested the inventory quality from its parameters: a the effects of this variable on richness, despite the fact that
(30.3427), b (0.3625), and determination coefficient (0.998). it used to be commonly found in other studies as important.
Only 83% of the total taxa were collected according to Clench Also we suggest it to be used as baseline for the management
estimations and 53 sampling points would be required to and conservation of these types of lotic systems. In addition,
collect 95% of the total taxa. this is the first report of performance of BMWP/Col test in
the area, appearing together with S-W and EPT richness as
adequate options for bioindication.
4. Discussion
On the other hand, metrics frequently used on bioindi-
The results showed the importance of taxa richness, the cation studies, here only showed a slight right trend
principal and simplest structural property characterizing the (Ephemeroptera, Trichoptera, and Chironomidae attributes)
macroinvertebrate community [40], to reflect the effects of or incorrect performance (ASPT and % EPT). Both mayflies
human impact on coastal tropical streams. Measured richness and caddisflies are sensitive to environmental stress [17].
and family richness were the best metrics to discriminate However, their use in bioindication should be carried out
between impact and nonimpact places and, in the analysis of considering the geographical patterns of taxa distribution and
each of the macroinvertebrate orders, only EPT and Odonata their adaptation to environmental conditions. Several orders
richness proved to be suitable. Moreover, this study highlights and families of macroinvertebrates in South America show
the right performance of adoption of the classic index BMWP different altitudinal and latitudinal distribution patterns.
to Colombia (BMWP/Col [10]) and Shannon-Weiner indices. For example, the diversity of families and genera of order
The good performance of these two biological indices is in Plecoptera in southern areas of the continent increases in
accordance with our expectations and other studies [24, 41], most Equatorial areas, and even within Equatorial areas
as well as EPT richness that decreases with the drop of water there are specific altitudinal variations in the same taxa
quality [42] and Odonata richness, showing the same nega- [19]. The latitudinal gradient in diversity is one of the most
tive response [43]. Nevertheless, it may come surprising that pervasive patterns characterizing life on earth. Unfortunately,
richness had better results than these classic metrics, due to our understanding of how taxonomic richness of stream
occasional poor sensitivity and high variability of the simplest invertebrates related to latitude is poor [53], affecting undesir-
metrics showing disturbances of low intensity or frequency ably the correct use of these metrics to assess the quality status
[20]. In spite of this, taxa number has been successfully used of streams in this region. In addition, the tolerance to pertur-
in bioindication throughout the world for a long time, that bations of taxa adapted to different environmental conditions
International Journal of Ecology 9

