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Reduction of sampling effort assessing macroinvertebrate assemblages for biomonitoring of rivers


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Biomonitoring methods based on macroinvertebrate assemblages are widely developed in streams and rivers. However, the use of invertebrates has been criticized due to the long time and expense of processing samples. Therefore, we evaluated the effectiveness of reducing the sampling effort from 20 to 5 samples to assess the stream macroinvertebrate community. In six streams in the Basque Country (North of Spain) 20 kick nets were collected following a multihabitat stratified sampling design. The macroinvertebrates were identified to family level and a smoothed family accumulation curve fitting the Clench function to the data was calculated for each stream. Richness was lower in 5 than in 20 samples. However, in general, the percentage of richness estimated with the subsampling may be considered representative of the existing taxa richness. Therefore, the study of five samples may be adequate for biomonitoring Basque streams, greatly minimizing time, effort and costs. RÉSUMÉ
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Knowledge and Management of Aquatic Ecosystems (2015) 416, 08
ONEMA, 2015
DOI: 10.1051/kmae/2015004
Reduction of sampling effort assessing macroinvertebrate
assemblages for biomonitoring of rivers
B. Gartzia De Bikuña(1),E.López
(1), J. Arrate(1),
A. Martínez(1),(2),,A.Agirre
Received October 2, 2014
Revised January 13, 2015
Accepted January 28, 2015
effort reduction,
Biomonitoring methods based on macroinvertebrate assemblages are
widely developed in streams and rivers. However, the use of invertebrates
has been criticized due to the long time and expense of processing sam-
ples. Therefore, we evaluated the effectiveness of reducing the sampling
effort from 20 to 5 samples to assess the stream macroinvertebrate com-
munity. In six streams in the Basque Country (North of Spain) 20 kick
nets were collectedfollowing a multihabitat stratified sampling design.The
macroinvertebrates were identified to family level and a smoothed family
accumulation curve fitting the Clench function to the data was calculated
for each stream. Richness was lower in 5 than in 20 samples. However, in
general, the percentage of richness estimated with the subsampling may
be considered representative of the existing taxa richness. Therefore, the
study of five samples may be adequate for biomonitoring Basque streams,
greatly minimizing time, effort and costs.
Réduction de l’effort d’échantillonnage pour l’évaluation des assemblages de macroinver-
tébrés pour la biosurveillance des rivières
Mots-clés :
cours d’eau,
de l’effort,
Les méthodes de biosurveillance basées sur les assemblages de macroinverté-
brés sont largement développées dans les ruisseaux et rivières. Cependant, l’uti-
lisation d’invertébrés a été critiquée en raison du long temps de collecte et du
coût de traitement des échantillons. Par conséquent, nous avons évalué l’effica-
cité de la réduction de l’effort d’échantillonnage de 20 à 5 échantillons pour éva-
luer la communauté des macroinvertébrés d’une rivière. En six rivières du Pays
Basque (nord de l’Espagne) 20 filets à main Kicker ont été recueillis suivant un
plan d’échantillonnage stratifié multihabitat. Les macroinvertébrés ont été identi-
fiés au niveau de la famille et une courbe de cumul de famille lissée de la fonction
de Clench ajustée aux données a été calculée pour chaque rivière. La richesse
était plus faible dans 5 échantillons que dans 20. Cependant, en général, le pour-
centage de la richesse estimée avec le sous-échantillonnage peut être consi-
déré comme représentatif de la richesse des taxons existants. Par conséquent,
l’étude de cinq échantillonspeut être adéquate pour la biosurveillance des rivières
basques, minimisant considérablement les efforts de temps et les coûts.
