ISSN 0032-9452, Journal of Ichthyology, 2017, Vol. 57, No. 5, pp. 739–746. © Pleiades Publishing, Ltd., 2017. Original Russian Text © O.A. Moreva, M.A. Predvighkin, V.V. Loginov, E.L. Vodeneeva, D.I. Postnov, I.E. Postnov, 2017, published in Voprosy Ikhtiologii, 2017, Vol. 57, No. 5, pp. 585–592.
Morphological Characteristics, Reproduction, and Food Habits of European Bitterling Rhodeus sericeus amarus (Cyprinidae) in the Alatyr River O. A. Morevaa, *, M. A. Predvighkina, V. V. Loginova, E. L. Vodeneevaa, b, D. I. Postnova, and I. E. Postnovc a
State Research Institute of Lake and River Fishery, Nizhny Novgorod Branch, Nizhny Novgorod, Russia b Nizhny Novgorod National Research State University, Nizhny Novgorod, Russia c Nizhny Novgorod State Agricultural Academy, Nizhny Novgorod, Russia *e-mail:
[email protected] Received April 27, 2016
Abstract⎯The data on the morphology, reproduction, and diet of European bitterling Rhodeus sericeus amarus in the Alatyr River (the Sura tributary) are presented. Differences between females and males have been revealed with respect to the complex of morphometric characters. It is assumed that the deviations of some meristic characters from those that are typical of European bitterling are due to the habitation of this population at the boundary of the species distribution. The species reaches sexual maturity at the age of 1–2 years; the individual fecundity is 103–525 (354) eggs. Bitterling is a typical phytophage. Keywords: European bitterling Rhodeus sericeus amarus, morphology, diet, population, Alatyr River DOI: 10.1134/S0032945217050125
European bitterling Rhodeus sericeus amarus is widespread in Europe from the Seine River (France) to the Neva and Volga rivers and is also known in the water bodies of the Black Sea basin and in the western part of the Caspian Sea. In the Volga River basin, it previously occurred in the tributaries of the middle reaches; however, it was not found in the upper and lower reaches of the basin. In the water bodies of the upper Volga, it was recorded for the first time in 1994 (Annotirovannyi katalog…, 1998; Yakovlev et al., 2001; Atlas…, 2002). At the beginning of the 2000s, bitterling was recorded in the rivers of Kaluga oblast and its number has permanently grown since that time (Korolev and Reshetnikov, 2005, 2008). Bitterling is characterized by its sharp and synchronous increase in a number of regions in the European part of Russia since the late 1990s (Korolev and Reshetnikov, 2005, 2008; Kozhara et al., 2007; Ivancheva and Ivanchev, 2008; Ivanchev and Ivancheva, 2010; Ryby v zapovednikakh Rossii, 2010). In Nizhny Novgorod oblast, bitterling inhabits the eastern boundary of the range and occurs only in the Sura and Sundovik basins (Klevakin and Moreva, 2008; Klevakin et al., 2008a, 2008b; Krasnaya kniga…, 2014; Ruchin et al., 2016). The species is dominant in some watercourses; however, its number is mostly low. At the same time, an intensive expansion of bitterling along the entire length of the Sura is observed. The species is listed in the regional
Red Books of Nizhny Novgorod oblast (2014) and the Chuvash Republic (2010). Bitterling was recorded in the Sura basin for the first time by Varpakhovskii (1884). According to his data, it inhabited former riverbeds and bay lakes with a sandy bottom and rarely occurred in the Sura; it was numerous in the upper part of the basin (within Penza guberniya at that time), rare in the middle reaches of the river, and absent in the lower reaches. Similar data were provided by Magnitskii (1928). At the present time, bitterling is widespread along the entire length of the Sura River and in many of its tributaries (Klevakin and Moreva, 2008; Klevakin et al., 2008a, 2008b; Ruchin et al., 2016). The taxonomic position of European bitterling is disputable. Subspecies R. sericeus amarus was described for the European part of Russia (Berg, 1949; Annotirovannyi katalog…, 1998; Ryby v zapovednikakh Rossii, 2010); some authors have lately elevated this subspecies to the level of species, namely R. amarus (Kottelat, 1997; Bogutskaya and Naseka, 2004; Kottelat and Freyhof, 2007). The objectives of this study were to investigate the morphology, food habits, and distribution of bitterling in the Alatyr River.
