Bosmina (Eubosmina),

Kotov, Alexey A., Ishida, Seiji & Taylor, Derek J., 2009, Revision of the genus Bosmina Baird, 1845 (Cladocera: Bosminidae), based on evidence from male morphological characters and molecular phylogenies, Zoological Journal of the Linnean Society 156 (1), pp. 1-51 : 29-34

SUBGENUS BOSMINA (EUBOSMINA) SELIGO, 1900

Bosmina Eubosmina Seligo, 1900: 67 ; Lieder, 1962: 317; Lieder, 1983a: 202–203; Lieder, 1983b: 128–134; De Melo & Hebert, 1994: 1812 (part, except of oriens ). Eubosmina (Eubosmina) in Taylor et al., 2002: 1494.

Type species: Bosmina coregoni Baird, 1857 . When Seligo (1900) described his new taxon, as well as in his subsequent paper ( Seligo, 1928), he discussed many species of Bosmina (Eubosmina) , without selecting a type species. Lieder (1962) said that the subgenus includes ‘ B. coregoni s. lat. ’: this sentence can probably be regarded as a typification of this genus-group name by a subsequent author (case 69 of ICZN, 2000).

Subgenus diagnosis based on male characters: Postabdomen conically tapering distally, not inflated, preanal margin in general straight, with very short setules. Gonopore opens distally. Postabdominal claw long, without a terminal spinule. Basal pecten of denticles not shifted from postabdominal claw to body of postabdomen, consisting of large, robust teeth, distal pecten consisting of long, fine setules. Antenna I with widened pre-aesthetasc portion. On subdistal lobe of limb I, a seta located at a distance from two others. Seta 2 on limb I very short.

Comments: This is the subgenus with the most confusion in the Bosminidae . About 100 (!) described nominal taxa of the genus Bosmina can be attributed to this subgenus. Previous proposals on introgressive hybridization ( Lieder, 1956, 1983a, 1996) have lacked evidence, but ecologically plastic characters certainly contribute to the species problem. Now the subgenus needs to be revised.

Palaearctic Bosmina (Eubosmina) cf. coregoni Baird, 1857 ,

Figs 17–19

Bosmina coregoni Baird, 1857: 21 , 24.