(1) Anbiotek S.L. Axpe Industrialdea, Ribera de Axpe 11 B-201, 48950 Erandio, Spain
(2) Laboratory of Stream Ecology, Department of Plant Biology and Ecology, University of the Basque Country,
P.O. Box 644, 48080 Bilbao, Spain
(3) URA. Agencia Vasca del Agua. C/ Orio, 1-3, 01010 Vitoria-Gasteiz, Spain
Corresponding author:
Article published by EDP Sciences
B. Gartzia De Bikuña et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 08
Streams and rivers are among the most threatened habitats in the world (Malmqvist and
Rundle, 2002). Since they provide important ecosystem services (Thorp et al.,2010), it is
crucial to understand the consequences of human perturbations on these ecosystems to
preserve or restore their integrity (Meybeck, 2003). Therefore, assessment and biomonitor-
ing programs are carried out widely by public authorities. In river biomonitoring, the aquatic
macroinvertebrates are the most commonly studied group (Bonada et al.,2006) since they
are sensitive to multiple ecological alterations (Johnson and Ringler, 2014). In particular, taxa
richness has been widely used because it is a key measurement to assess the structure of bi-
ological assemblages (Gotelli and Cowell, 2001). However, the use of invertebrates has been
criticized due to the long time and expensive costs of sampling, sorting, counting and identi-
fying them (Ciborowski, 1991). Therefore, since the effectiveness of biomonitoring protocols
depends mainly on the time required and on the overall costs, techniques that optimize the
cost-benefit have been developed (Marini et al., 2013; Pinna et al.,2013,2014). Neverthe-
less, caution is needed since the technique and the way in which samples are collected and
processed may influence the description of the studied community (Boonsoong et al.,2009;
Di Sabatino et al.,2014). In fact, reducing effort and costs is not the only aim of subsampling
methods, but also of paramount concern is the need to gain information not substantially bi-
ased by the procedure and capable of answering research questions (Barbour and Gerritsen
In Spain, as in other states in Europe, the methodology focused on benthic macroinverte-
brates established by the Water Framework Directive, WFD (EU, 2000), for river biomonitor-
ing is multihabitat stratified sampling (Barbour et al.,1999;AQEM,2002). However, the large
number of kick samples required in each stream increases the time, effort and costs, making
the application of this approach in programs with a great number of monitored systems nearly
impossible. Therefore, the goal of this work is to test if a significant reduction in the sampling
effort from 20 to 5 samples, that would minimize time, effort and costs, allows for the collec-
tion of representative information about the richness of macroinvertebrate communities for
The study was conducted in six streams in the Basque Country (North of Spain) flowing into
the Atlantic Ocean. The study sites differ in the basin area, but not in the water physico-
chemical characteristics. The main land uses of the catchments are native vegetation, conifer
plantations and farming, percentages varying among sites (Table I). The climate in this re-
gion is oceanic, with cool winters (mean winter temperature around 9 C) and warm summers
(mean summer temperature around 21 C), and with a mean annual rainfall of 10001200 mm,
evenly distributed throughout the year.
Benthic macroinvertebrates were sampled in late spring 2012 in three of the six streams
(S1, S2, S3) and in late spring 2013 in the other three (S4, S5, S6). At each site, multihabitat,
stratified and semiquantitative sampling was carried out, collecting 20 kick nets (25 ×20.5 cm;
500 µm) within a 100-m-long reach (Barbour et al.,1999;AQEM,2002). With each kick an
estimated stream bottom area of 0.05 m2(semiquantitative) was sampled. The habitats that
represented 5% of the total surface were sampled (multihabitat). The number of samples
taken in each habitat depended on the percentage that each habitat represented of the total
study reach surface (stratified). The habitats considered included rocky substrates, cover
B. Gartzia De Bikuña et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 08
Tab le I
Location, water physicochemical characteristics and basin land-use percentages of the studied streams.