739
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N
CHUVASH REPUBLIC
NIZHNY NOVGOROD OBLAST
Su
E
R ra
W
.
Lukoyanov
S
Pervomaisk 1
2
Bolshoe Boldino
Alatyr
3 4
Alaty
r R.
.
R tyr
5
Ala
6
9
7
Pochinki
10
Ardatov
8
THE REPUBLIC OF MORDOVIA
Fig. 1. Material collection areas in the Alatyr River in 2005 and 2015. Stations (d): (1) the village of Alatyr, (2) the village of Kanalgushi, (3) the village of Malinovka, (4) the village of Orlovka, (5) the village of Madaevo, (6) the village of Ilinskoe, (7) the village of Kergudy, (8) the village of Beregovye Syresi, (9) the village of Kalasevo, and (10) the city of Alatyr; (m) areas where bitterling Rhodeus sericeus amarus was recorded. Scale: 20 km.
MATERIALS AND METHODS The Alatyr River is the left first-order tributary of the Sura River and flows along the area of Nizhny Novgorod oblast, Mordovia, and Chuvashia. The source of the river is located approximately 10 km to the west of the city of Pervomaisk in Nizhny Novgorod oblast. The basic direction of the current is from the west to the east. The estuary is near the city of Alatyr in the Republic of Chuvashia. The length of the river is 296 km and the area of the catchment basin is 11200 km2. The river receives a total of 42 tributaries and there are 92 lakes and ponds in its catchment area. The largest tributaries are Rudnya and Insar. The width of the river in the sites of bitterling habitation in the middle and lower reaches is 25–50 m. The average depths are 2–3 m in the pool sites and 0.2–0.4 (up to 1.5) m in the riffles. The velocity of the current is 0.4–0.9 m/s in the river sites and 0.1 m/s in the site of the Turgenevsky reservoir damming. The bottom is sandy; it is significantly silted in the openings and presented as compact sand with crushed stone in the channel. The material was collected in the Alatyr River in the summer of 2005 and 2015 using a minnow drag (with a length of 10 m and a mesh of 4 mm) and ichthyological nets. Four sites were studied in 2005 (Fig. 1: stations 1, 3, 4, and 6) and seven sites were investigated in 2015 (stations 2, 4, 5, and 7−10). A total of 175 bitterling specimens were caught in four sites of the middle and lower reaches of the Alatyr River (stations 6−9) (including two specimens in 2005 and 173 speci-
mens in 2015). In June 18, 2015, 146 bitterlings were caught near the village of Kalasevo during the prespawning period at a water temperature of 20°C, of which 46 specimens were males and 100 specimens were females (32–68%). The mature individuals had a pronounced breeding dress and the females had partly developed ovipositors. All the 146 specimens were subject to laboratory treatment. The fish was measured using an electronic sliding caliper with an accuracy of up to 0.1 mm and weighted on VK-600 laboratory scales with an accuracy of up to 0.01 g. Standard methods of investigation (Pravdin, 1966) and Reshetnikov and Popov’s recommendations (2015) were used during the processing of the material on the age- and sex-related composition and fecundity as well as during the determination of morphometric and linear-weight characteristics. The pharyngeal teeth and vertebrates were not studied. The age of the fish was determined by their scales using an MBS-10 binocular. The rate of the fish growth was determined using the method of back calculations by the direct proportional relationship between the standard fish length (SL) and radius of annual scale rings (Pravdin, 1966). The food spectrum of bitterling was determined on the basis of the study of 20 intestines (10 males and 10 females at the age of 2+–4+). Zoobenthos and phytoplankton samples were collected from this region. Only algae were found in the bitterling intestines. The taxonomic composition of algae was identified JOURNAL OF ICHTHYOLOGY
