Ecological Profiles of Caddisfly Larvae in Mediterranean Streams

Environmental Pollution 132 (2004) 509–521 www.elsevier.com/locate/envpol

Ecological proﬁles of caddisﬂy larvae in Mediterranean streams: implications for bioassessment methods

N. Bonadaa,*, C. Zamora-Mun˜ ozb, M. Rieradevalla, N. Prata

aDepartment of Ecology, University of Barcelona, Diagonal 645, E-08028 Barcelona, Spain bDepartment of Animal Biology and Ecology, University of Granada, E-18071 Granada, Spain

‘‘Capsule’’: Ecological proﬁles of caddisﬂy larvae in Mediterranean streams using water quality variables.

Abstract

Caddisflies are a well represented group with high species diversity in Mediterranean climate rivers. Although they are widely used in water quality assessment, little is known of the ecological profiles of families or species. We present a simple score for ecological profiles which measures intolerance to water quality. The ecological profiles of caddisflies are diverse and the degree of tolerance at the family level is related to species diversity and the tolerance of individual species to water quality. Comparisons with the scores used in the biotic index IBMWP show general agreement between the degree of intolerance of a family and its score in the IBMWP, with few exceptions. Studies on tolerance are required to elucidate the autecology of taxa, and to develop biological indices, especially in areas with high species diversity. Ó 2004 Elsevier Ltd. All rights reserved.

Keywords: Trichoptera; Stream ecology; Tolerance; Water quality; Biological index

1. Introduction environmental gradient follows a unimodal distribution (Whittaker, 1967), have been developed to estimate taxa To predict and determine species distributions and optima and tolerances in relation to environmental abundances, and to assess disturbance in ecosystems, variables (e.g. ter Braak and Looman, 1986; ter Braak freshwater ecologists need to study the relationships and Van Dam, 1989). These methods have been between organisms and environmental variables. Species extensively used in Paleolimnology to infer past are considered tolerant when found in a wide range of environmental conditions (e.g. ter Braak and Van environmental conditions and intolerant when they are Dam, 1989; Birks et al., 1990; Bigler and Hall, 2002). restricted to a small window of ecological conditions Although multivariate models designed to assess water (e.g. see Cairns and Pratt, 1993). Organisms are often quality (e.g. RIVPACS, AusRivAS) involve the quan- considered tolerant or sensitive to pollution without tification of the ecological requirements of macro- detailed studies on their ability to thrive in polluted invertebrate communities (Wright, 1995; Smith et al., waters, and reports on the tolerance of individual species 1999), few studies, however, report the specific toler- to environmental variables are scarce (Verdonschot and ances of macroinvertebrate taxa (but see Verdonschot Higler, 1992; Lenat and Resh, 2001). and Higler, 1992). Several statistical procedures, based on the hypo- Ecological profiles for macroinvertebrate taxa are thesis that the abundance of organisms along an required to test the effectiveness of biological indices, to determine indicator species and to obtain autecological * Corresponding author. Fax: C34 93 4111438. information from environmental conditions (Moretti E-mail address: [email protected] (N. Bonada). and Mearelli, 1981). Indicator species have specific

