Phoxinus adagumicus, Artaev & Turbanov & Bolotovskiy & Gandlin & Levin, 2024

Artaev, Oleg N., Turbanov, Ilya S., Bolotovskiy, Aleksey A., Gandlin, Aleksandr A. & Levin, Boris A., 2024, Taxonomic revision of Phoxinus minnows (Leuciscidae) from Caucasus, with description of a new narrow-ranged endemic species, Zoosystematics and Evolution 100 (1), pp. 291-308 : 291

Phoxinus adagumicus sp. nov.

Figs 3 , 4

Phoxinus phoxinus - Berg 1949: 590 (Khabl, Abin, Shibik, Psebeps rivers and Abrau Lake); Sukhanova and Troitskiy 1949: 154, 164-165 (Khabl, Adagum, Shibik, Abin and Ayuk rivers); Emtyl et al. 1994: 137-141, figs 1-2 (Ayuk and Dyurso rivers); Reshetnikov et al. 2003: 301-302 (Kuban River); Otrishko and Emtyl 2013a: 20 (Kuban River).

Phoxinus phoxinus kubanicum Emtyl et Ivanenko, 2002 unavailable name: 90-92, fig. 69 ex Berg 1949 not P. adagumicus sp. nov. (Psekups River basin; Aphips, Il, Ubin, Abin, Adagum rivers and Abrau Lake); Otrishko and Emtyl 2013a: 20 (Kuban River).

Phoxinus phoxinus kubanicus [sic] - Karnaukhov 2020: 76-77 (Adagum and Psebeps rivers).

Phoxinus kubanicus [sic] - Otrishko and Emtyl 2013b: 22 (Adagum River); Otrishko and Emtyl 2013c: 69-70 (Adagum, Ubin, Aphips and Ayuk rivers).

Phoxinus colchicus - Kottelat and Freyhof 2007: 226 (southern tributaries of lower Kuban).

Phoxinus sp. - Artaev et al. 2021 (Zybza, Il, Psyzh, Shibik and Neberdjai rivers).

Phoxinus sp. Kuban Clade 19 - Palandačić et al. 2020: figs 1-2 (Kuban River); Bogutskaya et al. 2023: 6, Fig. 2 (Adagum River).

Type material.

Holotype, IBIW_FS_385, female, (57.5 SL mm, Genbank Accession numbers OR713923 - COI, PP351730 - cyt b), Russia, Krasnodar Krai, Kuban River drainage, Pryamaya Shchel River (Adagum River drainage) upstream Nizhnebakanskaya, 44.8538°N, 37.8417°E, 22 May 2023, I.S. Turbanov leg. Paratypes: 3 females, 2 males (IBIW_FS_386), SL 45.7-51.1 mm, 3 females, 2 males (ZISP 57031), SL 42.2-51.1 mm, 3 females, 2 males (ZMMU P-24612), SL 45.3-51.7 mm, all from the same locality and date as holotype.

Additional material.

Suppl. material 1.

Comparative material.

Suppl. material 1.

Material used in the genetic analysis.

Suppl. material 5.

Etymology.

The new species is named after the Adagum River, left tributary of the lower reach of the Kuban River, where the species occurs; adagumicus - an adjective.

Diagnosis.

Phoxinus adagumicus sp. nov. is distinguished from geographically close species ( P. chrysoprasius and P. colchicus ) by the presence and predominance of specimens with single-row pharyngeal teeth on one or both sides and a combination of characters, none of which is unique, as follows: head depth at nape 54.1-64.8% HL (mean 60.5), and head depth through eye 45.3-51.6% HL (mean 48.0); head length 2.7-3.7 (mean 3.1) times caudal peduncle depth in females and 2.7-3.2 (mean 2.9) times in males; body width at dorsal-fin origin 1.4-2 (mean 1.6) times caudal peduncle depth in females and 1.3-1.6 (mean 1.4) times in males; mean number of scale rows on left and right breast patches 3-9 (mean 6.1); scales below lateral line 8-14 (mean 11.8); number of circumpeduncular scales 37-50 (mean 41.5); 3rd-6th type of breast scalation (mode 4th type).

Description.