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according to the Identification Guides for Freshwater Algae in the Soviet Union (1951, 1953, 1954, 1955, 1959, 1962, and 1986). This article does not provide any data on the species composition; it considers higher rank taxa. The cells were calculated in the Nageotte chamber with a volume of 0.01 mL; from 10 to 20 fields of view were calculated. The frequency of occurrence of separate components in food (FO, %) was determined as the ratio of the number of intestines that contained a certain phytoplankton group to the total number of the studied fishes; the share of different algal groups in the bitterling food spectrum (% of the total cell number) was also determined. The statistical processing of the results used the methods of discriminant and regression analysis (Glants, 1998; Rebrova, 2002; Khalafyan, 2007). The data were processed using Statistica 6.0, Excel, and Biostat 2003 software packages. RESULTS AND DISCUSSION The meristic characters of the studied bitterling males and females in the Alatyr River are given in Table 1. With respect to the number of nonbranched rays in the anal fin and the number of gill rakers in the first gill arch, bitterling in the Alatyr River goes beyond the limits of the parameter variation that are known for the species under study (Atlas…, 2002; Ryby v zapovednikakh Rossii, 2010): A II−III vs. III, sb. br. 10−19 vs. 10−13. Possible morphological differences between bitterling females and males according to the complex of 26 morphometric characters were determined on the basis of the analysis of the sample of fish at the same age, namely, 11 males and 15 females at the age of 1+ and 29 males and 76 females at the age of 2+, to exclude the influence of age variability. Since not all characters were subject to normal distribution, we used a discriminant analysis that can be based on parametric and nonparametric criteria (Trukhacheva, 2013). The results of the analysis of gender differences between the two bitterling age groups (1+ and 2+) using the Wilks criterion and the squares of Mahalanobis distances and χ2 showed statistically significant differences between females and males (p < 0.0001). The differences between females and males at the age of 1+ were determined with respect to 14 characters: the distance from the origin of head to the anal orifice, length V, the smallest body depth, FL, the distance from the anal orifice to the end of tail, antedorsal distance, head depth near the occiput, the length of the caudal peduncle, the length of the base D, the length of the base A, postdorsal distance, the highest body depth, depth D, and the length of the postorbital region. At the age of 2+, the differences were determined with respect to seven characters: the width of the forehead, the highest body depth, antedorsal distance, the distance from the origin of head to the anal JOURNAL OF ICHTHYOLOGY
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Table 1. Meristic characters of bitterling Rhodeus sericeus amarus in the Alatyr River Character
Males (n = 46)
Females (n = 100)
40 −76 50.4 ± 0.98 11−19 (16) III−III (III)
41−68 49.8 ± 0.40 10−19 (15) III−III (III)
D2
8−9 (9)
9 (9)
P V A1
11−11 (11) 6−6 (6) II−III (III)
11−11 (11) 6−6 (6) III−III (III)
A2
8−9 (9)
9−9 (9)
FL, mm sb. br. D1
FL, fork length; sb. br., number of gill rakers in the first gill arch; D1 and D2, number of nonbranched and branched rays in the dorsal fin; P, number of rays in the pectoral fin; V, number of rays in the ventral fin; A1 and A2, number of nonbranched rays and branched rays in the anal fin; above the line and beyond the brackets—variation limits; below the line—mean value and its error; in brackets—mode.