Previous descriptions with information on males: Norman & Brady, 1867: 7–8; figs 1, 2 ( B. longispina ); P. E. Müller, 1870: 150–151; pl. 2, figs 3–8; pl. 3, fig. 11 ( Bosmina diaphana P.E. Müller, 1867 ); Stenroos, 1895: 25–26; figs 11–15 ( Bosmina brevispina Lilljeborg, 1890 in Sars, 1890); Lilljeborg, 1901: 237– 256; pl. 32, figures 4–13; pl. 33, figs 1–12; pl. 34, figs 1–12; pl. 35, figs 1–9; pl. 36, figs 1–12; pl. 37, figs 1–7 ( Bosmina obtusirostris Sars, 1861 ); 256–259; pl. 37, figs 8–9; pl. 38, figs 1–2 ( Bosmina longicornis Schoedler, 1865 ); 259–269; pl. 38, figures 3–17; pl. 39, figs 1–8; pl. 40, figures 1–10 ( B. longispina ); 269–274; pl. 40, fig. 11; pl. 41, figs 1–7 ( Bosmina insignis Lilljeborg, 1901 ); 275–284; pl. 41, figs 8, 9; pl. 42, figs 1– 9; pl. 43, figs 1–9; pl. 44, figs 1, 2 ( Bosmina mixta Lilljeborg, 1901 ); 284–298; pl. 44, figs 2–8; pl. 45, figs 1–11; pl. 46, figs 1–6; pl. 47, figs 1–8; pl. 48, figs 1–6 [ B. coregoni ]; 298–304; pl. 48, figs 7, 8; pl. 49, figs 1–12; pl. 50, figs 1, 2 ( Bosmina crassicornis Lilljeborg, 1887 ); 304–308; pl. 50, figs 3–12; pl. 51, figs 1– 5 [ Bosmina globosa Lilljeborg, 1901 ]; Keilhack, 1904: 564; text – fig. ( Bosmina coregoni gibbera Schoedler, 1863 ); Keilhack, 1908: 448; figs 12, 13 ( B. coregoni gibbera ); Zykoff, 1906: 479; figs 1, 2 ( B. insignis ); Keilhack, 1909: fig. 118 ( coregoni –lilljeborgii); Apstein, 1910: 11–12; figs 20–21 ( Bosmina maritima P. E. Müller, 1867 ); Burckhardt, 1941: 130–141; figs 3, 4, 12–15, 13′, 15′, 18, 21–23, 29 ( B. coregoni ); Purasjoki, 1958: 23–26; fig. 4 ( Bosmina coregoni maritima P. E. Müller, 1867 ); Šrámek-Hušek et al., 1962: 280–284; fig. 102 ( coregoni morph coregoni , coregoni m. longispina , coregoni m. poppei, coregoni m. longicornis ); Semenova, 1970: 50–51; figs a, b, v ( B. coregoni ); Flössner, 1972: 218–224; figs 102–104 [ B. (E.) longispina ]; 225–232; figs 106–108 [ B. (E.) coregoni ]; Sergeev, 1981 (coregoni maritima); Lieder 1983a: 209–211; figs 28–30 [ B. (E.) longispina longispina ]; 213–214; fig. 64 [ B. (E.) mixta kessleri Uljanin, 1874 ]; 215–216; fig. 88, 94; pl. 3, fig. 2 [ B. (E.) mixta cederstroemi Schoedler, 1865 ]; 223–224; pl. IV, fig. 1 [ B. (E.) coregoni thersites ]; Negrea, 1983: 227–229; fig 92 [ B. (E.) longispina ]; Margaritora, 1985: 61–64; fig. 27 ( E. coregoni ); 64–66, fig. 28 ( E. longispina ); Sars, 1993: 82–83; pl. 62–63 ( B. obtusirostris ); Hudec, 1995: 293– 295; pl. 1 [ B. (E.) longicornis kessleri ]; Kotov, 1996: 188–194; figs 1–5 [ B. (E.) longispina ]; Lord et al., 2006: pl. 1 [ B. (E.) coregoni gibbera ].

Material

‘ Bosmina coregoni sp. str.’: Russia (European). Lake Khotavets, Darwin National Reserve, Vologda Area , collected on 3 October 1994 by V. I. Lazareva, AAK 2004–005 ; a small un-named lake near Petrokrepost train station, Leningrad Area, collected on 16 September 2004 by A. A. Kotov, AAK M-034 .

‘ Bosmina coregoni kessleri’: Russia (European). Lake Glubokoe, Ruza District , Moscow Area, collected in September–December of 1994–1998 by A. A. Kotov, AAK 2004-040 - 043 .

‘ Bosmina longispina’ (including ‘obtusirostris’ and ‘lacustris’ morphs): Norway. MjIIIsa, east side, collected on 8 August 1965 by D. G. Frey, DGF 1632; Gelggojervi, Troms, collected on 27 August 2004 by D. J. Taylor & S. Ishida, AAK M-456 .

Iceland. A small lake near Asbyrgi, Northern Iceland, collected on 19 August 1977 by N. N. Smirnov (see Kotov, 1996) .

Ireland. Lough Leane, collected on 7 October 1985 by D. G. Frey, DGF 7628.

Finland. Kilpisjärvi , Lapin Lääni, collected on 27 August 2004 by D. J. Taylor & S. Ishida, AAK M-457 .

Russia (European). Vodoprovodnoe Lake, Verkhnee Yershovskoe Lake, and a small un-named lake, territory of the Belomorskaya Biological Station of Moscow State University , Murmansk Area , collected in August 1995 by A. Yu. Sinev, AAK 2003-006 , AAK 2004-018 - 020 ; Un-named lake 2, Rybachiy Peninsula, Murmansk Area , collected in August 2003 by Y. Galimov, AAK M-394 ; Lake Kumitchevo, Pinega Region, Arkhangelsk Area , collected on 15 August 2004 by N. Bayanov, NMK 2491 ; several bog lakes near Petrozavodsk, Karelian Autonomous Republic , collected from July 1970 to July 1971 by Z. I. Fillimonova, AAK 2004-026 , NNS 1997-159-160; Ladoga Lake immediately at the source of the Neva River, Leningrad Area , collected on 16 September 2004 by A. A. Kotov, AAK M-031 ; Rybinsk man-made lake at Mologa station, Yaroslavl Area , collected on 18 October 1994, AAK 2004-021 ; Lake Dubrovskoje, Darvin Reserve, Vologda Area , collected in September 1994 by V. I. Lazareva, AAK 2004-023 .