S1 S2 S3 S4 S5 S6
Watershed name Barbadun Arratia Altube Oria Altzolaratz Urumea
UTMX 488 696 518 568 504 944 561 781 564 110 587 359
UTMY 4 790 874 4 783 160 4 776 385 4 763 504 4 788 455 4 786 268
Basin (km2)47.9 137.7 192.9 59.8 21.9 156.7
Water temperature (C) 14.3 14.3 14.5 13.8 14.3 13.2
pH 7.8 7.9 8.1 8.0 7.9 8.1
Conductivity (µS·cm1)363.7 397.4 379.3 577.6 310.9 60.4
Total nitrogen (mg·L1)1.97 2.26 1.39 1.61 2.07 1.00
Total phosphorous (mg·L1)0.09 0.26 0.21 0.07 0.04 0.04
O2saturation (%) 86.7 91.1 92.9 94.3 93.1 111.9
Land use (%)
Native vegetation 36.9 24.1 50.8 46.2 55.8 77.0
Conifer plantations 20.9 57.5 31.9 29.6 10.6 18.4
Farming 40.2 17.4 16.1 23.4 33.3 4.6
Rocky 1.9 0.3 0.7 0.6 0 0
Urban 00.7 0.4 0.4 0.2 0
vegetation (aquatic bryophytes and algae), macrophytic vegetation (emerged, floating and
submerged macrophytes) and riparian vegetation (roots, vegetation over the channel and
vegetal detritus).
The macroinvertebrates were preserved in 4% formaldehyde for subsequent processing. In
the laboratory, each sample was divided into multiple subsamples. The fauna was studied in
a subsample, identifying the individuals to family level (Oligochaeta and Ostracoda to class)
following Tachet et al. (2002). The size of the analyzed subsample depended on the sample
size (following AQEM, 2002). The total number of individuals in each sample was estimated
by multiplying the number of each taxon by the inverse of the portion. From the portion of the
sample not analyzed, taxa previously not encountered were extracted avisu.
The cost of 20 and 5 samples’ collection and processing was calculated both in terms of time
and money, considering a price of 12 eper hour spent doing the field and laboratory work.
For each study site, a smoothed family accumulation curve was calculated using Esti-
mateS (100 randomizations; Colwell, 2000). This program computes sample-based rarefac-
tion curves for family richness estimation, presenting the mean number of random sample
re-orderings, and thus removing the possible effects due to the order by which the samples
have been listed. Using STATISTICA, we fitted a Clench function to the data of each study
site to assess the precision of our estimates of family richness. The equation of the Clench
function is Sn=an/(1 + bn), where Snis the observed family number for a given number of
samples, nis the number of samples, ais the new families’ increase rate in the first stages
and bis a parameter related to the curve form.
B. Gartzia De Bikuña et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 08
Tab le II
Values of the Clench function fitted to family accumulation curves for each stream and the representa-
tiveness of the estimated richness of the richness percentage collected with 20 and five kick samples.
Stream R2a b Final stage slope % taxa richness collected
20 kicks 5 kicks
S1 0.97 37.34 0.60 0.12 96.0 75.0
S2 0.98 15.88 0.35 0.24 91.5 64.0
S3 0.97 18.65 0.41 0.21 93.4 67.5
S4 0.98 24.15 0.75 0.09 96.5 79.0
S5 0.96 37.87 0.72 0.15 96.0 78.2
S6 0.99 42.41 0.99 0.01 97.0 83.3
Figure 1
Family accumulation curves for each stream. Black bars indicate the estimated family richness, taking
into account five samples.
The Clench function estimate of the number of families based on 20 samples represented
from 91.5% (S2) to 97.0% (S6) of the total estimated richness (Table II). In comparison, the
number of families estimated by collecting just five samples was lower (Figure 1), representing
from 64.0% in S2 to 83.3% in S6 of the total estimated richness (Table II).
From the practical viewpoint, the collection and processing of 5 samples is 3.3 times less
time-consuming and cheaper than for 20 samples (Table III).
Estimating lower taxa richness is common when attempting to minimize sampling efforts,
either when subsampling within the same technique or using simpler techniques. In this study,
reducing the sampling effort from 20 to 5 samples led to estimating lower taxa richness, but
the diminution was not significant. According to Moreno and Halffter (2000), the inventory of a
B. Gartzia De Bikuña et al.: Knowl. Manag. Aquat. Ecosyst. (2015) 416, 08
Table III
Cost in terms of time and money required to collect and identify macroinvertebrate assemblages with 5
and 20 samples.