The general appearance of P. adagumicus sp. nov. is shown in Figs 3 - 4 . Morphometric measurements for the holotype and type series with level of significance of sex-related differences are given in Table 2 ; meristic and qualitative characters for specimens from the type locality are given in Table 3 . Primary morphological data for specimens from the type locality (holotype, paratypes and additional material) are given in Suppl. material 2; meristic and qualitative characters of P. adagumicus sp. nov. and other Phoxinus spp. are given in Suppl. material 3; morphometric measurements of P. adagumicus sp. nov., P. chrysoprasius and P. colchicus and their comparison are given in Suppl. material 4.

Morphometrics (Table 2 , Suppl. materials 2, 4). The new species has a medium size - the maximum SL is 59.4 mm (male from the Il River). The new species has elongated head - head depth at nape (% HL) (holotype: 62.2, paratypes: 58.5-63.9, add. material 54.1-64.8); and head depth through eye (% HL) (holotype: 49.8, paratypes: 46.4-50.0, add. material 45.3-51.6). Head length 3.0 times caudal peduncle depth in the holotype, 2.8-3.2 in the paratypes, and 2.7-3.7 in the add. material.

Meristics (Table 3 , Suppl. material 3). Dorsal fin with 3 (sometimes 2, rarely 4) unbranched and 7½ branched rays. Anal fin with 3 unbranched and 7½ (rarely 6½) branched rays. Pectoral fin with 14-18 rays, often 16-17. Pelvic fin with 8 rays (rarely 7 or 9). Caudal fin with 19 rays (sometimes 18, rarely 20). Number of dorsal procurrent caudal-fin rays 9-13, often 10-12. Number of ventral procurrent caudal-fin rays 7-12, often 9-10.

The most common pharyngeal teeth formulae are 5-4 (n = 11), 5-4.1 (n = 6), 1.5-4 (n = 5) and 1.5-4.1 (n = 7) (Fig. 5 , Table 4 ). Total number of vertebrae in the holotype 41, 39-41 in the paratypes, and 39-42 in the add. material, commonly 40 or 41. Number of abdominal vertebrae in the holotype 22, 22-23 in the paratypes, and 21-24 in the add. material, commonly 22 or 23. Number of caudal vertebrae in the holotype 19, 17-19 in the paratypes, and 16-19 in add. material, commonly 18. Number of predorsal abdominal vertebrae in the holotype 15, 14-15 in the paratypes, and 14-16 in the add. material, commonly 15. Number of anal-fin pterygiophores in front of the first caudal vertebrae in the holotype 3, 3-6 in the paratypes, and 3-7 in the add. material, commonly 4 or 5. Difference in the number of abdominal and caudal vertebrae in the holotype 3, 3-6 in the paratypes, and 2-7 in the add. material, commonly 4 or 5.

Total number of scales in the lateral series 74-94, mean 84.5. Lateral line incomplete and discontinuous. Relative number of total lateral-line (pored) scales in specimens of 41-57 mm SL varies greatly from 26 to 92%, mean 58.5%. Number of scale rows on breast patches 3-6, commonly 4. Number of circumpeduncular scales 37-44, mean 41.3. Number of scales above lateral line 16-22, mean 18.4. Number of scales below lateral line 9-14, mean 11.8.

Gill rakers (in series from the type locality) on the first left arch 7-8 (mode 8), on the first right arch 7-9 (modes 7, 8, and 9) (Suppl. material 2).

Qualitative characters. Pectoral fins do not reach beginning of pelvic fins, except for a few males (ca. 7% in total). In most specimens (ca. 70%), the tip of upper lip above the horizontal level of lowest point of the eye, in some specimens (ca. 25%) at the level, and in 5% of the specimens below the level. Origin of the anal fin is mainly behind the vertical of the posterior insertion of the dorsal fin. (ca. 53%), often at the vertical (39%), rarely ahead (8%). Free margin of the dorsal fin mainly straight or slightly convex, anal fin slightly convex or rarely slightly concave. 3rd-6th type of breast scalation (mode 4th type).

Coloration. Live coloration of females outside the spawning period is brown, gray or light golden hues (see Fig. 4 ). In males, the color is similar, but with a greater dominance of golden or greenish hues. In spawning coloration of females, golden hue increases significantly and the coloration becomes more contrasting, in general. The spawning coloration of males is also more contrasting, with dominance of green color with variations towards yellow-green or black-green. The operculum stains are blue and the suboperculum is yellow in both sexes, but this is much more pronounced in males. Red hues appear in spawning coloration and are concentrated at the base of the pelvic, pectoral and anal fins, as well as around the mouth. The specimens preserved in formalin had a yellowish color, which is somewhat darker with a brown tint in the upper parts.