Russia (Asian). Several lakes in tundra, Tareya , Taimyr Autonomous Area , collected in July–August 1969 by Yu. I. Chernov, AAK 1999-051 , AAK 2004- 003 , AAK 2004-004 ; a small lake in tundra, Talnakh, Taimyr Autonomous Area , collected on 11 August 1974, AAK 2004-016 ; Teletskoye Lake near Iogatch, Altai Territory , collected on 1 September 2002 by O. S. Burmistrova, NMK 2516 ; Lake Leprindo, Chita Area , collected on 27 August 1998 by N. G. Sheveleva, AAK 2004-016 .

‘ Bosmina crassicornis’: Russia (Asian). Rybinsk Water Reservoir, Yaroslavl Area , collected on 25 September 2007 by V . I. Lazareva, NMK 2685 ; Bratsk Water Reservoir, Irkutsk Area , collected on 10 November 1998 by N. G. Sheveleva, AAK 2004-017 .

Diagnosis of adult male ( Figs 17A–D , 18G–M , 19 ): In all studied morphotypes, the male characters are more ‘generalized’ compared with female characters, i.e. (1) body less deep, lacking a hump; (2) if antenna I is very long in the female ( B. coregoni gibbera ), it is comparatively shorter in the male; by contrast, if the female antenna I is short ( B. crassicornis ), it is comparatively longer in the male; (3) if mucro is very long in the female ( B. longispina ), it is comparatively shorter in the male; by contrast, if mucro is short ( B. coregoni kessleri ) in the female, it is longer in males. In B. crassicornis the female has no mucro, but there is a small mucro in its male. As a result, males of all morphotypes are remarkably more similar in general appearance than are the females.

Dorsum from regularly arched from anteriormost point to posterodorsal angle ( B. crassicornis ) to concave ( B. longispina and B. kessleri ), posterior margin of valves high. Head with distinct anteroventral angle, anterior portion of rostrum straight or slightly concave, ocular dome absent or ill-defined. In anterior view, rostrum truncated. Lateral head pore at a great distance from lateral edge of head shield. Mucro of different length, seta kurzi short, a series of long setae at anteroventral portion of valve. Postabdomen elongated, with its ventral margin in general straight or slightly convex, preanal margin relatively short, with a slight depression, dorsodistal angle welldefined, anal margin aslant truncated. Postanal angle well-defined, postanal portion of postabdomen slightly narrowing towards distal end, blunt distally, where a single gonopore opens. There are several groups of relatively robust denticles on the postanal and middle portion of the postabdomen. Postabdominal claw long, bent, regularly narrowing distally, distal pecten as a row of numerous, long, fine setules, proximal pecten with several (normally between six and ten) relatively large teeth. Antenna I regularly bent in lateral view; in anterior view, its basal portion thick, with straight or slightly concave, serrated inner margin, wereas distal half thin, regularly bent and narrowing distally. Sensory seta long and male seta long: located on a marked pedestal. Antenna II with two short sensory setae on coxal part. Distal sensory seta short, not reaching distal end of basal segment of endopod. Limb I bears idl with an inflated basal portion, without a hillock basally, and with a conical distal portion terminating as a long, naked seta. Copulatory hook large and thin, not recurved to a parallel position with the idl, tip of hook with two ridges. Subdistal lobe large, with a long seta 1, a rudimentary setae near it, and another rudimentary seta at a distance from the two aforementioned setae; seta 2 very short.

