Зоологический журнал, 2020, T. 99, № 11, стр. 1242-1257

Examples of rare benthic Cladocera: two phytophilous species of Aloninae (Cladocera, Anomopoda, Chydoridae) from European Russia

A. Y. Sineva ab*, D. E. Gavrilko 3**

a Biological Faculty, M.V. Lomonosov Moscow State University
119234 Moscow, Leninskie Gory 1–12, Russia

b A.N. Severtsov Institute of Ecology and Evolution
119071 Moscow, Leninsky Prospect 33, Russia

c Department of Ecology, Institute of Biology and Biomedicine, Lobachevsky State University of Nizhniy Novgorod
603950 Nizhniy Novgorod, Gagarin Avenue 23, Russia

* E-mail: artem.sinev@gmail.com
** E-mail: dima_gavrilko@mail.ru

Поступила в редакцию 2.03.2020
После доработки 4.04.2020
Принята к публикации 4.05.2020

Полный текст (PDF)

Аннотация

Morphology of two extremely rare European species, Ovalona karelica (Stenroos 1987) and Graptoleberis smirnovi sp. n., of the subfamily Aloninae is studied in populations from the Nizhniy Novgorod Area, Russia. Graptoleberis smirnovi sp. n. differs from all other species of the genus in the unique morphology of the labrum, having a long, narrow, serrate process at the apex. Morphologically, it is close to another rare European species, Graptoleberis pannonica Daday 1904. The taxonomic positions and distributions of the study species are discussed.

Keywords: Cladocera, Aloninae, rare species, morphology, Nizhniy Novgorod, Russia

DOI: 10.31857/S0044513420110069

While Cladocera of the European part of Russia were intensively investigated from the second half of the 19th century (see review by Korovchinsky, 2012), benthic species of the group here are still far from fully studied. Early taxonomic studies (Fischer, 1848, 1849, 1854; Hudendorf, 1876; Stenroos, 1897; Werestschagin, 1911 and others) led to descriptions of numerous new taxa of Chydoridae and Macrothricidae, including several valid species – Graptoleberis testudinaria (Fischer 1848), Streblocerus serricaudatus (Fischer 1849), Alonella excisa (Fischer 1854), Leydigia acanthocercoides (Fischer 1854), Ovalona karelica (Stenroos 1897), Camptocercus fennicus Stenroos 1897. During the first half of the 20th century, taxonomic and morphological studies of planktonic and especially benthic Cladocera in general were in decline (Korovchinsky, 2007, 2012). All species of benthic Cladocera, listed in the monograph of Manuilova (1964) on Cladocera of USSR, were described in the 19th century.

New breath to the studies of benthic Cladocera of Russia was given by the efforts of Prof. Nikolai Nikolaevich Smirnov. His research started as ecological and morphological studies on common Chydoridae from European Russia, culminating in to date unsurpassed reviews of the world fauna of Chydoridae (Smirnov, 1971, 1996) and Macrothricidae (Smirnov, 1976, 1992). In these monographs, the morphology of all common benthic Cladocera from European Russia was described, and their taxonomic status was clarified. Together with his alumni, Prof. Smirnov published a new modern key for Cladocera of Russia (Kotov et al., 2010). By the efforts of Prof. Smirnov, the modern Russian school of cladoceran systematics was established, and his alumni continue taxonomic and morphological studies of both Russian and world fauna of Cladocera.

Still, а number of rare benthic species was recorded from European Russia only sporadically, and usually no detailed descriptions provided for them (see Smirnov, 1971, 1976; Kotov et al., 2010). Rare occurrences of species having their core distribution areas outside European Russia were revealed recently (Gavrilko et al., 2020; Zhiharev et al., 2020; Frolova et al., 2019). Some of such taxa were redescribed recently (Smirnov, 2004; Sinev, 2014; Zhiharev et al., 2020), but a number of them remain poorly studied.

Two rare European species of the subfamily Aloninae, Graptoleberis pannonica Daday 1904 and Ovalona karelica (Stenroos 1987), were found recently in Nizhny Novgorod Area, central part of European Russia (Gavrilko et al., 2020). They inhabit the coastal zone of the Gnilichka River, located on the outskirts of Nizhny Novgorod city. The river is characterized by low flow rates and abundant development of Stratiotes aloides L. in the dammed areas. The rare species are found only in dense thickets of S. aloides at a depth of up to 1 m. Debris of submerged macrophytes form a habitat and provide a substrate for the nutrition and movement of these crustaceans. However, these crustaceans had a low abundance in the sampled localities. O. karelica density reached a maximum of 12 000 ind./m3. The abundance of G. pannonica was lower, up to 30 ind./m3 (Gavrilko et al., 2020).

