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All issues Volume 55 (2019) Ann. Limnol. - Int. J. Lim., 55 (2019) 22 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 55, 2019
Article Number 22
Number of page(s) 16
DOI https://doi.org/10.1051/limn/2019019
Published online 15 November 2019

© EDP Sciences, 2019

1 Introduction

Water beetles are completely or partially adapted to life in freshwater (Jäch, 1998). They form an ecological group that consists of numerous families. Dytiscidae and Hydrophilidae are the most speciose families, followed by Hydraenidae, Elmidae, Scirtidae, Gyrinidae, Dryopidae, and Noteridae (Jäch and Balke, 2008).

For the most part, water beetles are not cosmopolitan; instead, most species are endemic (Sánchez-Fernández et al., 2008). The Mediterranean Basin is a hotspot of water beetle biodiversity and endemism, especially lotic ecosystems in Mediterranean peninsulas (Myers et al., 2000; Griffiths et al., 2004; Jäch and Balke, 2008). The study by Picazo et al. (2012) is one of the few to investigate the taxonomic, biological and ecological traits of water beetles in Mediterranean ecosystems. Such studies are notably lacking for eastern Mediterranean lotic ecosystems around the Balkan Peninsula.

Water beetles are often used as both bioindicators and biodiversity surrogates (Abellán et al., 2005; Eyre, 2006; Sánchez-Fernández et al., 2006, 2008; Moog and Hartmann, 2017) as they inhabit numerous types of aquatic habitats (Jäch and Balke, 2008). They are sensitive, and respond quickly, to changes in environmental conditions (Eyre et al., 1990). In particular, members of the family Elmidae are widely used as indicators of water quality and, to some extent, climate change (e.g. Eyre et al., 1993; Elliott, 2008).

Substrate type, hydrogeology and current velocity are the most important abiotic factors influencing the diversity and distribution of water beetles in lotic habitats (Bournaud et al., 1992; Eyre et al., 1993). The composition and structure of aquatic vegetation also play a role (Verberk et al., 2005; Elliott, 2008; Jäch and Balke, 2008). The distribution of some families in lotic habitats is particularly influenced by longitudinal gradients of certain factors (García-Criado and Fernández-Aláez, 1995).

The present study examined water beetles of the Dinaric Karst, which extends from northeastern Italy to Albania (Bonacci, 1987; Bonacci et al., 2009). In the northeastern part of this region lies Plitvice Lakes National Park (NP) with numerous springs, tufa barriers and barrage lakes. The lakes are a sensitive ecosystem maintained by self-biodynamic processes that form the tufa. Tufa formation strongly depends on environmental conditions, particularly the level of anthropogenic impact (Srdoč, 1985).

Water beetles of the Dinaric Karst have been studied by various researchers over the past centuries (e.g. Apfelbeck, 1894; Schlosser, 1877; Novak, 1952, 1970) but these studies have been sporadic and have focused mostly on Adephaga. Recently, Mičetić Stanković et al. (2018) surveyed water beetles of River Cetina, which is the first comprehensive study of water beetle ecology in southeastern Europe. Their earlier work identified nine Elmidae species in Plitvice Lakes NP (Mičetić Stanković et al., 2015).

The water beetles in Plitvice Lakes NP have previously been studied only as a part of the benthic community (Matoničkin and Pavletić, 1967; Habdija et al., 1994, 2004). These studies concluded that the aquatic vegetation, especially bryophytes, are biodiversity hotspots in the Park and serve as “a carrier of biodiversity of lotic habitats in the NP”. They also found that the distribution of water beetles is determined by the distribution of aquatic vegetation.

The present study in lotic habitats of Plitvice Lakes NP aimed to describe the ecological traits, various population characteristics and longitudinal distribution of benthic water beetle assemblages in selected habitats. We expected to find that (i) most species would show a narrow distribution, (ii) the distribution would depend on longitudinal gradients of ecosystem characteristics, and (iii) the water beetle populations described here would show potential for assessment of water quality in lotic habitats in southeastern Europe. Additionally, we investigated in detail the biological and ecological traits of Elmis bosnica Zaitzev, 1908, which in Europe is restricted to the Balkan Peninsula and whose ecology is poorly understood (Jäch et al., 2016; Mičetić Stanković et al., 2015, 2018).

2 Material and methods

2.1 Study area

This study of benthic water beetles was conducted during the period from February 2007 to January 2008 in Plitvice Lakes NP, which has a surface area of 29,482 ha and is located in the Dinaric continental sub-ecoregion (PPNPJ, 1984). An exceptional feature of this area that has drawn international interest is the coming together of water in the form of lakes and waterfalls, together with tufa barriers that transform the river valley into a cascade of 16 picturesque barrage lakes (PPNPJ, 1984; Srdoč, 1985). This area was designated as a national park in 1949 and recognized as a UNESCO World Heritage site in 1979. The barrage lakes are supplied with water primarily from the River Matica, formed from the confluence of two short mountain rivers, Bijela rijeka and Crna rijeka. The River Matica has an average flow of 2.42 m3 s−1 and width of 7 m (Biondić and Barbalić, 2004). The barrage lake system begins with Lake Prošće, which has a surface area of 68.2 ha and maximum depth of 37.4 m, and it ends with Lake Novakovića Brod, which has a surface area of 0.40 ha and maximum depth of 4.5 m (Petrik, 1958). The lowest site represents the end of the barrage lakes and forms the beginning of the river Korana (Riđanović, 1994).

