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Rana Macrocnemis Boulenger, 1885) (Amphibia, Anura) to Negative Temperatures on Land and to Hypoxia in Water During Overwintering

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Rana Macrocnemis Boulenger, 1885) (Amphibia, Anura) to Negative Temperatures on Land and to Hypoxia in Water During Overwintering Herpetology Notes, volume 13: 1079-1086 (2020) (published online on 28 December 2020) Resistance of the Iranian long-legged wood frog (Rana macrocnemis Boulenger, 1885) (Amphibia, Anura) to negative temperatures on land and to hypoxia in water during overwintering Nina A. Bulakhova1,2, Lyudmila F. Mazanaeva3, Ekaterina N. Meshcheryakova1,*, and Daniil I. Berman1 Abstract. We studied resistance of the frog Rana macrocnemis Boulenger, 1885 from the highlands of the Republic of Dagestan (Russia) to negative temperatures and to hypoxia in water, which allow this frog species to overwinter on land or in water bodies. The average supercooling point (SCP) for R. macrocnemis is -2.1 °C. However, the state of supercooling is unstable, quickly turning into freezing, which frogs can survive only for a few hours. For this species, the lower lethal temperature (LLT) is -1 °C: only 5% of frogs (one of 20 studied individuals) survived exposure to this temperature during five days. Such low cold resistance severely limits overwintering on land. When overwintering in water, R. macrocnemis is unable to survive oxygen deficiency for a long time. The lethal (lowest) concentration, which species tolerated for one day, is 1.3–1.9 mg/L. Only 37% of the frogs (three of eight individuals) survived the oxygen concentration of 3–4 mg/L longer than 15 days and only 13% (one of eight frogs) survived it longer than 50 days. Therefore, Rana macrocnemis is non-cold-resistant, oxyphilic, and in cold winter can survive only in the oxygen-rich water bodies. Its overwintering on land can be successful only in the warmest regions of the range. Keywords. Supercooling point, lower lethal temperatures, thresholds of hypoxia in water, hibernation, Dagestan, Russia Introduction an annual rainfall of less than 600 mm (Tarkhnishvili and Gokhelashvili, 1999). The Iranian long-legged wood frog (Rana macrocnemis A poorly studied aspect of R. macrocnemis ecology Boulenger, 1885) that belongs to the group of brown are localities and conditions of overwintering, which is frogs is an essential inhabitant of mountain forests and known to occur both on land and in water. Individuals mesophytic meadows of the Caucasus, Asia Minor, overwintering on land were found in the burrows of and North Western Iranian Plateau (Tarkhnishvili small mammals, gaps between tree roots, leaf litter, etc. and Gokhelashvili, 1999). In the forests of the (Tuniyev and Beregovaya, 1993; Askenderov, 2014). In northern foothills and in the mountains of the Central water, they were found in mountain rivers, streams, and Ciscaucasia, its population density reaches 1,000 per ha springs, where large clusters of frogs occasionally form, or more (Tertyshnikov et al., 1979). In the Caucasus, sometimes in silt at the bottom of backwaters (Popov, the upper distribution limit is 3,200 m above sea level 1958; Tuniyev and Beregovaya, 1993; Tarkhnishvili and (Alekperov, 1978). This frog rarely occurs in areas with Gokhelashvili, 1999; Askenderov, 2014). Tarkhnishvili and Gokhelashvili (1999) believe that the choice of overwintering location depends on age and habitat. For example, in forests, young individuals overwinter on land, and adults overwinter both on land and in water; in 1 Institute of Biological Problems of the North FEB RAS, subalpine meadows, they overwinter in lakes. According Magadan 685000, Russia. to Bülbül et al. (2019), R. macrocnemis remains on land 2 Research Institute of Biology and Biophysics, Tomsk State in the absence of suitable water bodies. It is generally University, Tomsk 634050, Russia. 3 Department of Zoology and Physiology, Faculty of Biology, difficult to determine the preferred overwintering sites Dagestan State University, Makhachkala, the Republic of based on the frequency of occurrences in water and in Dagestan 367000, Russia. the ground, since frogs are much easier to observe in * Corresponding author. E-mail: [email protected] water than in ground shelters. 1080 Nina A. Bulakhova et al. In soils, negative temperature (in addition to substrate p = 0.34) and males (U-test p = 0.79), the frogs were moisture) could be the main limiting factor for combined into a single sample. overwintering. In water, however, the limiting factor The frogs were placed in containers with wet moss, could be hypoxia (decrease in the concentration of and transported to the Laboratory of Biocoenology of dissolved oxygen). R. macrocnemis could be adapted to the Institute of Biological Problems of the North, Far hypoxia, since it overwinters not only in the mountain Eastern Branch of the Russian Academy of Sciences streams (Popov, 1958; Papanyan, 1961; Tarkhnishvili (Magadan, 59°34ʹ N, 150°48ʹ E), which had the and Gokhelashvili, 1999), where oxygen content is equipment necessary for the experiments. high, but also in the silt of river backwaters, lakes, and Ethical Compliance.