Sexual dimorphism. Significant differences were observed in 18 out of 41 morphometric characters (Table 2 ). In addition to some classical sex characteristics in Phoxinus minnows (e.g., narrower pectoral fins and less bright colors in females), females of the new species generally have shorter anal and pelvic fins, smaller eye diameter, and a higher ratio of predorsal length to head length.

Taxonomic remarks.

The presence of Phoxinus minnow in the left lower tributaries of the Kuban has been documented since the first half of the 20th century ( Malyatsky 1930; Berg 1949; Sukhanova and Troitsky 1949), and all previous researchers have attributed this population to P. phoxinus . Emtyl and Ivanenko (2002) used the name ' Phoxinus phoxinus kubanicum sp. nov.' for the minnows from Trans-Kuban rivers (Aphips, Il, Ubin, Abin, and Adagum) and Lake Abrau (Black Sea basin). Even though the name is accompanied by a comparative description, it cannot be considered as valid because it does not comply with the criteria stipulated in art. 16.4 of the International Code of Zoological Nomenclature ( Ride et al. 1999) for species-group names proposed after 1999, as it is not accompanied by an explicit preservation of a holotype or syntypes for the nominal taxon (art. 16.4.1.) and a statement of deposit in a collection (art. 16.4.2.) ( Bogutskaya et al. 2023). The names P. phoxinus kubanicum , P. phoxinus kubanicus [sic], and P. kubanicus [sic], after an attempt to describe this species ( Emtyl and Ivanenko 2002), were subsequently used several times ( Otrishko and Emtyl 2013a, 2013b, 2013c; Karnaukhov 2020); however, according to Bogutskaya et al. (2023), an ICZN commissioner, Nikita Kluge (pers. comm.), taxonomists Pyotr Petrov (pers. comm.) and Boris Kataev (pers. comm.), they cannot be considered as available names.

It is worth noting that the original description of ' P. phoxinus kubanicum ' does not correspond to the morphological diagnosis of minnows from the Adagum basin rivers obtained in this research. For example, the two-row formula (2.5-4.2) of the pharyngeal teeth is indicated ( Emtyl and Ivanenko 2002), but here, none out of 33 examined specimens had such a formula (Table 4 ). Also, it is necessary to emphasize that the given image of ' P. phoxinus kubanicum ' (fig. 69 in Emtyl and Ivanenko 2002) does not relate to this species but is borrowed from the monograph of L.S. Berg (1949, fig. 447) and refers to the minnows inhabiting Lovozero (Northern Russia), which most probably belong to Phoxinus sp. clade 17 of Palandačić et al. (2020). Thus, ' P. phoxinus kubanicum ' should be considered as an unavailable name.

Type locality.

Pryamaya Shchel River (44.8538°N, 37.8417°E) upstream of Nizhnebakanskaya, Krasnodar Krai, Russia. A tributary of the Bakanka River → Adagum River → Kuban River → Sea of Azov.

Distribution and habitats.

An endemic species living in the northwestern Caucasus in the Adagum River basin, a tributary of the Kuban (Fig. 1 ). The species has a rather limited range with only 55 km between most distant known occurrences. The species has been found only in small streams located in mountainous and foothill areas - in a zone of a width about 15-20 km along the northern slope of the western part of the Main Caucasian Range. Example of habitat for this species (Abin River) is shown in Fig. 6 . Habitat of P. adagumicus sp. nov. in other parts of the Kuban basin and on the Black Sea coast of the Caucasus (Lake Abrau) indicated according to literature data ( Berg 1949; Sukhanova and Troitskiy 1949; Emtyl et al. 1994; Emtyl and Ivanenko 2002; Karnaukhov 2020) was not confirmed by our research and may require additional study (see Discussion).

Morphological comparisons.

PCA of morphometric characters shows that P. adagumicus sp. nov. is more overlapping with P. chrysoprasius than with P. colchicus (Fig. 7 ). The highest loadings for P. adagumicus sp. nov. are: head length/caudal peduncle depth, body width at dorsal-fin origin/caudal peduncle depth and eye horizontal diameter (% interorbital width). Sex differences in all three species are divergent in the second component.

