Checklist of water bugs (Hemiptera: Heteroptera: Nepomorpha, Gerromorpha) of Slovakia

The water bugs represent a significant component of the freshwater biota, play an important role in trophic webs, and may have considerable economic importance. Nevertheless, systematic research of this group has been underdeveloped in Slovakia (central Europe) for decades. This work presents a list of water bug species of Slovakia based on an exhaustive review of the literature (time span: 1808–2013) and on more than 14,000 individuals collected during extensive field campaigns (2010–2014) or obtained from insect collections. Fifty-six species belonging to 11 families of Heteroptera were recorded from a total of 767 sites. Seven species were recorded for the first time from Slovakia during our research. Among those, the first exact records of Corixa panzeri Fieber, 1848, Sigara (Subsigara) distincta (Fieber, 1848), Notonecta (Notonecta) lutea Müller, 1776, Notonecta (Notonecta) maculata Fabricius, 1794 and Microvelia (Microvelia) buenoi Drake, 1920 are provided here. Confusion concerning the records of two additional species, Arctocorisa carinata carinata (C. R. Sahlberg, 1819) and Hesperocorixa parallela (Fieber, 1860) is clarified. The water bugs species inventory appears to be nearly complete (~97 %) given an asymptotic richness estimate. The occurrence of other species is discussed taking into account their habitat requirements and distribution in neighbouring countries. Recommendations for future research

The first evidence of water bugs from the area of Slovakia dates back to the Austro-Hungarian Empire. Besides Bartholomaeides (1808) mentioning Notonecta and Nepa in the list of insects of Levoča District, Horváth (1870Horváth ( , 1884Horváth ( , 1899 and Brancsik (1878Brancsik ( , 1880Brancsik ( , 1887Brancsik ( , 1891 pioneered the knowledge of the group. Most notably, Horváth compiled a catalogue of Heteroptera published in the series "Fauna Regni Hungariae" (Horváth 1897). Subsequent decades brought more taxonomic or faunistic investigations with the major contributions of Balthasar (1936Balthasar ( , 1942, Tamanini (1949), Soós (1959) and Wroblewski (1960). For detailed information on the history of Heteroptera research in the territory of Slovakia see Horváth (1897) and Stehlík & Vavřínová (1991). Hoberlandt (1977) summarized published data in a checklist of 44 water bug species from Slovakia. Late 20th century freshwater research was mainly ecologically oriented and water bugs were recorded only sporadically (e.g., Bulánková et al. 1994, Bulánková 1995, Elexová 1998a. Unfortunately, the latest checklist of aquatic and semiaquatic Heteroptera (Bulánková 2003) was based on only ~30% of published sources available and covers only 28 species and 2 genera without specifying species. Also, the Palaearctic catalogue of Heteroptera (Andersen 1995, Polhemus et al. 1995 includes information on the Slovak water bugs, but in several cases (especially in Notonectidae) the records from Slovakia are based on misinterpretation of the records from the former Czechoslovakia and in fact pertained to the Czech Republic; therefore, this catalogue also is insufficient as a checklist of Slovak water bugs. Thus, Hoberlandt's (1977) contribution remains the most comprehensive list of water bug species from Slovakia. Works focused on water bugs are still rare and rather local or include brief information on newly recorded species (e.g., Bryja & Kment 2004, 2007Faková 2005;Manko 2011;Kment et al. 2013;Reduciendo Klementová & Svitok 2014;Novikmec et al. 2015).
In order to fill an important gap in the knowledge of aquatic insects, we performed extensive surveys of water bug distributions in Slovakia. To do this we processed the material from museum, departmental and private collections as well as material from our own large-scale sampling conducted from 2010 to 2014. These data were supplemented by a complete literature review of all available publications with the aim to establish the first comprehensive checklist of aquatic and semi-aquatic Heteroptera of Slovakia.

Study area
Slovakia (16º50ʹ-22º34ʹE, 47º44ʹ-49º37ʹN) includes both mountainous and lowland landscapes, resulting in high elevational variability (94-2654 m a.s.l.). The mean annual temperature and total annual precipitation ranges from ~ 0.3 to 11.4ºC and 500 to 1400 mm, respectively. However, considerable regional climatic differences exist. The Pannonian lowland, the warmest part of the area, typically has mean annual temperatures of > 9ºC and relatively low total annual precipitation (< 600 mm). In contrast, mean annual temperatures in the coldest parts of the Carpathian Mountains are < 5ºC and precipitation totals are > 1000 mm. The largest part of the country belongs to the Black Sea drainage area (Danube River basin), whereas the minority is drained to the Baltic Sea (Vistula River basin) (Miklós 2002). Aquatic habitats included in the study range from temporary pools through permanent ponds, ditches and small streams to rivers and lakes.

