Ecologica Montenegrina 26: 137-146 (2019) This journal is available online at: www.biotaxa.org/em

https://zoobank.org/urn:lsid:zoobank.org:pub:0C283AE4-A94E-456D-9FD4-466A97D0BABB

A new from Qinling Mountains, China (: )

OLGA V. AKSENOVA1,2,3*, MAXIM V. VINARSKI2, ALEXANDER V. KONDAKOV1,2,3, ALYONA A. TOMILOVA1, VALENTINA S. ARTAMONOVA4, ALEXANDER A. MAKHROV2,4, OLEG D. KONONOV1, MIKHAIL YU. GOFAROV1,2, YUN FANG5 & IVAN N. BOLOTOV1,3

1N. Laverov Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Arkhangelsk, Russia 2Saint Petersburg State University, Saint Petersburg, Russia 3Northern Arctic Federal University, Arkhangelsk, Russia 4Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia 5Institute of Zoology, Chinese’s Academy of Science, Beijing, People’s Republic of China *Corresponding author: [email protected]

Received 30 November 2019 │ Accepted by V. Pešić: 28 December 2019 │ Published online 31 December 2019.

Abstract A new representative of the genus Radix has been recorded from eastern China, Radix dgebuadzei sp. nov. This peculiar species was recorded from the Qinling Mountains, a remote highland region sharing the high levels of faunal and floral endemism. The phylogeny indicate that the new species belongs to the Radix alticola species group, being sister to the widespread species R. plicatula (Yunnan and Gansu in China and Southeast Asia) and R. euphratica (Middle East, Central Asia, and Eastern Europe). At first glance, we could assume that Radix dgebuadzei sp. nov. represents a local lineage endemic to the Qinling Region, while this preliminary hypothesis needs to be confirmed in the future. Our novel discovery highlights that China harbors a largely endemic fauna of the Lymnaeidae and that isolated mountain ranges in East Asia could be considered evolutionary hotspots of the radicine pond snails.

Key words: Freshwater gastropods, Radix dgebuadzei sp. nov., Yangtze River basin, new species.

Introduction

In general, freshwater lymnaeids in China are rather poorly known. The body of available literature is chiefly based on conchological traits and do not contain information on the soft body anatomy let alone molecular data (Yen 1939; Liu et al. 1979; Quian et al. 2012; Sun et al. 2015). Recently obtained genetic data have revealed the uniqueness of the region and the presence of gaps in the of Chinese gastropods (von Oheimb et al. 2011; Aksenova et al. 2018). At the present time, only four species of the genus Radix s. str. confirmed by molecular data are known from China: Radix auricularia (L., 1758), R. plicatula (Benson, 1842), R. brevicauda (Sowerby, 1873), and R. makhrovi Bolotov, Vinarski & Aksenova, 2018 (Aksenova et

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NEW RADIX SPECIES FROM QINLING MOUNTAINS, CHINA al. 2018; Qin et al. 2019). Additionally, a new species and a new genus of lymnaeids have been described from the Tibetan Plateau as a result of our research (Aksenova et al. 2018). In addition to Tibet, the most interesting from this point of view are the Qingling Mountains forming a drainage divide between the Yellow and Yangtze River basins and running west to east, stretching across the Gansu, Shaanxi, and Henan provinces. It is known that the Yangtze River basin is one of the most species-rich regions for freshwater molluscs globally (Wu et al. 2019). In the present study, we describe one more species of Radix from the Qinling Mountains in China based on molecular and morphological evidences.

Materials and methods

The study is based on the material from the collection of the Russian Museum of Biodiversity Hotspots (RMBH thereafter), N Laverov Federal Center for Integrated Arctic Research of the Russian Academy of Sciences, Arkhangelsk, Russia. The lymnaeid snails were collected by V.S. Artamonova, A.A. Makhrov and Y. Fang in eastern China during the Russian-Chinese Scientific Expedition in September 2017 (Makhrov et al. 2019) (Fig. 1). The sampled specimens were preserved in 96% ethanol and deposited in the collection of RMBH and in the collection of the Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russian Federation (ZIN hereafter).

Figure 1. Type locality of Radix dgebuadzei sp. nov.: A) general map revealing the position of the Qinling Mountains in China (red frame); B) geographic position of the type locality (red star); C) and D) the type locality: Sun Jia He River in the vicinity of the Shangtan village, Gansu Province, China (Maps: M.Yu. Gofarov; photos: V.S. Artamonova).

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Table 1. List of COI sequences of Radix and Tibetoradix species used in this study.