can be variable [17, 54] and using order or even family infor- [57] and Chapman [7] classify water quality as good where
mation can be incorrect, thus adversely affecting the results BMWP and ASPT exceed 100 and 4.3, respectively. Shannon-
on the ecological quality. There are some taxa which are Wiener values lower than 1.5 are considered as low diversity,
widely distributed (e.g., Anacroneuria, Baetodes, Thraulodes, between 1.6 and 3.0 as medium diversity, and higher than 3.1
Leptohyphes, and Hydroptila) with different adaptation types as high diversity [40]. In this study we propose a richness
according to the environmental inhabitation. Consequently, measure percentage value to indicate human alterations in
assigning average value of tolerance for them could lead these streams. Only the nonimpact places present values
to erroneous result of quality. Therefore, we suggest that, over 25%; therefore, we recommend that the sampled points
although they showed suitable performance here (but not showing taxa richness under 25% of true regional richness
significant), the use of Trichoptera and Ephemeroptera taxa are considered as altered by anthropogenic impact on future
as bioindication parameters in this region must be taken evaluations. This regional richness, provided that we can
only as complement and reinforcement to the previously assume that all streams could have all taxa, will be obtained
discussed techniques. More extensive studies of latitudinal with Jack 2 nonparametric estimator and at least with four
and adaptation partners of these taxa in South America would samples of three minutes each, the minimum to achieve the
be necessary to get to the bottom of their real performance on observed regional richness (Figure 3). This is only a first
stream bioindication. Regarding Chironomidae, it is known proposal to correctly use this simple metric regarding ranks
that they are frequently more abundant in locations affected and limits of quality. Furthermore, according to Clench,
by organic effluents, although only half of chironomids taxa we collected 83% of the existing taxa carrying out only
follow this pattern [45]. We believe this might be the case samplings of three minutes in each place. We think that it is
in the present study. However, our taxonomic identification an acceptable value on bioindication studies; besides, 40 more
level for chironomids does not allow identifying which samples of the 13 listed in this study would be necessary to
species are being affected by water quality, showing only one catch up 95% of the overall samples (only 120 extra minutes
trend. Chironomidae does not seem to be a good indicator to collect 12% more).
of water quality, unless it includes the exact percentage of This study seeks to make the baseline of use of taxa
sensitive taxa. Finally, a high ASPT is considered indicative richness as bioindicators and presents the first taxon list of
of a clean site containing large numbers of high scoring this region. The limited sample numbers that we were able to
taxa [21]. However, other authors question the reliability get, due to social conflicts and other risks of the study area, do
of ASPT [55] due to the fact that this index displays the not allow reaching conclusions that are widely extrapolated to
average tolerance of all taxonomic groups represented within other areas; consequently, simple speculations of the possible
the study site but does not take into consideration their causes can be made. Nonetheless, we believe that these results
relative numbers. Moreover, in fluctuating streams where are clear enough and statistically significant to recommend
some orders as Plecoptera are less abundant, the use of these which attributes, from those largely used, and how they must
metrics cannot be suitable [11]. In this study, neither the use of be utilized as quality indicators for these streams. Through
ASPT nor the % EPT can be proposed, because they showed this study a great path is opened to research and establish
the contrary trend of performance in terms of bioindication. the baseline to develop a multimetric index that includes
More thorough research about these indices in this region to metrics suitable for this region (principally taxa richness, EPT
assess their suitable use must be carried out in the future. richness, S-W, and BMWP/Col or an own adaptation of this
Finally, to properly recommend the use of taxa richness to study area) and the design of a sampling protocol including
as principal parameter of bioindication, we must mention the most robust richness estimator, both nonparametric (Jack
three fundamental aspects. The taxonomic level used, the 2) and parametric (Clench), to establish sampling times and
ranks of quality, and the effort-results relationship. It has value ranks for the several used attributes.
been widely discussed what the best taxonomic level used
for bioindication studies is [56]. While it is true that the best Conflict of Interests
level used would be species, taxonomic studies of some taxa
make practically unviable work in many countries due to high The authors declare that there is no conflict of interests
economic cost required in training the specialist taxonomists, regarding the publication of this paper.
especially in Diptera (and particularly Chironomidae) [13].
An appropriate balance between quality outcomes and time
is adjusted using the family as taxonomic level. By doing Acknowledgment
so, the advantages of macroinvertebrates as bioindicators This research was funded by the CID (Research and Develop-
are maintained at this level and thus it is recommended ment Center) (PUCESE).
in many of protocols and studies also [11]. In some cases,
including the present research, different taxonomic levels
are used, for example, genus in Trichoptera, Plecoptera, and References
Ephemeroptera and family in Diptera [20]. In this study [1] W. Thuiller, “Biodiversity: climate change and the ecologist,”
more than 50% of taxa were identified up to genus, which Nature, vol. 448, no. 7153, pp. 550–552, 2007.
has been taken as a feasible and reliable surrogate of species [2] L. Kaufman, “Catastrophic change in species-rich freshwater
richness [40]. On the other hand, the most used indices on ecosystems: the lessons of Lake Victoria,” BioScience, vol. 42, pp.
bioindication have quality ranges for their values. Mason 846–858, 1992.
10 International Journal of Ecology

