Turcogammarus aralensis ( Uljanin, 1875 )

Copilaș-Ciocianu, Denis, Sarmanov, Aibek, Sergaliyev, Nurlan & Sidorov, Dmitry, 2022, Turcogammarus aralensis (Uljanin, 1875), a relict pontogammarid amphipod crustacean from the Aralo-Caspian paleobasin: redescription, phylogenetic position and biogeography, Zootaxa 5219 (2), pp. 101-120 : 106-113

Turcogammarus aralensis ( Uljanin, 1875)

Figures 3–8

Gammarus aralensis Uljanin in Fedchenko 1875: 1, pl. 5, figs 15-19 (original description), (type locality: in washed ashore Zostera at Zaliv Bolshoy Saryshiganak, Aral Sea, Kazakhstan).— Sowinsky 1894a: 392; 1894b: 15, pl. 1, figs 1-9, pl. 2, figs 10-18; 1898: 390; 1904: 408 ( Pontogammarus ).— Stebbing 1906: 459 (non D. haemobaphes ).

Pontogammarus aralensis (Uljanin) .— Martynov 1922: 13; 1924a: 37; 1924b: 214.— Behning et al. 1929: 104; 1936: 83, textfigs 1, 2; 1937: 168; 1938a: 214; 1940a: 383, Abb. 3; 1940b: 92, text-fig. 5a, b.— Schellenberg 1944: 194.—MordukhaiBoltovskoi 1960: 1464; 1964: 163; 1972: 14, 16; 1979: 13.— Mordukhai-Boltovskoi et al. 1969: 466, pl. 12, fig. 1,— Straškraba 1967: 207.

Pontogammarus aralensis setosus (Schäferna) .— Derzhavin 1938: 176. (non T. aralensis ).

? Pontogammarus crassus (Grimm in G.O. Sars 1894).— Behning 1938b: 292.

Dikerogammarus aralensis (Uljanin) .— Birstein 1945: 518.— Barnard 1958: 48.— Birstein & Romanova 1968: 253, fig. 266.— Dedju 1980: 24, 162.— Pjatakova & Tarasov 1996: 67.

Niphargoides aralensis (Uljanin) .— Dedju 1967: 35 ( Pontogammarus ).

Obesogammarus aralensis (Uljanin) .— Stock 1974: 83; Stock et al. 1998: 175.

Turcogammarus aralensis (Uljanin) .— Barnard & Barnard 1983: 546.— Copilaș-Ciocianu & Arbačiauskas 2018: 286, fig. 1f. — Matmuratov & Saparov 2020: 577.— Karaman 2021: 159.

non Pontogammarus cf. aralensis (Uljanin) .— Sket & Hou 2018: 6, suppl. 2.

Diagnosis (both sexes). Stout, but distinctly laterally compressed, medium-sized gammaroid amphipod with large well-pigmented eyes; body color yellowish / off-white in alcohol; antennae and pereopods comparatively short; antenna 1 slightly longer than antenna 2, both less than a third of total body length, antenna 2 flagellum with setae longer than article widths; gnathopod 2 larger than first gnathopod, each gnathopod with 1 mid-palmar spine (in males, but females lacking mid-palmar spines); coxal plates 1–4 fringed with a row of long setae along lower edges; metasome not keeled, smooth; urosomal segments 1 and 2 with bulging cones bearing spines (cone shaped cuticular protrusions); bases of pereopods 5–7 with short rare setae along posterior margins; epimeral plates 1 and 2 with posterior margins naked; uropod 3 exodopodite with plumose setae of equal length at margins. Body length up to 10.5–11.0 mm (males), 9.5 mm (female).

Ecology and biology. The species inhabits coastal and estuarine areas, standing waters in relict lakes or stagnant parts of rivers, benthic (0–10 m depth), but probably tends to patches of aquatic plants ( Filchakov 1994, attributed to phitophils), widely euryhaline (from 0.2 up to 55‰) ( Plotnikov et al. 2021), generally produces 3 generations per year ( Khusainova 1955), observed in the diet of whitebaits (roach, bream, shemaya) and shrimp Palaemon elegans Rathke, 1837 , in biofoulings ( Zevina et al. 1963; see also Copilaș-Ciocianu & Sidorov 2022).