orifice, snout length, total length (TL), and ventroanal distance. With respect to the type of diet, bitterling is classified as phytophages. It feeds mainly on plankton algae and fouling (Atlas…, 2002). The intestine is long and forms numerous loops; it is generally folded in one spiral that consists of four to six regular concentric coils. In the studied individuals, the average length of the intestine exceeds the length of the body by 1.5–1.7 times. The length of the intestine is larger in females than in males, which was recorded in all age groups. The relative length of the intestine increases with age: from 1.2–1.4 during the second year of life to 1.6–1.9 FL during the fourth year. The algae that were found in the intestines of bitterling from the Alatyr River were represented by 81 species belonging to six groups. Green (Chlorophyta) and diatomic (Diatomeae) algae were dominant with respect to the number of species (52 and 17, respectively). The diversity of other taxonomic groups is significantly lower: six blue–green (Cyanobacteria), three euglenic (Euglenoidea), two yellow–green (Xanthophyceae), and one dinophyte algal groups (Dinoflagellata). The ratio of different algal groups in the bitterling food spectrum (% of the total number of cells) was as follows: 47.2% green chlorococcal algae (Chlorococcophyceae), 29.8% diatoms, 19.1% blue–green algae, 1.7% green filamentous algae (Zygnematales, Ulotrichophyceae, and Oedogoniaceae algae), 0.7% green volvocal algae (Volvocophyceae), 0.7% dinophytes, 0.4% euglenic algae, and 0.4% yellow–green algae. Irrespective of sex, the diet of bitterling was basically represented by three algal groups: green chlorococcal algae, diatoms, and blue–green algae; however, the
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With respect to the number, green chlorococcal algae were dominant among plankton algae in the Alatyr River during the study period (75% of the total number; their share in the diet was 47%). A significant development in the Chlorophyta group was reached by the volvocal representative Pandorina morum. The absence of this species in bitterling intestines may be due to the fact that it has easily lysed pectic covers. The diatoms formed approximately 15% of the total number; however, their composition was largely represented by plankton forms, unlike the intestine contents, where species from benthos groupings were recorded. Blue–green algae were almost absent in the plankton algocenoses of the Alatyr River, while their benthic species occupied the third position in the bitterling diet. The dependence of the body weight (W, g) on the fish length (FL, cm) is described by the exponential equation W = aFLb (Shmal’gauzen, 1935): W = 0.0237FL2.9307 (R2 = 0.950, p < 0.05, n = 46) for males, W = 0.0309FL2.7981 (R2 = 0.900, p < 0.05, n = 100) for females, and W = 0.0280FL2.8489 (R 2 = 0.923, p < 0.05, n = 146) for both sexes. These dependences quite exactly describe the observed data (Fig. 2). The exponential coefficient b is close to three in most fish species and is usually higher in females than in males (Shibaev, 2015); according to our data, it is higher in males. Bitterling reaches the FL of 8–10 (usually 7–8) cm, the weight of 3–8 g, and the age of 5 years (Atlas…, 2002). The average size of the individuals at the age of 1 and 3 years in the Alatyr River are somewhat higher than that provided for bitterling from Sura and Kuban rivers (Table 2). The linear and weight growth of bitterling in the Alatyr River according to the observed and calculated (back calculation by annual scale rings) data is given in Tables 3 and 4. The significant differences in the standard length that was determined by the back calculation method were not revealed between males and females within each age group (t = 2.72, p = 0.07). The studied sample of bitterling from the Alatyr River was dominated by 2-year-old individuals (63% males and 76% females) (Fig. 3). It is believed that bitterling reaches sexual maturity at the age of 2–3 years (Atlas…, 2002). According to our data, some individuals (females with FL 38, 39,
8 7
Weight, g
6 5 4 3 2 1 0 3
4
5 6 Length, cm
7
8
Fig. 2. Length–weight correlation in bitterling Rhodeus sericeus amarus in the Alatyr River: W = 0.0280FL2.8489, R2 = 0.923, n = 146 spec.
