BENTHIC MACROINVERTEBRATES COMMUNITY AS ECOLOGICAL INDICATOR OF LAKE STATUS
ALPLAKESALPLAKES Alpine Lakes Network
BENTHIC MACROINVERTEBRATES COMMUNITY AS ECOLOGICAL INDICATOR OF LAKE STATUS
Natural History PROVINCIA AUTONOMA Museum of Trento DI TRENTO
Working group: Coordinator: Maria Cristina Bruno (researcher), Bruno Maiolini Invertebrate Zoology Mauro Carolli (researcher), and Hydrobiology, Mattia Dori (technician) Natural History Invertebrate Zoology and Hydrobiology, Museum of Trento Natural History Museum of Trento ALPLAKES
SUMMARY
Introduction pag. 2 1 Study area pag. 3 2 Materials and methods pag. 14 2.1 Spatial and temporal schedule pag. 14 2.2 Biological sampling pag. 14 3 Results pag. 17 3.1 Water quality pag. 17 3.2 Fauna pag. 17 3.2.1 Crustacea pag. 17 3.2.2 Hexapoda pag. 24 3.2.2.1 Odonata pag. 24 3.2.2.2 Ephemeroptera pag. 31 3.2.2.3 Diptera pag. 32 3.2.2.4 Other Hexapoda taxa pag. 33 3.2.3 Hirudinea pag. 35 3.2.4 Mollusca pag. 36 3.2.5 Other invertebrates pag. 38 3.2.6 Reptiles and amphibians pag. 39 3.2.7 Birds pag. 41 3.2.8 General remarks on invertebrate faunal assemblages pag. 44 3.3 Alien species pag. 46 3.3.1 The zebra mussel Dreissena polymorpha pag. 46 3.3.2 The American crayfish Orctonectes limosus pag. 47 4 Conclusions pag. 49 Acknowledgements pag. 50 References pag. 51
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INTRODUCTION
INTRODUCTION
Aquatic communities contain a variety of species that represent different trophic levels, taxonomic groups, functional characteristics, and tolerance ranges. Careful selection of target taxonomic groups can provide a balanced assessment, sufficiently broad to describe the structural and functional condition of an aquatic ecosystem and sufficiently practical to be used for widespread monitoring by non-specialist operators. Benthic invertebrate assemblages in lakes correspond to particular habitat types and may be classified according to the three basic habitats of lake bottom: littoral, sublittoral, and profundal. The littoral habitat of lakes usually supports larger and more diverse populations of benthic invertebrates than other zones (Wiederholm, 1984). The vegetation and substrate heterogeneity of the littoral habitat provide an abundance of microhabitats occupied by a diversified fauna. The littoral habitat is also highly variable and highly productive, due to seasonal variations, differences in land use and riparian vegetation, and direct climatic effects. The profundal habitat, in the hypolimnion of stratified lakes, is more uniform due to the more homogeneous substrate and organic matter source; hypoxia and anoxia in moderately to highly productive lakes are common in the profundal zone. We decided to sample the littoral area which, from previous research (Lencioni, 2005) appeared to have the highest number of species and individuals, and thus represented a subsample of each lake biodiversity. Macroinvertebrates have a great potential as biological indicators because they are ubiquitous, have low vagility, integrate the effect of multiple stressors on the aquatic system, and are relatively easy to sample and identify. However, their use in monitoring program is currently hampered by a lack of understanding of how they respond to environmental pressures. To assess the ecological status of six lakes in Trentino, we developed a research plan which included sampling, sorting and taxonomic identification of the macroinvertebrate fauna according to the protocol described in the present report. This protocol emphasizes a practical strategy for sampling invertebrate biodiversity in selected lakes. We selected simple, easily standardized methods, which are broadly applicable to different lakes at a reasonable cost and effort. The objective of this approach was to provide a broad, repeatable characterization of benthic macroinvertebrate fauna of different lakes, which can document spatial and temporal changes of biotic and environmental variables. Wide attention was given to the presence and the density of some invasive alien species like the Bivalvia Dreissena polimorpha and the crayfish Orctonectes limosus. We focused on areas of each lake characterized by different sets of those environmental conditions which can cause changes in community structure, and respond differently to nutrient loading and environmental pressures (e.g. substrate size, amount of organic matter, presence/absence of macrophytes, light, and oxygen concentration).
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Chapter 1 STUDY AREA
1.1. STUDY AREA We collected samples (Fig. 1.1) at six lakes in Trentino (NE-Italy, 46°N, 10-11°E): Terlago, Garda, Ledro, Levico, Caldonazzo and Cei, located in 3 watersheds (Sarca, Adige, and Brenta) (Figs. 1.2, 1.3). Criteria used to select the lakes were: the level of interest of the government environmental agencies, and the type of anthropic impact (e.g. land use, urbanization, tourism). The morphological and physical- chemical characteristics of the six lakes are presented in Box. 1 and summarized in Table 1.1, they are taken from the annual reports on the limnological characteristics of Trentino lakes (1995-1998) by the Agrarian Institute of San Michele all’Adige (IASMA), Trento (Corradini & Flaim, 1995, 1996, 1997, 1998).
Fig. 1.1 – Sampling of representative habitat under swan monitoring
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Table 1.1 – Morphometric, lithological, main chemical features and general information of the investigated lakes
Caldonazzo Cei Garda Ledro Levico Terlago Watershed Brenta Adige, R. of Sarca, Mincio, Sarca, Brenta Adige Cimone Po Ponale Stream Mountain Cima d'Asta - Mount Alpi Val di Alpi, Val di Cima d'Asta - Gazza – group Pasubio- Bondone Ledro valley Ledro valley Pasubio-Becco Paganella Becco di group Alps-Monte di Filadonna group Filadonna Baldo group chain chain Altitude (m 440 920 65 655 440 414 a.s.l.) Lake 84.2 - - 101,2 27 21,1 drainage basin (km2) Lake area 5.63 0,39 144.6 2.177 1.16 1,185 (km2) Volume 148,987,000 87,500 49,756,000,0 75,775,000 12,942,000 445,000 (m3) 00 Length (m) 4,735 450 5,500 2,830 2,840 1,500 Width (m) 1,870 140 3,500 770 900 280 Origin alluvional Landslide Moraine Moraine alluvional exharative damming damming damming, damming damming valley glacial, fluvial Lithology phyllads, Lias Lias and Rhetic gneiss, alluvial Lias gneiss limestone, dogger limestone limestone, debris, limestone red marl moraine Average 26.5 2,2 134,5 35 11.1 3,8 depth (m) Maximum 49 7,1 311 48 38 11 depth (m) Lake 2.3-3.6 nd nd nd 1.1 <1 theoretical water renewal time (years) Important Mandola, - Sarca Massangla, Maggiore, Terlago affluent (s) Palude, Spini, Assat di Vignola stream, f Merdar, Ischia Pur, Assat streams Maestro sterams, di Pieve canal fosso dei streams Gamberi, Important Brenta River Airone strema Mincio River Hydropower Brenta River Natural effluent (s) through connection sinkholes Lagabis lake with Lake Garda Trophic Mesotrophic Mesotrophic Mesotrophic Meso- Mesotrophic Eutrophic status oligotrophic Circulation Dimictic Dimictic - - Dimictic Dimictic Land use woodland, woodland, - urbanization urbanization and and agricultural agricultural Monitored 1973 1974 - 1973 1973 1973 since Notes - - - Hydroelectri - Floating c use, level (7-8 m) floating level
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Fig. 1.2 – Study area (Trentino, NE Italy, 46°N, 10-11°E)
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Fig. 1.3 – The six lakes investigated in Trentino
Fig. 1.4 – Caldonazzo (on the left) and Levico (on the right) lakes, view from the south
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Fig. 1.5a – Bathymetric maps of the six investigated lakes with location of the sampling stations (red circles)
Source: mod. from Tomasi, 2004.
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Fig. 1.5b – Bathymetric maps of the six investigated lakes with location of the sampling stations (red circles)
Source: mod. from Tomasi, 2004.
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Fig. 1.5c – Bathymetric maps of the six investigated lakes with location of the sampling stations (red circles)
Sinkhole • Sinkhole
Source: mod. from Tomasi, 2004.
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Box 1. The morphological and physical- chemical characteristics of the six lakes
Caldonazzo Lake
Watershed: Brenta Geology: phyllads, gneiss Origin: alluvial damming Altitude (m a.s.l.): 440 Lake drainage basin (Km2): 84.2 Lake area (Km2): 5.63 Volume (m3): 148,987,000 Maximum depth (m): 49 Mean depth (m): 26.5 Theoretical water residence time (years): 2.3-3.6 Important inlets: streams Mandola, Palude, Spini, Merdar, Ischia streams, “fosso dei Gamberi” Important outlet: Brenta River Circulation: dimictic Trophic status: mesotrophic Land use: agriculture, urbanisation, woodland.