Material and methods
The study is based on a dataset compiled from three sources of information: 1) Published data. Records of occurrence of aquatic and semi-aquatic Heteroptera in Slovakia were collected in a comprehensive literature survey of all available archive sources. As a result, data from 54 articles and 5 monographic studies covering the period 1808-2013 are included in the dataset (Fig. 1). The surveyed papers are marked with asterisks (*) in the References section.
2) Museum and private collections. We studied unpublished material in seven museum collections (National Museum in Prague, Czech Republic (CZ); Moravian Museum in Brno, CZ; Natural History Museum in Bratislava, Slovakia (SK); Central Slovakia Museum in Banská Bystrica, SK; Homeland Museum Hlohovec, SK; Vihorlat Museum Humenné, SK and The Western Slovakia Museum in Trnava, SK), one departmental collection (Dept. of Biology and General Ecology, Technical Univerzity in Zvolen, SK) and eight private collections (Peter Bitušík, Eva Bulánková, Jozef Cunev, Vladimír Hemala, Peter Manko, Jozef Oboňa, Filip Rovný and Matúš Šoltís). All material was determined to the lowest possible taxonomic level using determination keys by Savage (1999), Rabitsch (2005b) and Tempelman & van Haaren (2009). Note that the work of Bartholomaeides (1808) mentioning two genera (Notonecta and Nepa) is not included.
3) Extensive field survey. During 2010 to 2014, we conducted a large-scale sampling campaign across all of Slovakia. Samples were taken in various habitats using several sampling methods, including sweeping of aquatic plants above and below water, and quantitative and qualitative benthic sampling. Collected material was preserved in 70% ethanol and transferred to the laboratory for determination. Voucher material is housed in the collection of the Department of Biology and General Ecology, Technical University in Zvolen, Slovakia.
Records from those sources were included in the dataset only if the specimen was identified to the species level. Geographical coordinates and basic environmental characteristics of sampling sites were extracted from publications, unpublished records or directly measured in the field. Data from repeatedly sampled sites were pooled and presented only once.
In order to assess completeness of the species inventory, we constructed an analytical sample-based accumulation (rarefaction) curve with unconditional confidence intervals (Colwell et al. 2004). Consistent with the rarefaction method, we used the asymptotic richness estimator Chao2 (Chao 1987) to estimate the total number of water bug species, including those unobserved. Since detection probabilities of the species were relatively homogeneous (CV = 0.61) we used the bias-corrected form of the estimator (Chao 2005). The analyses were performed in EstimateS 9.1.0 (Colwell 2013) and Spade (Chao & Shen 2010).

Results
We recorded the occurrence of water bugs at 767 sites in Slovakia, with information obtained from unpublished sources (511 sites) and derived from the literature (256 sites). The sites were more or less evenly distributed in both the Pannonian and Carpathian regions (Fig. 2) and covered a range of environmental conditions; elevation: 96-2060 m, water pH: 4.6-9.7, water conductivity: 6-1725 µS.cm -1 (Fig. 3). The majority of the sampling sites was located in lower elevations (< 400 m) and the number of records steadily decreased toward higher elevations. However, accounting for the surface area of the elevational belts, the lowest sampling effort was encountered in mid-elevations (800−1200 m). Regarding water quality, attention has been paid chiefly to waterbodies that have relatively low conductivity (< 800 µS.cm -1 ) and are slightly alkaline (pH = 7.5-8.5).
The species inventory of water bugs appears to be nearly complete as the accumulation curve reached an asymptote (Fig. 5). Expected total species richness calculated by the Chao2 estimator was 58 species (95% CI: 56-70), meaning that only two species are expected to remain undetected. Overall, the analysis suggests a high degree of inventory completeness (~97 %).

Discussion
This paper presents the first comprehensive checklist of aquatic and semi-aquatic Heteroptera of Slovakia listing 56 species from 11 families. Here, we briefly discuss new records and completeness of the species inventory and provide some suggestions for further research of aquatic Heteroptera in the area.