percentage of chlorococcal algae, which are generally represented by plankton species, are somewhat lower and the share of benthic diatomic and blue–green alga species is higher in the diet of females than the respective products in the diet of males. According to the data of Novikov (2007), the food of bitterling in the Velya River (the Uglich Reservoir basin) and Yakchroma reservoir also includes only algae: diatoms (46−48%), protococcal algae (Protococcophyceae) (24−27%), euglenic algae (10−12%), volvocal algae and chrysophyceae algae (Chrysophyta), etc. The basic components included the species of the Scenedesmus, Dictyosphaerium, Pediastrum, Crucigeniella, and Coelastrum genera among representatives of the Chlorococcales order; Caloneis, Amphora, and naviculoid diatoms among diatom algae; and Oscillatoria among cyanoprocaryotes. The species of the genus Spirogyra are the most widespread among filamentous green algae. Representatives of chlorococcal algae, diatoms, and blue–green algae were recorded in all the studied intestines (FO = 100%); volvocal, filamentous, and yellow–green algae were revealed in 25% and dinophytes and euglenic algae were found only in 20% of the intestines.
Table 2. Average length (FL, mm) of individuals from different age groups of bitterling Rhodeus sericeus amarus in different water bodies of Russia Age, years River Alatyr Sura Kuban
1
2
3
4
41 34 36.7
45 46 45.6
54 52 –
70 – –
n, spec.
Source of information
146 39 64
Our data Klevakin et al., 2008a Yemtyl’ and Motruk, 2002
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Proportion of fishes, %
70
63.0
76.0
80
(а)
743
(b)
60
70
50
60 50
40 30
40
23.9
30 15.0
20
20
10.9
10
8.0
10 2.2
1.0
0
0 1
1
2
3
2
3
4
4
Age, years Fig. 3. (a) Male and (b) female age composition in bitterling Rhodeus sericeus amarus in the Alatyr River.
and 41 mm) mature even at the age of 1 year; from the age of 2 years, the prevailing part of the studied fish had gonads at the fourth maturity stage (Table 5). With respect to the type of spawning, bitterling is classified as ostracophils (females lay eggs into the pulmonary cavity of bivalve mollusks). Spawning is fractional; reproduction may last 3–5 spring and summer months. Prior to the spawning period, females develop an ovipositor that gradually grows and is filled with cylindrical eggs. As eggs are spawned, the ovipositor diminishes and, finally, forms a reddish wart with a size of 3.8 mm (Atlas…, 2002). Each of the females that we caught had eggs at the same maturity stage; i.e., the gonads did not have different egg portions. The ovipositor length was not more than 41% of FL at the time of catching. This index significantly varies at different stages of the spawning period. There were no eggs in the ovipositor. In the Table 3. Linear and weight growth of bitterling Rhodeus sericeus amarus in the Alatyr River (observed data)
area where bitterling was caught, we found a large bivalve pearl shell mollusk Unio rostratus (up to 13 spec./m2) with the pulmonary cavity into which females presumably lay eggs. According to the data of different authors, the bitterling fecundity is 220–430 eggs (Atlas…, 2002). According to our data, the individual fecundity of bitterling in the Alatyr River varies from 103 to 525 (354) eggs and grows as the age (Table 6) and weight (Fig. 4) of the female increase. Table 4. Average length (SL, mm) of individuals from different age groups of bitterling Rhodeus sericeus amarus in the Alatyr River (back calculation data) Age, years n, spec.
Sex Males Females Both sexes
1
2
3
4
29 31 30
39 37 38
48 43 46
64 57 61
46 100 146
Age, years n, spec.
Sex 1 Males Females Both sexes Males Females Both sexes
2
3
4
Length (FL), mm 40 46 54 41 45 54 41 45 54 Weight, g 1.3 1.6 2.5 1.3 1.8 2.8 1.3 1.7 2.7
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Table 5. Stages of gonad maturity in bitterling Rhodeus sericeus amarus from different age groups (% of the total number of fish at a specific age), June 18, 2015
70 70 70
46 100 146
Sex Males
7.3 6.4 6.8
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Maturity n, stage spec. III IV III IV
15 31 19 81
Age, years 1
2
3
4
100 0 80 20
14 86 8 92
0 100 12 88
0 100 0 100
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Table 6. Fecundity of bitterling Rhodeus sericeus amarus in the Alatyr River Fecundity Age, years
n, spec.
