Ponticola hircaniaensis, Zarei & Esmaeili & Kovačić & Schliewen & Abbasi, 2022

Zarei, Fatah, Esmaeili, Hamid Reza, Kovačić, Marcelo, Schliewen, Ulrich K. & Abbasi, Keyvan, 2022, Ponticola hircaniaensis sp. nov., a new and critically endangered gobiid species (Teleostei: Gobiidae) from the southern Caspian Sea basin, Zootaxa 5154 (4), pp. 401-430 : 408-421

Ponticola hircaniaensis sp. nov.

English name: Hyrcanian goby

( Figs. 5–6 , Table 4 )

Synonyms

Ponticola gorlap (Iljin, 1949) : Zarei et al. 2021: 1272, table 2 (partim: Kaboudval Stream)

Holotype. ZM-CBSU S101-6, male, 76.9 + 21.6 mm; Iran: Golestan prov.: Kaboudval stream, 36°53‘11.0“N 54°53‘37.8“E; F. Zarei, 27 August 2021.

Paratypes. ZM-CBSU S099-1 to S099-12, 7 males, 5 females, 52.8 + 14.0–80.8 + 20.4 mm; Y. Bakhshi, Z. Ganjali & A. Jouladeh-Roudbar, 28 August 2017.—ZM-CBSU S100-1 to S100-4, 4 males, 49.8 + 13.1–95.9 + 24.1 mm; F. Zarei & Y. Bakhshi, 31 August 2019.—ZM-CBSU S101-1 to S101-5 & S101-7 to S101-15, 9 males, 5 females, 54.9 + 15.0–91.3 + 26.0 mm; F. Zarei, 27 August 2021. All paratypes were collected from Iran, Golestan prov., Kaboudval Stream, 36°53’11.0”N 54°53’37.8”E.

Additional material. ZM-CBSU S099, 29 specimens, 21.8–62.7 mm SL; Y. Bakhshi, Z. Ganjali & A. Jouladeh-Roudbar, 28 August 2017.—ZM-CBSU S100, 26 specimens, 27.5–47.8 mm SL; F. Zarei & Y. Bakhshi, 31 August 2019.—ZM-CBSU S101, 9 specimens, 45.0– 50.2 mm SL; F. Zarei, 27 August 2021. All additional material was collected from Iran, Golestan prov., Kaboudval Stream.

Material used in the molecular genetic analysis. Mitochondrial COI: molecular IDs: P2776–P2778 (ZMCBSU P2776 to P2778), P162 (ZM-CBSU P162), 3432 (ZM-CBSU S101-2, paratype), 3433–3440 (ZM-CBSU S101-19 to S101-26), 3441 (ZM-CBSU S101-7, paratype), 3443 (ZM-CBSU S101-9, paratype), 3444 (ZM-CBSU S101-12, paratype), 16 specimens (GenBank accession numbers: MW393596 – MW393598 , and ON166711 – ON166723 ).—Nuclear S7: molecular IDs: 3432 (ZM-CBSU S101-2, paratype), 3438 (ZM-CBSU S101-24), 3435 (ZM-CBSU S101-21), 3443 (ZM-CBSU S101-9, paratype), 4 specimens (GenBank accession numbers: ON186768 – ON186771 ). All from Iran, Golestan prov., Kaboudval Stream, 36°53’11.0”N 54°53’37.8”E, F. Zarei & Y. Bakhshi, 31 August 2019 & 27 August 2021.

Material used in the otolith analysis. ZM-CBSU K18, K21, K24 & K28, S101-21, S101-26, 12/19–12/22, 12/26–12/31, 12/33–12/34, and 12/37–12/39, 21 specimens, 49.24–78.44 mm SL; Iran: Golestan prov., Kaboudval Stream, 36°53’11.0”N 54°53’37.8”E; F. Zarei & Y. Bakhshi, 31 August 2019.