According to Bledzki & Rybak (2016), Ovalona karelica is a “eurythermic, “Ice Age relict” species with a limited distribution, extremely rare in Europe, reported from swamps, marshes, old river oxbows, temporary waters, in dense vegetation (Sphagnum) or on muddy bottom with plant remains, among the roots of Hydrochariton, prefers weakly acidic waters with pH > 5.0”. In Russia, it was recorded only from northern portion of European Part (Smirnov, 1971; Sinev, 2002), so populations from Nizhny Novgorod are on the south-east margin of the species distribution area. Morphology of the species was redescribed by Hudec (2010) and Van Damme et al. (2011), but some important details of the thoracic limb morphology, like morphology of inner portions of limbs III–IV, remain unknown. Van Damme et al. (2010) placed this taxon in the pulchella-group of Alona s. lato, during revision of pulchella-group. Sinev (2015) placed O. karelica within the cambouei-group of the genus Ovalona, characterized by elongated postabdomen, but species relationships within the group remain obscure.

Graptoleberis pannonica Daday 1904 was described from Hungary, it differs from widespread Graptoleberis testudinaria and Neotropic Graptoleberis occidentalis Sars, 1901 in more elongated, low body, longer postabdomen with almost parallel dorsal and ventral margins in both males and females. The species is extremely rare, it was reported only from Hungary (Daday, 1904) and Slovenia (Hudec, 2010), and upper basin of the Don River, European Russia (Smirnov, 1971). It was never redescribed according to recent standards. The aim of present paper is to study morphology of two rare taxa from Nizhny Novgorod area and to clarify their taxonomic status.

MATERIALS AND METHODS

Animals and exuviae were selected from samples under a binocular stereoscopic microscope, placed on slides (in a drop of a glycerol-ethanol mixture), and studied using an optical microscope (Olympus CX41) and measured. Dissections for analysis of appendages were performed with electrogalvanically sharpened tungsten needles. Measurements were determined using an eyepiece-micrometer; all drawings were made with a camera lucida. For SEM examination, specimens were subject to critical point drying, coated with gold-palladium and studied using scanning electron microscopes JEOL JSM-6380LA and CAMSCAN S2.

Abbreviations in the illustrations and text. I–V = = thoracic limbs I–V; as = accessory seta of limb I; cbs = copulatory brush seta of limb I; e1 – e3 = endites 1–3 of limb I; ep = epipodite; ex = exopodite; gfp = gnathobase filter plates of limbs II–V; IDL = inner distal lobe of limb I; IP = interpore distance (distance between anterior and posterior major head ps); ms = male seta of limb I; ODL = outer distal lobe of limb I; pep = pre-epipodite; PP = postpore distance (distance between posterior head pore and posterior corner of head shield); s = sensillum.

Paper registration number in Zoobank. urn:lsid:zoobank.org:pub:AA7EE6BB-42F4-4EF5-87A9-33662A04533C.

RESULTS

Our data confirms the taxonomic status of Ovalona karelica from Nizhny Novgorod. Populations of Graptoleberis, identified earlier as G. pannonica, instead belong to a new species, G. smirnovi sp. n.

Ovalona karelica (Stenroos 1897)

Stenroos, 1897: 52–53, Fig. 5, 6 (Alona); Herr, 1917: 103–105, Fig. 30–33 (Alona); Herbst, 1962: 88, Fig. 66 (Alona), 1974: 134, Fig. 6–10 (Alona); Smirnov, 1971: 474–475, Fig. 464–465 (Alona); Hudec, 1980: 607–608, Fig. 1 (Alona), 1986: 188–191, Fig. 1–9 (Alona), 2010: 330–332, Fig. 81 (Alona); Flössner, 2000: 309–310, Fig. 114 (Alona); Sinev, 2002: 936–937, Fig. 3e, 4e (Alona); Van Damme et al., 2011: Fig. 1 A, C, E, D, G–I, K, Fig. 2 A–K (Alona); Sinev, 2015: 482-483, Fig. 11A-C ; Gavrilko et al., 2020: 153–154, Fig. 4.

Fig. 1.

Ovalona karelica (Stenroos1897) from Gnilichka River, Nizhniy Novgorod, Russia: a – juvenile female of instar II, b–k adult parthenogenetic female, l–n adult male (a–b, l lateral view; c – ventral margin of valves; d – posteroventral angle of valves; e – head pores; f–g – labrum; h–i – m, postabdomen; j, n antennule; k – antenna).

Fig. 2.

Ovalona karelica (Stenroos 1897), from Gnilichka River, Nizhniy Novgorod, Russia, adult parthenogenetic female: a–b – lateral view; c – dorso-lateral view; d – posteroventral angle of valves; e – head pores; f – postabdomen; g – postanal margin of postabdomen; h – postabdominal claw; i – antenna.

Fig. 3.