COI GenBank Species Specimen voucher No. Locality data Reference acc. no. Radix dgebuadzei MN718571 Mlym686/2 China: Gansu Province, Sun Jia He Present study sp. nov. River R. dgebuadzei sp. MN718572 Mlym686/3 China: Gansu Province, Sun Jia He Present study nov. River R. euphratica MH189866 Mlym39/1 Russia: Krasnodar Krai Aksenova et al. (2018) R. euphratica MH189867 Mlym40 Russia: Krasnodar Krai Aksenova et al. (2018) R. euphratica MN718570 Mlym68 Georgia: Tbilisi reservoir Present study

R. euphratica MH189943 Mlym138/1 Tajikistan: Bazovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189944 Mlym138/2 Tajikistan: Bazovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189945 Mlym138/3 Tajikistan: Bazovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189946 Mlym139/1 Tajikistan: Dushanbe City Aksenova et al. (2018) R. euphratica MH189947 Mlym139/2 Tajikistan: Dushanbe City Aksenova et al. (2018) R. euphratica MH189948 Mlym139/3 Tajikistan: Dushanbe City Aksenova et al. (2018) R. euphratica MH189970 Mlym149/1 Tajikistan: Dedovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189971 Mlym149/2 Tajikistan: Dedovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189972 Mlym149/3 Tajikistan: Dedovskoe Lake, Natural Aksenova et al. Reserve "Tigrovaya Balka" (2018) R. euphratica MH189976 Mlym151/1 Tajikistan: drainage ditch, near the Aksenova et al. village of Kurbonschahid (2018) R. euphratica MH189977 Mlym151/2 Tajikistan: drainage ditch, near the Aksenova et al. village of Kurbonschahid (2018) R. euphratica MH189978 Mlym151/3 Tajikistan: drainage ditch, near the Aksenova et al. village of Kurbonschahid (2018) R. euphratica MN718573 Mlym689/2 Uzbekistan: Xorazm Region, Amu Present study Darya River R. euphratica MN718574 Mlym689/3 Uzbekistan: Xorazm Region, Amu Present study Darya River R. euphratica MN718575 Mlym689/4 Uzbekistan: Xorazm Region, Amu Present study Darya River R. euphratica MN718576 Mlym689/5 Uzbekistan: Xorazm Region, Amu Present study Darya River R. euphratica MN718577 Mlym816 Russia: Kabardino-Balkar Republic Present study R. euphratica MN718578 Mlym850/1 Russia: Republic of Dagestan Present study R. euphratica KM206675 INHM MC217 Iraq: Basra, Garmat Ali GenBank R. euphratica KM206676 INHM MC218 Iraq: Basra, Garmat Ali GenBank R. euphratica KM206677 INHM MC219 Iraq: Basra, Khoura GenBank R. euphratica KM206679 INHM MC221 Iraq: Basra, Khoura GenBank R. euphratica KM206680 INHM MC222 Iraq: Missan, Al-Kahlaa GenBank R. euphratica KM206682 INHM MC224 Iraq: Missan, Al-Kahlaa GenBank ..continued on the next page

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COI GenBank Species Specimen voucher No. Locality data Reference acc. no. R. euphratica KM206684 INHM MC244 Iraq: Karbala, Ukhaidher GenBank R. euphratica KM206685 INHM MC245 Iraq: Kerbala, Ukhaidher GenBank R. euphratica KM206686 INHM MC202 Iraq: Babil, Al-Wardia GenBank R. euphratica KM206688 INHM MC227 Iraq: Basra, Garmat Ali GenBank R. euphratica KM206689 INHM MC214 Iraq: Wasit, Al-Hussainiya GenBank R. euphratica KM206690 INHM MC215 Iraq: Wasit, Al-Hussainiya GenBank R. euphratica KM206691 INHM MC216 Iraq: Wasit, Al-Hussainiya GenBank R. euphratica KM206693 INHM MC191 Iraq: Muthanna, Al-Rumaitha GenBank R. euphratica KM206694 INHM MC189 Iraq: Al-Qadisyah, Al-Sanniya GenBank R. alticola MH189949 Mlym140/1 Tajikistan: Western Pamir, Aksenova et al. floodplain of the Shahdar River (2018) R. alticola MH189950 Mlym140/2 Tajikistan: Western Pamir, Aksenova et al. floodplain of the Shahdar River (2018) R. alticola MH189951 Mlym140/3 Tajikistan: Western Pamir, Aksenova et al. floodplain of the Shahdar River (2018) R. alticola MH189953 Mlym142 /1 Tajikistan: thermal spring north of Aksenova et al. the village of Jelanda (2018) R. alticola MH189954 Mlym142 /2 Tajikistan: thermal spring north of Aksenova et al. the village of Jelanda (2018) R. alticola MH189964 Mlym147 /1 Tajikistan: cold brook near the Aksenova et al. fortress of Deruzh (2018) R. alticola MH189965 Mlym147/2 Tajikistan: cold brook near the Aksenova et al. fortress of Deruzh (2018) R. alticola MH189966 Mlym147 /3 Tajikistan: cold brook near the Aksenova et al. fortress of Deruzh (2018) R. alticola MH189973 Mlym150 /1 Tajikistan: Western Pamir, thermal Aksenova et al. spring north in the village of Jelanda (2018) R. alticola MH189974 Mlym150 /2 Tajikistan: Western Pamir, thermal Aksenova et al. spring north in the village of Jelanda (2018) R. alticola MH189975 Mlym150 /3 Tajikistan: Western Pamir, thermal Aksenova et al. spring north in the village of Jelanda (2018) R. alticola MN737036 Mlym688 Uzbekistan: Xorazm Region, Amu Present study Darya River R. sp. Trichonis EU818823 isolate 5433 Greece: Aetoloakarnania, Lake Albrecht et al. Trichonis, NW shore (2008) R. plicatula MN737033 Mlym676 China: Xinjiang, Bosten Lake Present study R. plicatula MN737034 Mlym679 China: Xinjiang, Korla Town Present study