Diagnosis. Ponticola hircaniaensis sp. nov. is distinguished from all other congeneric species in the Caspian Sea basin by the following combination of characters: D2 I/14–I/16 (usually I/15), A I/10–I/12 (usually I/11), LL 52–59; lower jaw slightly, if at all, prognathous; head and body yellowish brown, showing a reticulate brown pattern on a yellow background, D1 with a marginal bright orangish-yellow band and a dark anterior spot, P base upper part with a distinct dark brown stripe; D1 third spine length 13.4–18.3 % SL, D2 spine length 11.1–13.8 % of SL, caudalpeduncle length and depth 16.4–20.1 % and 11.1–12.8 % of SL, respectively, head depth at nape and eye 70.9–81.0 % and 52.5–66.0 % of HL, respectively. Dorsal rim of sagittal otolith with a broad concavity in the middle, dorsal depression absent or indistinct, SuL/SuH and SuH/OH ratio 1.47–1.82 and 0.34–0.40, respectively.

Description. All morphometric values in the text are presented as holotype first and paratypes, if different, in parentheses.

General morphology ( Fig. 5 ): Body proportions are given in Table 4 . Body moderately elongate, its depth at pelvic-fin origin 3.94 (3.78–4.78) in SL, at anal-fin origin 4.94 (4.82–5.52) in SL, laterally compressed posteriorly, with caudal peduncle moderately deep, caudal-peduncle depth 0.67 (0.57–0.76) of caudal-peduncle length. Head large, the length 3.32 (3.16–3.51) in SL, width 4.12 (3.62–4.48) in SL, its depth 4.11 (4.01–4.85) in SL and 1.0 (0.82–1.05) of width. Postorbital profile steep. Snout short, oblique, convex, longer than eye, its length 1.41 (1.13– 1.62) of eye diameter, 3.64 (3.11–3.91) in head length. Anterior nostril short, erect flared tube, the rim posteriorly elevated; posterior nostril pore-like, with more or less raised rim. Eyes dorsolateral, more lateral than dorsal, small, eye diameter is 5.15 (4.02–5.32) in head length, orbit slightly elevated. Interorbital wide, 1.44 (1.28–2.58) in eye diameter. Mouth directed obliquely upwards, lower jaw little if at all prognathous, upper lip widened in middle and swollen, angle of jaws below pupil. Cheek deep and prominent. Dentary in both jaws with conical teeth in outermost and innermost rows, irregular rows of smaller teeth in-between. Branchiostegal membranes fused to isthmus along the entire lateral margin of the isthmus, from immediately anterior to pectoral margin, gill openings restricted to pectoral-fin base.

Fins. D1 VI; D2 I/14–16 (holotype I/14; paratypes: I/14:8, I/15:18, I/16:4) (last bifid); A I/10–I/12 (holotype I/11; paratypes: I/10:2, I/11:21, I/12:7) (last bifid); P 17–20 (holotype, left side: 18; paratypes, left side: 17:2, 18:22, 19:5, 20:1), V I/5 + 5/I. Morphometric characters are given in Table 4. D 1 dorsal profile horizontal, lower than the highest part of D2 dorsal profile. First to fourth D1 spines becoming progressively longer, fifth D1 spine shorter than the second. First D1 spine almost as long as D2 spine. D2 highest in the middle. D1 and D2 connected by interdorsal membrane, interdorsal space between D1 VI and D2 I narrow. D2 originates slightly in front of vertical to anus. A originates below 4th to 5th branched rays of D2. A with last ray origin below origin of penultimate ray or below origin of last ray of D2. The D2 (except for large specimens) and A rays not reaching backwards the base of uppermost and lowermost caudal-fin rays, respectively. C rounded, shorter than head length. P reaches beyond vertical of D2 origin. P rays all branched, the uppermost rays not free from the membrane. V disc complete, rounded, originates slightly anterior of vertical through D1 origin, not reaching anus or rarely extending almost to anterior anus origin, the variability present in both sexes. V all rays branched. V anterior membrane present, lateral lobes of anterior membrane well developed and with pointed tips.