0269-7491/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2004.05.006 510 N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 requirements for several variables (Johnson et al., 1993) human impact (Prat and Ward, 1994) which involves that can vary at a higher taxonomic resolution (Resh a variety of river reaches with distinct water quality that and Unzicker, 1975; Cranston, 1990) and so several can broaden the tolerance range of caddisflies. authors have suggested caution in the use of higher taxonomic levels, like families, in bioassessment methods (e.g. Moog and Chovarec, 2000). Nowadays, the 2. Materials and methods taxonomic level to be used in applied studies raises controversy because the ecological patterns of species 2.1. Sampling sites and procedure and families can differ (Furse et al., 1984; Marchant, 1990; Rutt et al., 1993; Zamora-Mun˜ oz and Alba- One hundred and forty sampling sites were surveyed Tercedor, 1996; Hewlett, 2000). along the Spanish Mediterranean coast seasonally in At the family, species and individual levels, Trichop- 1999 and in 2000 (Fig. 1). Sites were more or less equally tera has been regarded as an appropriate group to assess distributed among 10 river basins, and they included water quality using larvae (e.g. see Resh, 1992) or adults reference and non-reference sites. Selected sampling sites (Malicky, 1981; Usseglio-Polatera and Bournaud, 1989). account for almost all river types present along the At the family and species levels, caddisflies have been Spanish Mediterranean coast in terms of flow, river size, related to several environmental variables and display riparian characteristics, geology and water quality some specific trends in ecological requirements (e.g. (Bonada et al., 2002; Robles et al., 2002). Macro- Basaguren and Orive, 1990; Dohet, 2002; Dohet et al., invertebrate samples were collected in riffles and pools 2002) but their tolerance ranges need to be qualified to with a kick-net of 250 mm mesh size. They were various environmental or chemical variables. Caddisfly preserved in alcohol 70% and sorted in the laboratory. ecological profiles can be obtained from studies analyz- Caddisfly taxa were sorted and identified at the maximal ing deformities and anomalies caused by pollution (e.g. possible level, and the rank of abundances was recorded Petersen and Petersen, 1983; Vuori and Kukkonen, for each taxon: 1 for 1–3 individuals, 2 for 4–10, 3 for 2002) and asymmetries (Bonada and Williams, 2002), or 11–100 and 4 for more than 100 individuals. Given the else from toxicity tests (Greve et al., 1998), which may large amount of undescribed larvae in the Iberian allow us to infer optima and tolerances for a single Peninsula (Vieira-Lanero, 2000), we could not identify species and one or a few variables. On the other hand, all taxa to the species level with certainty. When studies performed using large sets of field data including possible, pupae and adults were collected in the field several species are also useful (e.g. Gordon and Wallace, to corroborate larval identifications. In some cases 1975; Moretti and Mearelli, 1981; Basaguren and Orive, mature larvae were reared in the laboratory in some 1990; Verdonschot and Higler, 1992; Stuijfzand et al., cases using a system developed by Vieira-Lanero (1996). 1999). However, most of these studies are usually A database was assembled with records of caddisfly taxa performed in small areas, with insufficient data, or identified at the family and genus or species level without taking into account the abundance of organ- collected from all sites in all sampling seasons. From isms, and thereby caution should be taken when this database, only taxa collected in at least 10 samples extrapolating these results to other geographical areas (sites ! seasons) were used to check for tolerances to or for other taxonomic levels. various environmental variables, whereas the most The ecological profiles of caddisflies were obtained infrequent taxa were removed (Beraeidae, Calamocer- from studies in streams along the Iberian Mediterranean atidae, Ecnomidae and Goeridae). In total, we used 13 coast. The caddisflies in this area are an ideal group to families and 41 taxa at the genus or species level that study ecological profiles from the perspective of water were collected (Appendix). quality variables owing to four factors. First, the high The environmental variables considered in this study species diversity and endemicity of caddisflies in the were oxygen (mg/l), conductivity (mS/cm) (both directly Iberian Peninsula with a total of 390 species present (see measured in the field), ammonium (mg/l), P-phosphates updated checklist of Trichoptera from Iberian Peninsula (mg/l), suspended solids (mg/l), sulphates (mg/l) and in http://www.fauna-iberica.mncn.csic.es/), are the result chloride (mg/l) (which were analyzed in the laboratory). of the interactions between ecological and historical factors (Gonza´lez et al., 1987). Second, the harsh natural 2.2. Data analysis abiotic conditions in these Mediterranean ecosystems (see Gasith and Resh, 1999), which would influence the To calculate the tolerance levels for all caddisflies (13 high diversification of the ecological profiles of trichop- families and 41 genera/species) using the physico- terans. Third, the lack of information about autecology chemical data obtained at each sampling site and during studies of caddisflies in Mediterranean areas, except each season, a weighted average (WA) approach was those provided in taxonomic papers. Finally, the performed with the CALIBRATE vs 0.7 program significant river alteration in the Mediterranean area by (Juggins, 1997). The WA approach assumes that each N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 511

Pyrenees

FRANCE

Besòs Basin SPAIN Llobregat Basin

Mediterranean Sea Ranges

Iberian

Sampling site Mijares Basin

Mountain ranges Turia Basin Júcar Basin

Segura Basin

Sierra Nevada Almanzora Basin Aguas Basin

Adra Basin Guadalfeo Basin

Fig. 1. River basins and sampling sites in Mediterranean Spanish areas where caddisflies were collected. taxon has a Gaussian response to an environmental values the axis is drawn from 1 to 0. This is because variable, where the species optimum (the mode) and the chemical variables are positively correlated with pollu- tolerance (the standard deviation from the optima) can tion whereas higher concentration of oxygen are be calculated. This method has been widely applied in negatively correlated with pollution, and therefore low Paleolimnology to infer environmental conditions using values of chemicals and high values of concentration of optima and tolerances of several indicator organisms oxygen indicate intolerance to pollution. When joining (e.g. Birks et al., 1990; Bigler and Hall, 2002; Walker the plotted points of the tolerance ranges for all axes, et al., 1997). a shaded figure indicates the degree of tolerance for each Ecological profiles for each genus/species and for taxon, whereas the non-shaded area displays the degree family level were deduced from the tolerances for six of intolerance to pollution. Thereby, the caddisflies that measured environmental variables (oxygen, suspended were extremely sensitive to all environmental variables solids, P-phosphates, ammonium, sulphates and chlo- have a narrow shade and large empty areas, in contrast ride). Conductivity was not plotted owing to its high to very tolerant taxa (Fig. 2). In some polyhedral figures, correlation with chloride (r-Pearson = 0.87, P ! 0.01) because of the large value of the lower ( for chemical and sulphates concentrations (r-Pearson = 0.83, variables) or the small value of the upper ( for oxygen P ! 0.01). Profiles were drawn as a polyhedral figure concentration) tolerance limit, there is a non-shaded consisting of six axes, each representing one environ- area at the top of one or more axes, indicating that in mental variable, which were joined at their extremes our sampled area this species should be infrequent in (Fig. 2). On each axis the tolerance range was drawn values below ( for chemical variables) or above ( for after adjusting all the upper and lower values to between oxygen concentration) these conditions. The degree of 0 and 1 to allow comparison between axes. This the intolerance score (DIS) was determined using the adjustment was performed by dividing each environ- following formula: mental variable value by the maximum value recorded "# X5 of the tolerance range of that variable, for families and DIS ¼ð10=6Þ ð1 maxiÞCminj ; taxa at genus or species level, separately. For chemical i¼1 variables (i.e. suspended solids, P-phosphates, ammonium, sulphates and chloride) the axis is drawn from where i = chemical variables and j = oxygen concen- 0 outside (low values of the variable, intolerance to the tration. chemical) towards 1 in the center (high values of the This score ranges between 0 and 10 and indicates the variable, tolerance to the chemical), whereas for oxygen sensitivity of each species to pollution (high scores 512 N. Bonada et al. / Environmental Pollution 132 (2004) 509–521