Distribution (see map, Fig. 1 ). (i) Native (Aralo-Caspian) realm: Aral Sea ( Uljanin 1875; Sowinsky 1894a, 1904), lower reaches of the Syr Darya ( Filippov et al. 1993), lakes of the Akshatau and Sarykamysh system, West and East Karateren ( Matmuratov & Saparov 2020), northeastern Caspian (Dead Kultuk Sor and Sor Kaydak) ( Behning 1935, 1937, 1940b), northwestern Caspian (Dagestan) ( Amaeva et al. 2013) and (Kalmykia) ( Uryupova 2008), Zhem (Emba) River at Kulsary ( Copilaș-Ciocianu & Arbačiauskas 2018; present data), lower reaches of the Ural River, Shalkar, Balykty Sarkyl and Edilsor lakes ( Behning et al. 1929; Behning 1938a; see also Kulkina 1991; Tarasov 1995; Sarmanov et al. 2021; Sarmanov & Sultanov 2020), probably Yaskhan Lake ( Behning 1938b); var. caspia G.O. Sars, 1896 a poorly known form of ‘ G. aralensis ’ refers to P. robustoides (see Martynov 1924a) was reported from Kara-Bogaz-Gol (G.O. Sars 1896) and floodplain lakes in the Volga River basin at Selitrennoye ( Derzhavin 1912; see also Starobogatov et al. 1994).

(ii) Ancient migratory route: Manych-Gudilo ( Behning 1936; Tauson 1936; Kharin 1948; Shokhin & Sayapin 2005; Uryupova 2008; Stepanjan & Startsev 2014).

(iii) Peripheral (Ponto-Azov) range includes: Sea of Azov ( Sowinsky 1894b; Derzhavin 1925; MordukhaiBoltovskoi et al. 1969); lower reaches of the Don River ( Martynov 1922, 1924 a, 1924b; Uryupova 2008; Zhivoglyadova & Afanasyev 2018); Dniester Estuary, S. Bug and Cascade of the Dnieper Reservoirs ( Markovsky 1953; Dedju 1980; Pligin et al. 2013), Katlabuh Lake ( Hou & Sket 2015, with doubts) and estuaries of Kiziltashskiy Liman ( Rudakova et al. 2019).

Species is reported to be extinct in the Aral Sea ( Aladin et al. 2020) and lakes of the Bukhara region of Uzbekistan ( Mustafaeyvа & Mirzayev 2018). It is included in the Red Data Book of the Republic of Uzbekistan ( Kreuzberg 2019).

Material examined (new records). Kazakhstan: three specimens: 2 males ca. 11.0 mm, 10.5 mm (uropod 3, missing), 1 female ca. 9.5 mm (carrying 15 small eggs in brood pouch, damaged); Kulsary , Zhem (Emba) River; 47.051N, 54.060E; elevation ca. - 11 m; 15 May 2000; leg. K. Arbačiauskas ; MNHN-IU-2021-7289. Six specimens: 2 males, ca. 7 mm, 8 mm, 3 females, ca. 5 mm, 6 mm (2x), 1 juv.; Shalkar Lake (from three closely points); approx. 50.523N, 51.774E; elevation ca. 13 m; 17 April, 31 July, 28 August 2021; leg. A. Sarmanov; GTCA207-208 - NRC .