Newly recorded species
Microvelia buenoi and Corixa panzeri are evidenced here for the first time from Slovakia. Five other species (Arctocorisa carinata, Sigara distincta, Anisops sardeus, Notonecta lutea and N. maculata) were recorded for the first time during our study. While the records of A. sardeus and A. carinata were properly published (Reduciendo Klemenová & Svitok 2014, Novikmec et al. 2015, the remaining three species were mentioned only in a conference abstract (Klementová et al. 2012) and thus their exact records are provided here. Hesperocorixa parallela was recorded from Slovakia by Soós (1959), but that record was overlooked by all subsequent authors (cf. Hoberlandt 1977).
Comment. Arctocorisa carinata was listed from Slovakia in the checklist by Hoberlandt (1977) but omitted in Palaearctic catalogue by Polhemus et al. (1995). Štys (1976) wrote: '… known from Czechoslovakia from Štrbské pleso in High Tatra (Szilády, 1904, as Corisa cognata) only'. However, this information was apparently based on incorrect translation of the Hungarian text by Szilády (1904), who only mentioned Corisa cognata as another species that might occur in that mountain lake. The first record of A. carinata in Slovakia was thus provided by Novikmec et al. (2015). Remarks. The species was collected in the wide environs of Trenčín city in 1874-1915 when K. Brancsik was working in that area (Koleška 1979); information on the exact location and date of sampling are missing.
Distribution. This Palaearctic species is distributed longitudinally from Ireland to Tajikistan and latitudinally from Sweden to Algeria, Morocco and Tunisia (Jansson 1986, Polhemus et al. 1995, Protić 1998, Rabitsch & Zettel 2000, Dolmen 2004, Straka et al. 2009, Fent et al. 2011, Kment & Beran 2011. In Europe, C. panzeri is frequently found in coastal zones and becomes scarce in inland areas. In landlocked regions of Europe, records of the species are usually restricted to single specimens with the exception of the Pannonian lowlands (Straka et al. 2009, Kment & Beran 2011. Although the occurrence of this species in Slovakia was listed by Polhemus et al. (1995) and the species was collected in southern Slovakia by P. Štys (pers. comm.), there is no confirmed record so far. The first direct evidence, presented here, was obtained by our study of a single specimen collected by K. Brancsik and deposited in National Museum in Prague. Corixa panzeri prefers temporary, fish-less habitats with slightly saline waters, mineral-rich substrates and rich vegetation cover (e.g., Wróblewski 1980, Boix et al. 2001, Aukema et al. 2002, Straka et al. 2009). Comment. Hesperocorixa parallela is a mountain species with scattered occurrence in southern Europe, Caucasus, Transcaucasia, Turkey, Near East and Iran (Polhemus et al. 1995, Aukema et al. 2013. In Central Europe the species is cofined only to the Carpathians (Slovakia, Poland, Transcarpathian Ukraine, Romania) (Soós 1959, Polhemus et al. 1995 where it prefers small and shallow tarns usually above 1700 m a.s.l. (Wróblewski 1980). The Slovak record by Soós (1959) was overlooked by Hoberlandt (1977) and Polhemus et al. (1995).  , 9.viii.1967, 1 ♀, lgt. J. L. Stehlík, det. P. Kment (coll. Moravian Museum, Brno, Czech Republic).
Distribution. Sigara distincta is widespread in Europe, Siberia and north Africa, but is lacking in the southwestern part of Europe (Jastrey 1981, Nieser 1982. This species tolerates a wide range of habitats but prefers stagnant waters in higher elevations with low pH (5−6) and conductivity (< 200 µS.cm -1 ) (Mercken 1989, Lock et al. 2013 Remarks. The species was found in ombrogenous peat bog pools with pH of water from 4 to 6 (Hindák 2012). Distribution. Notonecta lutea is distributed in central, northern and eastern Europe, Russia and Kazakhstan (Jaczewski & Wróblewski 1978, Dioli 1994, Polhemus et al. 1995, Soós et al. 2009, Berchi 2013). This species is common in bogs overgrown with heather or Sphagnum spp. but can be also found in ditches or swamps with dystrophic, mixtrophic or eutrophic water (Jastrey 1981, Nieser 1982 Remarks. Notonecta maculata was found in small (7.2 m 2 , max. depth 0.25 m), fishless garden pond and lowland stream.
Distribution. This Holarctic species is distributed from the United Kingdom to northern China, Canada and northern United States. The southern boundary in Europe is delineated by France, Germany, Austria, Hungary, Romania and Ukraine; it is absent in southern Europe (Putshkov & Putshkov 1996, Rabitsch & Zettel 2000, Aukema et al. 2013, Kment et al. 2013, Berchi & Kment 2015. The species prefers shaded littoral zones of ditches, marshes and ponds, where it is particularly abundant among emergent macrophytes and submerged branches of shore vegetation (Wróblewski 1980, Aukema et al. 2002. Kurzatkowska (1999) considered M. buenoi a tyrphophilous species, inhabiting various dystrophic, polyhumic waters, especially in forests.