P-PH

O M SP U

H NI A O TE M

M S A S TE S A O H LID P S L SU

0P-P P-PH

H M O OXYGEN CHLORIDE M O U SP U SP I NI N H H O A O A M TE M TE P-PH Step 1 M M S S S A S E TE 0 A T O 0 A M S A S H SP O H U O P I L P L ID L LI U N S U D H S S 0 S A O Step 3a TE M

M S A S TE A SO H L LP ID U Sensitive taxa OXYGEN CHLORIDE OXYGEN 1 0 CHLORIDE S S Step 2a

0 P-P 0 P

-PH

H M O M U O SPH U SPH I OXYGEN CHLORIDE NI N 1 O 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 O M 1 A A M 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 TE M TE M

S S S S 0 A E T TE 0 S A 0 0 A A Step 2b O H S H L P O P ID L L L S U ID U 0 S Step 3b S 0 S

Tolerant taxa OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE

Fig. 2. Scheme of how the polyhedral figures to interpret ecological profiles were obtained. Step 1: Six axes joined at the center, each one corresponding to one environmental variable, were drawn: chloride (mg/l), sulphates (mg/l), ammonium (mg/l), P-phosphates (mg/l), suspended solids (mg/l) and oxygen (mg/l). Each axis was divided into 10 units to locate the standardized limits of the tolerance range, from 0 outside towards 1 in the center for chemical variables, and from 1 to 0 for oxygen concentration. Step 2: The upper and lower tolerance limits were drawn with a black point, and the area between them was shaded. Step 3: The axes were removed, obtaining only the shaded figure. Note that the oxygen axis is drawn in a different direction from the others. Two examples of ecological profiles of a sensitive (narrow shaded area; 2a and 3a) and a tolerant (wide shaded area; 2b and 3b) species are presented. denote intolerant species). DIS can be applied to a larger and chloride (up to 176 mg/l) concentrations and or smaller set of environmental variables taking into relatively low ammonium (up to 0.23 mg/l), but did account the variables positively and negatively correlat- not tolerate high concentrations of other chemical ed with pollution separately: variables. In contrast, larvae of Limnephilidae, Psycho- "#myiidae and Rhyacophilidae were tolerant to all Xni Xnj variables, but more sensitive to sulphates or chloride. DIS ¼ð10=nÞ ð1 max ÞC min ; i j Larvae of Philopotamidae tolerated high concentrations i¼1 j¼1 of suspended solids (up to 96 mg/l) and sulphates (up to 791 mg/l) but were sensitive to eutrophication and where n = number of variables used (ni C nj), i = variables positively correlated with pollution and j = var- toxicity. The most tolerant families were Glossosoma- iables negatively correlated with pollution. tidae, Hydropsychidae and Hydroptilidae, with DIS ranging from 2.69 to 3.56 (Table 1). Glossosomatidae were present at almost all conditions, except at very high 3. Results P-phosphates concentrations (up to 0.20 mg/l), whereas Hydropsychidae did not tolerate sulphates above At the family level, Brachycentridae, Lepidostomati- 435 mg/l or suspended solids above 70 mg/l. Hydro- dae, Odontoceridae and Sericostomatidae were the most ptilidae showed a similar profile to Hydropsychidae. sensitive to pollution, with DIS ranging from 8.45 to The DIS for families is positively related with scores of 7.45 (Fig. 3, Table 1). The larvae of Brachycentridae the Iberian biotic index IBMWP, with some exceptions. were intolerant to all the variables examined, although Glossosomatidae and Leptoceridae were more tolerant they were present at a wide range of oxygen concen- to environmental variables than expected from their trations ( from 7.4 to 12.6 mg/l). Larvae of the IBMWP score (8 and 10, respectively). At the same time, Lepidostomatidae, Sericostomatidae and Odontoceridae Limnephilidae were slightly more sensitive than Lep- tolerated slight increases in concentrations of ammoni- toceridae, but had a lower IBMWP score. um, P-phosphates and suspended solids. The larvae of Figs. 4–6 show the ecological profiles for caddisfly Leptoceridae tolerated high sulphates (up to 638 mg/l) genera and species. Hydropsychidae show variable N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 513

