Ecologica Montenegrina 34: 49-63 (2020) This journal is available online at: www.biotaxa.org/em http://dx.doi.org/10.37828/em.2020.34.6

Dragonflies from hot springs in Russia with a country-level checklist of known to occur in geothermal environments

OLGA V. AKSENOVA, GRIGORY S. POTAPOV*, YULIA V. BESPALAYA, YULIA S. KOLOSOVA, ILYA V. VIKHREV, ALEXANDER V. KONDAKOV, MIKHAIL YU. GOFAROV & IVAN N. BOLOTOV

N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Northern Dvina Emb. 23, 163000, Arkhangelsk, Russia *Corresponding author: [email protected]

Received 28 August 2020 │ Accepted by V. Pešić: 12 September 2020 │ Published online 15 September 2020.

Abstract Geothermal springs are known to harbor unusual assemblages of and worldwide. A review of original records and the body of available literature revealed that 27 species were recorded from hot springs in Russia so far and that the successful larval development in geothermal environments was discovered for 17 species. Among them, four species exclusively inhabit hot springs, i.e. Mnais costalis, sieboldii, melania (Kunashir Island), and O. albistylum (Eastern ). In Russia, these southern species are unable to develop beyond geothermally heated water bodies due to cold climate, and they exist as local geothermal populations there. Here, we report on several novel records of Odonata species from geothermal springs in eastern Russia. Four species were recorded on the Kunashir Island (Kurile Archipelago): Mnais costalis (adults), (adults and larvae), Orthetrum melania (adults), and Sympetrum pedemontanum elatum (adults and larvae). Two species were found in the Kamchatka Peninsula, i.e. Libellula quadrimaculata (freshly emerged imago and exuvia) and Aeshna juncea (larvae). To explain the origin of isolated geothermal populations of Odonata, three alternative hypotheses can be proposed as follows: (1) pre-glacial relicts; (2) mid-Holocene relicts (since the Holocene Climate Optimum); and (3) recent (late Holocene) populations founded by long-distance dispersal events. These scenarios are yet to be tested by means of a molecular approach.

Key words: Odonata, Eastern Siberia, Russian Far East, Kurile Archipelago, geothermal habitat, extreme environment, larval development, isolated population.

Introduction

Hot springs house distinctive communities because of stable temperature regime and high concentration of dissolved solids compared with those in non-geothermal habitats (Corbet 2004; O’Gorman et al. 2012). Geothermal sites in cold high-latitude and high-altitude areas could serve as local refugia for thermophilic and plants (Pleshanov et al. 2002; Kornobis et al. 2010; Bolotov et al. 2012). In temperate areas and high mountain ranges, various southern species of dragonflies and damselflies are

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DRAGONFLIES FROM HOT SPRINGS IN RUSSIA known to establish local populations in warm springs (Leggott & Pritchard 1986; Corbet 2004; Borisov & Haritonov 2004; Borisov 2009, 2014, 2015a; Haritonov & Borisov 2013). Occurrences of Odonata species from geothermal sites attracted a full attention of scientists since the end of the 19th century (Kellicott 1897). In a global summary, 38 species of Odonata were listed as permanent inhabitants of hot springs that can complete their life cycle in geothermal environments (Corbet 2004). This list contains 10 species that were thought to be recorded from hot springs in Russia (Corbet 2004), although most of these records are doubtful (Borisov 2014). Two species are known to occur near hot springs of the Kamchatka Peninsula, i.e. Aeshna juncea (Linnaeus, 1758) and graeseri Selys, 1887, although only adult dragonflies were collected there (Dumont et al. 2005). Recently, 23 Odonata species were recorded from hot springs around Lake Baikal based on comprehensive field surveys (Borisov 2014, 2016, 2017). Occurrences of three Odonata species from hot springs of the Kurile Archipelago were also registered, i.e. Mnais costalis Selys, 1869, Orthetrum melania (Selys, 1883), and Anotogaster sieboldii (Selys, 1854) (Paulson et al. 1998; Corbet 2004; Kotlyakov et al. 2009; Palatov 2014; Sasamoto et al. 2017). This study aims to describe several new records of Odonata species from geothermal springs of eastern Russia and to provide further notes on their biology and ecology based on the field observations. A complete checklist of Odonata species that are known to occur in geothermal environment in Russia is compiled based on published and original occurrence data and a critical revision of Corbet’s (2004) list of species.