Caldonazzo Lake is the largest lake in Trentino and it is located close to Levico Lake (Fig. 4), in the Upper Valsugana. The two lakes originated from Quaternary glaciers barred by alluvial conoids accumulated by their tributaries. The lakes fill a depression formed by two big tectonic rifts: the Belluno and the Valsugana rifts, and are excavated in phyllads and gneiss stones. A hill ridge of Pliocenic origin 600 meters wide separates Caldonazzo and Levico lakes. One branch of Brenta river springs from each of the lakes. During the ‘70s Caldonazzo lake become eutrophic, with consequent extensive fish mortality. To prevent eutrophy, all sewage was diverted, 5 Limno unites were installed to pump oxygen in the anoxic hypolimnion, and a siphon was placed near the Brenta outlet to eliminate nutrients accumulated in the deep waters. The most important human activity impacting lake Caldonazzo is tourism, because the lake represents a popular summer resort for local population and visitors from the nearby Trento, as well as from foreign countries. Caldonazzo lake is an important area for migratory and inland water birds, which stop here to nest or overwinter. Some species are included in the Red List of Italian species, such as Anas strepera, Aythya fuligula, and Aytyha niroca. Other are species of European Conservation Concern according to BirdLife International 2004, such as Aythya ferina, Numenius arquata, Larus canus. Part of the reed-beds are protected by the local government.
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Levico lake
Watershed: Brenta Geology: gneiss, alluvial Origin: alluvial damming Altitude (m. a.s.l.): 440 Lake drainage basin (Km2): 27 Lake area (Km2): 1.16 Volume (m3): 12,942,000 Maximum depth (m): 38 Mean depth (m): 11.1 Theoretical water residence time (years): 1.1 Important inlets: Maggiore and Vignola streams. Important outlet: Brenta river Circulation: dimictic Trophic status: mesotrophic Land use: woodland, agriculture and urbanisation.
The most important human activity around Levico lake is tourism, which concentrates on the southern shore. The remaining sections of the lake are well-preserved, the shores are quite steep and surrounded by woods and on the northern tip by wetlands. Several species of birds such as grebes, coots, grey herons, tupted duck and pochards nest or winter in Levico. Most of the lake freezes in winter and in recent years it hosts a wintering colony of about fifty grey herons, easily observed as they “queu” on the ice layers. The fish fauna is abundant and diverse with abundant populations of pike hunting in the reed-beds.
Cei lake
Watershed: Adige Geology: Limestone, alluvial deposits. Origin: landslide damming Altitude (m. a.s.l.): 920 Lake drainage basin (Km2): - Lake area (Km2): 0.039 Volume (m3): 87,500 Maximum depth (m): 7.1 Mean depth (m): 2.2 Theoretical water residence time (years): - Important inlets: - Important outlet: Airone stream, flowing into Lagabis lake. Circulation: dimictic Trophic status: mesotrophic Land use: woodland, pasture, urbanisation
Cei Lake is located in a little valley on a mountain range along the right side of Adige River. The lake originated around 1280 B.B. from a landslide from Monte Bondone. The geological setting of this area is represented by lias limestone, retic limestone and alluvial deposits. The nearby small lake Lagabis collects the effluent of Cei lake and water flows from there towards the Adige valley. Cei lake has been a designed as a protected biotope since 1992. The lake needs continuous cleaning and maintenance because it tends to fill quickly due to its high eutrophic status. Herpethological fauna is repreented by Bufo bufo, Elaphe longilissima, Hyla intermedia, Natrix natrix, Rana temporaria, Trirurus alpestris and Salamandra salamandra. Among birds, Alcedo atthis can be seen along the banks of this lake.
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Garda Lake
Watershed: Sarca Geology: lias limestone, dogger limestone, stratified dolomite Origin: (mixed) tectonic, fluvial, glacial exaration. Altitude (m a.s.l.): 65 Lake drainage basin (Km2): - Lake area (Km2): Trentino section 14.46, total 369.98 Volume (m3): 49,756,000,000 Maximum depth (m): Trentino section 311, total 346 Mean depth (m): 134.5 Important affluent(s): Sarca Important effluent(s): Mincio Trophic status: mesotrophic
Garda Lake is the largest Italian Lake, thus its biological status is difficult to assess. Only a small portion (4%) of the lake is in Trentino province, the most part is in Veneto and Lombardia regions. Garda Lake fills an ancient Pliocene valley formed during the last ice- age, when the erosive action of the great glaciers modified the width, depth and geology of this valley. At the end of the last ice-age the water coming from the Sarca basin filled this area forming Garda Lake. The geology of the area is much diversified: the western bank is lined with a chaotic mass of rocks, whereas more regular and stratified stones line the eastern bank. The main rocks are represented by lias limestone, dogger limestone and stratified dolomite. Garda Lake freezes seldom, and during the coldest winter days. For this reason and because of the particular thermic stratification, the limnologists consider Garda Lake a tropical lake. Another particular feature is the transparency of the water, which is the highest among European lakes. The most important human activity impacting the lake is tourism, while professional fishing has now only historical importance. Garda lake has two different fish assemblages: the northern part, which has deeper and colder waters, is rich in salmonids, whereas the southern part, where water is warmer, cyprinids are dominant. Reptiles and amphibians are Bufo viridis and Coluber viridiflavus (Caldonazzi et al., 2002). Garda Lake is an important area for birds, which find here the habitats to nest or overwinter. Some species such as Anas strepera, Anas clipeata, Aythya fuligula, Phalacorax carbo are included in the Red list of Italian species, with different threat level. Others species, such as Larus canus, are species of European Conservation Concern (Birdlife International, 2004; Pedrini et al., 2005).
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Ledro lake
Watershed: Sarca Geology: retic limestone Origin: morenic dam Altitude (m a.s.l.): 655 Lake drainage basin (Km2): Lake area (Km2): 2.177 Volume (m3): 75,775,000 Maximum depth (m): 48 Mean depth (m): 35 Important inlets: Massangla, Assat di Pur, and Assat di Pieve streams Important outlets: Artificial runoff to Garda’s lake Trophic status: meso- oligotrophic
Ledro Lake fills the eastern section of an ancient valley, which during the last ice-age was dammed by a moraine dammed, thus originating the lake. The dominant geological formation is retic limestone. Three streams are the most important affluent, but several subterranean springs also feed the lake. Ledro has an archaeological importance, because its banks host well-preserved the remains lake dwellings of Bronze Age. The area host the Pile Dwelling Museum of Marina di Ledro, a section of MTSN. Ledro lake has been used like a reservoir to produce electrical energy since 1928. Starting from 1949, water is pumped back from Garda Lake by a hydropower pump during low energy request periods, with subsequent frequent variation in level which cause in turn changes in the biological communities of the lake, especially in its planktonic component. This movement of water also promoted the introduction of the invasive mollusk Dreissena polymorpha from lake Garda.
Terlago lake
Watershed: Adige Geology: lias limestone, red marl Origin: exharative valley Altitude (m a.s.l.): 414 Lake drainage basin (Km2): - Lake area (Km2): 0.1185 Volume (m3): 445,000 Maximum depth (m): 11 Mean depth (m): 3.8 Theoretical water residence time (years): <1 Important inlets: Terlago stream, Maestro canal Important outlet: sinkhole Circulation: dimictic Trophic status: eutrophic Land use: agriculture, urbanisation
Terlago lake lies on a carbonatic exarative valley, shaped by a glacier during the last ice-age. The substrates are lias limestone and red marl. The lake has only subterranean outlets that flow into the Adige River 6 km north of Trento. The lake freezes every year for about one month and it is classified as a temperate lake. It has highly variable water levels because water can flow very fast through some carbonatic sinkholes, which were artificially enlarged and were used to empty the lake during floodings. In the last years the lake has become eutrophic due to the large load of nutrients used for agriculture in the surrounding area.
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Chapter 2 MATERIALS AND METHODS
2.1 SPATIAL AND TEMPORAL SCHEDULE The selected lakes were investigated in April, May, June and July 2006 (Table 2.1). Artificial substrates were deployed during the first sampling (beginning of May) and retrieved and replaced three times (May, June, July) after about 20 days.
Table 2.1 – Sampling dates for each lake
Lake Date Cei - 24/05/2006 15/06/2006 5/07/2006
Caldonazzo 3/05/2006 25/05/2006 14/06/2006 4/07/2006 Garda 4/05/2006 26/05/2006 15/06/2006 5/07/2006 Ledro 4/05/2006 26/05/2006 15/06/2006 5/07/2006
Levico 3/05/2006 25/05/2006 14/06/2006 4/07/2006 Terlago 4/05/2006 26/05/2006 14/06/2006 4/07/2006
For each lake we selected 4 littoral stations, except for Garda, which had only two stations. The littoral stations were at 0-1.5 m depth, and characterized by different slope, substrate, presence of macrophyte banks, organic matter content etc. The stations were located preferably in ecotones separating two different habitats (e. g. reed beds vs macrophytes) with the exception of lake Garda, where only two representative habitats were sampled, given the difficulty of an exhaustive research of Italy’s largest lake (Fig. 1.5a).