The geological bed inside the catchment area is composed of carbonates and dolomites, which form a cavernous shallow karst rich in springs and streams (Matoničkin and Pavletić, 1967). The climate alternates among moderately warm, rainy and snowy forest above 500 m a.s.l. (Makjanić, 1971/72). During the study period, annual precipitation was 1661 mm, with a minimum of 12 mm in April and maximum of 228 mm in October (Meteorological and Hydrological Institute of Croatia; www.meteo.hr). The greatest precipitation occurs during the autumn and winter months, when the air temperature can fall to −25 °C. In summer, the air temperature can be above 30 °C (Makjanić, 1971/72; Poje, 1989).

In order to investigate water beetles inhabiting “a carrier of biodiversity of lotic habitats in the Park” (Matoničkin and Pavletić, 1967; Habdija et al., 1994, 2004), the present study covered different areas of the lake system. The following 10 sites were sampled, including 12 microhabitats with aquatic vegetation (Fig. 1, Tab. 1):

  • Upper sites with rheocrene springs, and downstream sections of the small mountain rivers Bijela rijeka and Crna rijeka.

  • Tufa barriers: Labudovac, Kozjak-Milanovac and Novakovića Brod.

  • Lower sites with tufa deposits at the end of the barrage lakes: the Plitvica stream and the river Korana.

thumbnail Fig. 1

Position of Plitvice Lakes NP in Croatia. (b) Sampling sites in Plitvice Lakes NP. 1: Spring of the Bijela rijeka (SBR), 2: Upper reach of the Bijela rijeka (URBR), 3: Spring of the Crna rijeka (SCR), 4: Middle reach of the Crna rijeka (MRCR), 5: Lower reach of the Crna rijeka (LRCR), 6: Tufa barrier Labudovac (TBLB), 7: Tufa barrier Kozjak-Milanovac (TBKM), 8: Tufa barrier Novakovića Brod (TBNB), 9: River Korana in village of Korana (RK), 10: Plitvica stream (PS). *Sites from 6 to 8 are also presented in lateral profile because they are located at barriers between adjacent lakes.
Table 1

Characteristics of the sampling sites in Plitvice Lakes National Park. Abbreviations: SBR: Spring of the Bijela rijeka, URBR: Upper reach of the Bijela rijeka, SCR: Spring of the Crna rijeka, MRCR: Middle reach of the Crna rijeka, LRCR: Lower reach of the Crna rijeka, TBLB: Tufa barrier Labudovac, TBKM: Tufa barrier Kozjak-Milanovac, TBNB: Tufa barrier Novakovića Brod, PS: Plitvica stream, RK: river Korana in the village of Korana; A: angiosperms, B: bryophytes, p: pebbles, s: stones, tc: tufa chunks.

2.1.1 Sampling and identification of water beetles

Benthic water beetles were sampled monthly during the study period using a Surber sampler (25 × 25 cm) in all microhabitats with aquatic vegetation, except at the Lower reach of the Crna rijeka, where greater water depth required the use of a hand net. The same areas were sampled every month. The Surber and hand nets had a mesh size of 500 μm. Altogether 144 samples were analyzed, and the number of individuals was calculated for an area of 1 m2. Specimens were identified to the lowest possible taxonomic level using the following literature: Janssens (1965), Olmi (1976), Berthélemy (1979), Franciscolo (1979), Jäch and Brojer (2006), Pirisinu (1981). When necessary, specimens were identified by comparison with specimens held in the World Water Beetle Collection and Research Centre at the Natural History Museum in Vienna. Females of Elmis (Elmidae) and Helophorus (Helophoridae) could not be identified to species level, nor could most larvae. Voucher specimens of water beetles are housed in the Croatian Natural History Museum.

2.1.2 Abiotic and biotic environmental parameters

Abiotic and biotic parameters were analyzed at all 10 sites, always at the same location within the site and at the same time of day. The following physical and chemical properties of water were measured: pH (with pH meter WTW pH 330), water temperature, dissolved oxygen concentration and oxygen saturation (with WTW Oxi 330/SET oximeter), alkalinity (by titration with 0.1 M HCl), conductivity (with WTW LF 330 conductivity meter), current velocity (with P-670-M velocimeter), water depth (with hand-held meter) and nutrients [ammonium, by HRN ISO 70-3:1998 method; nitrate plus nitrite nitrogen (NO3-NO2), by HRN ISO 7890-3:2001 method; and orthophosphates, by HRN ISO 6878:2001 method]. Aquatic vegetation was identified according to the following literature for identification of aquatic bryophytes and aquatic angiosperms: Atherton et al. (2010), Casper and Krausch (2008a,b), Frahm and Frey (2004), Frey et al. (2006), Pavletić (1968), Smith (2004). For each sampling site, the geographical coordinates were recorded using a GPS (Garmin Oregon 550) and processed in ArcGIS software.