Squamation. Nape, predorsal area, upper 1/3 of opercle, posterior part of breast, and abdomen all covered with cycloid scales, and the rest of the body covered with ctenoid scales. Scales on caudal peduncle slightly enlarged. Cheek naked. Base of pectoral fin naked. LL 52–59 (holotype, left side: 55; paratypes, left side: 52:1, 53:7, 54:5, 55:3, 56:4, 57:8, 58:1, 59:1), TR 16–20 (holotype, left side: 19; paratypes, left side: 16:4, 17:5, 18:15, 19:5, 20:1), PD 19–23 (holotype 21; paratypes: 19:2, 20:8, 21:12, 22:7, 23:1).

Lateral line system ( Fig. 6 ). Cephalic canals. AOC, POC, and PC present. AOC with a single, unified interorbital section, carrying 12 pores: a pair of posterior nasal pores σ, single interorbital pores λ and κ, and paired ω, α, β, ρ; pores σ and ρ terminal, pore λ directly on the canal, pores κ and ω behind the canal, and pores α and β lateral of the canal. POC paired, each with two pores: θ and τ. PC paired, each side with three pores: γ, δ and ε. Head sensory papillae. Rows with range of number of sensory papillae in parentheses. Preorbital: median series in five rows: r 1 (6–9) and r 2 (7–8) as oblique rows opposite posterior nostril, extending over the canal section between λ and σ; midline of snout anterior of λ free of neuromasts; s 1 (7–11) and s 2 (8–11), as transverse rows anterior to σ; s 3 (13–18) as cluster anterior and lateral of s 2, reaching near to upper lip; lateral series in four rows, each doubled; c 2 oblique between the anterior and posterior nostrils, with lower section (7–9) often longer than upper (4–6); c 1 (10–14) transversal lateral of anterior nostril and dorsal of c 2 (10–13); c 2 and c 1 (7–9) in longitudinal and oblique rows, respectively; c 2 ventral of c 1, c 1 ventral of c 2 and dorsal of d 1 (22–26), oblique and posteriorly close to suborbital row 1. Suborbital: seven transversal (1–7) and two longitudinal (b, d) rows on cheek, rows 1–4 (1: 21–29, 2: 20–27, 3: 22–31, 4: 31–36) before longitudinal row b, long, ventrally extending to level of d, dorsally reaching close to eye except row 2 and sometimes row 3; rows 1 and 2 above and anterior to rear edge of jaws, row 3 right above or slightly behind the jaws angle; row 5 and 6 divided by b in short superior (5s: 9– 11, 6s: 7–9) and longer inferior (5i: 16–20, 6i: 12–18) sections; 5i ending above longitudinal row d, 6i passing behind row d, ending slightly below its level; 5i and 6i not confluent with each other; row 7 short (2–6), immediately anterior of pore α; row b (21–27) anteriorly reaching to below posterior end of pupil; row d long, not reaching 6i posteriorly, often distinctly divided and separable in two slightly overlapping parts, the anterior supralabial row d 1 oblique, following the border of the upper lip and reaching below the anterior origin of d 2 (21–24), the posterior row d 2 longitudinal on cheek; row d 1 anteriorly passing row 1. Asymmetrical variant specimens (30% of the material examined and only on the left side of the head) were found with one additional row before row b, i.e., five transverse suborbital rows before row b and eight transverse suborbital rows in total, or with four transverse suborbital rows before row b, but followed by one additional row below row b, i.e., three transverse rows below row b. Preoperculo-mandibular: not shown in Figure 4 . Three rows, e, i and f; external row e distinctly divided at articulation of lower jaws in anterior mandibular (e 1: 51–63) and posterior preopercular (e 2: 47–59) sections; anterior and posterior sections of internal row i (i 1, i 2) are continuous (93–123), their separation at articulation of lower jaws is indistinct; both usually with additional papillae and i 1 continuous with the symphyseal row f (10–14). Oculoscapular: eight transversal (z, q, u, trp, y, as 1 –as 3) and four longitudinal (x 1, x 2, la 2 –la 3) rows including the axillary series; x 1 long (17–20), parallel to and exceeding AOC, reaching to trp (5–6); x 2 (6–9) in elongation of x 1, above posterior fourth of opercle, parallel to and exceeding POC; z (7–9) in elongation of PC, ventrally reaching close to but not exceeding pore γ; y (7–8) immediately behind τ and below x 2; three short transverse rows in oculoscapular groove between ρ and θ; q (4–5) anterior most, close to ρ, extending ventrally of the oculoscapular groove and sometimes with one or two papillae dorsal of ρ; posterior most trp close to θ, extending dorsally and passing upwards the level of x 1; between q and trp a third transverse row named here row u (3–4) considering its position despite row being transverse; transversal axillary rows as 1 -as 3 long (as 1: 12–18, as 2: 13–17, as 3: 12–15); longitudinal axillary series represented by two rows (la 2: 2–4, la 3: 2–3). Opercular: three rows, one transversal (ot: 38–52), sometimes divided in two parts, and two longitudinal (os: 17–23, oi: 14–19) rows. Anterior-dorsal (occipital): five rows, two transversal (n and o) and three longitudinal (g, m and h); n (9–11) behind pore ω of AOC; rows o (6–10) widely separated; row g (7–12) posterior of o, not reaching row o anteriorly; m (5–8) almost parallel to g, behind and below it; h anterior to origin of first dorsal fin (D1), divided in two sections (h 1: 5–8, h 2: 3–6).