2.2 BIOLOGICAL SAMPLING The littoral area was sampled by sweeping the shoreline with a pond net of 100 µm mesh size. These kind of samples are qualitative, but are useful to expand the species lists. Quantitative samples were collected using two different artificial substrates: one is a classic plastic net bag containing a given amount of pebbles, collected locally and cleaned; the second one is a building brick with two rows of five holes (Fig. 2.1). One of each substrates was deployed at each station, and retrieved according to the schedule explained in the previous paragraph. Substrates were carefully washed in the field, the washout was filtered with the 100 µm mesh size pond net, and the filtered material was fixed in 70% ethanol and taken to the laboratory for identification at the appropriate taxonomic level under a dissecting stereoscope. The substrates were at times stolen or destroyed, mainly at Caldonazzo; due to lake level fluctuations, the substrates dried in one occasion at Terlago lake, and were submerged so deep that could not be retrieved in one occasion at one station at Ledro. Therefore we had a total of samples as in Table 2.2.
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Table 2.2 – Total number of substrates deployed and retrieved at each lake Number of substrates deployed Number of substrates retrieved Lake Net bag Brick Net bag Brick Cei 8 8 8 8 Caldonazzo 12 12 5 6 Garda 6 6 5 6 Ledro 12 12 11 11 Levico 12 12 12 12 Terlago 12 12 6 6
Invertebrates were identified to species using appropriate identification keys (Campaioli et al., 1994, 1999; Sansoni et al., 1988; Carchini et al., 1983; Belfiore et al., 1983; Chinery, 1987; Minelli, 1977; Rivosecchi, 1984). For microcrustaceans, identification required dissecting and mounting specimens in permanent slides with glycerine as medium, and identifying them with a phase-contrast microscope at 200 X, 600 X, 1,000 X. Identification followed Dussart (1967), Dussart and Defaye (1995).
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Fig. 2.1 – Preparation of a substrate, sampling, brick and some representative habitats
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Chapter 3 RESULT
3.1 WATER QUALITY Nitrogen and orthophosphate values were available only for Levico and Caldonazzo. Mean values were calculated on datasets published yearly by APPA and IASMA since 1995 (Table 3.1) (Corradini & Flaim, 1995, 1996, 1997, 1998).
Table 3.1 – Alkalinity and nutrient concentration (annual mean ± standard deviation) of the investigated lakes
Alkalinity TN N-NH4 N-NO2 N-NO3 P-PO4 TP (meq/l) (mg/l) (mg/l) (µg/l) (mg/l) (µg/l) (µg/l) 3.77±0.93 1.1±0.2 103±192 10±16 350±220 23±47 36±50 Caldonazzo Cei 156+3,8 - 37+31,6 - 200+184,6 2,5+0,55 - Garda ------Ledro 168+14 - 278+559 - 699+283 9+21 - Levico 2.76±0.59 1.1±0.2 257±460 17±25 434±214 17±46 32±52 Terlago 184+51 - 514+949 - 724+752 6,19+5,1 -
3.2 FAUNA 3.2.1 Crustacea Crustaceans are abundant and diverse, and one of the dominant groups in freshwater benthic habitats (i.e. they live associated with the substrate), due to their feeding habits. In fact, the largest and most common taxa are generally macrophagous herbivorous and scavengers (Isopoda, Amphipoda), or predators (Decapoda, some Cyclopoida, Amphipoda and Isopoda), the smaller taxa are usually microphagous selective deposit feeders, employing various methods to remove food from the sediments in which they live (Harpacticoida). Most of these taxa therefore represent the base of the lacustrine food-web, representing the first level of consumers. They are in turn prey for a wide variety of fishes, amphibian larvae, and macroinvertebrates. Benthic animals may live on the surface of the substratum, or borrow in the soft sediment. Small benthic crustaceans tend to be sedentary, whereas larger ones (such as Decapoda) are more vagile. In any case, because of their strict relationship with the sediment, which represents not only their living space, but also their food source, benthic crustaceans are affected by heavy metals, nutrients, pesticides, which deposit on the bottom of lakes. The presence of a diverse benthic crustacean community indicates good variety of habitats, and good water quality.
We collected a total of 4,622 crustaceans, belonging to the orders Amphipoda (184 individuals), Isopoda (275 ind.), Decapoda (11 ind.), Ostracoda (787 ind.), Cladocera (2742 ind.), and to the suborder Copepoda (order Harpacticoida, 400 ind., Calanoida, 2 ind., Cyclopoida, 221 ind.). Of these, only Amphipoda, Isopoda, and Copepoda were identified to the species level (Table 3.2) and were used for subsequent statistical analysis. These taxa are typically benthic, have low mobility, and we considered them to be good representatives of the entire benthic communities. Decapods were not included in the analysis because of their high mobility, which easily allows them to escape capture (at least with the sampling methods used in this study), with a subsequent underestimate of their densities. Cladocera are mostly planktonic (i.e. living in the water column), and therefore the values of their abundances at each station might have been biased by the sampling method, and they were not included in the analysis. Ostracoda are indeed a benthic taxa, but we did not identify them at species level, and we could not include them in the analysis.
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We averaged the values collected at the four (or two for Garda lake) replicates for all the crustaceans identified (see above), and used the average values for the analysis described below. We calculated the following indices (Table 3.3): 1) Total species (S): the number of species in each sample. i.e. species with non zero counts. 2) Total individuals (N): The number of individuals in each sample. 3) Margalef Index of species richness (d) = (S-1)/Log(N) 4) Shannon-Wiener diversity index (H')= - Σpi * ln pi, where pi is the proportion of the sample represented by species i, and ln is the natural logarithm We classified the lakes by running Cluster Analysis on the average number of crustaceans for each lake, transformed in Log (x+1), using Bray-Curtis Similarity Index, and UPGMA as clustering technique. We run multiple correlations between the faunal data and the following morphological characteristics of the lakes: altitude (m a.s.l.), lake area (km2), volume (m3), length (m), width (m), average depth (m), maximum depth (m).
In total, we used 1,082 crustaceans for our analysis. For each order, the number of species was as follows: 7 Harpacticoida, 9 Cyclopoida, 1 Calanoida, 1 Isopoda, 1 Amphipoda (Table 3.2). All taxa are known for Italian fauna, common in lentic waters (Ruffo and Stoch, 2005). However, most of the species had never been recorded in the sampled lakes (Table 3.4). The cluster analysis dendrogram of species abundance (Fig. 3.1) shows that Cei lake is most different from all the other lakes; followed by two groups, the first one represented by the lakes in the Brenta watershed (Caldonazzo and Levico), the second by the lakes in the Sarca (Ledro and Garda) and Adige (Terlago lake) watersheds. In the latter, Ledro and Garda lakes are more similar to each other than Terlago lake. The dominance plot calculated from the average abundances of each taxon for each lake (Fig. 3.2) represent the percentage contribution to the total of each of the species, which are ranked in order of importance. In Lake Levico crustaceans were most abundant (N=122, Table 3.3), and the community was the most diverse (H'= 1.96, S=17, Table 3.3), with several relatively abundant species, and several rare ones as well. In Caldonazzo lake crustaceans were quite abundant (N= 44, Table 3.3) and the community was quite diverse as well (H'= 0.9068, S=6, Table 3.3), with one dominant species and 5 rare ones. The remaining lakes had lower abundance and diversity, with few dominant species, and few rare ones. The less diverse lake was Cei (H'= 0.238, S=3, Table 3.3), the lake with fewer taxa was Ledro (S=2, Table 3.3), and the one with less abundant communities was Terlago (N=4, Table 3.3). Harpacticoida were the most abundant taxon of crustaceans (33%, Fig. 3.3), followed by Amphipoda (26%, Fig. 3.3), Isopoda (24%, Fig. 3.3), Cyclopoida (17%, Fig. 3.3). Calanoida represented only 0.16% of the total (Fig. 3.4). Harpacticoida were abundant at Levico, Caldonazzo and Cei lakes, and rare or absent in the remaining ones (Fig. 3.4). The opposite distribution was recorded for Amphipoda (Fig. 3.4). Isopoda were present in all lakes except Cei lake, and were more abundant at Caldonazzo and Levico lakes (Fig. 3.4). Cyclopoida were found only in Levico and Caldonazzo, they were the dominant taxon at Levico, and very rare at Caldonazzo lake (Fig. 3.4). Amphipoda abundances were positively correlated (p< 0.05000) with lake volume, width and maximum depth (r=1, 0.88, 0.99, respectively).
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Table 3.2 – Taxonomic status of collected crustaceans, and number of individuals and species collected for each taxon.
Subphylum Class Subclass Order N. individuals N. species Crustacea Branchiopoda Diplostraca Cladocera 2742 ? Crustacea Maxillopoda Copepoda Calanoida 2 1 Crustacea Maxillopoda Copepoda Cyclopoida 221 9 Crustacea Maxillopoda Copepoda Harpacticoida 400 7 Crustacea Ostracoda 787 ? Crustacea Malacostraca Peracarida Amphipoda 184 1 Crustacea Malacostraca Peracarida Isopoda 275 1 Crustacea Malacostraca Eumalacostraca Decapoda 12 1
Table 3.3 – Number of species (S), of individuals (N), Margalef species richness (d), and Shannon diversity index (H'), calculated over the average values for each lake.