Materials & Methods

Field surveys of dragonflies in geothermal habitats were conducted on the Kunashir Island in July 2011, and at the Kamchatka Peninsula in June 2013 and August 2014 (Table 1 and Figs. 1-4). Adult Odonata specimens were collected randomly by a butterfly net near hot springs and warm streams (Fig. 2), while larvae were sampled using a sieve and a standard hydrobiological net (mesh size 0.1 mm). Altogether 100 adult specimens, 12 larvae, and 2 exuvia were collected. The samples were deposited in the Siberian Zoological Museum [SZM], Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences (Novosibirsk, Russia), and the Russian Museum of Biodiversity Hotspots [RMBH], N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences (Arkhangelsk, Russia).

Table 1. Sampling localities of Odonata in eastern Russia.

Stolbovsky hot Neskuchensky hot The Valley of Karymshinsky hot springs, Kunashir springs, Kunashir Geysers, Parameters springs, Kamchatka Island, South Island, South Kamchatka Peninsula Kuriles Kuriles Peninsula Latitude 44.0072°N 44.4856°N 52.8125°N 54.4376°N Longitude 145.6831°E 146.0981°E 158.0975°E 160.1389°E Environment Warm springs and a Warm springs and Warm pool Warm lakelet warm stream warm streams Water temperature range (°C) 14.4-72.5 14.8-70 19-22.5 30-38 Mineral content of geothermal waters (mg×L-1): Na+ 101.3 51.8 128.0 N/A Ca2+ 16.0 43.1 10.7 N/A Mg2+ 2.93 17.05 0.24 N/A K+ 7.91 15.88 2.97 N/A 2– SO4 66.0 97.5 141.0 N/A Cl– 155.9 16.1 92.6 N/A Nitrogen content of geothermal waters (mg×L-1): + NH4 1.72 4.59 0.57 N/A – NO3 0.31 0.20 0.00 N/A

N/A – not available.

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Figure 1. Map of sampling localities of Odonata in eastern Russia: Stolbovsky hot springs (1); Neskuchensky hot springs (2); Karymshinsky hot springs (3); and the Valley of Geysers (4).

Field observations on behavior and biological features of populations associated with geothermal habitats were conducted. A digital thermometer (TK.5.05, TekhnoAS, Russia) was used for measuring of water and ground temperatures of geothermal sources in situ. Water samples for chemical analysis were obtained using 0.5 L polyethylene bottles that were kept cool and dark until transfer to the laboratory. In each site, the water samples were collected from an outflow stream or a pool accumulating geothermal waters from surrounding hot springs. Hydrochemical analyses were performed in the core facility center of the Northern Arctic Federal University, Arkhangelsk, Russia. Geographic position, hydrochemical content, and temperature range of geothermal waters at the sampling localities are presented in Table 1.

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Figure 2. Hot spring habitats and a live dragonfly on the Kunashir Island. (A) Neskuchensky hot springs, a habitat of Sympetrum pedemontanum elatum, Anotogaster sieboldii, and Orthetrum melania, 26 July 2011. (B) Stolbovsky hot springs, a habitat of Mnais costalis, Anotogaster sieboldii, and Orthetrum melania, 29 July 2011. (C) Male of Orthetrum melania near the Neskuchensky hot springs, 26 July 2011. (Photos: Yu. S. Kolosova [A, C] and O. V. Aksenova [B]).