0 P- 0 P- 0 P-

PHOSPHA PHOSPHA PHOSPHA

M M

ONIU ONIUM

TES TES TES MMONIU MM

0 AMM 0 A 0 A 0 SOL 0 SOL 0 SOL

IDS IDS IDS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Brachycentridae Glossosomatidae Hydropsychidae

0 P- 0 P- 0 P-

PHOSPHA PHOSPHA PHOSPHA

IUM IUM

ONIU

TES TES TES MMON MMON MM

0 A 0 A 0 A 0 SOL 0 SOL 0 SOL

IDS IDS IDS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Hydroptilidae Lepidostomatidae Leptoceridae

0 P- 0 P- 0 P-PHOSPHA

PHOSPHA PHOSPHA

M M

IUM

ONIU ONIU

M TES TES TES MMON

0 AMM 0 A 0 AM 0 SOL 0 SOL 0 SOL

IDS IDS IDS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Limnephilidae Odontoceridae Philopotamidae

0 P- 0 P-PHOSPHA 0 P-PHOSPHA

PHOSPHA

M M M

ONIU ONIU ONIU

TES TES TES MM

0 AMM 0 AMM 0 A 0 SOL 0 SOL 0 SOL

IDS IDS IDS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Polycentropodidae Psychomyiidae Rhyacophilidae

0 P-

PHOSPHA

ONIU

TES

0 AMM 0 SOL

IDS 0 SULPHATES

OXYGEN 1 0 CHLORIDE Sericostomatidae

Fig. 3. Ecological profiles for caddisfly families found in Mediterranean Spanish rivers. Chloride (mg/l), sulphates (mg/l), ammonium (mg/l), P- phosphates (mg/l), suspended solids (mg/l) and oxygen (mg/l) are plotted. Narrow ecological profiles indicate very sensitive families, whereas tolerant taxa present a wide ecological profile. Families are ordered alphabetically. tolerance (Fig. 4). Hydropsyche exocellata was the most concentrations of suspended solids (up to 28 mg/l) and tolerant species for all the parameters except sulphates sulphates (up to 272 mg/l) but at a wide range of (up to 302 mg/l). Profiles for Hydropsyche gr. pellucidula P-phosphates concentrations (up to 0.6 mg/l). The and Hydropsyche sp1 were similar: sensitivity to remaining hydropsychids were highly sensitive to envir- P-phosphates and ammonium, and tolerance to sus- onmental variables, e.g. Hydropsyche dinarica, which pended solids. In contrast, Hydropsyche infernalis was restricted to low concentration of sulphates (up to tolerated sulphates (up to 733 mg/l) but only low 45 mg/l), chloride (up to 18 mg/l) and suspended solids concentrations of suspended solids (until 27 mg/l). (up to 3.7 mg/l) but tolerated high concentrations of P- Cheumatopsyche lepida was mostly found at low phosphates (up to 0.6 mg/l) (Fig. 4), in contrast to 514 N. Bonada et al. / Environmental Pollution 132 (2004) 509–521