Lake S N d H' Garda 5 99 0.8705 0.7922 Ledro 2 17 0.353 0.6823 Terlago 4 4 2.2697 0.8572 Levico 17 122 3.3291 1.9638 Caldonazzo 6 44 1.3253 0.9068 Cei 3 34 0.5672 0.238
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Table 3.4 –Records of the collected Crustacea for the sampled lakes. RS= Ruffo and Stoch, 2005; MTSN= present study
MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN RS RS MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN MTSN RS MTSN MTSN MTSN MTSN MTSN MTSN RS RS MTSN Acanthodiaptomus denticornis Ectocyclops phaleratus Eucyclops serrulatus Eucyclops speratus Macrocyclops albidus Mesocyclops leuckarti Microcyclops rubellus Paracyclops chiltoni Nitokra hibernica crassa Attheyella Bryocamptus minutus Bryocamptus vejdowski Canthocamptus staphylinus Elaphoidella bidens Asellus aquaticus Echinogammarus stammeri
Class Class Calanoida Copepoda Maxillopoda Diaptomidae order Cyclopoida Subclass Copepoda Maxillopoda Cyclopidae Family Species Cei Terlago Levico Ledro Garda Caldonazzo Maxillopoda Copepoda Cyclopoida Copepoda Maxillopoda Cyclopidae Cyclopoida Copepoda Maxillopoda Cyclopidae Cyclopoida Copepoda Maxillopoda Cyclopidae Cyclopoida Copepoda Maxillopoda Cyclopidae Cyclopoida Copepoda Maxillopoda Cyclopidae Cyclopoida Copepoda Maxillopoda Cyclopidae Ameiridae Harpacticoida CopepodaMaxillopoda Canthocamptidae Harpacticoida Copepoda Maxillopoda Canthocamptidae Harpacticoida Copepoda Maxillopoda Canthocamptidae Harpacticoida Copepoda Maxillopoda Canthocamptidae Harpacticoida Copepoda Maxillopoda Canthocamptidae Harpacticoida Copepoda Maxillopoda Amphipoda Peracarida Malacostraca Gammaridae Amphipoda Peracarida Malacostraca Asellidae
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Fig 3.1 – Cluster Analysis (Bray-Curtis similarity Index, UPGMA clustering method), of the average abundances of crustaceans at each lake. Data transformed in Log (x+1)
CEI
CL
LV
Lake TR
GR
LD 1009080706050403020100 Similarity Index
Fig 3.2 –Dominance plot calculated from the average abundances of each taxon for each lake
100 Cei Caldonazzo 90 Garda Ledro 80 Levico Terlago 70
60
50 40 Cumulative Dominance%30 20 1 10 100 Species rank
Fig 3.3 – Percentage composition of crustaceans over all lakes
80
70
60
50
40
average n. ind. n. average 30
20
10
0 Garda Ledro Terlago Caldonazzo Levico Cei Calanoida 000010 Cyclopoida 0001540 Harpacticoida 8 0 1 21 41 33 Isopoda 16 10 3 22 26 0 Amphipoda 75 7 0 0 0 1
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Fig 3.4 – Average number of crustaceans collected at each lake
Isopoda Harpacticoida 24.02% 32.55%
Cyclopoida Amphipoda Calanoida 17.14% 26.13% 0.16%
The geographical position of the lakes appeared to determine the crustacean faunal composition: lakes in the Brenta and Adige watershed were different from the lakes in the Sarca watershed. Cei lake differed from all other lakes, even if in the same watershed of Terlago, probably because its small dimensions and the related reduced number of microhabitats do not allow the establishment of a complex benthic community (except for a high number of Harpacticoida, even though belonging almost exclusively to Bryocycamptus minutus, a common species in lentic habitats). Cei lake is also the only one at high altitude (920 m a.s.l.), and its watershed is hydrologically isolated from the other lakes in the area. Thus, the ecological conditions linked to altitude might have limited the dispersion of benthic taxa to this lake basin; dispersal might have been hindered also by the lack of direct connections with other watersheds. The second Adige watershed lake, Terlago lake, is very close to the limit of the Sarca river watershed, and its climate is influenced by Garda lake. Presumably, faunal exchange between Terlago and the lakes in the “lake valley” occurred, and benthic communities of these lakes were similar, although the small volume of the lake might account for the low number of individuals collected here. The Brenta watershed lakes (Levico and Caldonazzo) had high number of Harpacticoida, Cyclopoida, and Isopoda, whereas Amphipoda were dominant in lakes in the Sarca and Adige watershed. These two lakes can be considered “twin lakes”: they are located in close proximity (Fig. 3.3), they originated at the same time in the Quaternary by damming due to alluvial conoids accumulated by the glaciers. Even if nowadays they are not directly connected, it is likely that connections did exist in the past, allowing faunal exchanges. The present connections are represented by the main outlets, the two branches of the Brenta River (“Brenta di Levico” and “Brenta di Caldonazzo”), which join few km from the lakes, and which might represent a faunal exchange route for taxa able to move upstream. The higher diversity recorded at Levico lake is probably due to different water quality recorded for the two lakes. The most recent information on the trophic status of the two lakes (Corradini F. & Flaim G., 1995, 1996, 1997, 1998) report both Levico and Caldonazzo Lakes as eutrophic, but the trophic level of the latter is higher than that of the former. In a recent investigation on e heavy metal concentration in the two lakes (Ravera et al., 2005) the concentrations of six relatively abundant metals (Fe, Mn, Zn, Cu, Al, Ca) were higher in the water of Lake Caldonazzo than in Lake Levico. Because nutrients and heavy metals deposit on the bottom sediment, were they undergo microbial transformations, the higher water and sediment quality of Levico lake might be the reason for the higher diversity of benthic organisms recorded there. The Sarca watershed lakes (Garda and Ledro) had a similar faunal composition; however, Garda lake had higher number of taxa and individuals, due to the high volume and depth of this lake. We were not able to collect enough samples to cover all the variability in environmental conditions around Garda lake, so the diversity recorded there is probably an underestimate, because several more taxa of benthic crustacean are signaled for Garda lake (Ruffo and Stoch, 2005). The opposite distribution of the dominant taxa (Harpacticoida vs. Amphipoda) could be due to the different food item the two groups feed upon, due to their very different body sizes: they are both detritivorous gatherers, but while Echinogammarus stammeri is macrophagous, the Harpacticoida are microphagous.
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Copepoda (Harpacticoida and Cyclopoida) belong to the most abundant Italian freshwater families, Canthocamptidae and Cyclopidae, respectively. The taxa collected are species of high ecological plasticity (Jersabek et al., 2001), they are all ubiquitous in lotic habitats, widely distributed in Italy and Europe. Italian freshwater Amphipoda belong to 17 genera and 11 families. The genus Echinogammarus is abundant in Italy (13 species over 94 species recorded) (Ruffo and Stoch, 2005), the species ascribed to this genus, together with those of Gammarus and Niphargus represent more than 60% of Italian Amphipoda fauna. The last two species are common in the higher river reaches, and they are substituted by Echinogammarus in the lower reaches. Gammarus and Echinogammarus are common in lakes, in general they prefer well-oxygenated waters, and tend to colonize the rivers and lakes banks, hiding under the pebbles and stones or the hydrophitic riparian vegetation. Surface water Amphipoda play an important role in the foodweb, representing a relevant food source for fish. They can not be considered good bioindicators because they are tolerant to organic pollution, although they seem to be more sensitive to heavy metals. Italian freshwater Isopoda belong to 11 genera and 7 families, Asellidae being the family with the highest number of species (31 species, Ruffo and Stoch, 2005). Asellidae prefer lentic habitats, Asellus aquaticus is a common species in surface waters, it is abundant in northern Italy and becomes more rare along the peninsula. As for Amphipoda, Asellidae tend to concentrate along the shores and riverbanks, under the pebbles/rock, or vegetation. The two species of Isopoda and Amphipoda collected share the same role in the foodweb, both feeding on organic matter along the river shores.
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3.2.2 Hexapoda Hexapoda are, with Crustaceans, one of the dominant taxa in the sampled lakes (Fig. 3.5). They have a variety of different feeding habits. They can be predators (Odonata, some Diptera, Plecoptera, some Hemiptera), scrapers (some Ephemeroptera, Trichoptera), collectors (some Ephemeroptera, some Hemiptera), grazers (some Hemiptera). Some families as Chironomidae are widespread and use different feeding strategies occupying different trophic levels. We collected in total 4257 Hexapoda, most of which belonging to the Chironomidae family (4019 individuals). The remaining individuals were Ephemeroptera (79), Odonata (48), Trichoptera (24), Coleoptera (36), Diptera Ceratopogonidae (15). Few specimens belonged to other insect taxa. Odonata and Ephemeroptera were identified to species level.
Fig 3.5 – Percentage composition of invertebrate taxa over all lakes, and all samples.