Colouration. No distinct sexual dichromatism, or colouration differences in hybrids is evident on the specimens. In life: head and body yellowish brown; several large dark brown saddles on back below the dorsal fins and on the caudal peduncle; flanks covered with many dark brown spots and row of irregular and elongated dark blotches along the midline, all forming a reticulate pattern on a yellow background; cheek with brown reticulations or mottlings, and with a short brown longitudinal stripe starting below eye and going backwards about half way to preopercle; upper lip with reticulate patterns or mottles; P base with reticulate patterns, upper part with a distinct dark brown stripe. Breast, abdomen, and fins greyish. D1 with two to three brown horizontal bands, and a bright orangish-yellow horizontal band along upper edge of I–V interradial membrane, progressively narrowing posteriorly; upper anterior part of D1 with a dark oblique spot on I–II interradial membrane below the marginal band. D2 with three distinct longitudinal rows of yellowish-brown spots on proximal part, distal half with numerous small spots on the sides of the rays. Anal fin without any distinct band or mark. P rays yellowish. P and C with several concentric narrow rows of yellowish-brown spots, concentrated near base of fin. D2, A, and C with whitish fringe along the edge.

Preserved specimens: background colour of the preserved specimens less yellowish; brown saddles on back below D1 and D2 and on the caudal peduncle; flanks with row of large dark blotches along the midline. Head and body with less pronounced reticulate patterns. Cheek with a longitudinal dark brown stripe. Fins dark grey. D1 with a white band across upper edge, two to three horizontal dark bands, and a dark oblique spot between I–II. P base with a dark strip on the upper part. Horizontal rows and brown spots on all fins less distinct than in live specimens.