—All procedures were ponds (Popov, 1958; Askenderov, 2014), where hypoxic performed in accordance with international guidelines conditions are very likely. for biomedical research involving animals (Council In this study, we assessed the limits of physiological of International Organizations of Medical Sciences, capabilities of R. macrocnemis that define its 1985). The collection permit series 05 No. 0001 dated overwintering conditions on land and in water. The 9 October 2019 was issued by the Ministry of Natural first goal of the present work was the experimental Resources and Ecology of the Republic of Dagestan. determination of threshold cold resistance values of the Determination of cold resistance.—Animals in general species. The second goal was to determine the species’ possess two types of response to negative temperatures: resistance to deficiency of oxygen dissolved in water. (1) surviving the freezing of body fluids and (2) ability The response of R. macrocnemis to negative to remain in a supercooled state for a short or long time temperatures or hypoxia in water has never been studied (for these animals, freezing is fatal). An organism’s instrumentally, and the present study partially fills this ability to tolerate cooling below 0 °C is characterised gap. by two parameters: the supercooling point (SCP) and the lower lethal temperatures (LLT). Determination Material and methods of SCP allows to assess the minimum temperature at Specimen collection.—The mountainous part of which an animal can safely be supercooled for a brief Dagestan, where Rana macrocnemis were caught for period before freezing. Determination of LLT allows to the experiments, is located in the northeastern Caucasus (Fig. 1). The climate there is dry and temperate continental; in high mountain regions, winter begins already in October, and a perennial snow cover forms in November; annual precipitation in the mountains ranges from 800 to 1,200 mm. The coldest month is January with an average air temperature of -11 °C; frosts down to -30 °C, as well as thaws may also occur. Adult frogs were collected in late September until early October in two areas: on the Khunzakh Plateau (14 females and 9 males) in the vicinity of the Tumagari village (42º35ʹ N, 46º36ʹ E, 1,820 m a.s.l.) and in the Kazikumukhskoe Koisu River Valley (13 females and 4 males) in vicinity of the villages of Kumukh (42º10ʹ N, 47º06ʹ E, 1,540 m a.s.l.) and Vachi (42º04ʹ N, 47º13ʹ E, 1,770 m a.s.l.). The average body weight of female frogs caught in the above-listed locations was 34.0 ± 2.7 (16–53) g and 38.3 ± 3.6 (16.4–58.8) g, respectively; for males, it was 34.2 ± 3.2 (24.7–59.3) g and 30.5 ± 2.6 (26.7–38.1) g. Considering the small distance between collection sites, similar heights, and the absence of interpopulation Figure 1. Collection territory (star) of Rana macrocnemis differences in body weight between females (U-test used in our experiments. Resistance of Rana macrocnemis to negative temperatures and to hypoxia 1081 assess the negative temperatures at which an animal can Statistical analysis was performed using standard exist for a long time (several days). These parameters of methods in Statistica v.10. All mean values are given cold resistance were determined in a programmable test with ± standard error. chamber WT-64/75 (Weiss Umwelttechnik GmbH). Determination of resistance to hypoxia in water.— The frogs were put into overwintering condition Reaction to the deficiency of oxygen dissolved in water by acclimation (gradual decrease in temperature). was studied in two stages. During the first stage, we The acclimation within the range of 16 to 1–0 °C determined the concentration, short-term (24 hours) was implemented on a 38-day scheme: one day each exposure to which is lethal for R. macrocnemis. At the at 16, 10 and 8 °С; 14 days at 5 °С; one day at 3 °C; second stage, we determined the minimum concentration and 20 days at 1–0 °С. This procedure, as well as the that allowed an individual to survive for a long time, subsequent determination of lower lethal temperatures, at least a month. By analogy with the previously our was conducted in ventilated 1.8 L plastic containers 10 studied species (R. temporaria, R. dybowskii), it was set cm high, half-filled with wet moss. To monitor possible approximately 2 mg/L above the lethal threshold, in the temperature gradients in the test chamber, a calibrated range of 3–4 mg/L. iButton DS1922L temperature logger was placed in Acclimation in this experiment was a laboratory each container. Individual error of the loggers relative imitation of the moving of frogs from land to to the value declared by the manufacturer for devices of overwintering water bodies. For this purpose, the frogs this brand (± 0.5 °C) was 0.0 °C for one logger, and +0.2 acclimated to a temperature of 1 °C in groups of 5 °C for three loggers at 0 °C.
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