Nematoda Acarina 0% 2% Oligochaeta Molluschi Tricladida 13% 0% Aracnida 1% 0% Crustacea Hirudinea 43% 2%
Hexapoda 39%
3.2.2.1 Odonata Odonata are one of the most easily recognizable Hexapods taxa, because of their bright colours and large size. Dragonflies and damselflies all over the world are represented by 5000 species. They depend on aquatic habitats for their life cycle, because the eggs and larval instars develop in standing a slow-flowing freshwater. Egg hatching can occur few days after oviposition, or after several months. In the latter case the eggs overwinter protected under the vegetation, and hatch in spring. A pro-larva emerges from the egg, and it lasts only few seconds or minutes before molting into a neanid. The length of larval development differs between species: it spans from one year for Zygoptera to two- three years for Anisoptara. As they grow, larvae undergo approximately 10-20 molts, over a time between 3 months and 6-10 years depending on species. Instar number is not always fixed but may depend on seasonal conditions and food supply; molts are more frequent during summer. Wing pads develop externally from the 6-7th instar. Before metamorphosis, neanids stop feeding and begins to exit the water for short periods of times. The last neanid instar can live entirely out of water, without feeding. Metamorphosis is direct without a pupal stage and emergence takes place on a fixed support out of the water, sometimes at considerable distance from the water edge, over a period of 1-2 hours. Some genus like Calopteryx, Lestes prefer the emerging stalks of water plants as a substrate to metamorphose, some others families like Gomphidae prefer stones. The newly emerged adult is not sexually mature; it will become ready for reproduction after an average period of fifteen days. During this period the immatures move away from the area where they were born, and they can reach areas far from water, but they will return to the aquatic habitat when they are ready to reproduce. During the maturation time the full adult colour develops. Teneral (new) adults can be recognised by a glassy sheen of the wings. Additional colour changes occur later in life in some species. Larval and adult stages of dragonflies and damselflies are carnivorous. The size of the prey varies according to the size of the predator. The main preys are aquatic Hexapods such as Diptera, Trichoptera, and Ephemeroptera, but small vertebrates such as tadpoles and fish fry are not immune from attack. Prey may be stalked or ambushed. Captured prey is pulled back using powerful muscles in the labium and chewed by strong mandibles. Adult Odonata are
24 ALPLAKES visually oriented hunters with exceptional aerobatic ability and extremely acute eyesight thanks to the very large eyes and the extreme mobility of the head. Many are strong fliers, and to catch them can be extremely difficult. Their fly is extremely quick and it allows them to suddenly change direction. They can also hover in the air while they are flying. In general, Anisoptera are better fliers than Zygoptera. Dragonflies and damselflies fly during the day and they prefer sunlight. Only few tropical species are active during the night. One Italian specie is active in the twilight hours. They are territorial animals, only during the night the Odonata congregate in the congregation. For example, the territories of male Calopteryx have some areas like stones or stalks, where the insect rests. The male chooses one of this sites from which it starts to hunt or fight with others males. The male territory also an area with aquatic plants, which represents the oviposition area. Odonate mating is an elaborate process. When a female enters the male territory, the male goes straight her and flexes the abdomen to show the terminal part, which is brightly coloured. The male clasps the female by the head (Anisoptera) or prothorax (Zygoptera). The pair then fly together in tandem (male in front, female behind), often to a perch. The female bends her abdomen forward and downward to form the "wheel" position and connect with the secondary genitalia on segments 2-3 of the male, which previously have been charged with sperm from the primary genital opening on segment 9. Complex sperm displacement and sperm transfer activities then occur. A mating may last from several seconds to several hours, according to species. Then the female follows the male to the oviposition area. In some species the pair lay eggs together, maintaining the tandem hold. In others the male hovers above the female while she lays her eggs. During this last operation the male surveys and protects the female and, when another male enters the territory, the “owner” stands in front of it, opens the wings and tries to chase it away. The dragonflies and damselflies have an important role in the ecosystem, because they are predators and contribute to maintain populations structure They are food for several predators. Fishes, amphibians and birds prey both larvae and adult. Other aquatic insects like Nepa feed on Odonata larvae. Some protozoa and flatworms are parasites of this genus. In this research we found several species of Odonata, especially in Levico Lake, where we recorded 15 different species at different instar stages, belonging to six families. We used kick sampling to collect larvae, and we documented the presence of adults with a camera. Species were identified according to Carchini (1983), and D’Aguilar et al. (1990). Literature data (Conci & Nielsen, 1956), report 34 species of Odonata for this area, with representatives of each of the nine known families. A brief list of the ecological and biological features of the collected species, and photographic images, are presented below.
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Family Calopterygidae
Calopteryx virgo
This specie prefers clean, running waters in cold and woodland areas. Males of this genus at sexual maturity establish a territory. Length: 3 – 3,9 cm. Widespread and common in Italy.
Calopteryx splendens s.l.
Species living both in running and still waters, it can live in polluted waters. Length: 3 – 3,9 cm. Widespread in Italy. Common and abundant.
Family Platycnemidae
Platycnemis pennipes
Species living in every standing aquatic habitat: rivers, lakes, etc. Larvae can be found under aquatic vegetation near the banks. Length 2,7 – 3,1 cm. Widespread in Italy. With Ischnura elegans it is the most common and abundant Italian species.
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Family Coenagrionidae
Pyrrhosoma nymphula
Species living in running and still waters, from lowlands to mountains up to 1200 m a.s.l.. Length: 2,5 – 2,9 cm. Widespread in Italy. Common and abundant.
Cercion lindeni
Species living in slow and still waters. Length: 2,4 – 3 cm. Widespread in Italy. Common and abundant.
Coenagrion scitulum
Species living in still and running waters, in vegetation dominated by Myriophyllum. Length: 2,2 – 2,6 cm. Widespread in Italy, at low altitudes. Common but not abundant.
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Coenagrion puella
Species living in still waters up to 2000 m a.s.l. Length: 2,3 – 3 cm. Widespread in Italy. Common and abundant.
Ischnura elegans
Species which prefers still waters, it lives from lowlands, where it can be very abundant, to 2000 m a.s.l. Length: 2,2 – 2,8 cm. Widespread in Italy except in Sicily and Sardinia. One of the most common Italian species.
Ischnura pumilio
Species living in acid waters, but it can be found also in other habitats. Length: 2,2 – 2,5 cm. Widespread in Italy. Uncommon and locally rare.
Fig 3.6 – Some pictures of damselflies taken along the banks of Levico
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Family Aeshnidae
Aeshna mixta
Species living in still or slow-running waters. The adults can be found far from the water and sometimes they can undertake true migration. Length: 4,4 - 4,9 cm. Widespread in Italy. Common but not abundant.
Anax imperator
This specie prefers still waters, but the adults can hunt far from waters. Length: 5,3 – 6,1 cm. Widespread in Italy. Common and abundant.
Family Corduliidae
Cordulia aenea
This specie prefers still waters and lives up to 1800 m elevation. The adults are great fliers and can be found far from water. Length: 3,3 – 3,8 cm. Widespread in Northern Italy. Common and abundant.
Family Libellulidae
Libellula fulva
Larvae live in still or slow waters. Length: 2,6- 2,9 cm. Widespread in Italy. Common, but not abundant.
Orthetrum cancellatum
Larvae prefer still or slow waters, but can live in rivers or peat-moors The adults can be found far from waters. Length: 3,5 – 4 cm. Widespread in Italy. Common and abundant.
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Sympetrum striolatum
This species prefers still waters and lives from lowlands to 1800 m a.s.l. Widespread in Italy. Common and abundant.
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3.2.2.2 Ephemeroptera Italian mayflies include 105 species ascribed to 27 genera and 10 families (Ruffo and Stoch, 2005). Ephemeroptera derive their name from their short adult life, which lasts from few hours to few days. The larval instars live several months but in some species they may live two to three years. Ephemeroptera are not good fliers, so they cannot fly too far from the freshwater habitats in which they live, thus limiting their colonisation ability. Only occasionally they can undergo real migrations and fly for great distances. The Ephemeroptera are the only Hexapoda with a sub- imago instar that lasts few hours and then they moult to the sexual mature adult. The nymph instars live in running and still waters, from lowland lakes to mountain streams. According to their general form and behavior they can be divided in four groups: with flat body adapted to fast flowing waters (Oligoneuridae and Heptageniidae), burrowing species (Ephemeridae, Polymitarcidae), swimming species (Siphlonuridae, Baetidae) and walking species (Potamanthidae, Caenidae, Ephemerellidae, Leptophlebidae). All mayflies feed on plant material by scraping or collecting periphyton, algae, fallen leaves at different decomposition stages. Some species belonging to the genera Cloeon, Caenis and Ephemera are adapted to live in standing water.
In this research we found 79 individuals belonging to 5 different species of Ephemeroptera, most of them in Cei and Caldonazzo lakes (Fig. 3.7, 3.8). Some of these individuals (25 Caenidae and 2 Baetidae) were too young and it was not possible to identify them to species level. We identified four different species: the Baetidae Cloeon dipterum and the Caenidae Caenis horaria, C. lactea, C. luctuosa. Both species of Caenidae had not been previously recorded from Trentino.