Ovalona karelica (Stenroos 1897), from Gnilichka River, Nizhniy Novgorod, Russia: a–j thoracic limbs of adult parthenogenetic female, k–l thoracic limbs of adult male (a, k – limb I; b – IDL and ODL of limb I; c – limb II; d – exopodite of limb III; e – inner potion of limb III; f – exopodite of limb IV; g–h – inner portion of limb IV; i – limb V (preepipodite not shown); j – inner lobe of limb V; l – copulatory hook and IDL of limb I).

Fig. 4.

Graptoleberis smirnovi sp. n., from Gnilichka River, Nizhniy Novgorod Area, Russia: a –n adult parthenogenetic female, o–r adult male (a, o – lateral view (sculpture of valves and head shield not shown); b – dorsal view; c – outline of lateral view; d – outline of dorsal view; e – setae of anterior portion of ventral margin of valves; f – posterior portion of ventral margin of valves; g–h – posteroventral angle of valves; i – head pores; j, p – labrum; k–l, q – postabdomen; m – postabdominal claw from the inner side; n, r – antennule).

Fig. 5.

Graptoleberis smirnovi sp. n., from Gnilichka River, Nizhniy Novgorod, Russia, adult parthenogenetic female: a – lateral view; b – dorso-lateral view; c – dorsal view; d–e – ventral view; f – ventro-lateral view; g – ventral side of the head (position of frontal pore indicated by arrow); h – frontal pore; i – head pores.

Fig. 6.

Graptoleberis smirnovi sp. n., from Gnilichka River, Nizhniy Novgorod Area, Russia, adult parthenogenetic female: a – ventral rims of valves; b – setae of ventral rim of valves; c – postabdominal claw.

Fig. 7.

Graptoleberis smirnovi sp. n., from Gnilichka River, Nizhniy Novgorod Area, Russia, adult parthenogenetic female: a – posteroventral angle of valves; b – postabdomen; c – labrum; d – antennule; e–f – thoracic limbs.

Fig. 8.

Graptoleberis smirnovi sp. n., from Gnilichka River, Nizhniy Novgorod Area, Russia: a–o – antenna and thoracic limbs of adult parthenogenetic female, p–q – thoracic limbs of adult male: a–b – antenna; c, p – limb I; d – ODL of limb I; e – IDL of limb 1; f – limb II; g– scraping setae 4–5 of limb II; h – exopodite of limb III; i – inner potion of limb III; j – outer setae and main sensillum of limb III; k – gnathobase filter plate of limb III; l – exopodite of limb IV; m–n – inner portion of limb IV; o – limb V (preepipodite not shown); q – copulatory hook of limb I.

Studied material. Over 100 juvenile and adult parthenogenetic females, 8 adult males from Gnilichka river, Nizhniy Novgorod, Russia (56.205576° N; 43.756625° E, samples collected in 2.08.2017, 19.09.2018, 13.09.2019, 26.09.2019).

Description. Parthenogenetic female. General. In lateral view body regular ovoid, of moderate height (Fig. 1a1b; 2a–2c), maximum height at middle of body, in adults height/length ratio 0.65–0.7. Dorsal margin uniformly curved; postero-dorsal and postero-ventral angles broadly rounded; posterior margin uniformly curved; ventral margin almost straight; antero-ventral angle rounded. Body very strongly compressed laterally. Ventral margin (Fig. 1c) with about 38–50 setae, about 10–15 first setae long, other setae shorter. Postero-ventral angle (Fig. 1d; 2d) with about 100 short setulae not organized in groups but decreasing in size posteriorly. A row of very small setulae along the posterior margin on inner side of valve. Valves oblique. Cuticle of valves and head shield significantly thinner than in majority of Aloninae.

Head of moderate size, triangle-round in lateral view, rostrum short, pointing downward. Compound eye two times larger than ocellus. Distance from tip of rostrum to ocellus in adults slightly greater than that between ocellus and eye. Head shield with maximum width behind mandibular articulation, without any sculpture; rostrum short, broadly rounded; posterior margin of head shield broadly rounded, without notches. Three major head pores (Fig. 1e; 2e) with narrow connection between them, middle pore smaller than two others, PP about 0.6–0.8 IP. Lateral head pores minute, located at about 1.5 IP distance from midline, at the level between anterior and middle major head pore.

Labrum (Fig. 1f1g) large, labral keel very wide, with height equal to width, with broadly rounded apex; anterior margin of keel convex, posterior margin without any setulae.

Postabdomen (Fig. 1h–1i; 2f) narrow, with parallel margins, length about 2.8–3.0 times height. Ventral margin straight or weakly convex. Basis of claws separated from distal margin by a clear incision. Distal margin straight, distal angle rounded, prominent. Dorsal margin with distal part about 2 times longer than preanal one, with postanal portion somewhat longer than anal. Postanal portion of distal margin straight, anal portion weakly concave. Preanal angle well-defined, postanal angle weakly defined. Distal potion of postanal margin (Fig. 2g) with 3–4 long composite marginal denticles, followed by 5–6 groups of 3–4 much shorter elementary denticles, anal margin with 3–5 groups of marginal setulae. Length of distal denticles about 1.5 widths of claw base. 8–9 Lateral fascicles of setulae, postanal fascicles wide to very wide, closely spaced, consisting of ten or more setulae, with distalmost setula only slightly longer and thicker than others, as long as longest marginal denticles. Postabdominal claw (Fig. 2h) weakly curved, slightly longer than preanal portion of postabdomen. Basal spine very short, its length less than width of claw base, about 0.1 length of claw.