The occurrence of single-row pharyngeal teeth, frequent in P. adagumicus sp. nov. (Fig. 5 , Table 4 ), is rare in the genus Phoxinus . In comparison with the geographically neighboring species, P. colchicus and P. chrysoprasius , P. adagumicus sp. nov. has unique formulas of pharyngeal teeth: 5-4, 1.5-4, 5-4.1, 5-5.1 and 1.5-5.1. According to our data, P. colchicus and P. chrysoprasius do not show single-row formulae even on one side, while in P. adagumicus sp. nov. formula 5-4 is found in 1/3 of all studied specimens. In P. colchicus and P. chrysoprasius , formula 2.5-4.2 is modal, but this is absent among individuals of P. adagumicus sp. nov. Single-row pharyngeal teeth were indicated as a unique feature for P. apollonicus Bianco et De Bonis, 2015 from the basin of Lake Skadar in Montenegro ( Bianco and De Bonis 2015).

Compared to P. chrysoprasius from the rivers of the Crimean Peninsula ( Bogutskaya et al. 2023; this study), P. adagumicus sp. nov. has a more elongated head - head depth at nape (% HL) 54.1-64.8, mean 60.5 (vs. 58.9-70.7, mean 64.0) in both sexes; larger eyes relative to head height in females - head depth at nape/eye horizontal diameter 2.1-2.6, mean 2.3 (vs. 2.4-3.4, mean 2.7) (Suppl. material 4); less anal fin pterygiophores in front of the first caudal vertebrae (3-7, mean 4.4 vs. 4-8, mean 5.4); less total number of scales in the lateral series (74-94, mean 84.5 vs. 78-104, mean 90.5); less total number of scales in the lateral series (pored) (21-81, mean 58.5 vs. 46-84, mean 70.0); less mean number of scale rows on left and right breast patches (3-9, mean 6.1 vs. 6-11, mean 8.0); less number of circumpeduncular scales (37-44, mean 41.3 vs. 41-55, mean 46.2); and less number of scales below lateral line (8-14, mean 11.8 vs. 11-16, mean 13.8) (Suppl. material 3).

Compared to P. colchicus from the Khamyshinka River (Belaya River drainage, Kuban River basin), Adygea, Russia and the Dyurso, Khotetsai, Dzubga and Pshenaho rivers (Black Sea coast of the Caucasus), Krasnodar Krai, Russia (this study), P. adagumicus sp. nov. has lower caudal peduncle - minimum depth of caudal peduncle (% SL) 7.1-10.2, mean 9.1 (vs. 9.6-13.1, mean 11.2) and minimum depth of caudal peduncle (% length of caudal peduncle) 31.3-53.7, mean 40.6 (vs. 42-58.6, mean 49.5); more elongated head - head depth at nape (% HL) 54.1-64.8, mean 60.5 (vs. 61.4-74.7, mean 66.6); caudal peduncle depth in head length 2.7-3.7, mean 3.0 times (vs. 2.1-2.8, mean 2.4 times) (Suppl. material 4); less mean number of scale rows on left and right breast patches (3-9, mean 6.1 vs. 5-11, mean 8.3); 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 3rd-10th, 13th and 14th types with predominance of 6th type); and less number of scales below lateral line (8-14, mean 11.8 vs. 11-17, mean 13.4) (Suppl. material 3).

Compared to P. csikii from the Danube River basin, Montenegro and Bulgaria ( Bogutskaya et al. 2019, 2023), P. adagumicus sp. nov. has a smaller number of anal-fin pterygiophores in front of the first caudal vertebrae (3-7, mean 4.4 vs. 4-8, mean 6.7); and 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 3rd-9th and 11th types with predominance of 7th type) (Suppl. material 3).

Compared to P. abanticus Turan, Bayçelebi, Özuluğ, Gaygusuz et Aksu, 2023 from the Lake Abant basin in Turkey ( Turan et al. 2023), P. adagumicus sp. nov. has scales on the breasts in both sexes (vs. absence of scales on the breast in males); 15-24 scales above lateral line (vs. 11-14 scales); and 18-20 rays in caudal fin (vs. 15-16 rays).