Fig 3.7 – Percentage distribution of all Ephemeroptera in the six lakes.
Ephemeroptera distribution
Cei Caldonazzo Garda Ledro Levico Terlago
Fig 3.8 – Percentage distribution of Ephemeroptera species over the total.
Baetidae Iuv Cloeon dipterum Caenidae Iuv Caenis horaria Caenis lactea Caenis luctuosa
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3.2.2.3 Diptera Diptera is one of the largest insect orders with more than 80 000 known species. They have two pair of wings, but the second pair is reduced to a small thin structure used to balance the first pair during flight. Some parasitic species have reduced or no wings. All Diptera have sucking mouthparts, often adapted to pierce and suck in ematophagous species. They feed on a wide variety of organic material in different decomposition stages. Some Diptera are an hazard to human health because they are vectors for diseases like malaria or yellow fever. Chironomidae are widespread and represent the most abundant class of Hexapoda in most freshwater habitats. They can tolerate large gradient of pH, salinity, depth, oxygen concentration and temperature, thus they are able to live in littoral, sub-littoral and profundal zones. Chironomidae have particular adaptation: some species (Chironominae sub-family) have haemoglobin in the hemolymph and can survive low oxygen concentration in profundal habitats. Species belonging to sub-families Ortocladinae and Tanipodinae are more common in the littoral zone. Chironomidae have been used as biomonitors for lakes, because different communities can be distinguished on the basis of lake trophic status: oligotrophic lakes are characterized mainly by free-living species with high oxygen requirements, while eutrophic lakes are dominated by tube-dwelling species which possess haemoglobin to survive anoxia.
In the sampled lakes we found a great numbers of Diptera (Fig. 3.9) (4045 individuals), belonging to two different families Chironomidae (4019) and Ceratopogonidae (15). Few individuals were adult Diptera (11).
Fig 3.9 – Example of the percentage composition of Hexapoda community in two sampled lakes
Garda Hexapoda taxa Levico Hexapoda taxa
Coleoptera Ceratopogonidae Chironomidae Baetidae Ditiscidae Chironomidae Caenidae Hemiptera Sialidae Aeschnidae Caenidae Trichoptera Libellulidae Coenagrionidae Platycnemidae Trichoptera
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3.2.2.4 Other Hexapoda taxa Other insects found in low number were Hemiptera, (mostly Corixidae), Heteroptera (Nepa cinerea), Megaloptera (Sialis sp.), Coleoptera Ditiscidae, Trichoptera, Plecoptera (Nemourella picteti) (Fig. 3.10). A brief list of the ecological and biological features of the most important among these taxa is presented below.
Plecoptera In Italy there are 157 stonefly species ascribed to 7 families with 22 genera (Ruffo and Stoch, 2005). Stoneflies are generally restricted to fresh running waters with few exceptions as Nemurella picteti, living also in standing waters, Leuctra major, adapted to hyporheic habitats and springs, and Isoperla saccai, the only Italian species known to prefer spring habitats. All Plecoptera nymphs walk on the river bottom among the detritus or under stony substrates. The adults are poor flyers and for this reason their colonization ability is rather low, and they have a relatively high number of endemic species (49 in Italy). The life span of adults varies from few days in winter-emerging species to a couple of weeks for the summer-emerging ones. The nymphs feed on a wide variety of food sources and they can be shredders, herbivore- detritivores, or predators. These last belong to the families Perlidae, Perlodidae and Chloroperlidae and predation generally occurs in mature stages while younger individuals can be herbivorous.
Fig 3.10 – Neanid of the Plecoptera Nemurella picteti
Trichoptera Italian Caddiesflies number 416 species ascribed to 20 families and 93 genera (Ruffo and Stoch, 2005). It is a rather diversified group with aquatic larvae that colonize most freshwater habitats, from high elevation to lowland running and standing waters. Several species are adapted to live in standing or slow flowing waters, thus caddiesflies may be frequent in lakes and ponds. Most caddiesfly larvae build a case around their body for protection or anchorage to the substrate, using organic and/or inorganic material as fragments of leaves, twigs, empty shells and small stones. Free-living larvae may be predators as the Rhyachophilidae, or filtering collectors as Hydropsichidae, Polycentropodidae or Philopotamidae, the last two more likely to be collected in slow-flowing springs. These taxa build tubular nets, each species with a particular shape, anchored to the substrate with the mouth open towards the current, thus feeding on the trapped organic matter or small invertebrates. Case bearing larvae are generally herbivores, feeding on algae or organic material of different texture, behaving as scrapers, shredders or collectors. The form of the case may be minute purse-like (Hydroptilidae), shell-like (Helicopsychidae), and cylindrical of 3-4 cm length (Limnephilidae).
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Water beetles Several families of Coleoptera live in standing and running waters in both larval and adult stages. Larvae breath by means of different kinds of gills or through the tegument, while the adults use air that they can store beneath the elytrae or trap between the fine hair on their body, so that they can spend considerable time under water. Adults maintain flying capacity even if they spend their whole life in the water, this is an adaptation which allows them to colonize new habitats when environmental conditions become unfavorable. Adults of the families Dytiscidae, Haliplidae and Hydrophilidae have long and hairy hind legs that they use as oars to swim. In contrast, the Dryopidae, Elminthidae, Hydraenidae and Helophoridae walk on the bottom or among submerged vegetation. Finally, Gyrinidae have a peculiar way of swimming, circling very fast and in a group on the surface of the water and they are able to see both under and above the water surface, thanks to the double structure of their compound eyes. Dytiscidae and Gyrinidae are all predators, other families generally feed on vegetation or are omnivorous.
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3.2.3 Hirudinea Hirudinea or leeches are a class of the phylum Anellida. The species of this class live mainly in freshwater, but some species live in sea water or are terrestrial. They have a long and flat body, with evident annulations. The anterior part of the body is a sucker where the mouth opens. The posterior part is also a sucker, but it is used to adhere to the substrate. Hirudinea prefer living in habitats with stones or pebbles. In lakes or ponds they can be found within 1 or 2 meters deep; only few species can be found over 20 meters deep. Hirudinea can tolerate lack of oxygen for a long time, up to three-five days. All species of Hirudinea are predators that may suck body liquids from bigger animals or swallow small preys as other benthic invertebrates.
In this work we found 180 individuals, belonging to the families Erpobdellidae (41%) and Glossiphoniidae (10%). About half of the sampled specimens were very young and thus could not be identified further. Five species were found in the studied lakes, namely Erpobdella octiculata, E. testacea and Dina lineata, belonging to Erpobdellidae; Glossiphonia complanata and Hemiclepsis marginata belonging to Glossiphonidae (Fig. 3.11).
Fig 3.11 – Glossiphonia complanata (left) and Erpobdellidae (right)
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3.2.4 Mollusca Mollusca are the second largest phylum with 110000 different species. Their main characteristic are a soft body, a shell, that some species lost during their evolution, and a muscular organ (foot) differently developed among the species. Many species feed of algae, scratching them from the substrate using a rough tongue called radula; other are filterers, especially Bivalvia. This taxon is widespread in sea water, but the classes Gastropoda and Bivalvia colonized the inland freshwaters and Gastropoda live also in terrestrial habitats. We collected 153 individuals belonging to seven different families: Bythindae (51 individuals), Lymnaeidae (2 individuals), Physidae (34 ind.), Planorbidae (12 ind.), Valvatidae (1 ind.), Viviparidae (1 ind.) belonging to Gastropoda and Dreissenidae (12 ind.) belonging to Bivalvia (Fig. 3.12). The invasion of several lakes by the Zebra Mussel has severely reduced the original populations of the bivalves Anodonta and Unio, at least in the first phase of colonization.
Fig 3.12 – Gastropod mollusc and graph of relative presence of Gasteropoda genera in the six lakes
Gastropoda genera
Bythinia nd. Lymnaea nd. Physa nd. Anisus nd. Gyraulus nd. Planorbis nd. Segmentina nd. Valvata nd. Vivparus nd.
The sampling techniques used in this research are not very suited to collect molluscs so data we analyzed data from a recent research (Dalfreddo & Maiolini, 2004) that regarded four of the lakes included in the AlpLakes project. Table 8 summarizes the results from Dalfreddo & Maiolini, 2004, comparing the change in species occurred during the last sixty years. Lake Caldonazzo was the most diversified with 31 species, followed by Levico (21). Lake Ledro had a high diversity, now endangered by level fluctuations due to hydropower abstraction.
