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Overwintering and Cold Tolerance in the Moor Frog (Rana Arvalis, Anura) Across Its Range

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Overwintering and Cold Tolerance in the Moor Frog (Rana Arvalis, Anura) Across Its Range Canadian Journal of Zoology Overwintering and cold tolerance in the moor frog (Rana arvalis, Anura) across its range Journal: Canadian Journal of Zoology Manuscript ID cjz-2019-0179.R4 Manuscript Type: Article Date Submitted by the 08-Aug-2020 Author: Complete List of Authors: Berman, Daniil; Institute of Biological Problems of the North FEB RAS, FEB RAS Bulakhova, Nina; Institute of Biological Problems of the North FEB RAS, FEB RAS; Research Institute of Biology and Biophysics, Tomsk State University Draft Meshcheryakova, Ekaterina; Institute of Biological Problems of the North FEB RAS, FEB RAS Shekhovtsov, Sergey; Institute of Cytology and Genetics SB RAS; Institute of Biological Problems of the North FEB RAS, FEB RAS Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Rana arvalis, moor frog, geographic range, geographical variation of cold Keyword: tolerance, overwintering temperature conditions, lower lethal temperature, supercooling point https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 38 Canadian Journal of Zoology 1 Overwintering and cold tolerance in the moor frog (Rana arvalis, Anura) across its range D.I. Berman, N.A. Bulakhova, E.N. Meshcheryakova and S.V. Shekhovtsov D.I. Berman. Institute of Biological Problems of the North FEB RAS, Portovaya St. 18, 685000 Magadan, Russia (e-mail: [email protected]). N.A. Bulakhova. Institute of Biological Problems of the North FEB RAS, Portovaya St. 18, 685000 Magadan, Russia; Research Institute of Biology and Biophysics, Tomsk State University, Pr. Lenina 36, 634050 Tomsk, Russia (e-mail: [email protected]). E.N. Meshcheryakova. Institute of Biological Problems of the North FEB RAS, Portovaya St. 18, 685000 Magadan, Russia (e-mail:Draft [email protected]). S.V. Shekhovtsov. Institute of Cytology and Genetics SB RAS, Pr. Lavrentieva 10, 630090 Novosibirsk, Russia; Institute of Biological Problems of the North FEB RAS, Portovaya St. 18, 685000 Magadan, Russia (e-mail: [email protected]). Corresponding author: Nina A. Bulakhova (e-mail: [email protected]). https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 38 2 D.I. Berman, N.A. Bulakhova, E.N. Meshcheryakova and S.V. Shekhovtsov Overwintering and cold tolerance in the moor frog (Rana arvalis, Anura) across its range Abstract: Only two species of boreal Holarctic frogs (genus Rana) can survive freezing and overwinter on land; they are found in the subarctic and cold regions of North America (Rana sylvatica LeConte, 1825) and Eurasia (Rana arvalis Nilsson, 1842) and are an example of an unusual adaptive strategy of overwintering. Freeze tolerance (down to -16°C) of R. sylvatica has been thoroughly studied; however, little is known about cold resistance of R. arvalis in cold regions. We found that R. arvalis from European Russia and from West Siberia tolerate freezing down to -12 or -16°C, while frogs from Danish population survived freezing only to - 4°C (Voituron et al. 2009b). All of Draftthese populations, according to mtDNA markers, are closely related. We suggest that the observed differences in cold tolerance (-4°C vs -12 or - 16°C) could be caused either by adaptations to climatic factors or by differences in experimental protocols. The northeastern boundary of the geographic range of R. arvalis in Yakutia coincides with the transitional area between discontinuous and continuous permafrost; beyond this area, winter soil temperature sharply declines. The lower lethal temperature and overwintering ecology of R. arvalis in Siberia are similar to those of the North American R. sylvatica. Key words: Rana arvalis, moor frog, geographic range, geographic variation of cold tolerance, overwintering temperature conditions, supercooling point, lower lethal temperature. https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 38 Canadian Journal of Zoology 3 Introduction Only a few amphibian species inhabit cold northern and inner continental regions of Eurasia and North America. They possess amazing adaptive abilities to survive under extremely low winter temperatures. These adaptations have not been adequately studied yet, although the available data on the Siberian salamander (Salamandrella keyserlingii Dybowski, 1870), the wood frog (Rana sylvatica LeConte, 1825), and the Japanese tree frog (Hyla japonica Günther, 1859) are of significant interest (Berman et al. 1984, 2016b, 2016c; Storey and Storey 2004; Berman and Meshcheryakova 2012; Costanzo et al. 2013; Larson et al. 2014). In this context, cold tolerance of the moor frog (Rana arvalis Nilsson, 1842) deserves attention. This species is widespread inDraft the Palearctic, from France to