Taxonomy and trans-Beringian biogeography of the pond snails (Gastropoda: Lymnaeidae) of East Asia: an integrative view Author Aksenova, Olga V. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia aksyonova.olga@gmail.com Author Vinarski, Maxim V. Laboratory of Macroecology and Biogeography of Invertebrates, Saint Petersburg State University, 7 / 9 Universitetskaya Embankment, 199034 Saint Petersburg, Russia Author Itagaki, Tadashi Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Morioka, Iwate, Japan Author Ohari, Yuma Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, Morioka, Iwate, Japan & Laboratory of Parasitology and Zoology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Japan Author Oshida, Tatsuo Laboratory of Wildlife Biology, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Japan Author Kim, Sang Ki Nakdonggang National Institute of Biological Resources, Gyeongsangbuk-do, Sangju, 37242, Republic of Korea Author Lee, Jin Hee Daegu Science High School, Daegu, 42110, Republic of Korea Author Kondakov, Alexander V. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Khrebtova, Irina S. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Soboleva, Alena A. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Travina, Oksana V. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Sokolova, Svetlana E. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Palatov, Dmitry M. Laboratory of Macroecology and Biogeography of Invertebrates, Saint Petersburg State University, 7 / 9 Universitetskaya Embankment, 199034 Saint Petersburg, Russia & A. N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, 33 Leninsky Prospekt, 119071 Moscow, Russia Author Bespalaya, Yulia V. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia & Laboratory of Macroecology and Biogeography of Invertebrates, Saint Petersburg State University, 7 / 9 Universitetskaya Embankment, 199034 Saint Petersburg, Russia Author Vikhrev, Ilya V. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Gofarov, Mikhail Yu. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia Author Bolotov, Ivan N. N. Laverov Federal Center for Integrated Arctic Research of the Ural Branch of the Russian Academy of Sciences, Nikolsky Avenue 20, 163020 Arkhangelsk, Russia text Zoological Journal of the Linnean Society 2024 2024-08-03 201 4 1 24 http://dx.doi.org/10.1093/zoolinnean/zlae083 journal article 303333 10.1093/zoolinnean/zlae083 eee378cb-445c-4c72-9d56-8db55f4670f9 0024-4082 13772599 B848A01-DC8F-4759-91E9-237E4526462C Subfamily Lymnaeinae Rafinesque, 1815 Type genus: Lymnaea Lamarck, 1799 . Genus Dallirhytis Kruglov & Starobogatov, 1989 Kruglov and Starobogatov 1989: 15 . Figure 1. Species richness and distribution of pond snails ( Lymnaeidae ) on the eastern margin of Asia and Alaska. A, regional zonation of East Asia and Alaska based on the distribution of Lymnaeidae . The numbers in white circles indicate the number of species in corresponding regions. B, scatter plot of principal component (PC) analysis based on the presence–absence dataset of pond snails ( Lymnaeidae ) throughout regions of East Asia and Beringia. Distribution areas: ALA, Alaska; AMU, Amur River basin and Primorye; CHU, Chukchi Peninsula; HON, Honshu; HOK, Hokkaido; ḎM, Kamchatka Peninsula; KOL, Kolyma Highlands; KOR, Korean Peninsula; KUR, Kurile Archipelago; OKH, Okhotsk Sea Coast; SAK, Sakhalin Island. The data on pond snail occurrences are presented in Table 3. PC1 and component PC2 accounted for 38.8% and 21.1% of the total variance, respectively. The map was created using ESRI ARCGIS v.10 software (www.esri.com/arcgis). Figure 2. Maximum likelihood consensus phylogeny of the Lymnaeidae (five partitions: three codons of COI + 16S rRNA + 28S rRNA). Black numbers near nodes are bootstrap support values. Non-target clades are collapsed. The names of taxa recorded in the Far East are red; those having trans-Beringian (Holarctic) ranges are blue; that of the species endemic to Alaska is green; and the names of alien species are purple. The outgroup taxa are omitted. Information on COI , 16S rRNA, and 28S rRNA sequences that were used to build the tree is given in the Supporting Information (Table S1). Table 2. Taxonomic review of the pond snails ( Lymnaeidae ) from East Asia and Alaska.

Genus	Species	Type locality	Distribution
Subfamily Lymnaeinae Rafinesque, 1815
Tribe Lymnaeinae incertae sedis
Dallirhytis Kruglov &	Dallirhytis atkaensis ( Dall, 1884 )	USA: Aleutian Islands ( Dall 1884 ) Russia: Chukchi Peninsula;
Starobogatov, 1989 stat. rev.	Canada; and USA: Alaska and
Aleutian Islands
Galba Schrank, 1803	Galba pacifica	Japan: Hokkaido Prefecture,	Japan: Hokkaido; Russia: Sakhalin
Biei Town, the Ishikari River	Island and Kurile Archipelago,
system, a ditch near the	and Kamchatka
Rubeshibe Stream, 43.520331°N,
142.372452°E
Galba humilis a ( Say, 1822 )	USA: South Carolina, without a	North America, including the USA,
precise locality ( Say 1822 )	Canada, and Mexico; Japan:
Honshu (non-native) (Saito
2022)
Galba schirazensis a (Küster, 1862)	‘Schiras in Persien’ (Iran: Schiras,	Japan: Hokkaido (non-native);
approximately 29.5971°N,	Iran, Egypt, Reunion, Spain,
52.5834°E) (Küster 1862)	Dominican Republic, Mexico,
Colombia, Venezuela, Ecuador,
and Peru ( Lounnas et al. 2018 ,
Ohari et al. 2020 )
Walhiana Servain ,	Walhiana catascopium	‘The Delaware river and many	Russia: Kamchatka; Canada; USA
1882 = Walterlymnaea	(Say, 1817) comb. nov.	other waters of the United States’ (including Alaska); and
GreenStarobogatov & Budnikova, 1976	( Say 1817b )	land
syn. nov.