1
15
2
76
3
8
4
1
1−4
100
Body weight, g
individual, eggs/spec.
relative, eggs/g of weight
Gonad weight, g
1.3 − 2.4 1.9 1.8− 4.5 2.4 2.8− 4.4 3.3 6.4
103 −196 175 130 − 410 288 371−507 430 525
43 −136 97 59 −164 120 97 −172 133 82
0.04 − 0.23 0.12 0.05− 0.38 0.18 0.13 − 0.47 0.25 0.50
1.3−6.4 2.4
103 −525 354
43 −172 108
0.04 − 0.50 0.18
Maturity index, %
6.3 7.5 7.6 7.8 7.5
Above the line—the limits of variation of the index; below the line—the mean value.
The mean value of the maturity index (the gonad weight to fish weight ratio) is approximately the same for individuals at the age of 2–4 years; at the same time, the weight of gonads significantly varies within age groups. CONCLUSIONS (1) The studied sample of bitterling in the Alatyr River is dominated by 2-year-old individuals; the maximum age is 4 years and the male-to-female ratio is 1 : 2 in this sample. (2) Some meristic characters of bitterling from the Alatyr River deviate from those that are characteristic of this species: A II−III 8−9 vs. III 8−12, sb. br. 10–19 vs. 10−13. This is possibly due to the habitation of this population at the boundary of the species distribution. Additional data on other marginal populations are required.
(3) Statistically significant sex differences with respect to the complex of morphometric characters were revealed for bitterling. (4) Bitterling is a typical phytophage. The intestine is mainly filled with green chlorococcal algae (47%), diatoms (30%), and blue–green algae (19%); the former are dominant among plankton algae in the Alatyr River (75% of the total number). (5) The average length of the bitterling intestine exceeds the average body length by 1.5 to 1.7 times; the relative intestine length increases with age. (6) Bitterling reaches sexual maturity at the age of 2 years, although some mature individuals (females) were recorded event at the age of 1 year. The gonad weight in females of the same age varies greatly, which is possibly due to the fractional nature of spawning in this species. REFERENCES
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Annotirovannyi katalog kruglorotykh i ryb kontinental’nykh vod Rossii (Annotated Catalogue of Cyclostomata and Fishes from Continental Waters of Russia), Reshetnikov, Yu.S., Ed., Moscow: Nauka, 1998.
Fecundity, eggs
700 600 500
Atlas presnovodnykh ryb Rossii (Atlas of Freshwater Fishes of Russia), Reshetnikov, Yu.S., Ed., Moscow: Nauka, 2002, vol. 1.
400 300
Berg, L.S., Ryby presnykh vod SSSR i sopredel’nykh stran (Freshwater Fishes of Soviet Union and Adjacent Countries), Moscow: Akad. Nauk SSSR, 1949, part 2, pp. 469– 928.
200 100 0
1
2
3
4 5 Weight, g
6
7
Fig. 4. Dependence of the individual fecundity of bitterling Rhodeus sericeus amarus on the body weight: у = 89x + 68.1, R2 = 0.46, n = 100 spec.