[3] C. M. Pringle, F. N. Scatena, P. Paaby-Hansen, and M. [19] S. Tomanova, P. A. Tedesco, M. Campero, P. A. Van Damme, N.
Nunez Ferrera, “River conservation in Latin America and Moya, and T. Oberdorff, “Longitudinal and altitudinal changes
the Caribbean,” in Global Perspectives on River Conservation: of macroinvertebrate functional feeding groups in neotropical
Science, Policy and Practice, P. J. Boon, B. Davies, and G. E. Petts, streams: a test of the River Continuum Concept,” Fundamental
Eds., pp. 41–77, John Wiley and Sons, Durham, NC, USA, 2000. and Applied Limnology, vol. 170, no. 3, pp. 233–241, 2007.
[4] R. P. King and I. B. Ekeh, “Status and seasonality in the physico- [20] N. Prat, B. Rı́os, R. Acosta, and M. Rieradevall, “Los macroin-
chemical hydrology of a Nigerian headwater stream,” Acta vertebrados como indicadores de calidad de las aguas,” in
Hydrobiologica, vol. 32, no. 3-4, pp. 313–328, 1990. Macroinvertebrados bentónicos sudamericanos. Sistemática y
[5] D. Jacobsen, “The effect of organic pollution on the macroin- biologı́a, E. Domı́nguez and H. R. Fernández, Eds., p. 656,
vertebrate fauna of Ecuadorian highland streams,” Archiv für Fundación Miguel Lillo, Tucumán, Argentina, 2009.
Hydrobiologie, vol. 143, no. 2, pp. 179–195, 1998. [21] P. D. Armitage, D. Moss, J. F. Wright, and M. T. Furse, “The
[6] D. Ros, La contaminación del agua en el Ecuador una aprox- performance of a new biological water quality score system
imación económica, Instituto d Investigaciones Económicas, based on macroinvertebrates over a wide range of unpolluted
Quito, Ecuador, 1995. running-water sites,” Water Research, vol. 17, no. 3, pp. 333–347,
1983.
[7] D. Chapman, Water Quality Assessments. A Guide to Use
of Biota, Sediments and Water in Environmental monitoring, [22] J. Alba-Tercedor, P. Jáimez-Cuéllar, M. Álvarez et al., “Carac-
Chapman and Hall, 1996. terización del estado ecológico de rı́os mediterráneos ibéricos
mediante el ı́ndice IBMWP (antes BMWP’),” Limnetica, vol. 21,
[8] R. K. Johnson, “Spatiotemporal variability of temperate lake no. 3-4, pp. 175–182, 2004.
macroinvertebrate communities: detection of impact,” Ecolog-
[23] B. C. Chessman, “Rapid assessment of rivers using macroinver-
ical Applications, vol. 8, no. 1, pp. 61–70, 1998.
tebrates: a procedure based on habitat-specific sampling, family
[9] R. Figueroa, C. Valdovinos, E. Araya, and O. Parra, “Macroin- level identification and a biotic index,” Australian Journal of
vertebrados bentónicos como indicadores de calidad de agua Ecology, vol. 20, no. 1, pp. 122–129, 1995.
del sur de Chile,” Revista Chilena De Historia Natural, vol. 76,
[24] M. N. Strieder, L. H. Ronchil, C. Stenert, R. T. Scherer, and U.
pp. 275–285, 2003.
G. Nesiss, “Biological measures and water quality indices in a
[10] H. Zamora, “Adaptación del ı́ndice BMWP para la evaluación micro-watershed polluted with urban and tannery sewage in
de la calidad de las aguas epicontinentales en Colombia,” South Brazil,” Acta Biologica Leopoldensia, vol. 28, no. 1, pp. 17–
Unicauca-Ciencia, vol. 4, pp. 47–60, 1999. 24, 2006.
[11] E. Domı́nguez and H. R. Fernández, Calidad de los rı́os de la [25] L. Pizzolon and M. Miserendino, “The performance of two
Cuenca del Salı́ (Tucumán, Argentina) medida por un ı́ndice regional biotic indices for running water quality in Northern