Antennula (Fig. 1j) of moderate size, length about 2.5 widths. Antennular sensory seta slender, about 1/2 length of antennula, arising at 2/3 distance from the base. Nine terminal aesthetascs, two longest about 1/2 length of antennula, other seven of about 1/3 length of antennule.

Antenna II relatively short (Fig. 1k; 2i). Antennal formula, setae 0–0–3/1–1–3, spines 1–0–1/0–0–1. Basipodite robust, branches of moderate length and width, endopodite longer than exopodite. Basal segments of both branches 1.5 times longer than distal segments. Middle segments of endopodite with clusters of long setulae. Seta arising from basal segment of endopodite only slightly shorter than endopodite. Seta arising from middle segment of endopodite of similar size of shortest apical setae. On both branches, one apical seta much shorter than two others. Spine on basal segment of exopodite about 2/3 length of middle segment. Apical spine of exopodite as long as distal segment, apical spine of exopodite shorter than distal segment.

Thoracic limbs: five pairs.

Limb I (Fig. 3a3b) of moderate size. Epipodite ovoid. Accessory seta about 1/3 length of ODL seta. ODL with a long seta, armed with minute setulae in distal part (not shown on the drawing). IDL with three setae; seta 3 as long as ODL seta, seta 2 of about 3/4 length of seta 3, setae 2 and 3 armed with thin setulae in distal part; seta 1 very slender, of about 1/3 length of seta 3. Endite 3 with four setae, inner seta (1) much shorter than outer setae (a–c). Endite 2 with three setae (d–f), seta e as long as ODL seta, seta f slightly shorter than seta f. Setae a, b and d armed with very long setulae in distal part. Endite 1 with two 2-segmented setae (g–h), both setulated in distal part. Inner setae on endites 1–2 and seta g absent. Six-seven rows of thin long setulae on ventral face of limb. Two long ejector hooks of similar size, of same length as setae of endite 3.

Limb II (Fig. 3c). Exopodite elongated, without seta. Eight scraping setae (1–8), armed with thin spinules, increasing in length distally. Distal armature of gnathobase with four elements. Filter plate with seven setae, the posteriormost seta three times shorter than others.

Limb III (Fig. 3d3e). Epipodite oval; exopodite subrectangular, with seven setae. Seta 3 being longest, seta 6 and 4 about 2/3 length of seta 3, seta 1 of about 1/3 length of seta 3, other setae short. Seta 6 armed with thick long setulae in distal part, seta 7 armed with very short setulae in distal part, all other setae plumose. Distal endite with three setae, two distalmost members long and slender, sharp, with distal parts unilaterally armed with sharp denticles; basalmost seta shorter, bilaterally armed with setulae. Basal endite with four very short setae (4–7). Four short inner setae increasing in size basally. Gnathobase not clearly separated from basal endite. Distal armature of gnathobase with four elements: a large elongated conical sensillum, a thin, bent seta, and two sharp spines. Filter plate III with seven setae.

Limb IV (Fig. 3f3h). Preepipodite setulated, epipodite with short process. Exopodite subrectangular, with six plumose setae. Seta 1 longest, setae 2, 3 and 5 slightly shorter than seta 3, setae 4 and of about 1/3 length of seta 3. Inner-distal portion of limb IV with four setae and cylindrical sensillum: seta 1 slender, sharp; three flaming–torch setae (2–4) narrow, more than 2 times shorter than seta 1, each with reduced distal part, armed with 5–6 long thin setulae, decreasing in size basally. Small sensillum located between bases of setae 3–4. Three inner setae (a–c) long, increasing in size basally. Gnathobase with moderately long 2-segmented seta, only a little longer than seta 1, sensillum and small hillock distally. Filter plate with five setae.

Limb V (Fig. 3i3j). Preepipodite setulated. Epipodite oval, with very short process. Exopodite oval, with four plumose setae, decreasing in size basally; seta 1 1.5 times longer than exopodite, seta 4 four times shorter than seta 1. Inner limb portion as large rounded lobe with setulated inner margin, only slightly smaller than exopodite. At inner face, two setae, outer one equal in length to seta 3 of exopodite, inner one 1.5 times shorter. No filter plate.

Ephippial females were not present in the studied material.

Male. Body of adult male (Fig. 1l) low subrectangular, with almost straight dorsal and ventral margins, posterior margin of valves strongly convex. Height/ length ratio about 0.5. Eye of same size as in female, ocellus larger than in female. Rostrum in lateral view broader than in female.

