INTRODUCTION

Eastern Chukotka is a vast territory of the northeastern outskirts of the Asian continent, located on the Chukotka Peninsula. Until now, this Arctic region of Russia remains one of the least studied by ichthyologists (Barsukov, 1958; Chereshnev, 1983, 1996, 1998, 2008; Savvaitova, 1989; Skopets, 1991; Gudkov, 1995; Chereshnev et al., 2002; Shestakov, 2021). Geological and biogeographic studies have convincingly proved that this region of Chukotka belongs to the territory of Beringia, a vast land that periodically emerged at the end of the Cenozoic era between Asia and North America in the region of the Bering and Chukchi Seas and served as a transit corridor between the continents for the settlement of many taxa of plants and animals (including a number of fish species), as well as the arena of forming and speciation during the separation of continents (Yurtsev, 1974; Beringia …, 1976; Starobogatov, 1986; Chereshnev, 1998; Prozorova, 2001). However, it should be noted that modern reconstructions of the history of the formation of freshwater ichthyofauna in Beringia regions are difficult without a comprehensive study of the fish fauna living here, since the status and systematic position of many species still remain controversial or unclear, especially in the Chukotka Autonomous Okrug.

The remoteness of the region, small population, and underdeveloped industry contributed to the preservation of most of the unique pristine aquatic ecosystems and their inhabitants, which include the complex aquatic–botanical natural monument Thermalny (a section of the Gilmimliveem River valley), located on the territory of the Beringia National Park (Specially …, 2020). At the same time, it is obvious that further preservation of the diversity of the Arctic freshwater ichthyofauna during the period of global warming, which has been observed on Earth in recent decades, is impossible without monitoring the state of populations of commercial species and endemic, rare taxa of unique ecosystems in Northeast Asia.

This study is aimed at analyzing the taxonomic composition and biology of freshwater fish from the Gilmimliveem River in the area of thermal mineral springs (Bering Sea basin).

MATERIALS AND METHODS

The material was collected in July 2019 in the valley of the upper reaches of the Gilmimliveem River (65°48ʹ8.41ʺ N, 173°23ʹ59.19ʺ E), where thermal springs with water temperatures from +35 to +97°С and mineralization of 1.3–4.5 g/L are located for an 800-m distance, mainly along the right bank (Vakin, 2003). The Gilmimliveem River is the left tributary of the Vytgyrveem River, which flows into the Mechigmen Bay of the Bering Sea. Fish were caught with a spinning rod, a float rod, and a net in the riverbed and in numerous floodplain water bodies and lakes located on the floodplain terrace. Immediately after they were caught, large fish (grayling, Dolly Varden char) with straightened fins were photographed: several general shots were taken, as well as shots of the head and fins. Small fish (sticklebacks, sculpins) were fixed in 70% ethanol. In total, 25 Alaskan grayling Thymallus arcticus signifer (Richardson, 1823), 10 residential dwarf Dolly Varden char Salvelinus malma (Walbaum, 1792), 35 relict three-spined stickleback Gasterosteus cf. aculeatus Linnaeus, 1758, 17 nine-spined stickleback Pungitius pungitius (Linnaeus, 1758), and 23 western slimy sculpin Cottus cognatus cognatus Richardson, 1836 were analyzed. The collected material was processed in the field and in laboratories using standard ichthyological techniques (Taliev, 1955; Pravdin, 1966; Lakin, 1990; Zyuganov, 1991). In all fish, the length to the end of the scale cover (SL) and the Smith length (FL), body weight, sex, stage of maturity of the gonads, and age were determined. The age was estimated in grayling by scales, in other fish, by otoliths. The processing of the material (scales) included measurements of the radius of scales and annual rings, counting the number of sclerites in each annual zone for a more accurate determination of age. The value of the annual ring radius was determined as the distance from the center of the scale to the outer edge of the zone of wedged out sclerites (incomplete), or to the zones of resorption of sclerites along the lateral radius of the scale plate. The measurements were carried out using a computer system for image analysis and an MBS-10 microscope with an MU 900 digital camera, using AmScope ToupView 3.1 software. Due to the small number of samples and the absence of juveniles, the linear growth of the Alaskan grayling was analyzed according to the data of inverse calculations according to Lee’s formula using the Smith length (FL) (Chugunova, 1959; Mina, 1973).