Compared to P. septimaniae Kottelat, 2007 from the Herault River, France ( Bogutskaya et al. 2019), P. adagumicus sp. nov. has more total number of vertebrae (39-43, mean 40.4 vs. 37-41, mean 39.3); less number of anal-fin pterygiophores in front of the first caudal vertebrae (3-7, mean 4.4 vs. 4-7, mean 5.4); and 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 12th-14th types with predominance of 8th type) (Suppl. material 3).

Compared to P. lumaireul (Schinz, 1840) clades 1a and 1b from rivers in the Adriatic and Black Sea basins in Italy, Slovenia, and Croatia ( Bogutskaya et al. 2019), P. adagumicus sp. nov. has a smaller number of anal-fin pterygiophores in front of the first caudal vertebrae (3-7, mean 4.4 vs. 3-8, mean 5.5 and 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 2nd-7th types with predominance of 3rd type) (Suppl. material 3).

Compared to P. krkae Bogutskaya, Jelić, Vucić, Jelić, Diripasko, Stefanov et Klobučar, 2019 from the Krka River, Croatia ( Bogutskaya et al. 2019), P. adagumicus sp. nov. has more total number of vertebrae (39-43, mean 40.4 vs. 37-40, mean 38.4); more number of abdominal vertebrae (21-24, mean 22.5 vs. 21-22, mean 21.6); more number of caudal vertebrae (16-18, mean 18 vs. 15-18, mean 16.8); more number of predorsal abdominal vertebrae (14-16, mean 14.8 vs. 13-15, mean 14.0)and 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 3rd-7th types with predominance of 5th and 6th types) (Suppl. material 3).

Compared to P. marsilii Heckel, 1836 from the Danube River basin, Austria and Croatia ( Bogutskaya et al. 2019, 2023), P. adagumicus sp. nov. has 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 3rd-8th types with predominance of 6th type) (Suppl. material 3).

Compared to P. strandjae from the rivers of the Black Sea basin, Bulgaria and the rivers of the Marmara Sea, Turkey ( Bogutskaya et al. 2019, 2023), P. adagumicus sp. nov. has a smaller number of anal-fin pterygiophores in front of the first caudal vertebrae (3-7, mean 4.4 vs. 4-8, mean 5.6); and 3rd-6th types of scalation pattern of the breast and anterior belly with predominance of 4th type (vs. 3rd-12th types with predominance of 6th, 7th, 9th and 11th types) (Suppl. material 3).

Figures

Figure 1. Map of localities of Phoxinus spp. sampled for this study. Localities are designated in Suppl. material 1.

Figure 2. BI consensus tree of concatenated COI and cyt b mtDNA sequences representing all available Phoxinus species in Genbank combined with our data set. Number of some clades is given according to the study of Palandacic et al. (2020). Species from the Kuban basin are highlighted with color. Bootstrap values / posterior probabilities above 80 / 0.8 are shown; asterisks represent of 100 / 1 bootstrap / posterior probabilities values. Scale bar is in expected substitutions per site. The nodes with multiple specimens were collapsed to a triangle, with the horizontal depth indicating the level of divergence within the node.

Figure 3. Holotype of Phoxinus adagumicus sp. nov. (IBIW _ FS _ 385): A. General appearance of preserved specimen; B. Radiograph.

Figure 4. Live coloration of Phoxinus adagumicus sp. nov. from the Zybza River. Side and ventral views are of the same specimens (IBIW _ FS _ 339). Fish of spawning or post-spawning coloration were caught on 8 th May 2022.

Figure 5. Most frequent variants of formula of pharyngeal bones of Phoxinus adagumicus sp. nov.: A. Single-row formula 5 - 4 (in 33 % of specimens); B. Double-row formula 1.5 - 4.1 (in 21 % of specimens). Scale bar: 0.5 mm.

Figure 6. Abin River (44.7210 ° N, 38.2051 ° E; 18 Aug. 2016) - example of biotope of Phoxinus adagumicus sp. nov.

Figure 7. PCA of morphometric characters for Phoxinus spp. under comparison and loading plot showing how strongly each character influences principal components. Specimens of P. colchicus from the Kuban River basin (Khamyshinka River, a tributary of Belaya River) are encircled by black color.