Postabdomen (Fig. 1m) moderately long, with almost parallel margins in postanal portion, length about 2.5 maximum heights. Gonopores located at the end of the postabdomen, above the base of the claw. Dorso-distal margin weakly convex, dorso-distal angle broadly rounded. Preanal angle well-defined, postanal angle not defined. Distal part of postabdomen almost 2 times longer than preanal, anal and postanal portions of similar length. Clusters of short setulae in place of marginal denticles, postanal portion with 6–7 clusters of 3–7 setulae each. Lateral fascicles of setulae same as in female. Postabdominal claw 1.5 times shorter than in female, slightly shorter than preanal portion of postabdomen, basal spine very short.

Antennule (Fig. 1n) broad, length about two widths. Ten short terminal and two lateral aesthetascs, longest terminal aesthetascs are of about half length of antennule, lateral aesthetascs about 1/3 length of antennule. Male seta arising at 1/3 length from tip, not reaching to the end of antennule.

Limb I (Fig. 3l3k) with U-shaped copulatory hook, its distal portion 1.5 times longer than basal one. IDL seta 1 absent, setae 2 and 3 thin, of similar length, 3 times shorter than in female, male seta curved, as long as seta 3. Copulatory brush seta long, slightly shorter than IDL setае. A row of about 30 short thick setulae (cbs) on ventral face of limb below copulatory brush. Endite 3 with inner seta (1) much longer than in female, as long as setae a–c, armed with thin setulae in distal portion.

Size. In adult parthenogenetic female length 0.44–0.49 mm, height 0.26–0.34 mm, in instar II juvenile female length 0.38–0.40 mm, height 0.21–0.23 mm, no instar I juvenile females were found. In eight studied adult males, length 0.35–0.39 mm, height 0.16–0.20 mm.

Differential diagnosis. O. karelica clearly differs from most species of Ovalona in a very short basal spine of postabdominal claw, this character is shared only with O. bromelicola (see Sinev, 2002a, 2015). O. karelica differs from O. bromelicola in lower body, well-developed eye and ocellus, in straight, not curved postabdomen, in antennule with normally developed aesthetascs, and in small and narrow flaming-torch setae (2–4) of limb IV.

Distribution. Known from Germany, Slovakia, North-West Russia, Finland and Norway (Bledzki, Rybak, 2016). According to Ibrasheva & Smirnova (1983), O. karelica is found in Balkhash Lake in Kazakhstan, but this record should be rechecked.

Graptoleberis smirnovi Sinev et Gavrilko sp. n.

Gavrilko et al., 2020: 153, Fig. 3 (pannonica).

Zoobank registration number. urn:lsid:zoobank.org:act:F31BB7A2-5731-4638-A1FE-32458DF3629F.

Type locality. Gnilichka River, Nizhniy Novgorod, Russia (56.205576° N, 43.756625° E, samples collected 02.08.2017, 19.09.2018, 13.09.2019, 26.09.2019).

Holotype. A parthenogenetic female from the type locality, deposited at the collection of Zoological Museum of M.V. Lomonosov Moscow State University, accession number Ml-191

Allotype. An adult male from the type locality, deposited at the collection of Zoological Museum of M.V. Lomonosov Moscow State University, accession number Ml-192.

Paratypes. 25 parthenogenetic females, 2 males from the type locality, deposited at the collection of Zoological Museum of M.V. Lomonosov Moscow State University, accession number Ml-193.

Description. Parthenogenetic female. In lateral view body (Fig. 4a4b; 5a) of shape characteristic of the genus, very low, maximum height before the middle of the body, in adults height/length ratio about 0.4. Dorsal margin of valves uniformly curved; postero–dorsal angle broadly rounded; posterior margin weakly curved to almost straight, ventral margin straight. In dorsal view (Fig. 4c4d; 5b–5c), body rather broad, characteristic for the genus shape, dorsal margin of valves with clearly defined ridge, but without keel. In ventral view (Fig. 5d5f), aperture between the valves is very large; the valves form broad concave rims around it (Fig. 6a). Ventral margin with about 70 setae, first 50 setae spaced very densely (Fig. 4e; 6b), they are moderately long, their length less than width of ventral rim of valves, and armed with very long setulae, clusters of thick setulae near their bases. Next 20 setae (Fig. 4 f) shorter, sparsely spaced, evenly decreasing in length posteriorly, armed with short setulae. Posteriormost portion of ventral masrgin without setae and setulae. Postero–ventral angle (Fig. 4 f4h; 7a) with 3–5 large triangular denticles, increasing in size dorsally, without any setulae between them. A row of very small setulae along the posterior margin on inner side of valve. Sculpture of valves in shape of very prominent longitudinal lines, with less developed connections between them, forming elongated polygons.