Morphological analysis of Arctic grayling and Dolly Varden char was carried out using digital images in the Adobe Photoshop CS 6 program, counting the number of gill rakers on the first arch and perforated scales in the lateral line on fresh specimens. Sticklebacks and sculpins were measured in a fixed state in accordance with the recommendations of Pichugin et al. (2003, 2004) and Taliev (1955). Before calculating the meristic signs, the bone elements of sticklebacks and sculpins were stained with an alcohol solution of alizarin (Springer and Johnson, 2000).

The following morphological characters were assessed: D, A, V, P, c, ll, sp.br., r.br., and vert. When calculating the number of vertebrae in sticklebacks, the last one was considered to be a vertebra with two articular surfaces; in sculpin vertebrae, all vertebrae, including the last one, to which the rays of the caudal fin joined.

RESULTS AND DISCUSSION

The only information about the ichthyofauna of the upper reaches of the Gilmimliveem River are presented in the monograph by Chereshnev (1996), in which four fish species are indicated for this river: the East Siberian grayling Thymallus arcticus pallasii, the resident dwarf Dolly Varden char Salvenicus malma, the relict three-spined stickleback Gasterosteus cf. aculeatus, and the western slimy sculpin Cottus cognatus cognatus. According to the results of our survey, the presence of three fish species (S. malma, G. cf. aculeatus, and C. cognatus cognatus) is confirmed for the Gilmimliveem River. The Alaskan grayling Thymallus arcticus signifer and the nine-spined stickleback Pungitius pungitius were discovered for the first time; the East Siberian grayling Thymallus arcticus pallasii was not found.

Arctic Grayling

Thymallus signifer was described by Richardson in 1823 from the Great Slave Lake basin (Richardson, 1823). In the Russian literature, this taxon is considered to be a subspecies of the Siberian grayling T. arcticus signifer (Chereshnev, 1983, 1996, 2008; Chereshnev et al., 2002; Atlas …, 2003; Romanov, 2005; Knizhin, 2009). According to other authors (Mecklenburg et al., 2002; Weiss et al., 2020), it belongs to the group of Arctic grayling T. arcticus s. lat. The latest review of fish of the genus Thymallus (Dyldin et al., 2017) mentions 18 species, although it is noted that several taxa (including T. signifer) have a dubious status or require additional research.

Long-term studies of the distribution, morphology, and ecology of grayling in Eastern Chukotka have shown that three allopatric subspecies of Siberian grayling live here: East Siberian grayling T. arcticus pallasii, Kamchatka grayling T. arcticus mertensi, and Arctic grayling T. arcticus signifer (Chereshnev, 1994; Chereshnev et al., 2002). Based on the diagnostic scheme proposed by Chereshnev (2008), we attributed the graylings from the Gilmimliveem River to the Alaskan subspecies of the Siberian grayling. It is reliably diagnosed by the color of the body and the pattern on the dorsal fin, the proportions of the body and fins, and the number of scales in the lateral line.

Morphological description. D VIII – X 10–13, A III – IV 9–11, P I 13–14, V II 8–10; ll 83–103 (population average 92); sp.br. 17–21. Upper jaw is wide and short, extending posteriorly beyond the anterior margin of the eye, but not reaching its center; its length is 4.5–5.7% SL. The body is short and runny. Dorsal fin base length is 21.4–28.7% SL, height, 11.4–22.0% SL in the posterior part. Its posterior edge, when folded, does not reach the adipose fin. The scale cover is monochromatic, gray-brown or almost dark brown in large mature fish. There are small black spots (usually <20) on the front of the trunk. The caudal peduncle is colored the same as the body, or slightly lighter. The pectoral, anal, and caudal fins are dark gray. Pelvic fins have four to six oblique reddish stripes. Along the dorsal fin, there are four to six slightly ascending rows of rounded reddish spots with a matte edging; in the anterior part, the spots are small; in the posterior part, their size increases. Very rarely, some of the spots, merging with a wide red border, form intermittent vertical stripes between the last two or three rays.