The adult specimens from the Kunashir Island were identified by the late Dr. Anatoly Yu. Haritonov (Novosibirsk, Russia). Other imago samples were identified using an appropriate key (Haritonov 1986). The larvae were identified based on morphological features using available guides (Haritonov 1997; Lee and Jung 2012). Images of larvae samples were obtained using a stereomicroscope (Leica M165C, Leica Microsystems, Germany). Images of adult specimens were taken by a digital camera (Canon EOS 60D, Canon Inc., Japan).

Results

In total, our samples contain six Odonata species from geothermal habitats in eastern Russia: Mnais costalis, Anotogaster sieboldii, Orthetrum melania, and Sympetrum pedemontanum elatum from Kunashir Island, and Libellula quadrimaculata, and Aeshna juncea from Kamchatka (see Taxonomic Account and Figs. 2-5 for detail). Larvae of Anotogaster sieboldii, Sympetrum pedemontanum elatum, and Aeshna juncea were collected from warm geothermal waters (Figs. 2-4). Exuvia and a freshly emerged adult specimen of Libellula quadrimaculata supported its successful development in a warm pool of the Karymshina hot springs, Kamchatka (Fig. 4A-B). On the Kunashir Island, four species were recorded from geothermal areas (Table 2 and Figs. 3 and 5). Based on our randomly collected samples of adult specimens (Table 2), Sympetrum pedemontanum

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Table 2. Number and proportion of Odonata imago collected from geothermal sites of the Kunashir Island in July 2011

Stolbovsky hot springs Neskuchensky hot springs Number of Number of Species Proportion of Proportion of specimens specimens specimens (%) specimens (%) [♂/♀] [♂/♀] Mnais costalis Selys, 1869 6 [6♂] 20.7 0 0.0 Anotogaster sieboldii (Selys, 1854) 2 [1♂, 1♀] 6.9 5 [4♂, 1♀] 7.1 Orthetrum melania (Selys, 1883) 21 [18♂, 3♀] 72.4 21 [20♂, 1♀] 30.0 Sympetrum pedemontanum elatum (Selys, 1872) 0 0.0 44 [26♂, 18♀] 62.9 Total sample 29 100.0 70 100.0

Altogether 27 Odonata species are known to occur in geothermal springs in Russia (Table 3). The taxonomic assemblage is as follows: (1 species), Coenagrionidae (8 species), Lestidae (3 species), Aeshnidae (3 species), (2 species), (1 species), and (9 species).

Taxonomic Account

Family Calopterygidae Sélys, 1850

Mnais costalis Selys, 1869 Fig. 5A, 5B

Material examined. RUSSIA: Kunashir Island, Stolbovsky hot springs, 44.0072°N, 145.6831°E, 29 July 2011, around warm springs and streams, 6♂, Bolotov, Kolosova & Potapov leg. Field observations. A rather rare species (Table 2). A few egg-laying females were recorded in a warm stream of the Stolbovsky hot springs. Distribution. Endemic to Japan (Okuyama & Takahashi 2017), with a few isolated populations in hot spring sites on the Kunashir Island (Paulson et al. 1998; Kotlyakov et al. 2009; this study). Comments. Previously, it was thought to be a subspecies of Mnais pruinosa (Sélys, 1853) but recent molecular study revealed its validity as a separate species (Hayashi et al. 2004). However, multiple hybridization and mtDNA introgression events were discovered between these species (Hayashi et al. 2005). In the recent checklist of Russian Odonata (Malikova & Kosterin 2019), it is listed as the subspecies Mnais pruinosa costalis.

Family Aeshnidae Rambur, 1842

Aeshna juncea (Linnaeus, 1758) Fig. 4C, 4D

Material examined. RUSSIA: Kamchatka Peninsula, the Valley of Geysers, 54.4376°N, 160.1389°E, 13 August 2014, Lakelet Medvezhie, 1 larva, Aksenova & Soloviev leg. Field observations. This larva was collected from a shallow and swampy geothermal lakelet with clay bottom. We did not measure temperature in this water body but it ranges from 30 to 38°C (Lobkova et al. 2012). Distribution. Holarctic species (Haritonov 1986). It was recorded as an abundant species, which can successfully develop in warm waters, in geothermal areas of Eastern Siberia (Borisov 2014, 2016; Popova & Matafonov 2015). There is a record of imago near a geothermal site in Kamchatka (Dumont et al. 2005) and larvae from the Valley of Geysers (as Aeschna yuncea [sic!]; Lobkova et al. 2012).