2.1.3 Data analysis

Traits of benthic water beetles in Plitvice Lakes NP were analyzed in terms of (1) population aspects [species richness, abundance, seasonal dynamics and adult/larvae ratio (Ad/Lv)], (2) ecological aspects (biogeography and preferences for current velocity, water temperature, pH, alkalinity, oxygen, nutrients, conductivity, water depth and vegetation type), and (3) longitudinal distribution as described by Moog and Hartmann (2017). The percentage of water beetle abundance was calculated for each biocoenotic zone (Crenon-Rhithron-Potamon Concept). Biogeographical analysis was conducted according to Nilsson (2003, 2015), Fikáček et al. (2015), Jäch and Skale (2015), and Jäch et al. (2016), while zoogeographical categorization was conducted according to Vigna Taglianti et al. (1999) and Darilmaz et al. (2012). Species richness was calculated for each microhabitat. Pairwise dissimilarity between microhabitats was measured using non-metric multidimensional scaling analysis (NMDS) based on a Bray-Curtis similarity matrix (Zuur et al., 2007). A general linear model (GLM) was used to test the significance of variation among the sampling sites, classified as lower sites (KR, PS), barriers (TBNB, TBLB, TBKM), upper sites (MRCR, LRCR, URBR) and springs (SBR, SCR). Month was used as a random factor due to temporal pseudo-replication (Hurlbert, 1984), and multiple comparisons were performed using the post hoc Scheffe test.

Analyses were conducted using water beetle assemblages as the dependent variable and physical and chemical properties of water as independent variables. On the microhabitat scale, relationships of environmental factors (water velocity and depth) to annual mean density of water beetles were analyzed using Spearman's rank correlation coefficient (ρ). This analysis was performed separately for adults and for larvae. Prior to the correlation analysis, normality tests were performed for all data using the D'Agostino's K-squared test and the Kolmogorov-Smirnov (K-S) test. Canonical correspondence analysis (CCA) was used to estimate response of water beetle abundances to environmental variables, and results were assessed for significance using the Monte Carlo permutation test (with 999 permutations). Abundances of both larvae and adults were used. Biological data were log-transformed prior to analysis, while physical and chemical data were normalized. Analyses involved approximately 22 species and nine physical and chemical parameters at 12 microhabitats. A full draftsman's plot excluded orthophosphates and nitrites. Analyses were performed using SPSS 17.0 (SPSS Statistics, 2008) and CANOCO for windows software package ver. 5.0 (Ter Braak and Šmilauer, 2012). Figures were created using Adobe® Illustrator® CS6.

3 Results

3.1 Faunal assemblages and longitudinal distribution

A total of 13,675 individuals were collected belonging to seven families, 13 genera, and at least 22 species, 19 of which were named. Overall, the family Elmidae was the most diverse family with nine species (Tab. 2).

The lowest number of species was recorded in the spring of the Crna rijeka (SCR). The highest number of species was recorded in the Plitvica stream (PS). Elmidae and Scirtidae were most abundant, while Dytiscidae and Gyrinidae were least abundant. Elmis bosnica was dominant in all microhabitats of the upper sites, except at the lower reach of Crna rijeka, where Hydraena melas was dominant (Tab. 2). Water beetles were more abundant at tufa barriers than at all the other sites sampled. The most abundant water beetles were Riolus subviolaceus, R. cupreus and larvae of the family Scirtidae.

The highest number of water beetle species was found during four months (February, March, June, and July), while the lowest number was encountered in January. During all months of the study, we detected six elmid species; Hydrocyphon deflexicollis (Müller, 1821), which we identified based on adult specimens caught in the emergence traps positioned in sampled habitats; and other unidentified individuals of the family Scirtidae. Scirtidae pupae and five species (e.g. Laccobius striatulus and Oulimnius tuberculatus) were found only in one month (Tab. 3). Overall, the highest number of individuals was recorded at tufa barriers during the winter months (Fig. 2).

The Ad/Lv ratio differed greatly among species (Tab. 2), though it consistently showed a bias in favor of larvae (Fig. 2), especially among Elmidae (Limnius volckmari Ad/Lv = 0.113, Riolus species Ad/Lv = 0.286, Esolus parallelepipedus Ad/Lv = 0.074). Pupal stages of families Elmidae and Scirtidae were also found. Elmidae pupae were recorded during four months (January, June, August and November), while Scirtidae pupae were recorded only in June (Tabs. 2 and 3).

In the NMDS plot with a stress value of 0.09, microhabitats clustered into two groups: one contained upper sites, while the other contained the tufa barriers, Plitvica stream and Korana rijeka (Fig. 3). MGLM confirmed these results, showing significant differences between microhabitats at the barriers (TBKM, TBLB, TBNB) and microhabitats in the Bijela rijeka and Crna rijeka (barriers − springs: p = 0.007; barriers − upper sites: p = 0.002; p ≤ 0.05).