Description of specimen MNHN-IU-2021-7289. Male. Body 11.0 mm long. GENERAL BODY MORPHOLOGY ( Figs 3 , 7 ). Body stout, smooth, with discriminative dorsal cuticular outgrowths (hispid humps) on urosomal segments 1 and 2. Head as long as pereonite 1; rostrum indistinct; lateral cephalic lobe with recess, inferior antennal sinus moderate, rounded; eyes large. Pleonites lacking setae along lateral and dorsal margins; epimeral plates 1–3 with fascicle of long thin setae each anteriorly, ventral margins with stiff setae, especially pronounced in epimeron 2 with two rows of irregular bundles of setae subventrally, distoposterior corner receded in plate 1, produced and acute in plates 2 and 3. Urosome with noticeable cuticular elevations on dorsal surface of urosomites 1 and 2, armed with 4 or 5 notched spines in group, accompanied with short setae inserted among spines; urosomite 3 with lateral groups of spines at posterior margins, with couple of median bundles of short setae among spines. Telson longer than wide, deeply split, each lobe with 2 sub-apical notched spines each accompanied with 2 moderately long setae. ANTENNAE ( Figs 3 , 4A, 4B ). Antenna 1 0.28 times shorter than total body length, ca. 0.1 times longer than antenna 2; peduncular articles 1–3 in length ratio 1:0.5:0.3 with clusters of short setae in proximal parts, article 2 with group of setae in middle; primary flagellum with 19 segments, each bearing 1 minute aesthetascs accompanied by short setae on medial margin; accessory flagellum 4-articulate, with short notched spines on facial margin, 2 papoose setae apically. Antenna 2: gland cone short; peduncular articles 4 and 5 in length ratio 1:0.8, both densely setose with tight bundles of long stiff setae on medial face; flagellum 0.3 times shorter than peduncle (articles 4+5), with 6 segments densely setose with bundles of long stiff setae on lateral faces and apices; calceoli absent. MOUTH PARTS (typical gammarid, Fig. 5 ). Upper lip sub-rhomboid, with group of minute setae on apical part. Mandibles subequal: left mandible: incisor with 5 teeth, lacinia mobilis with 4 teeth; between lacinia and molar a row of 6 serrate spines. Right mandible: incisor process with 4 teeth, lacinia mobilis bifurcate, with several denticles, between lacinia and molar a row of 5 serrate spines; triturative molar process strong, with long plumose seta; mandibular palp article 2 longer than article 3 (distal), bearing row of about 17 rather long setae on inner margin; palp article 3 with 3 groups of 3, 4 and 7 A-setae, 3 C-setae, 4 E-setae and row of about 13 D-setae. Lower lip with ovate, somewhat cone-shaped inner lobes. Maxilla 1 asymmetric, palps long, with 2 plumose setae each on lateral faces, distally armed, left palp with 5 notched spines and 4 simple setae, right palp with 6 teeth and 2 setae; outer plate with 11 comblike, multi-toothed spines, inner lobes sub-triangular, with 14 plumose setae. Maxilla 2 ordinary, with oblique row of 12 rather long, plumose setae extending from medial margin onto inner face; both plates with numerous apical setae, some lightly plumose. Maxilliped normal: basal endite (= inner plate) sub-rectangular, with 3 strong peg-like spines and 5 nonplumose setae apically, 5 plumose setae on ventral face; outer plate sub-ovoid, with a row of 9 simple spines and 3 serrate spine-setae along outer margin, numerous stiff setae sub-marginally; maxilliped palp article 3 narrow, with 2 groups of long, stiff setae along lateral face; dactyl (article 4) with prominent strong nail bearing 5 setae at base. COXAL PLATES AND GILLS ( Figs 3 , 4 , 6 ). Coxae 1–4 deep, roughly square or rectangular, ventral margin slightly serrate with ca. 14–17 (48 in coxae 4) long setae, coxa 1 expanded towards ventral margin, coxa 2 narrowed towards ventral margin; coxae 5 and 6 with distinct anterior lobes with short stiff seta, posterior margin slightly notched bearing a row of setae; coxal plate 7 smallest, with distinct lobes, bearing 2 clusters of setae on anterior margin, posterior margin notched bearing a row of numerous setae; each plate 2–7 bearing single, sac-like coxal gill on long stalk. Ventral surface of pereon 7 bearing a pair of genital papillae. GNATHOPODS ( Figs 3 , 4C, 4D ). Gnathopod 1 (G1) moderately setose, basis (article 6) stout, with long non-plumose setae on anterior and posterior margins, anterior ones with a row of short setae; carpus (article 5) triangular, 0.32 × as long as propodus; propodus sub-triangular, ovate, palm concave with cutting margin developed and armed with 6 distally notched spines at defining angle; posterior margin as long as palm bearing a group of simple setae; dactylus with 1 seta on outer face, nail strong. Gnathopod 2 (G2) generally similar to gnathopod 1, but a little larger; carpus 0.29 × as long as propodus; propodus sub-rectangular, palm convex and armed with 5 distally notched spines at defining angle; dactylus similar to that of gnathopod 1. PEREOPODS ( Figs 3 , 6 ). Pereopods 3 and 4 (P3, P4) sub-similar, but pereopod 3 a little longer; bases narrow, with sets of long and short setae on both margins; merus (article 4) dilated, with 1 spine on postero-distal corner; lengths of merus: carpus: propodus is 1.0:0.8:0.8, furnished with (equally) dense brushes of long setae along posterior margins; carpus (article 5) and propodus (article 6) armed with posterior notched spines in the following manner 1-1-2 and 1-2-2-2 correspondingly; dactyli ca. 0.40 × as long as article 6, with a short nail. Pereopods 5–7 (P5–P7) sub-similar, but distinctly differs in size and shape of bases (article 2), lengths of bases 5: 6: 7 is 0.6: 0.8: 1.0; basis 5 broad, evenly elongated with postero-distal lobe weakly expressed, basis 6 tapering distally with postero-distal lobe truncate, basis 7 distinctly expanded, with distoposterior lobe distinctly expressed, distoposterior corner broadly rounded; dactyli similar to that of pereopods 3 and 4; pereopods 5–7 in length ratio 0.8:1:0.9. PLEOPODS AND UROPODS ( Figs 3 , 7 ). Pleopods 1–3 ordinary, peduncles with some groups of long, thin setae, coupling spines (retinacula) 2-hooked accompanied with 3 stiff, simple setae. Uropods 1–2 peduncles extending well beyond urosoma, rami slightly beyond terminal end of uropod 3 peduncle; peduncles with ca. 2 or 3 spines along edges, uropod I peduncle with 2 basofacial spines accompanied with group of setae, rami armed with 1 or 2 single spines along margins; uropod I inner ramus (= endopodite) with 2 long, stiff setae on dorsal face; both rami with 5 terminal notched spines. Uropod 3 of parviramous type (with inner ramus less than half of outer one), endopodite (= inner ramus) short, 0.2 × as long as outer, with 1 apical spine and 5 plumose setae on medial face, peduncle as long as urosomite 3, 0.55 length of outer ramus, bearing a group of ventrodistal notched spines, exopodite (= outer ramus) 2-articulate, proximal article with 3 groups of twin spines laterally and with moderately dense marginal brushes of long finely plumose setae, distal article short, with set of setae apically.