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Table 3. List of Odonata species recorded from hot springs of Russia

Taxon Region Development* Reference Zygoptera Calopterygidae ‡Mnais costalis Selys, 1869 Kuriles: Kunashir Confirmed Kotlyakov et al. (2009); this study Coenagrionidae Coenagrion armatum (Charpentier, Eastern Siberia Not confirmed Borisov (2016) 1840) C. johanssoni Wallengren, 1894 Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015) C. glaciale (Selys, 1872) Eastern Siberia Not confirmed Borisov (2014, 2016); Popova & Matafonov (2015) C. hastulatum (Charpentier, 1825) Eastern Siberia Not confirmed Borisov (2016); Popova & Matafonov (2015) C. hylas (Trybom, 1889) Eastern Siberia Not confirmed Borisov (2016) C. lunulatum (Charpentier, 1840) Eastern Siberia Not confirmed Borisov (2016) Enallagma cyathigerum (Charpentier, Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov 1840) (2015) Erythromma najas (Hansemann, 1823) Eastern Siberia Confirmed Belyshev and Gagina (1959); Popova & Matafonov (2015); Borisov (2016) Lestidae Lestes dryas Kirby, 1890 Eastern Siberia Confirmed Belyshev (1957); Belyshev & Gagina (1959); Borisov (2014, 2016); Popova & Matafonov (2015) L. sponsa (Hansemann, 1823) Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015) Sympecma paedisca (Brauer, 1877) Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015) Anisoptera Aeshnidae Aeshna caerulea (Stroem, 1783) Eastern Siberia Not confirmed Borisov (2016) A. crenata Hagen, 1856 Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015) A. juncea (Linnaeus, 1758) Eastern Siberia; Confirmed Dumont et al. (2005); Borisov (2014, 2016); Russian Far East: Popova & Matafonov (2015); this study Kamchatka Corduliidae Epitheca bimaculata (Charpentier, Eastern Siberia Not confirmed Belyshev & Gagina (1959); Popova & 1825) Matafonov (2015) Somatochlora graeseri Selys, 1887 Eastern Siberia; Not confirmed Dumont et al. (2005); Borisov (2014, 2016); Russian Far East: Popova & Matafonov (2015) Kamchatka Cordulegastridae ‡Anotogaster sieboldii (Selys, 1854) Kuriles: Kunashir Confirmed Kotlyakov et al. (2009); Palatov (2014); this study Libellulidae Leucorrhinia dubia orientalis Selys, Eastern Siberia Not confirmed Belyshev & Gagina (1959); Borisov (2014, 1887 2016); Popova & Matafonov (2015) L. intermedia Bartenev, 1910 Eastern Siberia Not confirmed Popova & Matafonov (2015); Borisov (2016) Libellula quadrimaculata Linnaeus, Eastern Siberia; Confirmed Takhteev et al. (2006); Borisov (2014, 2016); 1758 Russian Far East: Popova & Matafonov (2015); this study Kamchatka ‡Orthetrum albistylum (Selys, 1842) Eastern Siberia Confirmed Belyshev (1956, 1957, 1960); Belyshev et al. (1978); Borisov (2014, 2016); Popova & Matafonov (2015) ‡O. melania (Selys, 1883) Kuriles: Kunashir Confirmed Sasamoto et al. (2017); this study Sympetrum danae (Sulzer, 1776) Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015) ..continued on the next page

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Taxon Region Development* Reference S. flaveolum (Linnaeus, 1758) Eastern Siberia Confirmed Belyshev (1957); Borisov (2014, 2016); Popova & Matafonov (2015) S. pedemontanum elatum (Selys, 1872) Kuriles: Kunashir Confirmed This study S. pedemontanum pedemontanum Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (Mueller in Allioni, 1766) (2015) S. vulgatum (Linnaeus, 1758) Eastern Siberia Confirmed Borisov (2014, 2016); Popova & Matafonov (2015)

‡Only hot-spring-associated local populations are known in Russia. *Confirmed: reliable occurrence of larvae and (or) exuvia and (or) freshly emerged imago; not confirmed: only imago specimens were collected (Borisov 2016).