Table 1 was the most tolerant species, since it survived at Sensitivity to pollution (DIS value) for caddisﬂy families and genus/ relatively high concentrations of suspended solids (up to species collected from Spanish Mediterranean basins (Appendix). DIS 68 mg/l), P-phosphates (up to 0.38 mg/l) and chloride scores run from sensitive taxa at the top to tolerant taxa at the bottom. The score assigned to each family in IBMWP index is also presented (up to 83 mg/l). On the other hand, Halesus tessellatus, for comparison Potamophylax spp., Anomalopterygella chauviniana, Family DIS IBMWP Taxon DIS Allogamus sp. and Chaetopteryx sp. were restricted to score clean water. The two species of Potamophylax showed Brachycentridae 8.45 10 Halesus tessellatus 8.78 a similar pattern, but Potamophylax cingulatus was Lepidostomatidae 7.91 10 Philopotamus montanus 8.66 slightly more tolerant to ammonium (up to 0.6 mg/l). Odontoceridae 7.58 10 Micrasema moestum 8.58 Stenophylax sp. tolerated increased levels of ammonium Sericostomatidae 7.45 10 Potamophylax latipennis 8.41 and sulphates (up to 0.58 and 327 mg/l, respectively). Limnephilidae 6.53 7 Anomalopterygella 8.39 Rhyacophilids were sensitive to water quality (Fig. 5), chauviniana Leptoceridae 6.32 10 Allogamus sp. 8.37 except for Rhyacophila munda, which survived at higher Psychomyiidae 6.18 8 Chaetopteryx sp. 8.37 sulphates (up to 415 mg/l), chloride (up to 142 mg/l) and Rhyacophilidae 6.09 7 Micrasema longulum 8.26 concentrations of suspended solids (up to 132 mg/l). Polycentropodidae 5.06 8 Ithytrichia sp. 8.25 Rhyacophila dorsalis tolerated slightly higher P-phos- Philopotamidae 4.88 8 Rhyacophila nevada 8.24 phates (up to 0.63 mg/l) and ammonium (up to 0.54 mg/ Hydroptilidae 3.56 6 Potamophylax cingulatus 8.24 Hydropsychidae 3.22 5 Hydropsyche dinarica 8.10 l) concentrations. Except Mystacides azurea, which was Glossosomatidae 2.69 8 Lasiocephala basalis 8.02 sensitive to all chemical variables, the Leptoceridae were Odontocerum albicorne 7.91 tolerant to high sulphates and chloride concentrations Rhyacophila meridionalis 7.87 (especially Setodes argentipunctellus, with 1149 and Mystacides azurea 7.79 323 mg/l, respectively) (Fig. 6). A similar pattern was Stenophylax sp. 7.74 Limnephilus guadarramicus 7.64 observed in Polycentropodidae, with Polycentropus Hydropsyche brevis 7.62 kingi more tolerant to sulphates (up to 441 mg/l), Hydropsyche instabilis 7.60 chloride (up to 121 mg/l) and suspended solids (up to Halesus radiatus 7.50 124 mg/l) than other genera and species of the same Hydropsyche siltalai 7.45 family (Fig. 6). Finally, Micrasema was a sensitive Athripsodes sp. 7.39 Sericostoma sp. 7.35 genus, with Micrasema longulum being more tolerant to Plectrocnemia sp. 7.30 P-phosphates than Micrasema moestum (up to 0.59 and Rhyacophila gr. tristis 7.02 0.06 mg/l, respectively) (Fig. 6). Polycentropus ﬂavomaculatus 6.92 Overall, H. tessellatus was the most sensitive taxon, Cheumatopsyche lepida 6.86 with a DIS of 8.78, whereas H. exocellata was the most Tinodes sp. 6.82 Mesophylax aspersus 6.66 tolerant species (Table 1). Except for some species, Rhyacophila dorsalis 6.66 hydropsychids had a DIS of 3.22, consistent with the Hydropsyche sp1 6.14 patterns observed at the family level. Philopotamidae Polycentropus kingi 6.01 had DIS of 4.88, although one of the two species Hydropsyche infernalis 5.97 analyzed (P. montanus) was sensitive to pollution Hydropsyche gr. pellucidula 5.77 Setodes argentipunctellus 5.60 (DIS = 8.66), while the other, C. marginata, was not. Rhyacophila munda 5.54 Hydroptilidae followed a similar pattern, since Ithytri- Chimarra marginata 5.28 chia sp. and Hydroptila sp. showed DIS of 8.25 and 4.98, Hydroptila sp. 4.98 respectively. Species of Rhyacophilidae also showed Agapetus sp. 3.55 a range of DIS values between 8.24 and 5.54 (Table 1). Hydropsyche exocellata 2.59

4. Discussion Hydropsyche brevis. In Philopotamidae and Hydro- ptilidae, Chimarra marginata and Hydroptila sp. larvae The wide range of ecological profiles shown by survived in a wide range of values of environmental caddisfly families and species in the Mediterranean area variables, while Philopotamus montanus and Ithytrichia confirm the hypothesis that Trichoptera are an ideal sp. were more restricted to clean waters (Fig. 4). group to assess water quality (e.g. Resh, 1992; Dohet, Agapetus sp. was tolerant to high levels of suspended 2002) and provide a useful tool to protect aquatic solids (up to 91 mg/l), ammonium (up to 0.91 mg/l), ecosystems, especially the most sensitive species (de sulphates (1133 mg/l) and chloride (up to 362 mg/l), but Moor, 1999). In general, our results agree with the did not tolerate P-phosphates above 0.23 mg/l (Fig. 4). scarce available data reported to date. Regarding the Like Hydropsychidae, Limnephilidae also displayed ecological profiles of several species of Rhyacophila, variable ecological profiles (Fig. 5). Mesophylax aspersus Moretti and Mearelli (1981) found that R. dorsalis has N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 515

0 0 0 P P-P P

-P -P

H H H M M M O O O IU IU IU S S S

P N P N P N

H O H O H O

A M A M A M T T T M M M E E E

S A S A S A 0 0 0 0 SOLIDS 0 SOLIDS 0 SOLIDS

0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE H. exocellata H.gr. pellucidula H. sp1

0 0 0 P P P

-P -P -P

H H H M M M O O O IU IU IU S S S

P N P N P N

H O H O H O

A M A M A M T T T M M M E E E

S A S A S A 0 0 0 0 SOLIDS 0 S 0 S OLIDS OLIDS

0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE H. infernalis C. lepida H. siltalai

0 0 0 P P P

-P -P -P

H H H M M M O O O IU IU IU S S S

P N P N P N

H O H O H O

A M A M A M T T T M M M E E E

S A S A S A 0 0 0 0 SOLIDS 0 S 0 S OLIDS OLI DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE H. brevis H. instabilis H. dinarica

0 0 0 P P P

- -P -P P

H H H M M M O O O IU IU IU S S S

P N P N P N

H O H O H O

A M A M A M T T T M M M E E E

S A S A S A 0 0 0 0 SOLI 0 S 0 S OLI OLI DS DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE P. montanus C. marginata Agapetus sp.

0 0 P P

-P -P

H H M M O O

S IU S IU

P N P N H H O O A A M M T T M M E E

S A S A 0 0 0 SOLI 0 SOLIDS

DS 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Hydroptila sp. Ithytrichia sp.