Distribution. The range of the Arctic grayling is almost entirely located in North America on the coast of the Arctic Ocean to the Mackenzie River (Milner, 1874). In Russia, its distribution requires further clarification, while it has been recorded in some rivers of the eastern part of the Chukotka Peninsula and the Chegitun, Koolenveem, Utaveem, and Nunyamoveem rivers (Chereshnev, 1994, 1996, 2008). We have discovered this species in the basin of the Gilmimliveem River (area of thermal mineral springs) for the first time.

Lifestyle and biology. The features of the biology of the Asian populations of the Arctic grayling are not well understood. It is a typical freshwater fish, preferring slow-flowing river sections or floodplain and tundra lakes.

In our catches, graylings FL 192–405 mm, weighing 80–550 g, were found. Six-year-old fish dominated (FL 270–324 mm, 170–340 g) (Table 1). The largest known sizes of the Arctic grayling in the investigated water bodies of Eastern Chukotka were noted in Lake Maingykuivyn (Nunyamoveem River basin), 505 mm and 1210 g (Chereshnev et al., 2002). In our catches, the largest male had a length of 380 mm and a weight of 500 g (age 7+), the largest female was 405 mm and 550 g (8+).

Table 1.   The body length and body weight of individuals of different age of freshwater fish of the Gilmimliveem River
Full size table

According to the results of reverse calculations, the maximum increase in the body length of grayling was noted in the second year of life (on average, 70 mm per year), then over the next four years until the onset of maturity in the sixth year, it gradually decreased from 55 mm to 45 mm per year.

During the first summer of life, five to seven closely spaced sclerites form on the scales of juvenile grayling. The maximum number of sclerites is formed during the period of intense linear growth, in the second to third years of life (on average, 8.4–11.1 sclerites). Subsequently, their number decreases alongside with a decrease in body linear growth rate (on average, down to 5.0–6.5 sclerites). Moreover, when mature fish spawn, ≤4 sclerites are formed on the scales during that year (Table 2).

Table 2.   Growth of the Arctic grayling Thymallus arcticus signifer inhabiting the Gilmimliveem River under the calculated data and the number of sclerites in the annual rings of scale
Full size table

The linear growth rate of the Arctic grayling in the Gilmimliveem River, in comparison with other Chukchi populations, is the highest in the region. So, the most numerous graylings caught in the Gilmimliveem River belonging to the age group of 5+ years were significantly larger by body length (289 ± 5.5 mm) and weight (248 ± 16 g) than fish of the same age from the Koolenveem River, 257 ± 3.9 mm and 158 ± 28 g, respectively (Skopets, 1991).

Residential Dwarf Dolly Varden Char

A rare river ecotype of the anadromous Dolly Varden char Salvelinus malma is numerous and widespread in Eastern Chukotka (Chereshnev et al., 2002; Chereshnev, 2008).

Morphological description. D IV – V 8–10, A III – IV 7–8, P I 11–13, V II 7–8; sp. br. 19–23. The upper jaw is straight and long, extending beyond the posterior edge of the eye; its length is 8.5–13.6% SL. The general background of the body is silvery-blue with brown tints, and the belly is white. On the body, there are small (smaller than the pupil) numerous spots of red or yellow color. The paired fins are dark gray with a narrow orange border along the edges and a milky white outer ray.

Lifestyle and biology. Residential dwarf Dolly Varden char fattens throughout its life and reproduces in the river, preferring certain parts of it and not making significant migrations. In the upper reaches of the Gilmimliveem River, two mature males aged 3+ years (FL 200–205 mm, weight 65–80 g) and eight mature females aged 2–9+ years (FL 179–368 mm, weight 40–390 g) were caught. According to our observations, the maximum annual growth rate was noted up to the age of 2+ years (on average, 85 mm per year), then after reaching maturity, linear growth rate did not exceed 25–30 mm per year.