Family Cordulegastridae Calvert, 1893

Anotogaster sieboldii (Selys, 1854) Figs. 3B, 5C, 5D

Material examined. RUSSIA: Kunashir Island, Stolbovsky hot springs, 44.0072°N, 145.6831°E, around warm springs and streams, 29 July 2011, 1♂, 1♀, Bolotov, Kolosova & Potapov leg.; Kunashir Island, Neskuchensky hot springs, 44.4856°N, 146.0981°E, around warm springs and streams, 24-26 July 2011, 4♂, 1♀, Bolotov, Kolosova & Potapov leg.; the same locality, in warm and cold streams (water temperature range 13.6 to 22.5°C), 26 July 2011, 7 larvae of various size (maximum body length 14 mm), Bespalaya & Aksenova leg. Field observations. This species was not abundant in our collection sites (Table 2). The larvae were collected from warm and cold streams with water temperature of 13.6-19.8°С. Females were recorded laying eggs into a warm stream in the Stolbovsky hot springs area, and into a cold stream flowing from a hill slope above the Neskuchensky hot springs area. Conversely, hot springs could also serve as ecological traps for this species due to variable temperature conditions (Fig. 3A). We recorded females, which laid eggs into a hot stream section, the temperature of which decreased up to 28-30°С because of the temporal admixture of cold rainfall waters. However, the egg and larval development in this stream section seems to be impossible because its usual temperature is as high as 40ºС. Distribution. Japan, , southeastern , and Taiwan (Asahina 1959; Kiyoshi 2008), with a few geothermal populations on the Kunashir Island (Asahina 1959; Paulson et al. 1998; Kotlyakov et al. 2009; Palatov 2014; this study). The larvae of this species were previously recorded in warm springs and streams near the former Alekhina [43.9183°N, 145.5283°E] and Tretyakovo [43.9875°N, 145.6419°E] villages (Palatov 2014). Comments. This species shares two deeply divergent mitochondrial clades that can be considered separate species-level taxa (Kiyoshi 2008).

Family Libellulidae Rambur, 1842

Libellula quadrimaculata Linnaeus, 1758 Fig. 4A, 4B

Material examined. RUSSIA: Kamchatka Peninsula, Karymshina River valley, Karymshinsky hot springs, 52.8125°N, 158.0975°E, warm pool, 12 June 2013, 1♂ (newly emerged, near the pool), 2 exuvia, Bolotov leg. Field observations. These exuvia and adult specimen were collected on the shore of a small warm pool with water temperature of 30.5°С. This pool was situated in a mountain river valley that was largely covered by snow cover at the time of the sample collecting. Distribution. Migratory species, which is widespread throughout boreal zone of the Holarctic Region (Popova & Haritonov 2010). This species was previously recorded from hot springs in Canada (Pritchard 1991; Corbet 2004) and around Lake Baikal (Takhteev et al. 2006; Borisov 2014; Popova & Matafonov 2015).

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Figure 3. Microhabitats in the Neskuchensky hot springs, Kunashir Island, and Odonata larvae collected from this geothermal source. (A) Scheme of microhabitats within the geothermal system with water and ground temperature measurements during the period of 24-26 July 2011 (before heavy monsoon rainfalls). The black symbols indicate collecting sites of Anotogaster sieboldii (circles) and Sympetrum pedemontanum elatum (squares) larvae. The color arrows indicate the oviposion sites of A. sieboldii before (green) and after (red) heavy monsoon rainfalls. (B) Larvae of Anotogaster sieboldii, 26 July 2011. Scale bar = 2 mm. (C) Larvae of Sympetrum pedemontanum elatum, 26 July 2011. Scale bar = 2 mm. (Photos: O. V. Aksenova).