Postembryonic development: Juvenile male I ( Fig. 18A–C ) body shape similar to juvenile female I, and with posterior dorsal head pore present. Postabdomen with slightly convex preanal margin and slightly inflated ventral portion, a rudimentary gonoduct terminating far from the level of the anus, although the gonopore is absent. Postabdominal claw long, with distal and proximal pectens on female type, pre-claw pecten present. Antenna I fused with rostrum, only a pair of long sensory setae on rostrum. Antenna II with two short sensory setae on coxal portion, whereas there is no rudiment of anterior sensory seta. Limb I with idl small, subovoid, with a single rudimentary seta, copulatory hook short and thick, subdistal lobe not projected, with a single seta 1 (as in female).

Juvenile male II ( Figs 17E, F , 18D–F ) body shape as in juvenile female II. Postabdomen with straight to slightly concave preanal margin, ventral side inflated, rudimentary gonoduct reaches the level of the anus. Postabdominal claw long, distal pecten with fine setules, proximal pecten with a few slender spinules, pre-claw pecten with a few spinules. Antenna I fused with rostrum, which has a long sensory seta and a short male seta at the same level. Antenna II with two short sensory setae on coxal portion, and with a rudiment of a distal anterior seta. Limb I with idl large (but smaller than in adult), its distal portion conical, with a short seta and a second rudimentary seta; copulatory hook robust, with blunt tip bearing small denticles, subdistal lobe small, with two setae (1 and 1′) of somewhat different lengths, and a small rudiment of the third seta.

Comments. The species status of several of the studied populations is controversial. No specific primary and secondary sexual traits were found in males of the aforementioned ‘species’. It is clear that several forms are very closely related, and the paleolimnology and genetic distances suggest postglacial origins ( Haney & Taylor, 2003). Detailed genetic analysis of coexisting morphs and perhaps breeding studies are needed to further assess the species status of this relatively young group.

De Melo & Hebert (1994) proposed that B. maritima from North America is a valid species that is genetically distant from other Eubosmina . The presence of this species in North America seems to be a consequence of its introduction from Europe ( Haney & Taylor, 2003). It is unknown if the North American B. maritima re-evolved from invading B. (E.) cf. coregoni in North America, or if it represents an independent introduction of a Eurasian morphotype. Presently there are no morphological characters to distinguish saline populations ( B. maritima ) from B. longispina .

Nearctic ‘ Bosmina cf. longispina’

Figure 20

Material: A pond in Nome , Alaska, USA, collected on 26 September 2003 by D. J. Taylor, AAK 2004-052 .

Differences of adult male: Male of Nearctic ‘ B. longispina ’ differ from European eubosminids in having: (1) a larger distance between base of antenna I and anteroventral angle of head; (2) very large compound eye; (3) an especially thin distal portion of idl; (4) a depression on the tip of the copulatory hook.

Comments: Our note on the difference of Beringian Nearctic males from the Palaearctic males is based on only a single studied Nearctic population. But, there is a chance that we found some traits that are important for the eubosminid systematics beyond female characters. It is possible that the Nearctic ‘ B. longispina ’ belongs to another, undescribed species, as was proposed by Haney & Taylor (2003). If Beringian and Atlantic Nearctic species belong to a single species, then this species must be named Bosmina (Eubosmina) striata Herrick, 1882 .

Bosmina (Eubosmina) tanakai sp. nov.,

Figures 21–24

Bosmina coregoni seligoi forma Rühe in Uéno, 1933: 309–310; pl. 10, figs 9, 10.

Bosmina coregoni obtusirostris Sars in Uéno, 1938b: 285.

Bosmina (Eubosmina) longispina Leydig in Tanaka, 2000: 120–123; figs 10, 11.

? Bosmina coregoni Baird in Uéno, 1938a: 15–18, figs 20–33; Uéno, 1968: fig. 1J.

Not Bosmina amemiyai Brehm, 1925: 271–273 ; text – fig.

Not Bosmina coregoni yezoensis Uéno, 1933: 310 ; pl. 10, figs 11 and 12.

Etymology: This species is dedicated to Prof. S. Tanaka, a Japanese cladocerologist, who determined this species as B. longispina , but made the first adequate drawings of males of Japanese Eubosmina , and remarked on their differences from European representatives ( Tanaka, 2000).

Type locality: Ichiyanagi Numa Pond (40.912434°N, 141.365243°E), Rokkasho Village, Aomori Prefecture, Japan. The type series was collected on 29 November 2006 by S. Ishida .