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Table 3.5 – Present and past distribution of species in four of the six investigated lakes. N = new record, C = confirmed record, A = not confirmed record, *subfossil sample, **unpublished data, Bodon M. 2001
List of species Caldonazzo Levico Terlago Ledro Theodoxus danubialis (Pfeiffer, 1828) N Viviparus ater (De Cristofori & Jan, 1832) N N Viviparus contectus (Millet, 1813) C A Bithynia leachii (Sheppard, 1823) N Bithynia tentaculata (Linnaeus, 1758) C C C C Graziana alpestris (Frauenfeld, 1863) N Potamopyrgus antipodarum (Gray, 1843) N N Bythinella schmidtii (Küster, 1852) C C N* A** Marstoniopsis insubrica (Küster, 1853) N C N N Pyrgula annulata (Linnaeus, 1758) C Emmericia patula (Brumati, 1838) Valvata cristata Müller, 1774 C C N N Valvata piscinalis (Müller, 1774) C N N* C Valvata studeri Boeters & Falkner, 1998 A N* N* Physa (Physa) fontinalis (Linnaeus, 1758) N A** Physa (Physella) acuta Draparnaud, 1805 N N N Lymnaea stagnalis (Linnaeus, 1758) A A C* Stagnicola palustris (O.F. Müller, 1774) A Stagnicola vulnerata (Küster, 1862) N N N Galba truncatula (O.F. Müller, 1774) N C C Radix auricularia (Linnaeus, 1758) C C N A Radix peregra (O.F. Müller, 1774) C N A C Planorbis carinatus O.F. Müller, 1774 C N Planorbis planorbis (Linnaeus, 1758) A Anisus (Disculifer) vorticulus (Troschel, N* 1834) Bathyomphalus contortus (Linnaeus, 1758) C N Gyraulus (Armiger) crista (Linnaeus, 1758) C N* C Gyraulus (Gyraulus) albus (O.F. Müller, C C C C 1774) Gyraulus (Torquis) laevis (Alder, 1838) A Hippeutis complanatus (Linnaeus, 1758) N N N N Segmentina nitida (O.F. Müller, 1774) A Acroloxus lacustris (Linnaeus, 1758) C C N A** Ancylus fluviatilis O.F. Müller, 1774 N N Anodonta anatina Linné, 1758 C C A A Microcondylaea compressa Menke, 1830 A Unio mancus Lamarck, 1819 C C C Dreissena polymorpha (Pallas, 1754) C N N C Pisidium amnicum (O.F. Müller, 1774) N* Pisidium casertanum (Poli, 1791) C N N A Pisidium conventus Clessin, 1877 A Pisidium hibernicum Westerlund, 1894 A Pisidium lilljeborgii Clessin, 1886 C Pisidium milium Held, 1836 N A** Pisidium nitidum Jenyns, 1832 N N N C Pisidium obtusale Lamarck, 1818 N N A Pisidium personatum Malm, 1855 N N A** Pisidium subtruncatum Malm, 1855 N N N Sphaerium corneum (Linné, 1758) N C* A
Source: modified from Dalfreddo & Maiolini, 2004.
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3.2.5 Other invertebrates Other recorded freshwater invertebrates were Acarina, Araneae, Nematoda, Plathelminta and Oligochaeta (Fig. 3.13), the latter was most abundant in deeper waters. Tricladida are part of the phylum Plathelminta (i-e- flatworms) and colonise, with different species, both standing and running waters. The phylum Nematoda comprises about 90000 species; they are called cylindrical worms in contrast to the flat worms, on account of the general shape of their body. They have an important role in ecology because they are scavengers and feed on decomposing organic matter. Many species are parasite of animals and plants. In freshwater they live in the bottom sediments. Acarina are widespread in quite all freshwater habitat. The phylum comprises about 30000 described species, but they are estimated at least 500000 and many species are adapted to live in water (Idracnidae). Araneae are terrestrial animals but few species live near water because they preyion aquatic invertebrates. These species have developed adaptations to carry a reserve of air underwater for breathing while looking for they prey, or they capture emerging insects hidden in the leaves of aquatic vegetation. Oligochaeta belong to the phylum Annelida and they are so called because they have bristles that they use to move among the sediments. They live in every freshwater habitat: sand bottom, pebbles, submerged plants. They feed on algae and detritus, but some species are predators.
Fig 3.13 – A spider waiting for it’s prey near the water surface (left), a triclad flatworm (right)
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3.2.6 Reptiles and amphibians Amphibians derive their name from their “two lives”, as most species need water to reproduce, passing through a larval stage with aquatic respiration before becoming terrestrial adult. Their eggs have noi protective layer against desiccation, and their skin is permeable to air so they need to keep it constantly wet to avoid desiccation and promote gas exchanges, for these reasons their whole life depends on freshwater ecosystems. Reptiles are totally adapted to live on subaerial habitats and their reproduction is independent from water; however, some of them are totally adapted to live in water, as turtles or grass snakes. During the sampling campaign we recorded the presence of Trachemys scripta by visual census, which was documented by some photographic images (Fig. 3.14). This turtle is introduced from North America, it was imported as a pet animal and frequently released in the wild. Its presence in natural environments can be very impacting as it also feeds on water bird’s eggs and nestlings. The presence of reptiles and amphibians was deduced from recent literature (Caldonazzi et al. 2002) and from visual census, the list of species is reported in Table 3.6.
Table 3.6 – List of amphibians and reptiles found in bibliography and during sampling
Species Lake Year Amphibia Salamandra salamandra Caldonazzo 1991 Salamandra salamandra Cei 1990 Triturus alpestris Cei 1994 Bombina variegata Caldonazzo 1988 Bufo bufo Terlago 1992 Bufo bufo Ledro 1992 Bufo bufo Caldonazzo 1990 Bufo bufo Levico 2006 Bufo bufo Cei 1992 Bufo viridis Garda 1990 Hyla intermedia Cei 1993 Rana dalmatina Terlago 1992 Rana lessonae Levico 1988 Rana synklepton esculenta Levico 1988 Rana temporaria Cei 1994 Reptilia Lacerta bilineata Levico 1990 Lacerta bilineata Terlago 1990 Podarcis muralis Terlago 1990 Coluber viridiflavus Terlago 1990 Natrix natrix Caldonazzo 1986 Natrix natrix Cei 1990 Natrix tessellata Levico 1989-2006 Natrix tessellata Caldonazzo 1988 Natrix tessellata Terlago 1988 Trachemys scripta Levico 2006
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Fig 3.14 – Natrix tessellata, Trachemys scripta, Bufo bufo observed in Levico lake
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3.2.7 Birds The freshwater habitats are very important for some species of birds because they nest, winter or feed in these areas. The species list for the six lakes is taken from a recent study by Pedrini et al. (2005).
Table 3.7 – List of species (n = nesting, w = wintering, ow = occasionally wintering, nw = nesting and wintering). Redlist Italy CR: critically endangered; EN: in danger of extinction. Priority species in Europe (BirdLife International 2004) SPEC 1: Globally endangered; SPEC 2: endangered European species; SPEC 3: endangered non European species.
Specie Cei Cald. Garda Ledro Lev. Ter. Redlist Italy SPEC Cygnus olor n n Anser fabalis w w Tadorna tadorna ow EN Anas penelope ow ow ow Anas strepera ow ow CR 3 Anas crecca ow EN Anas platyrhynchos nw nw nw nw nw nw Anas clypeata w w EN 3 Aythya ferina w w w VU 2 Aythya nyroca ow CR 1 Aythya fuligula w w CR 3 Aythya marila ow ow 3w Clangula hyemalis ow ow Melanitta fusca w w 3 Bucephala clangula w w Mergus albellus ow ow 3 Mergus serrator ow ow Mergus merganser w w Gavia stellata ow ow 3 Gavia arctica w ow ow Tachybaptus ruficollis nw w nw Podiceps grisegena ow w ow Podiceps cristatus n n w n Podiceps auritus ow 3 Podiceps nigricollis w w Phalacrocorax carbo w w h EN EN Ardea cinerea nw w nw Casmerodius albus ow Egretta garzetta n n Nycticorax nycticorax n 3 Ixobrychus minutus n n 3 Botarus stellaris w ow EN 3 Rallus acquaticus n n n Gallinula chloropus nw n n n Fulica atra n n n n Gallinago gallinago w 3 Numenius arquata w 2 Acitis hypoleucos n n 3 Larus canus w w 2 Larus argentatus ow ow Larus michaellis w nw w Larus ridibundus w w Larus melanocephalus ow Larus minutus ow 3 Alcedo atthis nw nw nw nw 3 Motacilla flava n n n Cettia cetti n n n n Acrocephalus scirpaceus n n n Acrocephalus palustris n n n Acrocephalus arudinaceus n n n Sylvia melanocephala w Remiz pendulinus w w Emberiza schoeniclus nw
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Fig 3.15 – Left to right: Ardea cinerea, Phalacorax carbo, Aythya niroca, Podiceps cristatus, Aythya ferina
Source: Photo B. Maiolini & Bedin/ Archivio MTSN
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3.2.8 General remarks on invertebrate faunal assemblages The communities of the six lakes were considerably different. As the sampling design was not meant to be strictly quantitative, the total abundance of taxa was not used for comparison but analyses were performed using taxa richness, calculated using the highest taxonomic level of all invertebrates collected.