Variation. Our new data revealed minor discrepancies with the early species identifications originating from the Aral Sea ( Table 1 ); some features were either omitted by Sowinsky (1894a), or characteristic: G2 basis devoid of setae on anterior margin, segments of P5–7 seem to be covered with tufts of longer bristles, uropods 1 and 2 lacking sub-apical spines on rami. Noteworthy is the rather large difference between the total body size of adults: Sea of Azov basin 5.0– 7.5 mm ( Martynov 1924b); Manych 7.0– 7.5 mm ( Behning 1936); Shalkar Lake 7.5–8 mm ( Behning et al. 1929); Aral Sea 7.6–8.7 mm ( Sowinsky 1894a); Zhem (Emba) River 9.5–11.0 mm (our data); but without specifying the measurement method in previous works.

Sexual dimorphism. Weak, ordinary (accessory sex structures absent), expressed in the larger body size in males; females with oostegites (brood plates) on limbs 2 to 5 large, oblong, truncate apically, plate 5 slender ( Fig. 8C ). Sexually dimorphic appendages both antennae and gnathopods somewhat smaller and less densely setose in females, flagellum of antenna 2 with setae shorter than article widths; among other things females is different by lacking mid-palmar spines on both gnathopods ( Figs4E, 4F ) and pereopods 3–4 propodi without bundles of long setae.