The longitudinal distribution of benthic water beetles in Plitvice Lakes NP is shown in Figure 4. The highest proportion of crenal species was recorded in springs, while littoral species reached their highest proportion in the Bijela rijeka. Along the length of the Crna rijeka, the proportion of crenal species decreased while the proportion of rhithral and potamal species increased. Rhithral species made up the highest proportion at the other sites sampled.

Table 2

Taxonomic list, abundance, species richness and distribution of larval and adult stages of water beetles in Plitvice Lakes NP from February 2007 to January 2008. Abbreviations: Lv.: larval stage, Ad.: adult stage; S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. Sampling sites are abbreviated as in Table 1.

Table 3

Seasonal dynamics of water beetles at 12 microhabitats from February 2007 to January 2008 in Plitvice Lakes NP.

thumbnail Fig. 2

Temporal variation in abundance of water beetles and overall adult/larvae ratio from February 2007 to January 2008 in Plitvice Lakes NP.
thumbnail Fig. 3

NMDS analysis of microhabitats in Plitvice Lakes NP from February 2007 to January 2008. Abbreviations: S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. For locality abbreviations, see Figure 1.
thumbnail Fig. 4

Longitudinal distribution of water beetles in Plitvice Lakes NP. Abbreviations of biocoenotic regions: EUC: Eucrenal, HYC: Hypocrenal, ER: Epirhithral, MR: Metarhithral, HR: Hyporhithral, EP: Epipotamal, MP: Metapotamal, LT: Littoral. For locality abbreviations, see Figure 1.

3.2 Biogeographical analysis of water beetles and population dynamics of Elmis bosnica

The biogeography of the identified benthic water beetles in Plitvice Lakes NP is shown in Figure 5. Biogeographical analysis showed dominance of the European chorotype in water beetle assemblages, which comprised mainly typical southeastern and Mediterranean species. The lowest proportion was recorded for Balkan chorotypes and widespread species.

The phenology and Ad/Lv ratio of Elmis bosnica in the Bijela rijeka and Crna rijeka are presented in Figure 6. The Ad/Lv ratio of the species differed greatly among the microhabitats of these rivers. The difference was especially evident when only spring microhabitats with bryophytes were compared. From August to October and from May to July, larvae were considerably more abundant than adults at sampling site SCR S3, while the converse was true at sampling site SBR S3.

Spatial variation in abundance was recorded both for larvae and adults of Elmis bosnica in the Bijela rijeka. Adults were more numerous in bryophytes than angiosperms at all microhabitats. The abundance of both life stages decreased along the length of the Crna rijeka. Larval stages were more frequent there than adults, especially at the downstream site LRCR, where only larvae occurred during four months of the study (April, May, June and November) (Tab. 2, Fig. 6).

thumbnail Fig. 5

Biogeography of identified water beetles in Plitvice Lakes NP. Abbreviations of biogeographical chorotypes: AE: Asiatic; B: Balkan; BT: Balkano-Turanian; CAE: Centralasiatic-European; E: European; TE: Turano-European; TEM: Turano-Europeo-Mediterranean.
thumbnail Fig. 6

Seasonal dynamics and adult/larvae ratio of Elmis bosnica in the Bijela rijeka and the Crna rijeka from February 2007 to January 2008 at: a) springs and b) along the watercourse. Abbreviations: Ad.: adult stage, Lv.: larval stage; S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. For locality abbreviations, see Figure 1.

3.3 Environmental characteristics and water beetles

The aquatic vegetation sampled in the microhabitats included bryophytes (seven species) and angiosperms (two species) (Tab. 2). The highest species richness of plants was recorded at the tufa barrier Kozjak-Milanovac.

Elmis bosnica had its highest abundance in the bryophyte community consisting of Cinclidotus aquaticus and Platyhypnidium riparoides. Limnius volckmari preferred the angiosperm Apium repens. Hydraena melas was recorded in both bryophytes and angiosperms. All three species of Riolus were most abundant in a community that consisted of four bryophyte species. Individuals of the family Scirtidae were most abundant in communities of Hygroamblystegium fluviatile and H. tenax var. tenax (Tabs. 1 and 2).