Relict Three-Spined Stickleback

This is a rare endemic form of the three-spined stickleback Gasterosteus cf. aculeatus. In northeast Asia, it is represented by only one confirmed population (in lakes and puddles formed at the site of the exit of thermal mineral springs on the rocky above-floodplain terrace of the right bank of the Gilmimliveem River). According to Chereshnev (1983, 1989, 2008), the relict form of the three-spined stickleback is close in some taxonomic features to the usual (typical) form of the species inhabiting various parts of its vast amphiboreal range covering the northern parts of the Atlantic and Pacific Oceans. However, there are several significant anatomical differences between this population and the anadromous marine form of the species from different water bodies of the Far Eastern seas, which, together with the unique habitat conditions, may indicate the species rank of isolation of the relict three-spined stickleback of Eastern Chukotka. More detailed studies using other methods (biochemical genetics, DNA analysis, etc.) may help clarify the taxonomic status.

Morphological description. D III (10) 11–12, A I 7–9, P 10–11, V I 1; r.br. 3; sp.br. 20–23; vert. 30–31. The total number of bony lateral plates on the left reached (30) 31–34. There are three spines in front of the dorsal fin, of which the second one is the longest (9.4–12.1% SL), the third was the shortest. The ventral fin includes one spine (11.4–16.5% SL) without a tubercle at the base and one inner soft unbranched ray. There is a small spine at the beginning of the anal fin. The head is relatively large (30.4–34.3% SL), the mouth is almost terminal and extending. The considered population of three-spined stickleback belongs to the trachurus phenotype (Zyuganov, 1991). The bony carapace is massive; the bony keel is well pronounced on the caudal peduncle. The anlage and development of lateral bone plates in juveniles corresponds to the description given for G. aculeatus by Zyuganov (1991). The highest body height is 22.5–26.5% SL, the lowest, 3.8–4.9%; caudal peduncle length 10.8–16.5% SL. The caught specimens had a gray coloration with a green tint of the head, trunk from above, and from the sides. The belly is gray or light brown.

Lifestyle and biology. The stickleback lives in small (30–60-cm deep), often overgrown lakes and puddles with warm mineralized water (temperature in the surface layer is 20–45°C) and a silty bottom. According to the hydrochemical type, these are nitrogen-carbonic baths with low chloride calcium-sodium mineralization (Vakin, 2003). Three-spined stickleback was not found in nearby freshwater lakes, puddles and channels located in the floodplain zone of the Gilmimliveem River, and in the river’s main channel.

Our collections included sticklebacks aged 1+... 3+ years, SL of 17–51 mm, and body weight 0.08–2.55 g (Table 1). The maximum annual linear growth (body length) is noted during the first year of life (on average, 22 mm). In general, the relict three-spined stickleback was characterized by a medium growth rate. The dimensional characteristics of different age groups in the studied population coincide with those for residential sticklebacks of the rivers of northwestern Kamchatka (Pichugin et al., 2008) and are on average lower compared to anadromous sticklebacks of the Anadyr River estuary and Seutakan River, by 20–23 mm at the age of 3+ (Chereshnev, 2008).

As a rule, the populations of three-spined sticklebacks are represented by more females than males within the range (Zyuganov, 1991; Pichugin et al., 2003; Chereshnev, 2008; Grushinets et al., 2018). Our sample was represented by males (it was not possible to determine the sex of five individuals that were 17–22-mm long), and only two sticklebacks were mature females at the age of 3+. The gonads of both females contained eggs of two generations. The first female (51 mm, 2.22 g) had 148 eggs of the first generation (1.2–1.3 mm in diameter), and the second female (50 mm and 2.55 g) had 292 eggs (1.5–1.7 mm). The size of eggs of the second generation in both females varied from 0.4 to 0.6 mm. Spawning occurs in August (Chereshnev, 2008); this is also indicated by the absence of breeding coloration of mature sticklebacks in the collections of the last third of July.

All caught fish had food in their stomachs and intestines, represented mainly by benthic organisms.