Fig. 4. Ecological profiles for caddisfly genus/species grouped by families. Chloride (mg/l), sulphates (mg/l), ammonium (mg/l), P-phosphates (mg/l), suspended solids (mg/l) and oxygen (mg/l) are plotted. Narrow ecological profiles indicate very sensitive genus/species, whereas tolerant taxa present a wide ecological profile. a wider ecological profile than Rhyacophila gr. tristis,as Tolkamp, 1983; Basaguren and Orive, 1990; Gallardo- observed in this study. R. dorsalis has been found in Mayenco et al., 1998; Usseglio-Polatera and Bournaud, headwater and midstream rivers with different biological 1989). We found the same results at the species level of quality (Bonada, 2003). Hydropsychidae is regarded as Hydropsychidae, but at the family level Glossosomati- a very tolerant family all over the world (e.g. Mackay, dae are more tolerant than Hydropsychidae, especially 1979), with species being segregated within different to salinity. On the other hand, our study suggests that at water quality characteristics along the river (Gordon the family and species levels certain caddisflies are and Wallace, 1975; Ross and Wallace, 1982; Gallardo- sensitive to some variables but more tolerant to others, Mayenco et al., 1998). H. exocellata is regarded as one pointing to a high ecological diversification in the of the most pollution tolerant species (e.g. Higler and sampled Mediterranean rivers. This phenomenon is 516 N. Bonada et al. / Environmental Pollution 132 (2004) 509–521

0 0 0 P P P

-P - -P P

H H H O M O M O M S IU S IU S IU P N P N P N H H H O O O A A A M M M T T T E M E M E M S S S A A A 0 0 0 SOLIDS 0 0 SOLIDS 0 SOLIDS

0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE L. guadarramicus M. aspersus Allogamus sp.

0 0 0 P P P

-P -P -P

H H H M M O O M O

S IU S IU S IU P N P N P N H H H O O O A A A M M M T T T M M E E M E S S A S A A 0 0 0 SOLIDS 0 0 S 0 SOLIDS OLIDS

0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE P. cingulatus P. latipennis A. chauviniana

0 0 0 P P P

-P -P -P

H H H O M O M M O S S IU IU S IU P P N N P N H H H O O O A A A M M M T T T E M E M M E S S A A S A 0 SOLI 0 0 SOLIDS 0 0 S 0 OLI DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Chaetopteryx sp. H. radiatus H. tessellatus

0 0 0 P P P

-P -P -P

H H H

O M O M O M

S IU S IU S IU

P N P N P N H H H O O O A A A M M M T T T E M E M E M

S S S A A A 0 SOLI 0 0 S 0 0 SOLI 0 OLI DS DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Stenophylax sp. Rh. dorsalis Rh. meridionalis

0 0 0 P P-P P

-P -P

H H H M M O O O M

S S IU IU S IU P P N N P N H H H O O O A A A M M M T T T M M E E E M

S S S A A A 0 0 0 0 SOLIDS 0 SOLI 0 S OLI DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Rh. munda Rh. nevada Rh. gr. tristis

Fig. 5. Ecological profiles for caddisfly genus/species grouped by families. Chloride (mg/l), sulphates (mg/l), ammonium (mg/l), P-phosphates (mg/l), suspended solids (mg/l) and oxygen (mg/l) are plotted. Narrow ecological profiles indicate very sensitive genus/species, whereas tolerant taxa present a wide ecological profile. rarely noticed in the literature because most studies have The appropriate taxonomical level to be used in water been performed using few species or species from a single monitoring is highly controversial, especially when family. Moreover, most studies on the effects of specific testing whether environmental requirements for lower chemical variables on caddisfly behavior, life history and taxonomical levels can be extrapolated to the level of metabolic processes include only one or two chemical family or order (Resh and Unzicker, 1975; Cranston, variables (see Resh, 1992). This hinders the interpreta- 1990; Lenat and Resh, 2001). We found similar tion of results obtained using numerous chemical ecological profiles at all taxonomical levels when a family variables (Stuijfzand et al., 1999), as in the present has few species (e.g. Odontoceridae) or when a family study. displays a restricted profile (e.g. Brachycentridae and N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 517

0 0 0 P P P

-P -P - P H H H M M O M O O IU S IU S S IU P N P N P N H H O O H O A A M M A M T T T M M E M E E S A S A S A 0 0 0 0 SOLIDS 0 SOLIDS 0 SOLIDS

0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Sericostoma sp. O. albicorne Tinodes sp.

0 0 0 P P P

- - -P P P

H H H M M O M O O

S S IU IU S IU P P N N P N H H H O O O A A A M M M T T T M M E M E E

S S S A A A 0 0 0 SOLI 0 0 S 0 S OLIDS OLI DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE Athripsodes sp. S. argentipunctellus M. azurea

0 0 0 P P P

- -P -P P

H H H M M M O O O IU S IU S IU S N P N P N P H H O H O O A A M A M M T T T M M M E E E

S A S A S A 0 0 0 0 SOLIDS 0 S 0 S OLI OLI DS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE P. kingi P. flavomaculatus Plectrocnemia sp.