southwestern Yakutia. It is found in the North, up to the zonal tundra in Fennoscandia, in European Russia, and in Siberia; to the south as far as northwestern China and Transbaikalia (Bannikov et al. 1977; Borkin et al. 1984). Of all species of the genus Rana, only R. arvalis and R. sylvatica can survive freezing. The Alaskan R. sylvatica tolerate exposure down to -16°C (Costanzo et al. 2013) and probably even to -18°C (Larson et al. 2014); this is the highest cold tolerance so far observed within the genus Rana. In contrast to R. sylvatica, the studied populations of Rana arvalis from Denmark could withstand only -4°C for 3-4 days (Voituron et al. 2009b). Winter temperatures in northern Asia are much lower than in Denmark. For example, in the city of Olekminsk (southwestern Yakutia), the average January air temperature is below -32°C with the absolute minimum of -59°C (Izyumenko 1989). Two hypotheses can be suggested on how the moor frog manages to overwinter. The first is overwintering in water, a highly effective way to avoid very low negative temperatures. Overwintering in water was mentioned for moor frogs in Central Russia, northern West Siberia, and Yakutia (Krasavtsev 1939; Belimov and Sedalishchev 1979; Matkovskiy and Starikov 2011). However, Krasavtsev https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 38 4 (1939) reported that overwintering in water is extremely rare for this species (only three findings with one or two individuals in each). Two other sources did not list any specific records. If R. arvalis overwinter in water, cold tolerance can be limited just to a few degrees below zero as known for frog species overwintering in water (Lotshaw 1977; Costanzo et al. 1993; Voituron et al. 2005, 2009a; Berman et al. 2017). The second option is overwintering on land, which requires much higher cold tolerance, as demonstrated for the wood frog (R. sylvatica) in Alaska. Indeed, the moor frog is known to overwinter on land almost everywhere across its range, in contrast to other Rana species of the northern Palearctic. It usually overwinters in pits with a thick layer of leaf litter, between tree and stump roots, etc. (Krasavtsev 1939; Terentyev 1950). Therefore, in order to survive in Siberia, especially in its northeast, R. arvalis must have a muchDraft higher cold tolerance than that found in the Denmark population. It is unclear how exactly the moor frog manages to survive in regions with harsh winter. It could be that cold tolerance of this species is geographically variable, similar to that observed for wood frogs (R. sylvatica). In contrast to northern populations (Fairbanks, Alaska), wood frogs from southern populations have much lower cold tolerance; they survived at -5°C for 14 days in Pennsylvania, USA (Layne 1995) and at -6°C for 11 days in Ottawa, Canada (Storey and Storey 1984). In the same way, higher cold tolerance would be expected in moor frogs (R. arvalis) from Siberia than in those from Denmark. However, we have not found any studies of the moor frog that would specifically address temperature regimes in the overwintering sites on land for this species. To search for such overwintering sites is extremely time-consuming and does not guarantee success. The only way to clarify this issue is to conduct experiments in order to determine a potential cold tolerance of the moor frogs from the regions with a harsh winter. Since the mechanisms of https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 38 Canadian Journal of Zoology 5 geographic variation of cold tolerance are yet unknown, one cannot exclude the possibility that it is genetically determined (Larson et al. 2014). The goal of this study was to determine cold tolerance of moor frogs from the regions with strongly differing winter climates: European Russia and Siberia. We also conducted phylogenetic (mtDNA marker) analysis of all studied moor frog populations in order to determine their genetic similarity. Materials and Methods Animals Live moor frogs were collected from two populations from the south of West Siberia (near Karasuk town, Novosibirsk Оblast, 53°N, 78°E, n = 60; near Podgornoye village, Tomsk Оblast, 57°N, 82°E, n = 28), Draftas well as from one population from European Russia (near Chernogolovka town, Moscow Oblast, 56°N, 38°E, n = 47) (Fig. 1). The maximum cold tolerance could be expected in the easternmost part of the species’ range (southwestern Yakutia); however, collecting there was not possible since R. arvalis is listed as a rare species in the local Red Book (2010). Adult frogs from West Siberia (average mass 13.1±0.3 g) were collected in mid- August – early September; in Chernogolovka (14±0.6 g), in September. In order to study their cold tolerance, the animals were delivered to the Laboratory of Biocenology of the Institute of Biological Problems of the North in Magadan in
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