R. plicatula MN737035 Mlym681 China: Xinjiang, Bosten Lake Present study R. plicatula MH190049 Mlym686/1 China: Gansu Province, Sun Jia He Aksenova et al. River (2018) R. plicatula JN794514 PVVO-2011 isolate Vietnam: Kon Tum Province von Oheimb et al. 9370 (2011) R. natalensis HG977206 isolate Cabo Verde Cabo Verde GenBank R. natalensis LC015519 Rnh2.6 Egypt: Beni Suef, Al-Wasta GenBank R. natalensis MN737037 Mlym743 Uganda: Lake Albert Present study R. rufescens MH190025 Mlym605 Myanmar: Myaung Lake Aksenova et al. (2018) R. rufescens KT160297 isolate: Dhumre River Nepal Devkota et al. Chitwan NP (2016) R. rufescens JN794493 UGSB 7498 Myanmar: Indawgyi Lake von Oheimb et al. (2011) ..continued on the next page

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COI GenBank Species Specimen voucher No. Locality data Reference acc. no. R. rubiginosa MH189925 Mlym107 Indonesia: North Sumatra, Toba Aksenova et al. Lake (2018) R. rubiginosa MH189926 Mlym108 Indonesia: Flores Island, Sano Aksenova et al. Ngoang Lake (2018) R. rubiginosa KX056255 MlymB63 Thailand Aksenova et al. (2016a) R. brevicauda JN794464 UGSB 7432 China: Tibet Autonomous Region von Oheimb et al. (2011) R. brevicauda JN794477 UGSB 7446 China: Tibet Autonomous Region von Oheimb et al. (2011) R. brevicauda JN794431 UGSB 7399 China: Tibet Autonomous Region von Oheimb et al. (2011) R. auricularia KU950448 Mlym58 Russia: Severnaya Dvina delta, Aksenova et al. Lapominka village (2016b) R. auricularia MH189895 Mlym156/3 Russia: Yamalo-Nenets Autonomous Aksenova et al. Area, Krasnoselkup village (2018) R. auricularia MH189996 Mlym159 Russia: Moscow Region, Serpukhov Aksenova et al. district, the village of Turovo (2018) R. makhrovi MH189860 Mlym35 China: Tibet, roadside ditch, west of Aksenova et al. the mouth of the Lhasa River (2018) R. makhrovi MH189861 Mlym36 China: Tibet, roadside ditch, west of Aksenova et al. the mouth of the Lhasa River (2018) R. makhrovi MH189862 Mlym36/1 China: Tibet, roadside ditch, west of Aksenova et al. the mouth of the Lhasa River (2018) Tibetoradix MH189865 Mlym38 China: Tibet, Lhasa River basin Aksenova et al. hookeri* (2018) T. kozlovi* MH190046 Mlym685/1.1 China: pool in the Requ Qu River Aksenova et al. valley (Yellow River basin) (2018) *These species were used as outgroup for Maximum likelihood analyses.