Fig 3.16 – Number of taxa found in the lakes
45 40 35 30 25 20 n°taxa 15 10 5 0
O CEI IC CALD LAGO GARDA LEDRO LEV R TE Lakes
As shown in figure 3.16, Levico lake had the highest number (39) of recorded taxa, followed by Caldonazzo lake with 35 taxa. The lowest number was found in lakes Ledro and Garda lakes. Ledro has frequent changes of level due to hydropower production /Fig. 24). Ledro is also the lake with the less variability of habitat along its shores. The few taxa found in Lake Garda are due to very low sampling effort respect the complexity of Italy’s largest lake.
Spatial and temporal variability was found in several occasions. From Fig. 3.17 it appears that: a) Caldonazzo lake had the highest number of taxa in CL1, the station less disturbed by human activities. The graph shows also that the main variation was among sampling points, with minor changes between dates. b) In Cei lake the number of taxa increased from June to July in every sampling point, with the exception of CEI4. c) Garda and Ledro were the lakes with the lowest number of taxa. In Garda lake the highest value of taxa richness was recorded in May, probably during thermic stratification. Also in Ledro lake the highest record is during the May sampling d) In Levico lake highest values were recorded in May, except for LV1 which had higher diversity in June. e) Terlago had a low diversity due to ample level excursions . During the last sampling in July some substrates were dry due to these variations and several terrestrial taxa were present, especially in TR2 where we found the highest diversity among the sampling points. With the exception of Crustacea, the level of identification for all other taxa was too low to allow statistical analysis and to draw conclusions on the trophic state of the lakes. Nonetheless, the information provided by these taxa are consistent with results obtained using the finer identification of Crustacea. Further identification was not in the aims of this project but the biological material that was collected and preserved in the Museum collections will be valuable for future analysis.
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18 18 Cei 16 Caldonazzo 16 14 14 12 12 10 10 taxa ° taxa
° 8
8 N N 6 6 4 4 2 2 0 0 CL1CL2CL3CL4 CEI1 CEI2 CEI3 CEI4 a) stations b) stations 03-mag 25-mag 14-giu 04-lug 24-mag 15-giu 05-lug
18 18 16 Ga r da 16 Ledro 14 14 12 12 10 10 taxa taxa ° °
8 N 8 N 6 6 4 4 2 2 0 0 GR1stations GR2 LD1 LD2stations LD3 LD4 c) 04-mag 26-mag 15-giu 05-lug d) 04-mag 26-mag 15-giu 05-lug
18 Levico 18 16 16 Terlago 14 14 12 12 10 10 taxa taxa °
° 8
8 N N 6 6 4 4 2 2 0 0 LV1 LV2 LV3 LV4 TR1 TR2 TR3 TR4 e) stations f) stations 03-mag 25-mag 14-giu 04-lug 04-mag 25-mag 14-giu 04-lug Fig 3.17 – Number of taxa per lake, station and season
In Figure 3.18 we compared the results from two different sampling techniques (kick and artificial substrates). Kick sampling was generally more efficient respect to the artificial substrates, which were sometimes accidentally lost or ruined by vandals. Artificial substrates were selective for some taxa such as Hirudinea and Mollusca, whereas bricks were very useful to collect the crayfish Orconectes limosus. On the whole the use of different techniques proved to be valuable to collect a wide variety of taxa.
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Fig 3.18 – Number of taxa sampled with kick net and artificial substrates 30 N° taxa Kick Substrate 25
20
15
10
5
0 CEI1 CEI2 CEI3 CEI4 CL1 CL2 CL3 CL4 GR1 GR2 LD1 LD2 LD3 LD4 LV 1 LV 2 LV 3 LV 4 TR1 TR2 TR3 TR4
Fig 3.19 – Ledro lake with evidence of level variations at station LD3
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3.3 Alien species
3.3.1 The zebra mussel Dreissena polymorpha (Pallas, 1771) The Zebra mussel (Dreissena polymorpha Pallas, 1771) is a bivalve mollusk native of the Ponto-Caspian and the Aral Sea basins and associated estuaries. Starting from the 18th century, this species colonized most European rivers and lakes, generally transported by commercial boats. In fact, while the larval stages are planktonic, the adult bivalves produce bissus with which they attach to any kind of hard substrate. The first appearance of D. polymorpha in Italy was in lake Garda in 1991, probably arrived attached to tourist boats previously harbored in central European lakes, thanks to its capacity of surviving exposure to air for several days. In the following years the entire lake was colonized to a depth of about 50 meters and following the Mincio, Garda’s main outlet, expanded in the Po and its main tributaries.
Fig 3.19 – Colonization of Trentino freshwater bodies by Dreissena polymorpha.
1971
first appearance of D. polymorpha in Italy was in lake Garda in 1971, probably arrived attached to tourist boats previously harbored in central European lakes, thanks to its capacity of surviving exposure to air for several days. In the following199 years the entire lake was colonized to a depth of about 50 meters and following the2 Mincio, Garda’s main outlet, expanded in the Po and its main tributaries.
Fig. 25. Colonization of Trentino freshwater bodies by Dreissena polymorpha.
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In Trentino the second lake to be colonized was Lake Ledro, near Garda and, in 1992 the species appeared in Lake Caldonazzo, occupying all suitable substrates in few years. Neighboring lake Levico was “conquered” at the end of the ‘90s and from there the zebra mussel started to colonize its outlet, the Brenta river. To date, the Zebra mussel has been recorded also in lakes Tenno and Terlago and during the present research we confirmed its presence in Lake Terlago.
Fig 3.20 – Dreissena polymorpha
3.3.2 The American crayfish Orctonectes limosus
Crayfish (Crustacea Decapoda) are the biggest living freshwater invertebrates with 540 known species worldwide, mostly concentrated in North America and Australia. Only 6 species belong to the European fauna, all within the family Astacidae, with the two genera Astacus (A. pachypus, A. astacus, A. leptodactylus) and Austropotamobius (A. pallipes, A. torrentium, A. berndhauseri). In Italy only the subspecies A. pallipes italicus is considered autochthonous and was present in all the country, probably with different subspecies that are currently being studied and identified. Populations of A. astacus are present in streams near the Austrian border. Due to their dimension, abundance and wide distribution, crayfish have been used as food by men since ancient times. Only at the end of the 19th century populations of crayfish in all Europe were severely reduced by the spreading of the crayfish pest, caused by a parasite fungi (Aphanomyces astaci), probably accidentally introduced from North America. The pest, growing pollution and habitat reduction have largely reduced European crayfish populations. Actions to stop this decline started in 1982 when Astacus astacus, Austropotamobius pallipes and Austropotamobius torrentium were mentioned in Appendix III of the Bern Convention, and in 1992 they were included in the Appendix V of the Habitat Directive (92/43/Eec). Furthermore Austropotamobius pallipes was indicated as a severely endangered species and special protected areas were designated for its protection. During the Alplakes research a consistent population of the alien species Orconetes limosus Rafinesque, 1817 was found in lake Levico and in its outlet Brenta and one individual in lake
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Terlago. We found no evidence of A. pallipes in lake Caldonazzo, where a population had indeed been present in recent years. O. limosus is native of the eastern coast of North America and first appeared in Europe at the end of the 19th century. In Italy it was found for the first time in 1991 in lake d’Iseo from where it colonized the whole Po basin. Now it is present in most areas of northern and central Italy and is rapidly colonizing new areas, thanks to its resistance to pollution, its capacity of exploiting many different food resources and its high reproductive rate.
Fig 3.19 – Orconectes limosus and Dreissena polimorpha in lake Levico
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Chapter 4 CONCLUSION
The general aim of the Interreg III B Alpine Space project ALPLAKES was to foster exhange of information regarding the sustainable use of lakes in the Alpine region. In particular the work package V aimed to build a common knowledge regarding the ecological condition of the lakes and of their shores. To meet this goal, the personnel of the Museo Tridentino Scienze Naturali prepared a sampling design that was carried out in lakes Cei, Caldonazzo, Ledro, Levico, Garda and Terlago. Further information was gathered from literature in order to produce a “snapshot” of these lakes. Though the aim of the WP5 was not strictly scientific and so identification to species level was performed only for selected taxa, nonetheless results are consistent with more detailed analyses from published long term studies. In lake Levico dragonflies and damselflies were studied in detail, as this taxon is rather promising as indicator of overall ecological quality of lakes. All Odonata species are in fact predators at all life stages and thus dependent on different preys which in turn depend on habitat heterogeneity and water quality. Follow up activities of this project appear extremely interesting. The Alps in fact are more and more frequently referred to as “the water towers of Europe” as many important rivers have their headwaters there, and the demand of water for multi- purpose uses is increasing. Many Alpine rivers and lakes suffer from water abstraction due to hydropower production, production of artificial snow, agricultural, industrial and civil uses. Land claiming for agriculture and urbanization have reduced the extension of these ecosystems, threatening Alpine biodiversity and ecosystem benefits. For all these and other reasons, the sharing of common knowledge, sustainable management guidelines and awareness of the problems is viewed as a fundamental step for the preservation of the future preservation of Alpine water resources.
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ACKNOWLEDGEMENTS
We wish to thank the personnel of the Agenzia Provinciale Protezione Ambiente of Trento for help in the field when sampling deep substrates in lakes Garda, Terlago and Ledro and for data on chemical analyses of the lakes.
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