Completeness of the species inventory
The last extensive checklist of water bugs from Slovakia comprised 44 species (Hoberlandt 1977) and this number expanded to 56 species by 2015. Based on the total richness estimate, we expect that future surveys will add few additional species into the checklist (Fig. 5) , 1926, and N. (N.) reuteri reuteri Hungerford, 1928 may be reasonably expected given their environmental requirements and their presence in neighbouring countries (Wróblewski 1980, Kment & Smékal 2002, Polhemus et al. 2005, Rabitsch 2005a, Boda et al. 2015. TABLE 1. Checklist of aquatic and semi-aquatic Heteroptera (Nepomorpha and Gerromorpha) occurring in Slovakia and references to the first records. The species list is arranged by infraorder, family, genus, (subgenus), species and subspecies, and follows standard nomenclature (Andersen 1995, Polhemus et al. 1995, Aukema et al. 2013.
Another Euro-Siberian species with occurrence expected in Slovakia is Cymatia bonsdorffii. This species is distributed in Europe (except for south Europe), Siberia, Russia, Kazakhstan, Mongolia, and China and it occurs in all neighbouring countries except Hungary (Polhemus et al. 2005). In central Europe, C. bonsdorffii dwells in dystrophic waterbodies with well developed vegetation, lower pH and low conductivity (Bonte et al. 2001, Kurzątkowska 2008. Corixa dentipes is widespread in Europe and known in all neighbouring countries except Hungary (Polhemus et al. 1995, Boda et al. 2015. The species dwells in various habitats with shallow water and rich detritus supply (e.g., ponds, ditches), very low pH (3-5) and low conductivity (< 500 µS.cm -1 ) avoiding eutrophic waters (Wollmann 2000, Bonte et al. 2001. It was recorded from Trenčín environs by Brancsik (1887), but later the record was found to be based on misidentification of Corixa punctata (see Horváth 1897: 45).
Hesperocorixa castanea occurs through northern and western Europe, western parts of central Europe and in the Iberian Peninsula (Polhemus et al. 1995). The species is known from the Czech Republic (western Bohemia) and Poland and Polhemus et al. (1995) listed its occurrence in Slovakia with a question mark. We found several juvenile and/or female specimens of small Hesperocorixa in Tatra Mountains that resembles H. castanea. However, only adult and fully developed males can be reliably determined to the species level. Thus we tentatively identified those individuals as H. moesta, which are morphologically very similar species from the same lineage (Dunn 1979, Jansson 1986). Hesperocorixa castanea is considered a typical raised bog species with preference for shallow, acidic waters of low conductivity (van Duinen 2003, Lock et al. 2013, Hannigan & Kelly-Quinn 2014.
Ongoing climate change was suggested to be the major driving force behind the recent range shifts of heteropteran species (Rabitsch 2008). Expansions of A. sardeus (see Reduciendo Klementová & Svitok 2014 and references therein) and Microvelia pygmaea (Kment et al. 2013) in central Europe are such examples. However, the effect of elevated temperatures is complex and can alter not only distributional ranges but also phenology, voltinism, physiology and behaviour of Heteroptera and ultimately the structure of communities (Musolin 2007). Consequently, species turnover induced by climate change should be expected.

Recommendations for future research
By extensive sampling and study of available data on water bugs from Slovakia, we have attempted to establish the first comprehensive species list. Despite the considerable effort, several species are expected to be missing in the inventory. We consider this checklist as a first step towards knowledge of the regional water bug fauna and its effective biological conservation. We suggest that future research in the area should focus on: 1 sampling specific habitats that were overlooked in previous research such as dystrophic waterbodies, newly created waterbodies in initial succession stages, or larger pristine streams, which may harbour previously unrecorded species (e.g. Cymatia bonsdorffii, Corixa dentipes, Hesperocorixa castanea, Notonecta reuteri, N. obliqua and Sigara hellensi); 2 describing diversity patterns and clarifying underlying mechanisms; 3 identifying the major threats to diversity of water bugs; and 4 establishing a well-documented national red list of threatened species.