The ranges of measured environmental variables are presented in Table 1. GLM analysis indicated significant differences among sampled sites in the following physical and chemical properties of water: water temperature (barriers − springs: p ≤ 0.0005, barriers − upper sites: p ≤ 0.0005, upper sites − lower sites: p = 0 0.005, p ≤ 0.05), oxygen concentration (springs − upper sites: p = 0.022, p ≤ 0.05), oxygen saturation (barriers − springs: p = 0.002, p ≤ 0.05, springs − lower sites: p ≤ 0.0005), pH (barriers − springs: p ≤ 0.0005, barriers − upper sites: p = 0.002, p ≤ 0.05, springs − lower sites: p ≤ 0.0005), conductivity (barriers − springs: p ≤ 0.0005, barriers − upper sites: p ≤ 0.0005, springs − lower sites: p ≤ 0.0005, springs − upper sites: p ≤ 0.0005), alkalinity (barriers − springs: p ≤ 0.0005, barriers − upper sites: p ≤ 0.0005, springs − lower sites: p = 0.001, p ≤ 0.01, upper sites − lower sites: p ≤ 0.0005), nitrates (barriers − springs: p ≤ 0.0005, barriers − lower sites: p = 0.055, p ≤ 0.05, barriers − upper sites: p ≤ 0.0005), velocity (barriers − springs: 0.0028, p ≤ 0.01, barriers − upper sites: 0.009, p ≤ 0.01) and water depth (barriers − upper sites: 0.025, p ≤ 0.05). Based on Spearman's correlation coefficient, Hydraena melas and H. subintegra annual mean density correlated positively with current velocity at microhabitat URBR S2 (ρ = 0.651, p = 0.041, N = 10; p ≤ 0.05). Scirtidae correlated positively with water depth at SBR S2 (ρ = 0.711, p = 0.021, N = 10; p ≤ 0.05) and URBR S2 (ρ = 0.793, p = 0.006; p ≤ 0.01, N = 10) but negatively at TBKM S3 (ρ= −0.655, N = 10; p ≤ 0.05). Larval annual mean density correlated negatively with water depth for Elmis bosnica at URBR S3 (ρ = −0.722, p = 0.018, N = 10; p ≤ 0.05) as well as Riolus subviolaceus and R. cupreus at TBKM S3 (ρ = −0.754, p = 0.012, N = 10; p ≤ 0.05).

CCA eigenvalues for the first two axes were 0.541 and 0.157, accounting for 83.1% of the variance in the species-environment relationship. The Monte Carlo permutation test showed that the ordination was significant (first axis: F-ratio = 18.212, p = 0.0020; overall: trace = 0.839, F-ratio = 3.419, p = 0.0020). The first canonical axis strongly correlated with nitrates (R 1 = 0.6979) and ammonium ions (R 1 = 0.6923). Axis 2 showed the highest correlation with water depth (R 2 = 0.4143). Based on the ordination plot (Fig. 7), Oulimnius tuberculatus, Esolus parallelepipedus and all three species of Riolus showed the strongest correlation with current velocity, water temperature and oxygen saturation. Hydraena melas, H. subintegra, H. riparia, Elmis bosnica and Limnius volckmari showed the strongest correlation with conductivity and water depth. Alkalinity was the most significant factor for Elmis aenea, E. rioloides, Ochthebius metallescens, Laccobius striatulus and Scirtidae.

thumbnail Fig. 7

Canonical correspondence analysis of water beetles in Plitvice Lakes NP. Abbreviations: Elm_a_r: Elmis aenea/rioloides, Lim_vol_sp: Limnius volckmari/sp., Riol_cup_sub: Riolus cupreus/subviolaceus. Other taxa are abbreviated as in Table 2.

4 Discussion

Water beetles are one of the most studied insect groups in the western Mediterranean, especially in southeast Spain (e.g. Ribera, 2000; Abellán et al., 2005; Sánchez-Fernández et al., 2006, 2008). We are unaware of similar studies of water beetles in the eastern Mediterranean, with the exception of the work by Darilmaz et al. (2012) on zoogeography of water beetles in northern Turkey. The present study presents the first comprehensive investigation of population aspects and ecological traits of water beetles in oligotrophic hydrosystems with tufa formation in southeastern Europe. The results of this study, many of which are the first to be reported for water beetles, can help guide further investigations of these animals and their ecology in oligotrophic hydrosystems in the eastern Mediterranean.

4.1 Faunal assemblages and longitudinal distribution

Previous investigations of the water beetles in Plitvice Lakes NP were conducted sporadically (Matoničkin and Pavletić, 1967; Matoničkin et al., 1971), and the present study identified 11 species not previously reported in the NP. In this area, species richness of water beetles appears to be as high as that of other benthic insects (see Kučinić and Malicky, 2002; Popijač and Sivec, 2009; Ivković et al., 2010, 2012, 2014; Previšić et al., 2010, 2013; Vilenica et al., 2014).

The genus Elmis dominated at all sites sampled, except in the lower reach of the Crna rijeka, where the slower current and dense angiosperms favor the detritophilous Hydraena melas (Jäch et al., 2005). We detected only E. bosnica in the spring areas of the Bijela rijeka and Crna rijeka, in contrast to a previous study of freshwater habitats in Plitvice Lakes NP (Matoničkin and Pavletić, 1967), which detected Elmis maugetii in the spring areas of both rivers. This earlier result is therefore doubtful (see Mičetić Stanković et al., 2015), especially since these two species are difficult to distinguish. Furthermore, the present study revealed a wider distribution of the genus Hydraena throughout Plitvice Lakes NP than previously recorded (Matoničkin and Pavletić, 1967; Matoničkin et al., 1971).