Orthetrum melania (Selys, 1883) Figs. 2C, 5E, 5F

Material examined. RUSSIA: Kunashir Island, Stolbovsky hot springs, 44.0072°N, 145.6831°E, around warm springs and streams, 29 July 2011, 18♂, 3♀, Bolotov, Kolosova & Potapov leg.; Kunashir Island, Neskuchensky hot springs, 44.4856°N, 146.0981°E, around warm springs and streams, 24-26 July 2011, 20♂, 1♀, Bolotov, Kolosova & Potapov leg. Field observations. We observed mating behavior of this species at the Stolbovsky and Neskuchensky hot springs. The egg-laying females occurred at the Stolbovsky area, where it was the most abundant Odonata species (Table 2).

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Distribution. Japan, Korea, continental China, Taiwan, and Vietnam (Yong et al. 2014; Sasamoto et al. 2017), with a few geothermal populations on the Kunashir Island (Sasamoto et al. 2017; this study). The Neskuchensky hot springs harbors the most northeastern population of this species. Several geothermal populations of this species are also known to exclusively occur in hot springs of eastern Hokkaido (Corbet 2004; Sasamoto et al. 2017). Orthetrum-like larvae recorded in a geothermally heated section of the Kislaya River on the Kunashir Island [approx. 44.0036°N, 145.7672°E] (Konakov 1956) most likely belonged to Orthetrum melania. Comments. Morphological analyses of Orthetrum melania samples from the Kunashir Island indicated that these specimens belong to the nominate subspecies (Sasamoto et al. 2017).

Sympetrum pedemontanum elatum (Selys, 1872) Figs. 3C, 5G, 5H

Material examined. RUSSIA: Kunashir Island, Neskuchensky hot springs, 44.4856°N, 146.0981°E, around warm springs, 24-26 July 2011, 26♂, 18♀ (several of them freshly emerged), Bolotov, Kolosova & Potapov leg.; the same locality, warm stream and pool (water temperature range 19.0 to 22.5°C), 26 July 2011, 4 larvae of various size (maximum body length 16 mm), Bespalaya & Aksenova leg. Field observations. We observed mating behavior, mass emergence of the imago, and numerous exuvia near thermal streams on the Neskuchensky area, where it was the most abundant Odonata species during the observation period (Table 2). Larvae were collected from a warm pool with water temperature 22.3°С and ground temperature up to 41°С, and from a warm stream with water temperature of 19.0°С, which flows into a hot stream at the foothill (Fig. 3A). Distribution. This subspecies is endemic to Japan, Sakhalin, and Kuriles (Popova 2004; Higashikawa et al. 2016). Asahina (1959) listed the occurrences of this species from Seseki [Goryachiy Plyazh geothermal site: approx. 44.0258°N, 145.8603°E] and noted that these specimens most likely migrated from Hokkaido. Comments. Sympetrum pedemontanum elatum was considered a valid insular subspecies of the widespread Palearctic species (Popova 2004).