Taxonomic remarks. Turcogammarus aralensis is a characteristic digger-ecomorph with shortened limbs and antennae, merus of P3 and P4 dilated, P7 basis expanded, along with presence of urosomal cones that probably are an adaptation mechanism against predatory fishes (Copilaș-Ciocianu & Sidorov 2022), or palaemonid prawns. The species was described rather superficially by Uljanin (1875, as belonging to Gammarus ) based on a single sample from Aral, omitting important details. It was scrupulously re-described by Sowinsky (1894a) on extensive collections from the South Bay of the Rebirth Is. in Aral. Subsequently, T. aralensis was repeatedly reported in numerous publications (see above), that greatly expanded its range. However, its morphological variability remains little studied, which has necessitated a comparative study of occurrence records from various remote populations in the Ponto-Caspian basin to understand species-specific limits and variability. Based on the data of comparative morphological analysis and molecular phylogenetics we came to the conclusion that T. aralensis is a sister species to O. crassus . Both share several similarities such as the stout habitus, large eyes, setation of the antennae and pereopods 3–4, and poorly setose posterior margin of pereopod 7 basis. However, T. aralensis can be separated clearly from O. crassus by the presence of urosomal cones (absent in O. crassus ), a denser setation of the lower margins of coxal plates 1 to 4, and the presence of short setae on the inner and outer surface of basipodites of pereopods 5–7 (absent or poorly developed in O. crassus ).

With respect to the remaining two species of Turcogammarus , T. aralensis most resembles T. turcarum ( Stock, 1974) sharing sub-similar urosomal cones, but can be distinguished from the latter by clear differences in armament of uropods 1 and 2 rami, by the short and sparse setation of the posterior margin of basis of pereopod 7 (long and dense setae in T. turcarum ); from T. spandli (Karaman, 1931) is clearly distinguished by the absence of cuticular carina on the pleosomal segments. Our molecular phylogeny indicates that the genus may not be monophyletic as T. aralensis and T. spandli appear distantly related ( Fig. 2 ). However, we lack sequences of T. turcarum , and the single marker mitochondrial phylogeny lacks sufficient phylogenetic signal to confidently resolve deep nodes. As such, the validity of the genus Turcogammarus still remains to be tested in the future.

Figures

FIGURE 1. Distribution map of pontogammarid amphipod Turcogammarus aralensis (Uljanin, 1875) in the Ponto-Aralo- Caspian basin, with reference data on sequenced specimens (red circles—literature records, black circles—new records). Each point may represent 1–3 closely adjacent localities (for further explanation, see text).

FIGURE 2. Maximum-likelihood phylogeny based on the COI marker. Numbers at nodes represent values of the ultrafast bootstrap support and Shimodaira-Hasegawa approximate likelihood ratio test. Gray boxes on the right indicate the results of the species delimitation analyses using ASAP, PDT and PTP.

FIGURE 3. Habitus of Turcogammarus aralensis (Uljanin, 1875), lateral view, MNHN-IU-2021-7289, male, 11.0 mm.

FIGURE 4. Turcogammarus aralensis (Uljanin, 1875), MNHN-IU-2021-7289. A–D, male, 11.0 mm. (A) Antenna 1. (B) Antenna 2. (C) Gnathopod 1. (D) Gnathopod 2.—E, F, female, 9.5 mm. (E) Gnathopod 1, setation omitted. (F) Gnathopod 2, setation omitted.

FIGURE 5. Turcogammarus aralensis (Uljanin, 1875), MNHN-IU-2021-7289, male, 11.0 mm. (A) Maxilla 1, right. (B) Palp of maxilla 1, left. (C) Maxilla 2. (D) Mandible, left. (E) Mandible, right. (F) Lower lip. (G) Upper lip. (H) Maxilliped.

FIGURE 6. Turcogammarus aralensis (Uljanin, 1875), MNHN-IU-2021-7289, male, 11.0 mm. (A) Pereopod 3. (B) Pereopod 4. (C) Pereopod 5. (D) Pereopod 6. (E) Pereopod 7.

FIGURE 7. Turcogammarus aralensis (Uljanin, 1875), MNHN-IU-2021-7289, male, 11.0 mm. (A) Urosoma, dorsal view. (B) Epimeral plates 1–3. (C, D, E) Pleopods 1–3. (F) Uropod 1. (G) Uropod 2. (H) Uropod 3. (I) Telson.

FIGURE 8. Turcogammarus aralensis (Uljanin, 1875), MNHN-IU-2021-7289, female,9.5 mm. (A) Head with antennae (part.). (B) Pereopod 3. (C) Pereopod 5 (part.). (D) Pereopod 6 (part.). (E) Pereopod 7. (F) Uropod 1. (G) Uropod 2. (H) Uropod 3. (I) Telson.