Nine Spined Stickleback

A numerous and widespread species, Pungitius pungitius, inhabits various biotopes of water bodies in Northeast Asia.

Morphological description. Specimens with an SL of 30.8–49.0 mm. D X – XI 10–12, A I 9–10, P 10, V I 1; r.br. 3; sp.br. 11–12; vert. 34–35. The total number of lateral bone plates on the anterior part of the body on the left was 2–3, on the caudal peduncle on the left, 9–10. There are usually 11 weakly serrated spines in front of the dorsal fin; the length of the first spine is 5.1–6.4% SL. There are also almost smooth spines on the pelvic fin (10.4–12.9% SL) and at the beginning of the anal fin. Head length was 27.6–28.4% SL and they had a semi-dorsal mouth. The body is elongated and banded; its maximum height is 20.0–22.3% SL. The caudal peduncle is long (15.2–19.8% SL) and low (2.7–3.6% SL). According to the number and location of the lateral bone plates on the body, the nine-spined stickleback inhabiting the Gilmimliveem River belongs to the leiurus phenotype with a keel (Zyuganov, 1991). The general color of the body is gray-green, the head and back are dark gray from above, while the underside of the head, belly, and fins are light brown.

Distribution. The range is extremely wide and covers the basins of the Arctic and boreal seas of the Northern Hemisphere. On the Chukchi Peninsula, the species is widespread, often found in frozen thermokarst lakes (resistant to oxygen deficiency).

Lifestyle and biology. The resident form is found in the floodplain zone of the Gilmimliveem River; it inhabits small freshwater lakes and channels with a sandy-pebble or silty bottom, overgrown with higher aquatic vegetation.

The considered sample is represented by specimens with an SL of 21–49 mm, weight 0.10–1.61 g, and an age of 1+... 3+ (Table 1). Our data is evidence on a fairly high growth rate. According to the data of Chereshnev (2008), similar linear growth rates were noted for the resident stickleback inhabiting the middle reaches of the Anadyr River (near the village of Markovo), although they were noticeably lower compared to the semi-anadromous population from the Anadyr River estuary, where the food supply was much richer.

In our catches of stickleback, males dominated females (2 : 1). The minimum size and weight of mature males was 33 mm and 0.41 g, while females were 37 mm and 0.53 g.

The caught fish fed mainly on benthic organisms. In three individuals, the ostracod Cypria kolymensis Akatova, 1975 (up to 66 specimens) was noted in the food bolus.

Western Slimy Sculpin

The slimy sculpin Cottus cognatus was described by Richardson in 1836 from Big Bear Lake in the basin of the Mackenzie River in northern Canada (Richardson, 1836). In 1961, McAllister and Lindsey (1961) identified two subspecies within the C. cognatus species of North America: C. cognatus cognatus and C. cognatus gracilis. According to several morphological characters, in northeast Asia, this taxon is considered to be a Beringian subspecies of the North American slimy sculpin C. cognatus cognatus (Chereshnev, 1976, 2008; Atlas …, 2003; Parin et al., 2014). According to FishBase and Eschmeyer’s Catalog of Fishes, this subspecies is not currently distinguished and appears as the slimy sculpin C. cognatus (Fricke et al., 2021; Froese, Pauly, 2021).

Morphological description. Specimens of SL of 44.3–73.4 mm. DI (7) 8–9, DII 16–18, A 12 (13), P 12–14, V I 3–4; r.br. 6; sp.br. 4–6 (stamens are short, tubercular); vert. 32–33 (11–12 trunk, 20–21 caudal). The head is rounded dorsally, large, 25.5–31.6% SL; large eyes (17.5–25.2% s); the interorbital distance is small (8.6–14.0% s), smaller than the eye diameter. There are three spines on the preopercular bone. The mouth is large and terminal; the upper jaw reaches the vertical of the middle of the eye. The body is rounded in the anterior part and evenly tapers towards the end of the tail; the maximum body height is 16.8–22.3% SL. The caudal peduncle is long, 13.5–20.0% SL, its height is 6.2–7.7% SL. The pelvic fins do not reach the anal fin and begin somewhat in front of the beginning of the first dorsal fin. The coloration of the head from above and from the sides, the back and sides of the body are dark gray with small dark spots. The belly and lower part of the caudal peduncle are light yellow. Pelvic and anal fins without rows of spots.