biótico, Serie Conservación de la Naturaleza. No. 12, Fundación Patagonian Andes,” Acta Limnologica Brasiliensa, vol. 13, pp. 11–
Miguel Lillo, Tucumán, Argentina, 1998. 27, 2001.
[12] R. Arocena, “La comunidad bentónica como Indicadora de [26] H. R. Fernández, F. Romero, and E. Domı́nguez, “Intermoun-
zonas de degradación y recuperación en el Arroyo Toledo tain basins use in subtropical regions and their influences on
(Uruguay),” Revista de Biologı́a Tropical, vol. 43, pp. 643–655, benthic fauna,” River Research and Application, vol. 24, pp. 1–13,
1996. 2008.
[13] R. Acosta and N. Prat, “Chironomid assemblages in high [27] V. M. Junqueira and S. C. M. Campos, “Adaptation of the
altitude streams of the Andean region of Peru,” Fundamental BMWP method for water quality evaluation to Rio das Velhas
and Applied Limnology, vol. 177, no. 1, pp. 57–79, 2010. watershed (Minas Gerais, Brazil),” Acta Limnologica Brasilien-
[14] D. F. Baptista, D. F. Buss, M. Egler, A. Giovanelli, M. P. Silveira, sia, vol. 10, pp. 125–135, 1998.
and J. L. Nessimian, “A multimetric index based on benthic [28] J. Giacometti and F. Bersosa, “Macroinvertebrados acuáticos y
macroinvertebrates for evaluation of Atlantic Forest streams at su importancia como bioindicadores de calidad del agua en el
Rio de Janeiro State, Brazil,” Hydrobiologia, vol. 575, no. 1, pp. rı́o Alambı́,” Boletı́n Técnico 6, vol. 2, pp. 17–32.
83–94, 2007. [29] L. R. Holdridge, W. C. Gmlke, W. H. Hatheway, T. Liang, and
[15] O. Fossati, J.-G. Wasson, C. Héry, G. Salinas, and R. Marı́n, J. R. . Tosi, Forest Environments in Tropical Life Zones: A Pilot
“Impact of sediment releases on water chemistry and Study, Pcrgmon, Oxford, UK, 1971.
macroinvertebrate communities in clear water Andean [30] N. L. Poff and J. V. Ward, “Implications of streamflow variability
streams (Bolivia),” Archiv für Hydrobiologie, vol. 151, no. 1, pp. and predictability for lotic community structure: a regional
33–50, 2001. analysis of streamflow patterns,” Canadian Journal of Fisheries
[16] R. Acosta, B. Rı́os, M. Rieradevall, and N. Prat, “Propuesta de and Aquatic Sciences, vol. 46, no. 10, pp. 1805–1818, 1989.
un protocolo de evaluación de la calidad e Guardar ecológica de [31] S. Fenoglio, G. Badino, and F. Bona, “Benthic macroinvertebrate
rı́os andinos (CERA) y su aplicación a dos cuencas en Ecuador communities as indicators of river environment quality: an
y Perú,” Limnetica, vol. 28, no. 1, pp. 35–64, 2009. experience in Nicaragua,” Revista de Biologia Tropical, vol. 50,
[17] N. Bonada, N. Prat, V. H. Resh, and B. Statzner, “Developments no. 3-4, pp. 1125–1131, 2002.
in aquatic insect biomonitoring: a comparative analysis of [32] J. Biggs, P. Williams, M. Whitfield, G. Fox, and P. Nicolet,
recent approaches,” Annual Review of Entomology, vol. 51, pp. Biological Techniques of Still Water Quality Assessment: Phase 3.
495–523, 2006. Method Development, Environment Agency, Bristol, UK, 2000.
[18] P. J. Pave and M. Marchese, “Invertebrados bentónicos como [33] P. D. Armitage and I. Pardo, “Impact assessment of regulation
Indicadores de calidad del agua en rı́os urbanos (Paraná-Entre at the reach level using macroinvertebrate information from
Rı́os, Argentina),” Ecologycal Society of Australia, vol. 15, pp. mesohabitats,” Regulated Rivers, vol. 10, no. 2–4, pp. 147–158,
183–197, 2005. 1995.
International Journal of Ecology 11