Walhiana arctica (Lea, 1864)	Canada: Ontario, Moose River of	USA: Alaska; Northern Canada
comb. nov.	Hudson’s Bay	eastwards to Newfoundland
( Burch 1989 )
Ladislavella B. Dybowski, 1913	Ladislavella liogyra (Westerlund,	‘Sibirien, Sud-Ussuri-Gebiet,	Russia: Ussuri River basin,
1897)	Dorf Griqorjewskoje’ (Russia:	Primorye, and Sakhalin Island
southern part of the Ussuri
Region, Grigoryevskoye village,
approximately 44.16°N, 132.00°E)
( Westerlund 1897 )
Pseudosuccinea Baker, 1908	Pseudosuccinea columella a (Say,	‘Stagnant waters and miry places	North America; as a non-
1817)	[of North America]’ ( Say 1817b ) indigenous species is widely
distributed over tropics and
subtropics, including Japan
Tribe Lymnaeini Rafinesque, 1815
Lymnaea Lamarck, 1799	Lymnaea sorensis B. Dybowski ,	Russia: ‘Lake Baikal, Bolshoy Sor	Widespread throughout North
1912	Bay’ ( Dybowski 1912 )	Asia: Western Siberia: Tyumen
Region; Eastern Siberia: Altai
Mountains, Lake Baikal, Yakutia;
Mongolia; northern China:
Xinjiang, and Kamchatka
Subfamily Amphipepleinae Pini, 1877
Tribe Peregrianini Bolotov, Vinarski & Aksenova, 2023
Kamtschaticana Kruglov &	Kamtschaticana kamtschatica	‘Kamtschatka’ (Middendorff	Widespread throughout North
Starobogatov, 1984	( Middendorff, 1850 )	1850); ‘See Kainytschin, ohnfern Asia: Eastern Siberia and
RusNishne-Kamtschatsk’ (Russia:	sian Far East from Lake Baikal
Kamchatka, a lake near the	through the Amur River basin to
former Nizhne-Kamchatsk vil-	Kamchatka, Magadan Region,
lage, approximately 56.3819°N,	and Chukotka Peninsula; several
161.1570°E) (Middendorff,	times mentioned for Alaska
1851)

Table 2. Continued

Genus	Species Type locality		Distribution
Kamtschaticana Japan: Hokkaido Prefecture,		Japan: Hokkaido
nipponica = Radix sp. Ra-c2	Sarabetsu village, the Tokachi
Ohari et al. , 2020	River system, Itarataraki Stream,
42.627161°N, 143.265175°E
Kamtschaticana sp.1 (possible not available		Russian Far East: Kamchatka and
undescribed species)	Sakhalin Island
Tribe Austropepleini Bolotov, Vinarski & Aksenova, 2023
Orientogalba Kruglov &	Orientogalba hokkaidoensis Japan: Hokkaido Prefecture,		Japan: Hokkaido and Honshu
Starobogatov, 1985	Hokuto City, a ditch near the
Hikirichi Stream, 41.842808°N,
140.634441°E
Orientogalba ollula ( Gould, 1859 ) Streams and marshes on Hong		East Asia: Korea, Japan (Hokkaido
Kong Island ( Gould 1859 )	and Honshu); Central Asia:
Uzbekistan; South Asia: Nepal; and
China: Tibet and Hong Kong
Tribe Radicini Vinarski, 2013
Radix Montfort, 1810	Radix auricularia (Linnaeus, 1758) Europe (Vinarski and Kantor		Widespread throughout Northern
2016)	Eurasia, Kurile Archipelago,
Sakhalin Island, Japan, Alaska
and West Canada (British
Columbia)
Radix onychia ( Westerlund, 1883 ) ‘Japan, ad litora lacus Biva’		Japan: Honshu (endemic to Lake
(Japan: shores of Lake Biwa)	Biwa)
( Westerlund 1883 )
Radix plicatula (Benson, 1842) ‘Ponds’ (China: Zhoushan Island, East Asia: Amur Basin, Korea,
= Radix coreana (Martens,	approximately 30.0578°N,	and Japan: islands of Hokkaido,
1886) syn. nov.; Type locality:	122.1381°E) (Vinarski et al .	Honshu, Kyushu, Shikoku,
‘Changjin, Prov. Hamgyöngdo, 2020)		and Okinawa; Southeast Asia:
Korea’ (North Korea: South	Vietnam, South China: Yunnan,
Hamgyŏng Province, Changjin		Taiwan, Hong Kong; Eastern
County) ( Martens 1886 );	China: Jiangsu, Hebei; Northern
= Radix sp. Ra-03 (Ohari et al. ,	China: Xinjiang; and Eastern
2020)	Tibet: Gansu
Probable synonyms:
= Radix japonica (Jay, 1857) ;
Type locality: Simoda (Japan:
Honshu, Simoda, approximately
34.6795°N, 138.9453°E) (Jay
1857)
= Radix hamadai Habe, 1968 ;