Distribution. Most of the range of the western slimy sculpin covers the river basins of the northwestern North American continent. In Northeast Asia, it is distributed in reservoirs and watercourses along the Arctic coast east of the Amguema River and to the southwest along the Bering Sea coast to the Khatyrka River (Chereshnev, 1996).

Lifestyle and biology. The species prefers clean flowing water bodies with a pebble bottom, avoids frozen thermokarst lakes and sections of rivers with slow current and a muddy bottom.

The sample was represented by individuals with a length (SL) of 25–73 mm, weight of 0.30–7.10 g, and age of 1+... 3+ years (Table 1). According to our data, the slimy sculpin in the upper reaches of the Gilmimliveem River grows relatively slowly. The sculpins caught in the middle reaches of the Anadyr River were characterized by higher average annual growth rates in terms of body length and body weight. In particular, these parameters were nearly the same in fish from both rivers at the age 1+, but a year later, the sculpins from the Anadyr River grew faster (15 mm and 0.31 g), and at the age 3+, this difference was 12 mm and 1.6 g (Chereshnev et al., 2001).

The first mature individuals were recorded at the age of 3+; the minimum sizes of the first maturing males were 53 mm and 3.7 g, while females were 48 mm and 2.6 g.

A portion of the caught specimens had no food in the stomach (26%), the rest fed on benthic organisms, mainly chironomid larvae (the frequency of occurrence reached 87%).

CONCLUSIONS

In the upper reaches of the Gilmimliveem River (area of thermal mineral springs) five species of freshwater fish have been found: Arctic grayling T. arcticus signifer, resident dwarf Dolly Varden char S. malma, relict three-spined stickleback G. cf. aculeatus, the nine-spined stickleback P. pungitius, and the western slimy sculpin C. cognatus cognatus. Arctic grayling in Northeast Asia is represented by regional populations; in the Gilmimliveem River (basin of the Mechigmen Bay of the Bering Sea), it has been recorded for the first time. It reliably differs from the East Siberian grayling T. arcticus pallasii in body coloration and pattern on the dorsal fin. Also, the body of T. arcticus signifer is slenderer, the dorsal fin is relatively short and low and does not reach the adipose fin when folded. A relict three-spined stickleback has been found only in shallow lakes and channels of thermal mineral springs in the upper reaches of the Gilmimliveem River. It differs from the anadromous stickleback in several anatomical features (Chereshnev, 2008). It lives in unique environmental conditions beyond the physiological capabilities known for species G. aculeatus (Zyuganov, 1991; Smirnov and Smirnova, 2019). Nine-spined stickleback in the floodplain zone of the upper Gilmimliveem River has been discovered for the first time as well. It is found in small freshwater lakes and channels with a sandy-pebble or silty bottom, overgrown with higher aquatic vegetation. It was not recorded in the biotope of three-spined stickleback (shallow reservoirs with warm mineralized water). Western slimy sculpin occurs in eastern Chukotka in many river basins. It differs from other sculpins of Northeast Asia in a number of characteristic morphological features: the palatine bones are usually without teeth and there are no transverse rows of dark spots located on the pelvic fins. Residential dwarf Dolly Varden char, in contrast to anadromous Dolly Varden char, numerous and widespread in Eastern Chukotka, does not make annual feeding migrations to the sea. The average size–age characteristics of fish in the Gilmimliveem River have been assessed. According to the calculated data, the rate of linear growth of grayling in this reservoir is the highest in Eastern Chukotka. The observed linear growth of three- and nine-spined sticklebacks in the Gilmimliveem River is comparable to that in residential (freshwater) populations of the rivers of Chukotka and northwestern Kamchatka but is lower compared to anadromous and marine sticklebacks of the region.