Discussion

Species richness of Odonata in hot springs in Russia Corbet’s (2004) global checklist of dragonflies and damselflies associated with geothermal habitats contains 10 nominal taxa from Russia. Two taxa, i.e. Lestes uncatus Kirby, 1890 (a synonym of L. dryas Kirby, 1890) and Orthetrum albistylum (Selys, 1848), were given based on correct references to works of Belyshev (1957, 1960). Conversely, eight other taxa were listed by Corbet (2004) with reference to the work of Haritonov (1989), which does not contain information on habitat preferences of these species. These taxa are as follows: Coenagrion armatum (Charpentier, 1840), C. concinnum Johanson, 1859 [=C. johanssoni Wallengren, 1894], C. lanceolatum (Selys, 1872), Enallagma belyshevi Haritonov, 1975 [=E. circulatum Selys, 1883], E. cyathigerum Charpentier, 1840, E. nigrolineatum Belyshev & Haritonov, 1975, Lestes dryas Kirby, 1890, and L. sponsa (Hansemann, 1823). Borisov (2014) has already noticed this mistake for several taxa, mentioned above. Hence, these eight taxa were incorrectly included to the checklist (Corbet 2004), although some of them (i.e. Coenagrion armatum, C. johanssoni, Enallagma cyathigerum, Lestes dryas, and L. sponsa) were found to occur in geothermal sites by other authors (see Table 3). In summary, 27 Odonata species are known to occur in geothermal habitats in Russia (Table 3) that represents 17.8% of the total number of species in the country’s fauna (152 species: Malikova & Kosterin 2019). Among these taxa, 17 species were found to complete their life cycle there, while the possibility of successful larval development in geothermal environments is yet to be confirmed for 10 species. The majority of species recorded from geothermal sites are also found in non-geothermal localities (23 species, 85.2% of the total number of taxa). However, four species in Russia are strongly associated with hot spring environments and are unknown beyond heated geothermal sites, i.e. Mnais costalis, Anotogaster sieboldii, Orthetrum melania (Kunashir Island), and O. albistylum (Eastern Siberia) (Table 3).

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Figure 4. Habitats, exuvium, and larva of Odonata in geothermal areas of the Kamchatka Peninsula. (A) Warm pool near the Karymshinsky hot springs, 12 June 2013. (B) Exuvium of Libellula quadrimaculata on the shore of this pool. (C) Lakelet Medvezhie in the Valley of Geysers, 13 August 2014. (D) Larva of Aeshna juncea collected from this lakelet. Scale bar = 2 mm. (Photos: O. V. Aksenova).

Local populations of southern Odonata species in hot springs The white-tailed skimmer Orthetrum albistylum (Selys, 1848) represents the most striking example of a species being associated with geothermal environments in high latitudes (Belyshev 1956, 1957, 1960; Belyshev & Gagina, 1959; Pleshanov et al. 2002; Pleshanov 2009; Takhteev et al. 2006; Borisov 2014, 2016). Viable populations of this southern species were recorded from 16 hot spring localities around Lake Baikal (Eastern Siberia), ca. 770 km northward of the northern boundary of its range in China (Borisov 2017). These local populations and their unique habitats must be protected as regional natural reserves (Kosterin et al. 2004). It was thought that the Siberian populations were isolated since the Tertiary (Belyshev 1956) or the Holocene Climate Optimum as relict fragments of the former continuous range of this species (Borisov 2014, 2017). Conversely, those local isolates can be originated more recently and can be connected with populations within its range via long-distance dispersal events (Borisov 2014, 2017). The latter hypothesis aligns with recent data on high dispersal capabilities of dragonflies (Anderson 2009; Haritonov & Popova 2011a, b; May 2013; Borisov 2015b). It is also supported by examples of vagrant southern species

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Figure 5. Odonata specimens from geothermal habitats of the Kunashir Island [RMBH]. (A) Mnais costalis, male, 29.vii.2011. (B) M. costalis, male, 29.vii.2011. (C) Anotogaster sieboldii, male, 26.vii.2011. (D) A. sieboldii, female, 24.vii.2011. (E) Orthetrum melania, male, 29.vii.2011. (F) O. melania, female, 29.vii.2011. (G) Sympetrum pedemontanum elatum, male, 26.vii.2011. (H) S. pedemontanum elatum, female, 24.vii.2011. Corresponding labels are presented below each specimen. (Photos: Yu. S. Kolosova).