Otolith. ( Figs. 1 & 7a–d , Table 5 ). The five specimens with the new species haplotype were not examined for their otoliths since they were (i) fixed in 10% formaldehyde solution (formaldehyde causes decalcification and degradation of otoliths) for subsequent morphological analyses, (ii) included as paratypes (4 of 5; see material examined). Therefore, otoliths from a total of 21 specimens from the Kaboudval Stream (including several specimens with the gorlap haplotype) were examined using light microscopy and digital photographs. All otoliths were similar in general morphology, thus, four of these otoliths ( Fig. 7 a-d) were selected randomly for SEM imaging, morphometric measurements, and description. The otoliths have a parallelogram shape, with marked preventral and posterodorsal projections. The otolith length to height (OL/OH) ratio is 1.22–1.39; the dorsal rim with a broad concavity in the middle, smooth; predorsal angle orthogonal; posterodorsal projection highly positioned, broad, long, pointed or blunt, and slightly bent outwards. The anterior rim usually lacks incision, or is sometimes incised at or slightly above the level of ostium, inclined at 72.30–84.29° (β). Posterior rim almost parallel to the anterior rim or a little less oblique, inclined at 101.31–104.86° (γ), with a concavity (incision or notch) below the posterodorsal projection at or slightly below the level of cauda. Angle of preventral to posterodorsal traverse 24.36–34.14° (δ). Ventral rim horizontal and smooth; preventral projection usually long, sometimes short, pointed or blunt; posteroventral angle usually orthogonal. Sulcus centrally positioned, sole-shaped, anteriorly inclined at 10.22–19.06° (α), very deep with developed ostial lobe. Sulcus moderately long, and very wide; the ratio of sulcus length to height (SuL/SuH) 1.47–1.82. The sulcus height to otolith height (SuH/OH) ratio is 0.34–0.40. Subcaudal iugum present, short (usually 1/3 cauda length), slender, below the anterior part of the cauda. Ventral furrow running with a moderate distance to ventral rim, curved upwards anteriorly to or slightly below the level of the ostial apex and turning upwards to the level of the caudal tip or slightly below it. Dorsal depression indistinct or absent. Otolith variables and shape indices are provided in Table 5 .

Sexual dimorphism. Sexes can be distinguished externally by the shape of the urogenital papilla, which is conical in males with pointed posterior edge, and wider, trapezoid and with villous posterior edge in females. Males grow to a larger size (up to 120.0 mm total length vs. 101.2 mm for female maximum recorded total length). All morphometric and meristic characteristics are overlapping, males however, (i) tend to have a deeper cheek (18.02–24.37 vs. 16.92–19.61% of Hl), (ii) are dominated by individual (14 of 21) with 15 branched rays in the second dorsal fin [vs. 14 branched rays in females (6 of 10)], and (iii) show a larger range of pectoral fin rays (17–20 vs. 18–19).

Etymology. Named for Hyrcania , the Greek name for the south Caspian region where the species occurs.

Distribution and conservation. Ponticola hircaniaensis sp. nov. is known only from its type locality, located 1 km south of the city of Aliabad-e-Katul ( Figs. 8–9 ). Its small population is confined to a single area (extent of occurrence <2 km 2) above the Zarrin Gol Dam (IUCN criteria B1 and Ba for critically endangered species) ( Fig. 9 ). Habitat fragmentation by the dam is likely to block gene flow, resulting in decline of genetic diversity, and possibly increases competition for spawning territories and resources, and increases hybridization with P. gorlap . Moreover, according to our field observations, there is a decline in quality of habitat at Kaboudval due to excessive grazing, erosion, and human effects [IUCN criterion Bb(iii)]. In addition, Pseudorasbora parva (Temminck & Schlegel, 1846) and Gambusia holbrooki Girard, 1859 , two of the most successful invasive fish species in the world with negative impacts on native fish species, have established populations at Kaboudval. For example, high densities of P. parva have severe and significant impacts on native trophic food webs, resulting in overlap with native fishes trophic niches, increased egg predation, and transmission of the novel fungal fish pathogen Sphaerothecum destruens , which is responsible for the decline of many native fish populations ( Andreou et al. 2012). Based on the extremely small area of endemism threatened by negative anthropogenic impact we suggest that P. hircaniaensis sp. nov. should be classified as Critically Endangered (CR) species, fulfilling geographic range criteria (extant of occurrence combined with two more conditions) for this category, according to the IUCN (2012) red list categories.