Person number 5 samples 20 samples
Habitat identification (h) 20.33 1.00
Sample collection (h) 20.42 0.75
Sample processing (h) 12.00 8.00
Total t i m e ( h·person1)3.50 11.50
Total p r i ce (12 e·h1·person1)42 138
particular group is consideredrepresentativeof its existing species richness when the number
of sampled species reaches at least 70% of the estimated number of species present. In
this study, four of the six cases were over this threshold, and in the other two (S2 and S3)
the values were very close. Additionally, in these two streams, the percentages collected
from the estimated maximum family richness value with 20 samples were also lower than
those in the other four streams, the richness value not reaching the asymptote of the curve.
These lower values were attributed to the river bed substratum and not to differences in
water physicochemical properties, basin size or land uses. In fact, the river bed was covered
by boulders and bedrock in these two streams, which complicated the collection of samples
with the kick net.
Moreover, despite losing taxa richness, it has been shown that subsampling within the same
sampling technique allows obtaining a representative view of the structure of benthic macroin-
vertebrate communities and that the differences among systems remain, their application be-
ing acceptable in biomonitoring (Marini et al.,2013; Pinna et al.,2013,2014). In contrast, using
different techniques to minimize effort can lead to bias in the information on the structure of
biological communities (Di Sabatino et al.,2014).
In conclusion, the reduction of the sampling effort from 20 to 5 samples may provide a repre-
sentative view of the macroinvertebrate community composition in these streams. Therefore,
the collection of five samples may be sufficient for biomonitoring Basque streams, allowing
savings on time, human effort and costs. These savings, simplifying the spatial sampling ef-
fort, would provide greater temporal effort with a similar cost estimate. Thus, managers and
policy-makers could carry out more exhaustive monitoring in systems where steps to improve
the ecological status are being applied.
This study was supported by a contract undertaken with the Basque Water Agency (URA).
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Cite this article as: B. Gartzia De Bikuña, E. López, J.M. Leonardo, J. Arrate, A. Martínez, A. Agirre,
A. Manzanos, 2015. Reduction of sampling effort assessing macroinvertebrate assemblages for
biomonitoring of rivers. Knowl. Manag. Aquat. Ecosyst., 416, 08.
... For example, Carlisle et al. (2008) showed that the macroinvertebrate model was the most precise compared to the diatom and fish models. However, the use of macroinvertebrates has been criticized due to long-time requirements and expensive costs of sampling, sorting, counting, and identifying them (De Bikuna et al., 2015) and this is likely to affect the effectiveness of biomonitoring protocols using macroinvertebrate communities (Pinna et al., 2014). ...
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This review presents the state-of-the-art of benthic soft-bodied algae as biondicators of stream and river water quality, with emphasis on bioassessments set by the legislation (e.g., European Water Framework Directive, USA Clean Water Act) to promote the restoration and ensure ecological sustainability of water resources. The advantages and shortcomings of a variety of bioassessment field and laboratory methods for algae are discussed. The increasing use of soft-bodied algae in biotic indices to assess individual anthropogenic stressors, and in multimetric indices of biotic integrity to evaluate ecological condition in streams is summarized. Rapid microscopic and molecular approaches for inferring nutrient supply with heterocystous cyanobacteria and other sensitive algae are proposed. The need of better understanding of soft-bodied algae as bioindicators is discussed and suggestions are made for obtaining meaningful bioassessment information with cost-efficient efforts. © R. Stancheva and R.G. Sheath, published by EDP Sciences, 2016.