Type locality: ‘Kobaru, Takeda
City, Oita Pref., Kyushu’ (Japan:
Kyushu, Ōita Prefecture, Taketa, Kobaru, approximately
32.8738°N, 131.3581°E) ( Habe
1968)

aNon-native species. Type species: Lymnaea petersi Dall, 1905 = Limnaea ovata var. atkaensis Dall, 1884 (by original designation). Diagnosis: Shell medium in size, ovate-conical to almost ear-shaped, with well-developed acute spire ( Fig. 3A, B ). Whorls are conspicuously inflated. Praeputium cylindrical, oblong, dark-pigmented; penis sheath rather short and compact; its length is 2.5–3.0 less than the praeputium length ( Fig. 4A ). Penis with a (rudimentary) ring-shaped fixing swelling [ Walter (1969) calls it the ‘penial knot’]; prostate with a single internal fold. Species richness: This is a monotypic genus. In addition to Dallirhytis atkaensis , Kruglov and Starobogatov (1989 , 1993 ) listed another species, Lymnaea petersi Dall, 1905 . However, we synonymize both species based on examination of samples of Ly. petersi kept in ZIN . We found that the conchological variability of Ly. petersi falls within the range of variability of D. atkaensis . The ranges of both taxa as accepted byKruglov and Starobogatov (1993) overlap almost completely. Dallirhytis atkaensis has a very characteristic shell appearance and can hardly be confused with another pond snail species of Beringia. Figure 3. Shells of the Lymnaeinae species. A, Dallirhytis atkaensis (USA, Alaska, Birch Lake; RMBH). B, Dallirhytis atkaensis (Russia, the Chukchi Peninsula, an unnamed lake; ZIN). C, Galba sibirica (Mongolia, the Teellin-gol River; after Vinarski et al. 2017b ). D, Galba truncatula (Russia, Irkutsk Region, vicinities of Kirensk Town; LMBI). E, Ladislavella liogyra (Russia, Amur basin, vicinities of Nikol’sk-Ussuriysky Town; ZIN). F, Walhiana arctica (Canada, Ontario, Hudson’s Bay; NHMUK). G, Walhiana catascopium (Canada, British Columbia, Aintworth hot springs; RMBH). H, Walhiana catascopium (Russia, Kamchatka, Azabachye Lake; RMBH). I, Lymnaea jugularis (USA, Michigan, the Rouge River; NHMUK). J, Lymnaea sorensis (Russia, Lake Baikal, a syntype; ZIN). K, Lymnaea jugularis (USA, Minnesota, a neotype with label; ZIN). Scale bars: 2 mm in C, D, F–H; 5 mm in A, B, E, I–K. Photographs: Maxim V. Vinarski (A–F, I–K) and Olga V. Aksenova (G, H). Figure 4. The copulatory apparatuses of the pond snails discussed in the taxonomic account. A, Dallirhytis atkaensis (Russia, the Chukchi Peninsula, Lake Vaaliuchio). B, Galba sibirica (Mongolia, the Teellin-gol River; after Vinarski et al. 2017b ). C, Galba truncatula (Abkhazia, Gagra District, wet shore of Inkit Lake; after Vinarski et al. 2017b ). D, Ladislavella liogyra (Russia, Primorye, a pool near Lake Lebedinoye). E, Walhiana catascopium (Russia, Kamchatka, Azabachye Lake; RMBH). F, Lymnaea sorensis (Russia, Kamchatka, Kamchatka River; RMBH). G, Kamtschaticana kamtschatica (Russia, Magadan Region, a water reservoir; after Vinarski et al. 2021 ). H, Orientogalba ollula (Russia, Primorye Territory, near Possiet Settlement; after Kruglov 2005 ). I, Radix auricularia (Russia, Tyumen’ Region, Vylposl channel near Labytnangi Town). J, Radix plicatula (China, Bejing, an artificial pond in the former Emperor’s summer palace; after Vinarski et al. 2020 ). K, Radix cf. hamadai (Japan, Matsumae; after Vinarski et al. 2020 ). Scale bars: 1 mm. Photographs: Maxim V. Vinarski (A–D, G, I–K) and Olga V. Aksenova (E, F). Distribution: A Beringian taxon known from Alaska , the Yukon Territory , northern British Columbia , and the Chukchi Peninsula ( Burch 1989 , Kruglov 2005 , Aksenova et al. 2023 ).