Ecology. Ponticola hircaniaensis sp. nov. is an exclusively freshwater species, restricted to a very shallow foothill stream (0.1–0.3 m depth, 1–2 m width) with slow current ( Fig. 9 ). The bottom is muddy-sandy or composed of cobbles and boulders, pebbles and gravel, and the banks are vegetated. The collecting site was at the altitude of 196 m a.s.l., and 79 km inland from the Caspian Sea. Syntopic fish species were Alburnoides tabarestanensis MousaviSabet, Anvarifar & Azizi, 2015 , Gambusia holbrooki Girard, 1859 , Hemiculter leucisculus (Basilewsky, 1855) , and Pseudorasbora parva (Temminck & Schlegel, 1846) .

Figures

FIGURE 1. Left sagittal otolith (inner face) of Ponticola hircaniaensis sp. nov. (ZM-CBSU K28, 66.65 mm SL, Kaboudval Stream), showing the terminology of characters and otolith shape outline (red line). OL, maximal otolith length; OL2, minimal otolith length measured at maximum ingression of concavity of posterior rim; OH, maximal otolith height; OA, otolith area; OP, otolith perimeter; SU, sulcus; ca, cauda; os, ostium; ol, ostila lobe; CL, colliculum length measured along its axis; si, subcaudal igum; α, inclination angle of ostium measured from tip of ostium through midpoint of sulcus height at collum; β, inclination angle of anterior rim; γ, inclination angle of posterior rim; δ, inclination of line connecting preventral angle with tip of posterodorsal projection.

FIGURE 4. Genetic alignment of the nuclear S7 gene fragment between 466 and 547 nucleotide positions. Chromatograms show the hybrid [middle: molecular ID: 3435 (GenBank number: ON186770), Kaboudval Stream] individual’s heterozygous peaks (underlined with black bars) at the diagnostic sites, where Ponticola hircaniaensis sp. nov. [top: molecular ID: 3432 (Gen- Bank number: ON186768), Kaboudval Stream] and P. gorlap [bottom: molecular ID: 2786 (GenBank number: ON186767), Babolroud River] present fixed differences.

FIGURE 5. Ponticola hircaniaensis sp. nov.: (A) ZM-CBSU S101-6, male, holotype, 76.9 mm SL; (B) ZM-CBSU S099-5, male, paratype, 73.6 mm SL; (C) ZM-CBSU S099-11, male, paratype, 76.0 mm SL. All from the Kaboudval Stream, southern Caspian Sea basin. Photos by F. Zarei, Y. Bakhshi, & A. Jouladeh-Roudbar.

FIGURE 6. Head lateral line system (left side) of Ponticola hircaniaensis sp. nov. ZM-CBSU S099-8, paratype, male, 78.4 mm SL, Kaboudval Stream, south Caspian Sea basin. Terminology in text. Drawing by F. Zarei.

FIGURE 7. Otolith morphology (sagittae, inner face) of the studied Ponticola spp. (a–d) Ponticola hircaniaensis sp. nov.: ZM-CBSU K18, K21, K24, and K28, respectively (64.0–74.6 mm SL). (e–h) Ponticola iranicus: ZM-CBSU 37, 40, 141, and 144, respectively (71.6–76.4 mm SL). (i–l) Ponticola patimari: ZM-CBSU P2, P3, P4, and P6, respectively (53.9–65.2 mm SL). (m–p) Ponticola gorlap: ZM-CBSU 44, 45, 46, and 48, respectively (71.6–86.5 mm SL). (q–r) Ponticola iljini: ZMMSU P-23516 (90–95 mm SL) (refigured from Vasil’eva et al. 2016). (s–t) Ponticola kessleri: non-cataloged specimens from the RBINS collection (77–92 mm SL) (refigured from Jacobs & Hoedemakers 2013). (u–v) Ponticola syrman: ZM-CBSU 77, and 78, respectively (128.1–181.4 mm SL).

FIGURE 8. Distribution map of the Ponticola spp. in the south Caspian Sea basin, showing the type locality of Ponticola hircaniaensis sp. nov., Kaboudval Stream (large black square). Map by F. Zarei.

FIGURE 9. Habitat of Ponticola hircaniaensis sp. nov., above the Zarrin Gol Dam (A), Kaboudval Stream (B). Photos:A from Google Earth, B by F. Zarei.