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Local populations of Mnais costalis, Anotogaster sieboldii, and Orthetrum melania were recorded from several geothermal areas of the Kunashir Island. These species have Japanese-Korean affinities (Asahina 1959; Kosterin et al. 2004; Kiyoshi 2008; Okuyama et al. 2013). Based on our data, these species can be abundant locally near geothermal springs on Kunashir (Table 2) as does Orthetrum albistylum in hot springs around Lake Baikal (Borisov 2014, 2017). It is known that hot spring areas of the Kunashir Island house isolated populations of numerous thermophilic animal species, e.g. the Far Eastern skink Plestiodon finitimus Okamoto & Hikida, 2012 (Squamata: Scincidae), Japanese cave cricket Diestrammena japanica Blatchley, 1920 (Orthoptera: Rhaphidophoridae), and Japanese earwig Eparchus yezoensis (Shiraki, 1905) (Dermaptera: Forficulidae) (Krivolutskaya 1973; Basarukin 1982; Kotlyakov et al. 2009; Okamoto & Hikida 2012). The origin of Kunashir’s isolates of southern odonates is also unclear, and can be explained by both the “ancient relict” and the “recent long-distance dispersal” hypotheses as that of Orthetrum albistylum (see above). On the Kunashir Island, larvae of Anotogaster sieboldii and Sympetrum pedemontanum elatum were recorded only in peripheral warm areas of geothermal systems within the water temperature range of 13.6- 22.5°C, avoiding hot sections of geothermal sources with higher temperatures (Fig. 3A). Similar behavioral patterns were recorded for Orthetrum albistylum larvae in a hot spring in the Baikal Region (Belyshev 1960). In Kamchatka, larvae of Libellula quadrimaculata developed in a warm pond with temperature of 30.5°C, and those of Aeshna juncea in a lakelet with temperature of 30-38°C. In hot springs of the Lake Baikal area, Odonata larvae were recorded within the maximum temperature range of 27.0-34.5°C (Borisov 2014). Isolated populations of Argia vivida Hagen in Selys, 1865 from geothermal springs of the USA in laboratory experiments preferred the temperature range of 23-32°C (Leggott & Pritchard 1986). Eggs of several Odonata species can develop under water temperature up to 30-35°C (Pritchard et al. 1996). We discovered females of Anotogaster sieboldii laying eggs into hot section of geothermal stream (40°C), the temperature of which had decreased (28-30°C) after heavy monsoon rains due to influence of cold rainfall waters. It can be considered a kind of ecological trap for dragonflies because a subsequent increasing of water temperature will kill these hatchlings. Finally, it is still unclear whether local isolates of southern species represent relict populations surviving since past warm climate episodes or were founded by long-distance dispersal events more recently. Broad-scale phylogeographic surveys of model taxa strongly associated with hot springs such as Mnais costalis, Anotogaster sieboldii, Orthetrum melania, and O. albistylum are urgently needed to understand the origin of isolated Odonata populations in geothermal areas.

Conclusions

 Hot springs in Russia house 27 Odonata species, representing 17.8% of the country’s species richness of this group.  Successful larval development in geothermal springs of Russia was confirmed for 17 species.  Four species in Russia are unknown beyond hot springs: Mnais costalis, Anotogaster sieboldii, Orthetrum melania (Kunashir), and O. albistylum (Siberia).  New records and ecological data for six Odonata species from hot springs in Russia are reported here.  Future studies should be focused on molecular genetic and phylogenomic analyses of isolated geothermal populations of southern dragonfly species to estimate their origin, distinctiveness, and phylogeographic patterns.

Acknowledgements The Ministry of Science and Higher Education of the Russian Federation supported this work as follows: project АААА-А17-117033010132-2 to Y.V.B., project АААА-А18-118012390161-9 to M.Y.G., project АААА-А18-118011690221-0 to G.S.P, and project FSRU-2020-0007 to I.N.B. The Russian Science Foundation supported O.V.A., I.V.V. and A.V.K. under project No. 19-04-00066. We are deeply grateful to the late Dr. Anatoly Yu. Haritonov (Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia), who identified our samples of adult Odonata specimens from the Kunashir Island. Special thanks go to Mr. Maxim A. Antipin and Mrs. Irina A.

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Nevedomskaya (Kurilsky State Nature Reserve, Yuzhno-Kurilsk, Russia), Mr. Nikolay Solovev (Kronotsky Nature Reserve, Elizovo, Russia) and Mr. Oleg N. Bespaliy (Arkhangelsk, Russia) for their excellent fieldwork assistance.

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