The distribution of benthic water beetles along a river follows a longitudinal gradient, reflecting the changes in habitat (Berthélemy, 1964; Brojer et al., 2017). The present results showed the same tendency: the species richness of water beetles increased with distance from the spring area. Species with a narrow distribution range prefer upper sites, while widely distributed species, especially of the European chorotype, prefer lower sites and tufa barriers. Our results are consistent with the idea that the genus Elmis is a good indicator of stream zonation, as suggested by Bournaud et al. (1992): we found Elmis bosnica only in upper sites, in accordance with the hypothesis that it is the only Elmis species in springs and spring areas of the Dinaric Karst (Mičetić Stanković et al., 2015, 2018). Conversely, spring areas in Austria and Central Europe are inhabited with three Elmis species: E. aenea, E. latreillei (Bedel, 1878) and E. rietscheli Steffan, 1958 (Brojer et al., 2017). E. aenea and E. rioloides show similar traits both in the Plitvice Lakes NP (present study) and in the River Cetina (Mičetić Stanković et al., 2018). The highest abundance of these lotic species was recorded at high-flow sites distant from spring areas. The rhithral features of both species have also been noted in rivers and streams in other parts of Europe (e.g. Olmi, 1976; Hebauer, 1994a,b; Eyre et al., 2006).

Most water beetle species in Plitvice Lakes show a narrow distribution, and are present elsewhere in southeastern Europe and the Middle East (Nilsson, 2003, 2015; Fikáček et al., 2015; Jäch and Skale, 2015; Jäch et al., 2016). This is consistent with Croatia's position in southern Europe.

4.2 Temporal dynamics of the Ad/Lv ratio and Elmis bosnica abundance

Previous studies showed that water beetle species richness increases in the summer and decreases during the winter (Nilsson, 1996; Giller and Malmqvist, 1998). The present study showed seasonality of abundance and species richness, but the two variables peaked at different periods of the year. Species composition caused seasonal dynamics to differ between adults and larvae. For instance, Hydraenidae lay their eggs in spring and early summer (Hansen, 1996), which could contribute to the observed peak in species richness in March. The fact that Hydraenidae are mostly terrestrial, at the larval stage (Olmi, 1976; Hansen, 1996), may contribute to the observed lower overall species richness in winter. The results of the present study confirmed that the life stages of Elmidae overlap during a one-year cycle (Berthélemy and De Riols, 1965; Dietrich and Waringer, 1999; Elliott, 2006). Additionally, the present study found that Elmis adults were most abundant from May to August, while Elmis larvae dominated in autumn and winter, which concurs with studies by Berthélemy and Ductor (1965) and by Dietrich and Waringer (1999).

The seasonal dynamics of Limnius volckmari in the present study are similar to those described by Maitland (1967). Nilsson (1996) found that adults of Elmidae emerged in early summer after the pupation of overwintering larvae, and that oviposition took place in summer, such that higher numbers of small larvae were recorded during late summer and early autumn.

Our study found different seasonal dynamics for specimens of the family Scirtidae between the upper sites and other sites sampled. The Scirtidae recorded from the upper sites (mainly Elodes) show the same winter-only presence as described by Cuppen (1993). At other sites in our study, Scirtidae (mainly Hydrocyphon deflexicollis) were present throughout the year. This difference may reflect warmer water temperatures and/or more plentiful food in downstream areas than in organically depleted spring areas, which should be explored in further studies. The stably favorable conditions in downstream areas may support development of numerous scraper and collector-gatherer larvae of this family.

Matoničkin and Pavletić (1967) recorded a significant decrease in the number of adults of Elmis bosnica, which they misidentified as “E. maugetii”, during the winter months in the Crna rijeka, which was also the case in the present study. In the Bijela rijeka, in contrast, this species was detected throughout the year. This difference, which has also been reported for Diptera at the same sites (Ivković et al., 2015), may be due to differences in flow permanence and current velocity during the study period. For instance, flow permanence and current velocity varied more in the spring of Crna rijeka than in the spring of the Bijela rijeka. Furthermore, the spring of the Crna rijeka is shaded by dense coniferous forest, while the spring of the Bijela rijeka is unshaded, with dense aquatic vegetation (Ivković et al., 2015). The spring of the Bijela rijeka thus appears to provide conditions more favorable for water beetles than the spring of the Crna rijeka. Indeed, Giller and Malmqvist (1998) and Erman (2002) stressed canopy coverage as a major environmental determinant of the composition of benthic communities in rivers and streams. The present study showed that Elmis bosnica adults prefer bryophytes, which are preferred by other Elmis species as well (Berthélemy, 1966).

4.3 Environmental characteristics and water beetles

Comparison of the physico-chemical characteristics of the water in Plitvice Lakes NP between the present study and the 1960s (Petrik, 1961; Matoničkin and Pavletić, 1967) confirms an increase in anthropogenic pressure in the Park. Those studies in the 1960s already showed that tourism had led to nutrient enrichment (ammonium ion concentration) in the NP, especially in the Crna rijeka. The results of the present study highlight the substantial increase in anthropogenic pressure on the NP through tourism, reinforcing the need to balance economic growth with sustainability (Mužinić and Filipović, 2006).

Elodes sp. showed a distribution pattern throughout the Plitvice Lakes NP similar to that of Elmis bosnica, while Hydrocyphon deflexicollis showed a distribution similar to that of larvae of Riolus subviolaceus and R. cupreus. These habitat preferences may reflect larval morphology (Elliott, 2008). Elodes sp. and larvae of E. bosnica have broadly flattened bodies and prefer habitats in upper sites with abundant moss cover on a solid riverbed, in contrast to H. deflexicollis and Riolus species, which have a cylindrical body shape and prefer tufa barriers with tufa chunks and associated mosses.