The identification of collected snails as belonging to an undescribed species was carried out on the basis of shell morphology, anatomy of reproductive organs, and molecular data. Measurements and dissections of snails were performed following the standard scheme (Kruglov 2005). We examined taxonomically significant parts of the male and female reproductive systems, including the copulative apparatus, the prostate, the bursa copulatrix and its duct. The photographs of shells and internal structures were made using a stereomicroscope (Leica M165C, Leica Microsystems, Germany) with a digital camera (Canon EOS 1100D, Canon, Japan). DNA extraction, PCR, sequencing and sequence alignment were performed as described in our previous work (Bolotov et al. 2017; Aksenova et al. 2018). This study includes new DNA sequence data for 14 Radix specimens (Table 1). New sequences of the mitochondrial cytochrome c oxidase subunit I (COI) (14 sequences) and the nuclear large ribosomal RNA (28S rRNA) gene fragment (2 sequences) were amplified from these Radix samples. The maximum likelihood phylogenetic analyses were based on the COI data set of the radicine pond snails with 32 unique haplotypes (Table 1). These analyses were carried out with an online version of IQ- TREE v1.6.11 (Trifinopoulos et al. 2016) using an ultrafast bootstrap algorithm (Hoang et al. 2017) and an automatic identification of the most appropriate substitution models (Kalyaanamoorthy et al. 2017). Sequences of two species of genus Tibetoradix Bolotov, Vinarski & Aksenova, 2018 were used as outgroup. To estimate the phylogeographic relationship between haplotypes of the new species and other Radix taxa, we applied a network-based approach using Network v. 4.6.1.3 software with default settings (Bandelt et al. 1999). The molecular diagnosis of the new species was designed as described by Aksenova et al. (2018). Mean uncorrected COI p-distance to the sister species was calculated using MEGA 7 (Kumar et al. 2016). The molecular diagnosis of the new species was designed as described in Bolotov et al. (2017).

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Description of the new species

Family Lymnaeidae Rafinesque, 1815 Subfamily Amphipepleinae Pini, 1877 Genus Radix Montfort, 1810

Radix dgebuadzei Aksenova, Vinarski, Bolotov & Kondakov sp. nov. Figs. 1–4, Table 2 https://zoobank.org/urn:lsid:zoobank.org:pub:0C283AE4-A94E-456D-9FD4-466A97D0BABB

Type series. The holotype and paratype are deposited in ZIN (accession numbers: 1-515/2019 and 2- 515/2019, respectively), and 3 paratypes are deposited in RMBH (accession numbers: MLym-686/2, MLym- 686/3, MLym-686b). The reference DNA sequence numbers of the paratypes MLym-686/2 and MLym- 686/3 are presented in Table 2.

Table 2. Shell measurements (mm) and reference DNA sequences for the type series of Radix dgebuadzei sp. nov.

NCBI’s Body Status of Specimen Shell Shell Spire Aperture Aperture Whorls GenBank acc. whorls specimen voucher No. height width height height width number nos. (COI/28S height rRNA) Holotype 1-515/2019* 9.2 5.9 2.9 7.7 6.1 3.4 3.50 n/a Paratype 2-515/2019* 6.6 4.6 2.3 6.6 5.2 2.9 3.25 n/a Paratype Mlym-0686/2** 8.3 5.3 2.5 7.4 5.8 4.0 3.12 MN718571/ MN719901 Paratype Mlym-0686/3** 8.8 5.2 2.9 7.9 5.8 3.3 3.12 MN718572/ MN719902 Paratype Mlym-0686b** 10.5 6.9 3.1 9.3 7.4 5.2 3.25 n/a *ZIN; **RMBH; n/a – not available

Type locality. CHINA: Qinling Region, Gansu Province, Sun Jia He River (Yangtze River Basin), in the vicinity of the Shangtan village, lakelet on the shore, 33.6673°N, 106.2220°E, altitudes 1000 m above sea level, 09.ix.2017, V.S. Artamonova, A.A. Makhrov & Y. Fang leg.

Etymology. Species is named in honor of Dr. Yury Yu. Dgebuadze, an Academician of the Russian Academy of Sciences, leading hydrobiologist, well-known researcher of Central Asia, and the organizer of the Russian-Chinese scientific expeditions for freshwater biodiversity studies throughout the Qinling Mountains and Tibetan Plateau.

Differential diagnosis. Externally, shell of Radix dgebuadzei sp. nov. is rather similar to the shells of Radix plicatula and R. euphratica (Mousson, 1874) (see Aksenova et al. 2018 for their morphological characteristics), but the new species can be distinguished from the latter taxa by a smaller size (shell size of Radix plicatula and R. euphratica may reach 20 mm or a bit more) and by spire height and aperture shape (Fig. 2G, J). Also, Radix dgebuadzei sp. nov. has a darker mantle pigmentation and clearer “freckles” (small black dots) on the foot (Fig. 2C, D) compared to the two other species (Fig. 2H, I, K).