0 0 0 P P P-

-P -P P

H H H M M M O O O IU IU S S IU S N P P N P N H O H O H O A A M A M M T T T M M M E E E

S A S A S A 0 0 0 0 SOLI 0 SOLIDS 0 S OLIDS DS 0 SULPHATES 0 SULPHATES 0 SULPHATES

OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE OXYGEN 1 0 CHLORIDE L. basalis M. longulum M. moestum

Fig. 6. Ecological profiles for caddisfly genus/species grouped by families. Chloride (mg/l), sulphates (mg/l), ammonium (mg/l), P-phosphates (mg/l), suspended solids (mg/l) and oxygen (mg/l) are plotted. Narrow ecological profiles indicate very sensitive genus/species, whereas tolerant taxa present a wide ecological profile.

Lepidostomatidae). In other cases, like the abundant sensitivity (or tolerance) of taxa, they can be used to Hydropsychidae and Hydroptilidae, the ecological obtain a biological index using caddisflies at the genus/ patterns at the family level largely differ from those species level, as the saprobic method used in Austria. obtained for some species. Resh and Unzicker (1975) However, caddisfly larval identification is not easy, examined the tolerance of Ceraclea sp. (Athripsodes sp.) especially in areas in which larvae are poorly known, and found specific pollution tolerances at the genus and like the Iberian Peninsula (see Vieira-Lanero, 2000). species levels, in agreement with some of our results. Although some errors are incorporated, indices at the Therefore, the use of the family level may underestimate family level may be adequate in terms of cost-efficiency, higher water qualities, especially when habitat structure especially when few taxonomic experts are available or temporality yields poor macroinvertebrate diversity (Lenat and Resh, 2001). (e.g. Bonada, 2003), because scores at the family level The biological index IBMWP ( former BMWP0d usually use intermediate species tolerance values (Za- Alba-Tercedor and Sańchez-Ortega, 1988; Alba- mora-Mun˜ oz and Alba-Tercedor, 1996; Lenat and Tercedor, 1996; Alba-Tercedor and Pujante, 2000), Resh, 2001). In this regard, in very poor water quality which is highly sensitive to water quality, has been ex- conditions, indices at family level may overestimate tensively applied in the Iberian Peninsula (e.g. Camargo, water quality more than those based on species. 1993; Zamora-Mun˜ oz et al., 1995; Zamora-Mun˜ oz and Biological indices at the species level have been used in Alba-Tercedor, 1996; Garcıá-Criado et al., 1999). Over- some countries (e.g. the saprobic system in Austria) all, scores assigned to caddisfly families in the IBMWP providing good results (Moog and Chovarec, 2000). As agree with the tolerance to pollution for each family in the DIS values obtained here are indicative of the the Mediterranean sampled area, and minor modifica- 518 N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 tions need to be applied only in some cases, particularly and results should be interpreted with caution. More- in Glossosomatidae and Leptoceridae, specially for the over, some variables that have been overlooked because family Glossosomatidae because some larvae of the they were unavailable would refine the final ecological Agapetus genus were found in semiarid areas with profiles to water quality variables. For example, heavy lower water quality than would be expected from metals (Besch et al., 1979; Darlington et al., 1987), a score of 8 in the IBMWP. Although the conductivity hydrocarbons (Simpson, 1980) and pesticides (Dećamps in that area may have a geological origin, larvae are et al., 1973), significantly affect caddisfly taxa. tolerant to high ammonium, suggesting a re-adjustment of its IBMWP score. The divergences between DIS and IBMWP scores observed in Glossosomatidae may be 5. Conclusions related to the specific sensitivities displayed by several species present in some areas but absent in others. In Results from the application of weighted average this regard, Agapetus fuscipes (central and western approaches allowed us to obtain ecological profiles for European species) has been considered as a very water quality variables and to make them comparable to sensitive species (Gonza´lez del Tańago and Garcıáde bioassessment methods based on scores of tolerance. Jaloń, 1984; Wallace et al., 1990), whereas Agapetus Using a large set of caddisfly data collected throughout incertulus (species from the Iberian Peninsula and the Spanish Mediterranean coast it was found that there North Africa) has been found in slightly polluted was a high variability for ecological profiles in taxa, streams with high salinity (see Bonada, 2003). In the ranging from very intolerant (e.g. Brachycentridae, same sense, the IBMWP score assigned to Leptoceridae Lepidostomatidae) to fairly tolerant taxa (mostly diverge much from the DIS value obtained from our Hydropsychidae). The degree of tolerance at the family data set, probably due to the species S. argentipuncte- level is related to the diversity of species and the llus which tolerates high concentrations of sulphates tolerance range of individual species. Moreover, certain and chloride. This species inhabits medium and low caddisfly families and species are sensitive to some reaches of the rivers, often eutrophic and mineralized variables but more tolerant to others. A simple score to naturally (e.g. Gonza´lez del Tańago and Garcıáde determine the degree of intolerance of all caddisflies was Jaloń, 1984). In relation to these results, we propose calculated from the ecological profiles (DIS) and a change in IBMWP scores of Glossosomatidae family compared with the scores used in one of the most from 8 to 6, and for the Leptoceridae family from widely used biological indices in Spain, the IBMWP. A 10 to 9. general association between IBMWP scores and DIS is Ecological profiles are dynamic assessments that can noticed except for certain families like Glossosomatidae vary in space and time, and so studies performed in or Leptoceridae, which contain some species that are small areas or for short periods may be incomplete tolerant to salinity and some toxicity. (Moretti and Mearelli, 1981). Moreover, environmental variables may also change widely in time and space, thus hindering the establishment of organism tolerances to Acknowledgements pollution (Resh and Unzicker, 1975). Therefore, when ecological profiles are obtained from field data instead This research was supported by the GUADALMED of experimental studies, large sets of data integrated in Project, www.guadalmed.org (HID98-0323-C05 and time and space are required to determine the species REN2001-3438-C07) and a pre-doctoral grant from autoecology with certainty. We provide an easy, simple the Ministerio de Ciencia y Tecnologıá to N.B. We method to calculate the ecological profiles of species thank all Guadalmed members for data collection and based on analyses widely applied in other areas of chemical analysis, Dr. Marcos A. Gonza´lez, Dr. ecology. However, several considerations should be Fernando Cobo, Dr. Rufino Vieira-Lanero and Dr. taken into account when tolerances are calculated MaJose´Servia´for their help in caddisfly identifications, assuming a unimodal distribution of organisms. In some and two anonymous referees for their valuable com- cases, organisms can fit a bimodal, multimodal or skewed ments on the manuscript. distribution (Hengeveld, 1990). Several factors are considered responsible for the deviation: biotic interactions (Westman, 1991), life cycle stage (Verdonschot and Higler, 1992) and lack of gradient of the environ- Appendix mental variable (Wiens, 1989). However, in most cases, probably because data are incomplete, it is not possible to List of caddisfly families and genus/family recorded determine whether organisms display a unimodal distri- from Mediterranean Spanish basins with the frequency bution with certainty (Verdonschot and Higler, 1992). (N ) of each taxon expressed as number of samples Thus these considerations should be taken into account (sites ! seasons) where the taxon was present. N. Bonada et al. / Environmental Pollution 132 (2004) 509–521 519