Vegetation type and structure highly influenced water beetle assemblages throughout the Park, as angiosperms increase beetle species richness more than bryophytes do. Angiosperms increase habitat complexity and therefore the diversity of benthic invertebrates (Giller and Malmqvist, 1998, Mičetić Stanković et al., 2018). Our finding of high abundance of water beetles at the tufa barriers, especially Kozjak-Milanovac, where aquatic vegetation was also most diverse (four bryophyte species), may be explained by the water quality as well as by dense and diverse moss cover. The water that pours over the tufa barrier from Lake Kozjak to Lake Milanovac is organically enriched because it originates in the epilimnion layer. This provides favorable conditions for the development of a rich phytobenthos layer on the surface of bryophytes. Indeed, Plenković-Moraj et al. (2002) already reported the dominance of diatoms (Bacillariophyceae) in the tufa barriers in Plitvice Lakes NP. This environment should also provide optimal conditions for scraper and collector-gatherer Riolus species, since diatoms are the preferred food of Riolus subviolaceus (Beier, 1948; Jäch, 1982). This likely explains why R. subviolaceus and R. cupreus dominated in the tufa barriers in the present study.

Esolus and Limnius in our study preferred vegetation growing on riverbeds formed of coarse sediment particles over vegetation growing on riverbeds formed of solid stones. This contrasts with the preference of Elmis, which is consistent with the study by Elliott (2008).

Our analysis confirms several previously reported water beetle habitat preferences, such as the preference of Elmis aenea for alkaline water (Eyre et al., 1993; Mičetić Stanković et al., 2018). It also confirms published preferences of Esolus parallelepipedus, Riolus subviolaceus and R. cupreus for high oxygen content and fast current (Bournaud et al., 1992; Hebauer, 1994a; Dietrich and Waringer, 1999). It supports the eurytopic character of E. parallelpipedus (García-Criado et al., 1999), which we detected at upper sites, tufa barriers and lowest sites. The published preference of R. subviolaceus and Hydraena minutissima for calcareous substratum (García-Criado et al., 1999) likely explains why these species were absent from upper sites without tufa deposits in our study. Hydraena gracilis preferred high alkalinity in our study, in agreement with work by Eyre et al. (1993). In our study, Hydraena minutissima was recorded only in substrates with bryophytes, consistent with its preference for mountain springs, rivers and streams, and the presence of Fontinalis bryophytes (Pirisinu, 1981; Hebauer, 1994a; Klausnitzer, 1996). Hydraena riparia, which is widely distributed throughout the Palearctic Region (Jäch and Skale, 2015), showed a preference for moderate current velocity and angiosperms in our study, consistent with results from Bournaud et al. (1992). Helophorus brevipalpis strongly preferred angiosperms in the riparian zone in our study, consistent with other work (Bournaud et al., 1992; Eyre et al., 1993; Hebauer, 1994a) but in contrast to one analysis suggesting a eurytopic character for this species (Foster et al., 2014).

While supporting numerous aspects of the literature on water beetle habitat preferences, our study also substantially extends the literature with some first insights. Our results suggest that Elmis aenea and E. rioloides prefer shallower water depth, and that E. bosnica is bryophilous and prefers low water temperatures (Mičetić Stanković et al., 2015, 2018). Our results further suggest that the poorly studied Hydraena subintegra, endemic to the Balkan Peninsula (Jäch and Skale, 2015), prefers deeper water with higher conductivity and slower current. Individuals of the family Scirtidae in Plitvice Lakes NP appear to favor deeper, alkaline water and fast current, consistent with previous studies (Bournaud et al., 1992; Cuppen, 1993). Elodes sp. shows a preference for mountainous lotic habitats, especially the Bijela rijeka, which has an open canopy (Ivković et al., 2015). On the contrary, Hydrocyphon deflexicollis seems to prefer tufa barriers, which have a cavernous structure and fast current. Our study suggests that the distribution of Limnius volckmari can depend on water depth and conductivity, in contrast to the suggestion of Maitland (1967). Further studies should explore whether this discrepancy is true or reflects the influence of other variables, such as biotic interactions.

In conclusion, the present study is the first comprehensive analysis of population aspects and ecological traits of water beetles in specific karst habitats. Benthic water beetles, especially Elmidae, may be useful as environmental descriptors because their composition and distribution are strongly influenced by nutrients and water depth, as well as other abiotic and biotic factors. The extreme sensitivity of Elmis bosnica to environmental conditions means that this species should be included in conservation and protection programs at spring areas in southeastern Europe. Permanent conservation programs are needed to protect these unique habitats.