Head large, in lateral view narrow subtriangular, with no defined rostrum and convex ventral margin. Compound eye two times larger than ocellus. Head shield with a broad, rounded anterior portion, without defined rostrum, maximum width at the middle of anterior portion. Posterior portion of head shield triangular, with obtuse posterior angle. Sculpture of head shield polygonal, similar to these on valves. Elongated frontal head pore located on ventral side of head shield between bases of antennules (Fig. 5g–5h). Three major head pores of same size (Fig. 4i; 5i), with a narrow connection between them, PP about 0.5 IP. Lateral head pores large, only slightly smaller than major head pores, located very close to middle major head pore.

Labrum (Fig. 4j; 7b) of moderate size, labral keel moderately wide, with a long narrow process at the apex, armed with numerous clusters of short thick setulae – such morphology of labrum is unique for family Chydoridae. Anterior margin of keel convex, posterior margin almost straight.

Postabdomen (Fig. 4k–4l; 7c) narrow, weakly narrowing distally in postanal portion, length about 3–3.5 height. Ventral margin strongly convex. Basis of claws not separated from distal margin by incision. Dorsal margin coming to the base of the claws, distal angle not developed. Dorsal margin with distal part about 2 times longer than preanal one, with postanal portion 1.5 times longer than anal. Anal and postanal portions of distal margin straight or slightly concave. Preanal angle weakly defined, postanal angle not defined. Postanal margin with 6–7 groups of 8–15 very short spinules, anal margin with several groups of similar setulae. 7–8 Wide lateral clusters of short setulae of equal thickness and similar length in each. Cluster at postanal margin consists of longest setulae, width of postanal fascicles, length and number of setulae in each decrease distally. Postabdominal claw (Fig. 4m; 6c) very short, curved, 2–2.5 times shorter than preanal portion of postabdomen. Basal spine very short and thin. Inner side of claw with a row of 3–5 strong denticles along convex margin and 2 clusters of setulae in central portion.

Antennula (Fig. 4n; 7d) of moderate size, length about 2 widths. Antennular sensory seta slender, almost as long as antennula, arising terminally. Nine terminal aesthetascs, two longest about 1.5 times longer than antennula, others of about 0.66–1.0 length of antennule.

Antenna II relatively short (Fig. 8a8b). Antennal formula, setae 0–0–3/0–1–3, spines 1–0–1/0–0–1. Basipodite robust, branches of moderate length and width, endopodite shorter than exopodite. Exopodite with length of segments increasing distally, basal segment 1.5 times shorter than distal segment. Еndopodite with basal segmenst being longest, middle segment two times shorter than basal segment, distal segment 1.5 times shorter than basal segment. Exopodite setae of similar size and thickness. Seta arising from middle segment of endopodite short, geniculated at the point of articulation, only slightly longer than apical segment. Two of apical setae of endopodite longer and much thicker than exopodite setae, third seta short, as long as exopodite itself. Spine on basal segment of exopodite very short. Apical spines two times shorter than respective apical segments.

Thoracic limbs: five pairs (Fig. 7e7f ).

Limb I (Fig. 8c8e) massive, much larger than other limbs. Epipodite ovoid with long massive process, 3 times longer than exopodite itself. Accessory seta about 1/3 length of ODL seta. ODL with a long seta. IDL with three setae; seta 2 and 3 of about 1/2 and 2/3 length of ODL seta, respectively, armed with densely spaced thin setulae in distal part; seta 1 slender, of about 1/4 length of ODL seta. Endite 3 with four setae, setae a–b long, as long as IDL seta 2, inner seta (1) and seta c 1.5 times shorter. Setae a–b bilaterally armed with short thick setulae in distal portion, seta с armed with long thin setulae in distal portion. Endite 2 with thin inner seta (2) and three short outer setae (d–f) of similar length, seta d armed as seta c, setae e–f unilaterally armed with thick spinules. Endite 1 with inner seta (3) two times shorter than inner seta 2, and two short 2-segmented setae (g–h), both setulated in distal part. Seta i absent. Two short ejector hooks, one1.5 times longer than other. Anterior face of limb with numerous very thin setulae, and with short setulated process at basal end, armed with setulae, such structure is not present in other genera of Aloninae.

Limb II (Fig. 8f8g). Exopodite elongated, without seta. Eight scraping setae (1–8). Seta 1 shorter than seta 2, both of them armed with small spinules. Seta 3 much thicker than setae 1–2, armed with thick spinules. Setae 4–5 of peculiar shape, thick, with shortened blunt distal portion, armed with denticles of moderate size, much shorter than setae 3 and 6. Setae 6–8 thin, armed with thin spinules, seta 8 two ties shorter than setae 6–7. Distal armature of gnathobase with four elements. Filter plate with seven setae, the posteriormost seta four times shorter than others.