Family N Genus/species N Brachycentridae Ulmer, 1903 37 Micrasema longulum McLachlan, 1876 10 Micrasema moestum (Hagen, 1868) 23 Glossosomatidae Wallengren, 1891 61 Agapetus sp. Curtis, 1834 38 Hydropsychidae Curtis, 1835 449 Cheumatopsyche lepida (Pictet, 1834) 10 Hydropsyche brevis Mosely, 1930 23 Hydropsyche dinarica Marinkso¨vic, 1979 10 Hydropsyche exocellata Dufo¨ur, 1841 136 Hydropsyche gr. pellucidula 159 Hydropsyche infernalis Schmid, 1952 31 Hydropsyche instabilis (Curtis, 1834) 115 Hydropsyche siltalai Do¨hler, 1963 30 Hydropsyche sp1 13 Hydroptilidae Stephens, 1836 254 Hydroptila sp. Dalman, 1819 222 Ithytrichia sp. Eaton, 1873 10 Lepidostomatidae Ulmer, 1903 62 Lasiocephala basalis (Kolenati, 1848) 59 Leptoceridae Leach, 1815 95 Athripsodes sp. Billberg, 1820 38 Mystacides azurea (Linnaeus, 1761) 21 Setodes argentipunctellus McLachlan, 1877 21 Limnephilidae Kolenati, 1848 222 Allogamus sp. Schmid, 1955 15 Anomalopterygella chauviniana (Stein, 1874) 12 Chaetopteryx sp. Stephens, 1829 11 Halesus radiatus (Curtis, 1834) 18 Halesus tessellatus (Curtis, 1834) 30 Limnephilus guadarramicus Schmid, 1955 29 Mesophylax aspersus (Rambur, 1842) 60 Potamophylax cingulatus (Stephens, 1837) 13 Potamophylax latipennis (Curtis, 1834) 29 Stenophylax sp. Kolenati, 1848 13 Odontoceridae Wallengren, 1891 12 Odontocerum albicorne (Scopoli, 1763) 10 Philopotamidae Stephens, 1829 83 Chimarra marginata (Linnaeus, 1767) 55 Philopotamus montanus (Donovan, 1813) 14 Polycentropodidae Ulmer, 1903 139 Plectrocnemia sp. Stephens, 1836 23 Polycentropus kingi McLachlan, 1881 27 Polycentropus ﬂavomaculatus (Pictet, 1834) 19 Psychomyiidae Walker, 1852 64 Tinodes sp. Curtis, 1834 44 Rhyacophilidae Stephens, 1836 224 Rhyacophila gr. tristis Pictet, 1834 13 Rhyacophila dorsalis (Curtis, 1834) 35 Rhyacophila meridionalis Pictet, 1865 23 Rhyacophila munda McLachlan, 1862 63 Rhyacophila nevada Schmid, 1952 61 Sericostomatidae Stephens, 1836 74 Sericostoma sp. Latreille, 1825 61

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