Acknowledgements

This comprehensive study in Plitvice Lakes NP was conducted with the permission of the Ministry of Environmental and Nature Protection of the Republic of Croatia (RN: 532-08-02-1/7-06-3; 532-08-02-1/7-06-3). The authors would like to thank Andreja Komljenović, Martina Krbavčić, Sanja Žalac, Bruno Polak, Matija Šimac and Prof. Zlatko Mihaljević for their indispensable assistance during the field investigations. Many thanks are due to Mr. Ivančica Krulik, Mirjana Jelenčić and Sanja Sviben for help with sorting the collected material. We are grateful to Michaela Brojer (Naturhistorisches Museum Wien, Austria) for assistance with the identification of certain specimens, and to Prof. Antun Alegro for help with the identification of aquatic vegetation. We thank Dr. Gabor Várbíró and Dr. Debarshi Dey for help in statistical analysis. We thank Dr. Anita Belančić for literature loan. We are very grateful to Dr. Adrian C. Pont (Oxford University Museum of Natural History, UK) and Dr. Bradley Sinclair (Canadian National Collection of Insects and Ottawa Plant Laboratory − Entomology Canadian Food Inspection Agency) for proofreading the manuscript. The study is a result of projects No. 119-1193080-1206 (PL: M. Kučinić) and No. 119-1193080-3076 (PL: M. Kerovec) supported by the Croatian Ministry of Science, Education and Sports.

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Cite this article as: Mičetić Stanković V, Jäch MA, Ivković M, Stanković I, Kružić P, Kučinić M. 2019. Spatio-temporal distribution and species traits of water beetles along an oligotrophic hydrosystem: a case study. Ann. Limnol. - Int. J. Lim. 55: 22.

All Tables

Table 1

Characteristics of the sampling sites in Plitvice Lakes National Park. Abbreviations: SBR: Spring of the Bijela rijeka, URBR: Upper reach of the Bijela rijeka, SCR: Spring of the Crna rijeka, MRCR: Middle reach of the Crna rijeka, LRCR: Lower reach of the Crna rijeka, TBLB: Tufa barrier Labudovac, TBKM: Tufa barrier Kozjak-Milanovac, TBNB: Tufa barrier Novakovića Brod, PS: Plitvica stream, RK: river Korana in the village of Korana; A: angiosperms, B: bryophytes, p: pebbles, s: stones, tc: tufa chunks.

In the text
Table 2

Taxonomic list, abundance, species richness and distribution of larval and adult stages of water beetles in Plitvice Lakes NP from February 2007 to January 2008. Abbreviations: Lv.: larval stage, Ad.: adult stage; S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. Sampling sites are abbreviated as in Table 1.

In the text
Table 3

Seasonal dynamics of water beetles at 12 microhabitats from February 2007 to January 2008 in Plitvice Lakes NP.

In the text

All Figures

thumbnail Fig. 1

Position of Plitvice Lakes NP in Croatia. (b) Sampling sites in Plitvice Lakes NP. 1: Spring of the Bijela rijeka (SBR), 2: Upper reach of the Bijela rijeka (URBR), 3: Spring of the Crna rijeka (SCR), 4: Middle reach of the Crna rijeka (MRCR), 5: Lower reach of the Crna rijeka (LRCR), 6: Tufa barrier Labudovac (TBLB), 7: Tufa barrier Kozjak-Milanovac (TBKM), 8: Tufa barrier Novakovića Brod (TBNB), 9: River Korana in village of Korana (RK), 10: Plitvica stream (PS). *Sites from 6 to 8 are also presented in lateral profile because they are located at barriers between adjacent lakes.
In the text
thumbnail Fig. 2

Temporal variation in abundance of water beetles and overall adult/larvae ratio from February 2007 to January 2008 in Plitvice Lakes NP.
In the text
thumbnail Fig. 3

NMDS analysis of microhabitats in Plitvice Lakes NP from February 2007 to January 2008. Abbreviations: S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. For locality abbreviations, see Figure 1.
In the text
thumbnail Fig. 4

Longitudinal distribution of water beetles in Plitvice Lakes NP. Abbreviations of biocoenotic regions: EUC: Eucrenal, HYC: Hypocrenal, ER: Epirhithral, MR: Metarhithral, HR: Hyporhithral, EP: Epipotamal, MP: Metapotamal, LT: Littoral. For locality abbreviations, see Figure 1.
In the text
thumbnail Fig. 5

Biogeography of identified water beetles in Plitvice Lakes NP. Abbreviations of biogeographical chorotypes: AE: Asiatic; B: Balkan; BT: Balkano-Turanian; CAE: Centralasiatic-European; E: European; TE: Turano-European; TEM: Turano-Europeo-Mediterranean.
In the text
thumbnail Fig. 6

Seasonal dynamics and adult/larvae ratio of Elmis bosnica in the Bijela rijeka and the Crna rijeka from February 2007 to January 2008 at: a) springs and b) along the watercourse. Abbreviations: Ad.: adult stage, Lv.: larval stage; S2: microhabitat with angiosperms; S3: microhabitat with bryophytes. For locality abbreviations, see Figure 1.
In the text
thumbnail Fig. 7

Canonical correspondence analysis of water beetles in Plitvice Lakes NP. Abbreviations: Elm_a_r: Elmis aenea/rioloides, Lim_vol_sp: Limnius volckmari/sp., Riol_cup_sub: Riolus cupreus/subviolaceus. Other taxa are abbreviated as in Table 2.
In the text

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