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Information on both structure and function is essential to evaluate the ecological integrity of stream ecosystems and their response to natural and anthropogenic disturbance. Leaf-bags have been widely employed to assess stream ecosystem processes and the degree of leaf mass consumption has been proposed as one of the most useful functional descriptor in aquatic environments. However, the breakdown rate of leaves has been compared with structural indicators of macroinvertebrate assemblages derived from leaf-bags or from benthic samples, without any direct comparison on the characteristics of com -munities sampled with the two methods. The main objective of the paper is to conduct a comparative analysis of the structure, functional organization and biological traits of macroinvertebrate assemblages from artificial leaf packs and from benthic samples of a third-order stream in the Central Apennines (Italy). Of the 43 macroinvertebrate taxa globally found in our survey, 9 showed low ability or scarce attitude to colonize leaf-bags, while 6 rare taxa were exclusively sampled in artificial leaf packs. Both assemblages were characterized by the dominance of Chironomidae, though they were more abundant in leaf-bags (71% of total individuals collected) than in benthic samples (44%). Conversely, the mayfly Baetis sp. comprised more than 17% of total individuals collected with Surber nets and only 5% of leaf-bag assemblages. We found that compared to benthic assemblages, leaf-bag communities were less diversified with a lower richness and a lower number of Ephemeroptera, Trichoptera and Plecoptera (EPT) taxa; significant differences also emerged in assemblage composition. Contrary to what expected, artificial leaf packs resulted not particularly attractive for shredder organisms and were mainly colonized by collectors. Also the biological trait profiles of the leaf-bag community were significantly different from those shared by resident benthic taxa. Our findings could have profound implications in the assessment of the structural and functional integrity of stream ecosystems and in studies on freshwater biodiversity and ecosystem functioning. In these studies, the two methods (leaf-bags and Surber nets) should be regarded as complementary and not alternative.
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Stream bioassessment studies usually use a single taxonomic group, most commonly fish or macroinvertebrates. However, differences in the life histories, habitat preferences, and physiological and behavioral traits of each assemblage may cause differences in their responses to environmental degradation. These factors can lead to discrepancies in overall assessments of ecological integrity. The Onondaga Lake Watershed (NY) has had a diverse history of pollution from multiple impacts, and the lake and several subsites are listed as USEPA Superfund sites. The response of fish and macroinvertebrate assemblages to environmental variables in the Onondaga Lake Watershed was assessed at 17 stream reaches in 2007, 2010, and 2011 using assemblage-specific metrics and indices of biotic integrity. Land use and substrate composition variables were significantly correlated (p < 0.05, r > |0.3|) with the first two macroinvertebrate PCA axes and were related to a downstream gradient of increased habitat degradation for the major tributaries. Water chemistry variables, canopy cover, and stream width were significantly correlated (p < 0.05, r > |0.3|) with the first two fish PCA axes. PCA axes for fish and macroinvertebrate assemblages were not significantly correlated, suggesting that the major environmental variables affecting fish and macroinvertebrate assemblages differed. Pearson correlations between the macroinvertebrate Biological Assessment Profile (BAP) and the fish Index of Biotic Integrity (IBI), and the macroinvertebrate Percent Model Affinity (PMA) and IBI were not significantly correlated. The macroinvertebrate metrics Percent Model Affinity (PMA) and BAP were positively and significantly correlated with Visual Habitat Assessment (VHA) scores, and the fish IBI was not significantly correlated with the VHA, further illustrating differences of fish and macroinvertebrates in their response to environmental variables. Results suggest that the use of multiple assemblages may be warranted for future assessments of stream quality and the development of effective monitoring programs in the Onondaga Lake Watershed.