Molecular diagnosis. The most reliable method of identification of this species is molecular diagnostics. Phylogenetically, the new species is most closely related to Radix plicatula and R. euphratica (mean uncorrected COI p-distances 7.7% and 5.8%, respectively) (Fig. 3) but can be distinguished from all other Radix congeners by 3 fixed nucleotide substitutions in the COI gene as follows: 212 C, 314 T, 485 C. The nucleotide substitutions that distinguish the new species from the other are synonymous. Two previously unknown haplotypes were found within the studied sample (Fig. 4). The 28S gene fragment has not unique substitutions.

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Figure 2. Shell shape, mantle and foot pigmentations, and fragments of the reproductive system of lymnaeids: A) Radix dgebuadzei sp. nov., the holotype, shell (ZIN); B) R. dgebuadzei, shells of the paratypes (RMBH); C) R. dgebuadzei, mantle pigmentation, a paratype (RMBH); D) R. dgebuadzei, pigmentation on the back of the head, a paratype (RMBH); E) R. dgebuadzei, the copulatory apparatus of a paratype (RMBH); F) R. dgebuadzei, a fragment of the female reproductive system of the paratype (RMBH); G) R. plicatula, shells of samples from Sun Jia He River, China (RMBH); H) R. plicatula, mantle pigmentation (RMBH); I) R. plicatula, pigmentation on the back of the head (RMBH); J) R. euphratica, shells of samples from Tajikistan (RMBH); K) R. euphratica, mantle pigmentation (RMBH). Scale bar = 2 mm. (Photos: O.V. Aksenova, M.V. Vinarski).

Figure 3. Maximum likelihood phylogeny of Radix species based on the COI barcode sequence dataset (n=56). Radix dgebuadzei sp. nov. is in red. Black numbers near nodes are bootstrap support values. Scale bar indicates the branch length.

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Description. Shell morphology. Shell small (up to 10.5 mm in height) (Fig. 2A, B), relatively thick-walled, light brown colored, ovoid or drop-like in shape, with moderately enlarged body whorl and relatively high spire (spire constitutes approximately 1/3 of a total shell height). Whorl number 3.12–3.50. Tangential line almost straight. Whorls very weakly convex, separated by shallow suture. Shell surface sculpture represented by thin axial growth lines. Aperture ovoid, its basal margin evenly rounded. Columellar fold almost invisible. Columellar lip thin and narrow, umbilicus absent. The measurements of the type series are presented in Table 2. Soft body. Mantle black with white spots and “freckles” on the foot (Fig. 2C, D). Reproductive anatomy. The structure of the copulatory organ is typical for the radicines (Fig. 2E). Praeputium is oblong, light gray, its width is almost the same along the entire length. The penis sheath narrower, its distal end somewhat swollen. The praeputium length slightly shorter or equal to the length of the penis sheath. The spermathecal duct long (Fig. 2F). Prostate with a single fold inside (not shown).

Habitat. The type specimens were collected from a fast-flowing mountain river with transparent water, rapids and runs, on the stones.

Distribution. Known only from its type locality, the Sun Jia He River, Gansu Province, China (Fig. 1). It is likely that this species can also be found in surrounding areas of the Yangtze River basin.

Figure 4. Median-joining network of the COI sequences of the Radix alticola species group (R. alticola, R. dgebuadzei sp. nov., R. euphratica, R. plicatula, and R. sp. Trichonis) (n=56). The red numbers near branches indicate the numbers of nucleotide substitutions between haplotypes. Size of circles corresponds to the number of available sequences for each haplotype (smallest circle = 1 sequence).

Discussion

Our novel data reveals that it is necessary to continue research on the diversity of freshwater mollusks in China. There is a plethora of nominal species of Chinese aquatic gastropods described on the basis of shell

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Acknowledgements This study was supported by the Ministry of Science and Higher Education of Russia, the Ministry of Europe and Foreign Affairs of France (MEAE), and the Ministry of Higher Education, Research and Innovation of France (MESRI) under project No. 05.616.21.0114 of the Hubert Curien Partnership (PHC) for the Franco-Russian Cooperation for Science and Technology (PHC Kolmogorov 2019). The work was carried out with the support and equipment of the Russian Museum of Biodiversity Hotspots, N. Laverov Federal Center for Integrated Arctic Research, Russian Academy of Sciences, a Unique scientific setting (www.ckp-rf.ru/usu/352654). The authors are thankful for the help during field trip to their colleagues V.V. Bobrov, E.A. Koblik, V.S. Lebedev, S.V. Pavlova, B.I. Sheftel.

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