Limb III (Fig. 8h8k). Epipodite oval; exopodite of irregular shape, with seven setae, lateral setae (1–2) located the exopodite base, terminal setae (3–5) located extremely close to each other. Seta 3 being longest, seta 6 slightly shorter than seta 3, seta 4 and 6 of about 1/3 length of seta 3, other setae very short. Setae 3–4 with very broad basal portion, seta 5 very small and thin. Setae 1–2 plumose, seta 3 with basal portion setulated unilaterally, distal portion with numerous thin long setulae, seta 4 with numerous thin long setulae, seta 5 naked, seta 6 bilaterally armed with short thick setulae in distal part, seta 7 bilaterally armed with very short setulae in distal part. Distal endite with three setae, distalmost seta (1) s long and slender, sharp, with distal part unilaterally armed with sharp denticles; seta 2 four times shorter, without any denticles, basalmost seta (3) strongly curved, shorter than seta 1, bilaterally armed with thin setulae. Basal endite with four moderately long setae (4–7), large curved sensillum located near their bases. Only three inner setae (a–d) of similar size, Gnathobase not clearly separated from basal endite. Distal armature of gnathobase with three elements: short curved seta, and two short spines. Filter plate III with seven setae.

Limb IV (Fig. 8l8n). Preepipodite setulated, epipodite without process. Exopodite subrectangular, with six short plumose setae, length of longest seta (5) about length of exopodite. Seta 3 slightly shorter than seta 1, other setae of similar length, about 1/2 length of seta 5. Inner-distal portion of limb IV with four setae and large conical sensillum: seta 1 slender, sharp, armed with spinules; three flaming-torch setae (2–4) narrow, of similar size, more than 2 times shorter than seta 1, each with reduced distal part, armed with 4–6 short setulae. Three inner setae (a–c) short, increasing in size basally. Gnathobase with very long 2-segmented seta, 1.5 times longer than seta 1, sensillum and small hillock distally. Filter plate not found.

Limb V (Fig. 8o). Preepipodite setulated. Epipodite oval, with long curved process 2 times longer than exopodite itself. Exopodite strongly bilobed oval, with four plumose setae, setae 1–3 short, decreasing in size, seta 4 1.5 times longer than seta 1. Inner limb portion small e rounded lobe with setulated inner margin, located at significant distance from exopodite. At inner face, two short setae of similar size. No filter plate was found.

Ephippial females were not present in the studied material.

Male. Body of adult male (Fig. 4o) very low subrectangular, with maximum height at posterior margin of head shield, with straight to weakly concave dorsal margins; posterior margin of valves convex. Height/ length ratio about 0.35. Compound eye and ocellus larger than in female. Labrum as in female (Fig. 4p)

Postabdomen (Fig. 4q) moderately long, evenly narrowing distally, length about 3.5 maximum heights. Ventral margin straight, ventro-distal angle well-defined, almost right-angled. Gonopores located at the end of postabdomen, above the base of claw. No defined dorso-distal margin and dorso-distal angle, postanal margin coming to the base of claw. Dorsal margin weakly convex in preanal portion, weakly concave in anal portion, strongly concave in postanal portion. Preanal and postanal angles not defined. Distal part of postabdomen1.5 times longer than preanal, anal and postanal portions of similar length. Postanal margin with 5–6 clusters of small spinules, similar to those of female, with 4–8 spinules in each. Lateral clusters of setulae similar to those of female, additional small clusters located in distal portion of postabdomen. Postabdominal claw extremely short, 2 times shorter than in female, its length only 1.5 times greater than width of claw base, basal spine not found. Inner side of claw with a row of 2–4 strong denticles along convex margin.

Antennule (Fig. 4r) broad, length about two widths. Only ten terminal aesthetascs longer than antennules, two longest terminal aesthetascs of about 2 lengths of antennule. Male seta not found.

Limb I (Fig. 8p8q) with very short U-shaped copulatory hook, its distal portion only slightly longer than basal one. IDL seta 1 not found, setae 2 and 3 each two times shorter than in feamel, male seta thin straight, shorter than seta 2; no cluster of numerous dense setulae present in female. Copulatory brush seta of moderate size, as long as male setа. Anterior face of limb below copulatory brush without any setulae. Endite 3 with inner seta (1) almost as long as IDL seta 2, armed with thin setulae in distal portion.

Size. In adult parthenogenetic female length 0.50–0.65 mm, height 0.21–0.32 mm, in instar II juvenile female length 0.45–0.48 mm, height 0.18–0.19 mm, no instar I juvenile females were found. In three studied adult males, length 0.41–0.43 mm, height 0.15–0.16 mm.