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The effectiveness and accuracy of biomonitoring programs, based on benthic macroinvertebrates, is strictly related to the sampling design and effort, whereas the feasibility depends on the economic sustainability of sample collection and processing methodologies. In the last decade, how to improve the Rapid Bioassessment Protocols (RBPs) maintaining the accuracy of the results has been a topic recurrently debated among researchers. It is well known that the sample unit size (i.e., surface of the sampled area, SUS) and the sieve mesh size (SMS), selected to collect and to retain benthic macroinvertebrates from soft-bottom samples, may affect the evaluation of the aquatic ecosystem ecological status; however, studies analyzing the combined influence of SUS and SMS on assessment tools are lacking, in particular for transitional water ecosystems. Even if the Water Framework Directive (WFD) suggests rapid and cost-effectiveness sampling effort and procedures, the identification of optimal SUS and SMS is a basic step to improve the RBPs and to meet WFD suggestions. Therefore, this research analyses the effects of four soft-bottom sample unit sizes (0.0225 m2, 0.0450 m2, 0.0675 m2, 0.0900 m2), and three sieve mesh sizes (4 mm2, 1 mm2, 0.25 mm2) on the selection of benthic macroinvertebrates and, thus, on assessment tools, in a Mediterranean lagoon. A sampling survey was performed in September 2009 at a perturbed and an unperturbed study site in the Lesina lagoon (SE Italian coastline); three replicates were taken for each SUS and SMS using an Ekman–Birge grab (15 cm × 15 cm). The samples were sieved on a column of three sieves, with decreasing mesh size. Benthic macroinvertebrates were sorted, identified, measured, weighted and included in twelve datasets (4 SUS × 3 SMS). Sampling effort (SE) was calculated for each SUS and SMS combination as: SE = [SUS m2 × (1/SMS mm2)] × 100. Four simple community descriptors (numerical density, taxonomic richness, biomass density, individual body-size) and four ecological indicators (AMBI, BENTIX, BITS, M-AMBI) were compared for each combination of SUS and SMS in both study sites. Simple community descriptors and ecological indicators varied significantly between perturbed and unperturbed study site. The results showed that SMS had significant effects on simple community descriptors and ecological indicators, except for BITS index. Conversely, no significant differences were observed for different SUS analyzing simple community descriptors and ecological indicators, except for taxonomic richness and M-AMBI index. The response of the ecological indicators was only slightly affected by the SMS, whereas SUS choice did not influence the ecological status assessment. Anyway, using the larger SMS (4 mm2), all ecological indicators showed either the same ecological quality status as the 1 mm2 and 0.25 mm2 SMS or, in some cases, one class higher, except for the AMBI index.
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Assignment of values for natural ecological benefits and anthropocentric ecosystem services in riverine landscapes has been problematic, because a firm scientific basis linking these to the river's physical structure has been absent. We highlight some inherent problems in this process and suggest possible solutions on the basis of the hydrogeomorphic classification of rivers.We suggest this link can be useful in fair asset trading (mitigationand offsets), selection of sites for rehabilitation, cost-benefit decisions on incremental steps in restoring ecological functions, and general protection of rivers.
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1 - The accurate evaluation of benthic macroinvertebrate taxonomic diversity in transitional water ecosystems is strictly related to sampling effort and, usually, biomonitoring protocols define the sampling effort needed to the elaboration of a specific ecological indicator. The time-lag between the sampling event and the final assessment of ecological status, and to overall costs for sampling, personnel and sample treatment suggest a reduction of sampling effort. 2 - How to simplify methods and to reduce efforts without compromising the ecological validity of taxonomic diversity indicators is a topic recurrently debated in the procedures for sampling protocol implementation. Regarding this topic, the identification of optimal sample unit size (SUS) and sieve mesh size (SMS) is still lacking, mainly for benthic macroinvertebrates of Mediterranean transitional water ecosystems. 3 - The present study analyzes the effect of the increasing the sampling effort in terms of sample unit size (SUS; 0.0225 m2, 0.0450 m2, 0.0675 m2, 0.0900 m2) and sieve mesh size (SMS; 0.5 mm, 1 mm, 2 mm) on the estimation of taxonomic diversity in a Mediterranean lagoon. Benthic macroinvertebrates were collected in September 2009 at two locations, considering a perturbed and a relatively unperturbed study site of Lesina lagoon (South-East Italy). Samples were sieved on a column of three decreasing mesh sizes of sieves. Taxonomic richness (S), Shannon–Weaver index (H’), Simpson index (λ) and Taxonomic distinctness (TD) were calculated for each study site, SUS and SMS combination, and replicate. The difference between perturbed and relatively unperturbed site was tested according to the variation of sampling effort using three-way ANOVA tests. 4 - As expected, the accuracy of the results increased with increasing of SUS and SMS, the difference between perturbed and relatively unperturbed study site were always highlighted by each taxonomic diversity index, independently by used SUS and SMS. The variation of taxonomic diversity indicators seems to depend mainly by used sieve mesh size suggesting the reduction of sampling effort through the reduction of sample unit size. 5 - Finally, this contribution could be useful in harmonizing sampling methodologies for the costeffectiveness taxonomic diversity estimation and biomonitoring programs.