Type material

Holotype: Ephippial female in 90% alcohol, MGU Ml 65. Label of the holotype: ‘ Bosmina tanakai sp. nov., 1 eph. fem. from Ichiyanagi Numa Pond, Aomori Prefecture, Japan, collected on 28 November 2006 by S. Ishida, HOLOTYPE’.

Figures

Figure 17. Bosmina (Eubosmina) cf. longispina: from a lake in tundra, Tareya, Taimyr Autonomous Area, Asian Russia. A, adult male; B, head of adult male, anteroventral view; C, D, postabdomen and its distal portion; E, juvenile male II; F, head of juvenile male II, anteroventral view; G, adult parthenogenetic female, general view; H, head of adult parthenogenetic female, anteroventral view. Scale bars: 100 Mm for (A, B, E, G, H); 10 Mm for (C, D, F).

Figure 18. Bosmina (Eubosmina) cf. longispina: male from a lake in tundra, Tareya, Taimyr Autonomous Area, Asian Russia. A, juvenile male I, lateral view; B, postabdomen of juvenile male I; C, distal portion of limb I of juvenile male I, inner view; D, juvenile male II, general view; E, postabdomen of juvenile male II; F, limb I of juvenile male II, inner view; G, adult male (third instar), general view; H, anteroventral portion of valve of adult male, inner view; I, mucro of adult male, inner view; J, postabdomen of adult male; K, distal portion of adult male; L, limb I of adult male, inner view; M, tip of copulatory hook of adult male. Scale bars: 100 Mm.

Figure 19. Adult male of Bosmina (Eubosmina) cf. crassicornis: from Bratsk Water Reservoir, Irkutsk Area, Asian Russia (A–E). Adult male of Bosmina (Eubosmina) cf. kessleri: from Lake Glubokoe, Ruza District, Moscow Area, European Russia (F–L). A, general view; B, head in anterior view; C, mucro; D, postabdomen; E, distal portion of limb I; F, general view; G, head in anterior view; H, setae at anteroventral portion of valve; I, mucro; J, K, postabdomen; L, distal portion of limb I. Scale bars: 100 Mm.

Figure 20. Bosmina (Eubosmina) cf. longispina: adult male from a pond in Nome, Alaska, USA. A, lateral view; B, C, head in lateral and anterior view; D, setae at anteroventral portion of valve, inner view; E, mucro, inner view; F, G, postabdomen; H, antenna I, anterior view; I, proximal portion of basal segment of antenna II; J, K, distal portion of limb I in inner (anterior) and external (posterior) view. Scale bars: 100 Mm.

Figure 21. Bosmina (Eubosmina) tanakai sp. nov.: ephippial female from Ichiyanagi Numa Pond, Aomori Prefecture, Japan. A, lateral view; B, head, lateral view; C, D, head, anterior view; E, F, region of lateral head pore; G, setae at anteroventral portion of valve; H, I, mucro, inner view. Scale bars: 100 Mm.

Figure 22. Bosmina (Eubosmina) tanakai sp. nov.: female from Ichiyanagi Numa Pond, Aomori Prefecture, Japan (A, D–G), and from Konuma (B) and Kussharo (C), Hokkaido Prefecture, Japan. A–C, body outline of large adult; D, E, postabdonem of large adult; F, midgut with loops of an atypical specimen; G, juvenile female. Scale bars: 100 Mm.

Figure 23. Bosmina (Eubosmina) tanakai sp. nov.: adult male from Ichiyanagi Numa Pond, Aomori Prefecture, Japan. A, general view; B, head, lateral view; C, D, head, anterior view; E, frontal head pore; F, region of lateral head pore; G, mucro, inner view; H, I, postabdomen, lateral view; J, distal end of postabdomen, ventral view; K, aesthetasc region of antenna I. Scale bars: 100 Mm.

Figure 24. Bosmina (Eubosmina) tanakai sp. nov.: adult male from Ichiyanagi Numa Pond, Aomori Prefecture, Japan. A, antenna II; B, distal anterior seta; C–E, limb I; F, tip of copulatory hook; G, subdistal lobe in distal view. Scale bars: 100 Mm.