[34] H. R. Fernández and E. Domı́nguez, Guı́a Para La Determi- pollution from Spen Beck, West Yorkshire,” Earth and Environ-
nación De Los Artrópodos Bentónicos Sudamericanos, Univer- ment, vol. 3, pp. 369–406, 2008.
sidad Nacional De Tucumán, Facultad De Ciencias Naturales e [51] R. G. Death, “The effect of patch disturbance on stream
Instituto, 2001. invertebrate community structure: the influence of disturbance
[35] R. W. Holzenthal, R. J. Blahnik, A. L. Prather, and K. M. Kjer, history,” Oecologia, vol. 108, no. 3, pp. 567–576, 1996.
“Order Trichoptera Kirby, 1813 (Insecta), Caddisflies,” Zootaxa, [52] J. K. Jackson and B. W. Sweeney, “Present status and future
no. 1668, pp. 639–698, 2007. directions of tropical stream research,” Journal of the North
[36] A. Foggo, S. D. Rundle, and D. T. Bilton, “The net result: American Benthological Society, vol. 14, no. 1, pp. 5–11, 1995.
evaluating species richness extrapolation techniques for littoral [53] B. A. Hawkins, “Ecology’s oldest pattern,” Trends Ecology and
pond invertebrates,” Freshwater Biology, vol. 48, no. 10, pp. 1756– Evolution, vol. 15, pp. 390–391, 2001.
1764, 2003. [54] C. R. Townsend and A. G. Hildrew, “Species traits in relation to
[37] A. S. Melo and C. G. Froehlich, “Evaluation of methods for a habitat templet for river systems,” Freshwater Biology, vol. 31,
estimating macroinvertebrate species richness using individual pp. 265–275, 1994.
stones in tropical streams,” Freshwater Biology, vol. 46, no. 6, pp. [55] P. E. Kirsch, “Benthic Macroinvertebrate Diversity and Biotic
711–721, 2001. Indices Analysis of Lakes Wrights, Springfield, Mc Grath, Kearney
[38] R. K. Colwell and J. A. Coddington, “Estimating terrestrial and Morris, and an Upgraded Analysis of Lakes Dollar, Russell,
biodiversity through extrapolation,” Philosophical transactions Stillwater, Papermill and Kinsac within the Halifax Regional
of the Royal Society of London B, vol. 345, no. 1311, pp. 101–118, Municipality (HRM), Nova Scotia, Canada,” Project E-3, Soil
1994. and Water Conservation Society of Metro Halifax, 1999.
[39] R. K. Colwell, Estimates: StatiStical Estimation of Species Richnes [56] A. S. Melo, “Effects of taxonomic and numeric resolution on the
and Shared Species From Samples, Version 7. USer’s Guide and ability to detect ecological patterns at a local scale using stream
Application, University of Connecticut, Storrs, Conn, USA, macroinvertebrates,” Archiv für Hydrobiologie, vol. 164, no. 3, pp.
2004, http://purl.oclc.org/. 309–323, 2005.
[40] A. E. Magurran, ,Measuring Biological Diversity, Blackwell [57] C. F. Mason, Biology of Freshwater Pollution, Prentice Hall,
Publishing, Oxford, UK, 2004. London, UK, 4th edition, 2002.
[41] M. P. Silveira, D. F. Baptista, D. F. Buss, J. L. Nessimain, and M.
Egler, “Application of biological measures for stream integrity
assessment in south-east Brazil,” Environmental Monitoring and
Assessment, vol. 101, no. 1–3, pp. 117–128, 2005.
[42] C. I. Weber, “Biological field and laboratory methods for
measuring the quality of surface waters and effluents,” Tech.
Rep. EPA-670/4-73-001, Environmental Protection Agency,
Cincinnati, Ohio, USA, 1973.
[43] T. E. Clark and M. J. Samways, “Dragonflies (Odonata) as
indicators of biotope quality in the Kruger National Park, South
Africa,” Journal of Applied Ecology, vol. 33, no. 5, pp. 1001–1012,
1996.
[44] D. R. Barton, “The use of Percent Model Affinity to assess the
effects of agriculture on benthic invertebrate communities in
headwater streams of southern Ontario, Canada,” Freshwater
Biology, vol. 36, no. 2, pp. 397–410, 1996.
[45] F. O. Arimoro, R. B. Ikomi, and E. Efemuna, “Macroinvertebrate
community patterns and diversity in relation to water quality
status of River Ase, Niger Delta, Nigeria,” Journal of Fisheries
and Aquatic Science, vol. 2, no. 5, pp. 337–344, 2007.
[46] J. M. Hellawell, Biological Surveillance of Rivers: A Biological
Monitoring Handbook, Natural Environmental Research Coun-
cil, Water Research Centre, 1978.
[47] R. W. Sites, M. R. Willig, and M. J. Linit, “Macroecology of
aquatic insects: a quantitative analysis of taxonomic richness
and composition in the andes mountains of Northern Ecuador,”
Biotropica, vol. 35, no. 2, pp. 226–239, 2003.
[48] R. A. Mittermeier, N. Myers, and C. G. Mittermeier, Hotspots:
Earth’s Biologically richest and most Endangered terrestrial ecore-
gions, University of Chicago Press, Chicago, Ill, USA, 2000.
[49] R. L. Vannote, G. W. Minshall, K. W. Cummins, J. R. Sedell,
and C. E. Cushing, “The river continuum concept,” Canadian
Journal of Fisheries and Aquatic Sciences, vol. 37, no. 1, pp. 130–
137, 1980.
[50] C. L. Wenn, “Do freshwater macroinvertebrates reflect water
quality improvements following the removal of point source
Journal of Journal of International Journal of

Waste Management Environmental and

Public Health
Ecology

The Scientific
Hindawi Publishing Corporation
World Journal
Hindawi Publishing Corporation Hindawi Publishing Corporation
Scientifica
Hindawi Publishing Corporation Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Journal of
Ecosystems

International Journal of

Hindawi Publishing Corporation

Oceanography
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Submit your manuscripts at

http://www.hindawi.com

International Journal of Journal of

Atmospheric Sciences
Hindawi Publishing Corporation
Marine Biology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Applied &
International Journal of Journal of International Journal of Environmental Journal of
Biodiversity Geological Research Forestry Research Soil Science Climatology
Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Volume 2014 Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com http://www.hindawi.com Volume 2014

Journal of Advances in

Geophysics
International Journal of
Journal of Computational Advances in Environmental
Earthquakes
Hindawi Publishing Corporation
Environmental Sciences
Hindawi Publishing Corporation Hindawi Publishing Corporation
Meteorology
Hindawi Publishing Corporation
Chemistry
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014