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Bogutskaya, N.G. and Naseka, A.M., Katalog beschelyustnykh i ryb presnykh i solonovatykh vod Rossii s nomenklaturnymi i taksonomicheskimi kommentariyami (Catalogue of Agnatha and Fishes of Fresh and Saline Water of Russia with Nomenclature and Taxonomic Comments), Moscow: KMK, 2004. JOURNAL OF ICHTHYOLOGY
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MORPHOLOGICAL CHARACTERISTICS, REPRODUCTION Emtyl’, M.Kh. and Motruk, E.V., The Amur bitterling (Rhodeus sericeus Amarus) in the Kuban River basin, Mater. XV mezhrespublikanskoi nauchno-prakticheskoi konferentsii “Aktual’nye voprosy ekologii i okhrany prirody ekosistem yuzhnykh regionov Rossii i sopredel’nykh territorii” (Proc. XV Interresp. Sci.-Pract. Conf. “Ecology and Protection of Natural Ecosystems of Southern Regions of Russia and Adjacent Territories”), Krasnodar, 2002, pp. 145–147. Glantz, S.A., Primer of Biostatistics, New York: McGrawHill, 1997, 4th ed. Ivanchev, V.P. and Ivancheva, E.Yu., Kruglorotye i ryby Ryazanskoi oblasti i prilezhashchikh territorii (Cyclostomata and Fishes of Ryazan Oblast and Adjacent Territories), Ryazan: Golos Gubernii, 2010. Ivancheva, E.Yu. and Ivanchev, V.P., Dynamics of fish species composition and the results of ichthyologic monitoring in the central steam of Oka River (Ryazan oblast), Vopr. Ikhtiol., 2008, vol. 48, no. 5, pp. 625–633. Khalafyan, A.A., STATISTICA 6. Statisticheskii analiz dannykh: uchebnik (STATISTICA 6: Statistical Data Analysis. Handbook), Moscow: Binom-Press, 2007. Klevakin, A.A. and Moreva, O.A., Supplement to the section “Fishes and Cyclostomata” in the Red Data Book of Nizhny Novgorod oblast, in Redkie vidy zhivykh organizmov Nizhegorodskoi oblasti (Rare Species of Living Organisms of Nizhny Novgorod Oblast), Nizhny Novgorod: Kom. Prirod. Nizhegorod. Obl., 2008, no. 1. pp. 41–69. Klevakin, A.A., Anuchin, Yu.V. and Moreva, O.A., Distribution of Amur bitterling (Rhodeus sericeus Pallas, 1776) in the Sura River basin (Nizhny Novgorod oblast), Mater. mezhdunarodnoi nauchnoi konferentsii “Problemy bioekologii i puti ikh resheniya” (Proc. Int. Sci. Conf. “Problems of Bioecology and Their Solutions”), Saransk, 2008a, pp. 147– 149. Klevakin, A.A., Anuchin, Yu.V., Moreva, O.A., and Bayanov, N.G., Distribution of fishes fixed in the Red Data Book in the river basins of different landscape zones of Nizhny Novgorod oblast, Mater. Vserossiiskoi shkoly-konferentsii “Ekosistemy malykh rek: bioraznoobrazie, ekologiya, okhrana” (Proc. All-Russ. School-Conf. “Ecosystems of Small Rivers: Biological Diversity, Ecology, and Protection”), Borok: Inst. Biol. Vnutr. Vod, Ross. Akad. Nauk, 2008b, pp. 163–166. Korolev, V.V. and Reshetnikov, Yu.S., Rare and low-value species of Cyclostomata and fishes in Kaluga oblast, Mater. IV (XXVII) konferentsii “Bioresursy Belogo morya i vnutrennikh vodoemov Evropeiskogo Severa” (Proc. IV (XXVII) Conf. “Biological Resources of the White Sea and Inland Reservoirs of European North”), Vologda, 2005, part 1, pp. 205–209. Korolev, V.V. and Reshetnikov, Yu.S., Rare species of Cyclostomata and fishes of upper Oka River basin within Kaluga oblast, Vopr. Ikhtiol., 2008, vol. 48, no. 5, pp. 611– 624. Kottelat, M., European freshwater fishes. An heuristic checklist of the freshwater fishes of Europe (exclusive of former USSR), with an introduction for non-systematists and comments on nomenclature and conservation, Biologia, 1997, vol. 52, suppl. 5, pp. 1–271. JOURNAL OF ICHTHYOLOGY
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Translated by D. Zabolotny
JOURNAL OF ICHTHYOLOGY
Vol. 57
No. 5
2017