Differential diagnosis. Graptoleberis smirnovi sp. n. differs from all other known species of the genus in unique morphology of labrum, with long narrow spined process at the apex (see Alonso, 1996; Hudec, 2010; Van Damme, Dumont, 2010), and never reported for any other genera of Aloninae. It also differs from G. testudinaria and G. occidentalis Sars1901 in low elongated body without developed dorsal keel, and in longer, only weakly narrowing distally postabdomen of the female, armed with much smaller marginal spinules. In general morphology, G. smirnovi is similar to G. pannonica, but differs from it in morphology of the antenna. According to Hudec (2010), G. pannonica has a longer spine on the basal segment of the exopodite, only two times shorter than the middle segment, and longer seta on the middle segment of the endopodite, 2.5 times longer than the apical segment.

Distribution. To date known only from Nizhniy Novgorod Area of Russia.

DISCUSSION

Our data clarify the position of Ovalona karelica within the genus. According to the morphology of the postabdomen, it belongs to the cambouei-group of the genus (Sinev, 2015). It has narrow flaming-torch setae (2–4) on the inner portion of limb IV, an apomorphy shared by the terminal clade of the group – Paleotropical O. cambouei (Guerne et Richard 1983), Australian O. pulchella (King 1853) and O. archeri (Sars 1888), Neotropical O. glabra (Sars 1901) and Mexican O. aguascalientensis (Sinev et Silva-Briano 2012). These setae in O. karelica are elongated and bear long setulae, like those of O. archeri; in all other species of the clade these setae are very short and have shortened setulae. The gap between areas of distribution of O. karelica and O. cambouei, which is present in Europe in Spain and Italy only, is quite wide, and suggests ancient separation between these two species, which can be evaluated only by genetic methods.

The general morphology of G. smirnovi sp. n., including that of the ventral margin of the valves, is similar to that in other species of the genus. Comparison of thoracic limb morphology of G. smirnovi sp. n. with that of G. testudinaria (Fryer, 1968; Alonso 1996; Hudec, 2010) revealed only a few significant differences between the species. In G. testudinaria, scraping seta 3 of limb II is of similar morphology with setae 1–2. We did not find filter plate V , present in G. testudinaria, in G. smirnovi sp. n. Thoracic limbs of the other recognized species of the genus, G. pannonica and G. orientalis, are not studied. Obviously, habits of G. smirnovi are similar to that of G. testudinaria (see Fryer, 1968).

Both Ovalona karelica and Graptoleberis smirnovi, as well as G. pannonica, are among the most rare European cladocerans. The rarity in freshwater cladocerans and copepods could be explained by different reasons: highly specialized niches, low competitive abilities, or limited colonization ability (Hessen, Walseng, 2008). Both studied species appear to fit the first two criteria. In the studied area they were found only in a specific habitat (dense stands of S. aloides), and their density was much lower than that of co-occuring potential competitors – Alona affinis, Flavalona costata, Coronatella rectangula for Ovalona karelica and Graptoleberis testudinaria for G. smirnovi sp. n. Males of both O. karelica and G. smirnovi sp. n. were already present in studied water bodies in August, and only a few living specimens were found during sampling in September. In contrast, most co-existing species of Chydoridae had no gamogenetic specimen in August, and were abundant in samples at even at the end of September.

Smirnov (1999) and Smirnov, Kotov (2018) suggested that extremely specialized cladocerans are “victims of morphological radiation”, occupying narrow ecological niches, usually living in restricted biotopes and never demonstrating high density in these water bodies. The genus Camptocercus is a prime example of such a group. But even within this genus, rarity of species varies greatly. C. rectirostris is rather common in West Palearctic (Smirnov, 1971, 1999), while its congener C. fennicus is very rare (Sinev, 2014). In long-studied Lake Glubokoe, the former species is rather abundant and found every year (observation of the first author), while C. fennicus was found only once during the last 20 years (Sinev, 2014). But morphologically, C. fennicus is very close to C. uncinatus, a rather common species in the East Palearctic (Sinev, 2014). Two more species of the genus, North Palearctic C. lilljeborgi and Beringian C. streletskayae are also extremely rare, while North American C. rotundus is rather common (Sinev, 2014, 2018).

Graptoleberis smirnovi sp. n. at first glance appears to be an extremely morphologically specialized species, fitting all “victim of morphological radiation” criteria of Smirnov, Kotov (2018). But comparison of morphology of this species with that of its rather successful congeners, G. testudinaria and G. occidentalis, reveals only a few significant differences in outer morphology, and none in limb morphology. The genus Graptoleberis, while being among the most morphologically specialized Aloninae, appears to be an exception to the criteria of Smirnov and Kotov (2018). Graptoleberis is rather successful, is distributed worldwide, and occurs in the littoral among macrophytes, one of most common habitats of benthic Cladocera. But “victim of morphological radiation” criteria can be fully applied to its closest relative, the extremely specialized monotypic genus Kisakiellus Sousa et Elmoor-Loureiro, 2018 which inhabits small streams in Brazil (Sousa, Elomoor-Loureiro, 2018). In our opinion, the Smirnov and Kotov (2018) approach can explain general rarity of such extremely specialized genera, but not rarity of its species, which is subject to broad variations.

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