Biapertura affinis ( Leydig, 1860 )

Sinev, Artem Y., 2020, Re-evaluation of the genus Biapertura Smirnov, 1971 (Cladocera: Anomopoda Chydoridae), Zootaxa 4885 (3), pp. 301-335 : 306-310

Biapertura affinis ( Leydig, 1860)

Baird 1843: 92–93, Pl. 3: Fig. 9–11 ( Alona quadrangularis ); Liévin 1848: 40, Pl. 10: Fig. 6–7 ( Alona quadrangularis ); Leydig 1860: 233, Pl. 9: Fig. 68–69 ( Lynceus ); Sсhödler 1863: 18–19, Pl. 1: Fig. 17 –22 ( Alona spinifera ); P. E. Müller 1867: 175–176, Pl. 3: Fig. 22–23, Pl. 4: Fig. 1–2 ( Alona oblonga ); Stingelin 1895: 244–246, Pl. 7: Fig. 32–33 ( Alona ); Lilljeborg 1901: 454–461, Pl. 66: Fig. 18–21, Pl. 67, Fig. 1–17 ( Lynceus ); Stingelin 1906: 324–325, Pl. 13: Fig. 18 ( Alona ); Sars 1916: 221–223, Pl. 34, Fig. 1–1a ( Alona ); Behning 1941: 312–315, Fig. 129 ( Alona ); Herbst 1962: 89, Fig. 69 ( Alona ); Smirnov 1971: 467–474, Fig. 582–588, 590; Flössner 1972: 318–321, Pl. 151( Alona ); Negrea 1983: 325–329, Fig. 133A–P; Alonso 1996: 345–346, Fig. 154A–S ( Alona ); Sinev 1997: 47–55, Fig. 1–3 ( Alona ); Sinev 1998: 58, Fig. 5 ( Alona ); Sinev 2000: 197–202, Fig. 1 –22 ( Alona ); Sinev 2009: 49–51, Fig. 5–6 ( Alona ); Flössner 2000: 297–300, Pl. 110 ( Alona ); Hudec 2010: 306–309, Pl. 73( Alona ); Sinev et al. 2020: 128–129, Fig. 6 G–L, 7 ( Alona ).

Material examined for this study. Over 50 parthenogenetic and ephippial females; over 20 males from Lake Glubokoe, Ruza District , Moscow Area , Russia, 08–09.2019, coll. by A.Y. Sinev; over 50 parthenogenetic females, 13 ephippial females, 8 adult males, numerous exuvia from Klein Vaal River , Transvaal Province , Republic of South Africa, 28.09.1990, coll. D.G. Frey, DGF–8926; over 50 parthenogenetic females, 2 ephippial females, 3 adult males, numerous exuvia from Elias Gaat at West End , River Crossing , South of Caledon , Cape Province, Republic of South Africa, 20.10.1990, coll. D.G. Frey, DGF–8969; 13 parthenogenetic females, 1 adult male from Diep Rivier crossing, between Knysna and George, Cape Province, Republic of South Africa, 27.10.1990, coll. D.G. Frey, DGF–8984 .

Material examined earlier. See Sinev (1997, as A. affinis var. affinis and A. affinis var. ornata ; 2000) and Sinev et al. (2020) for the list of material from Eurasia and Sinev (2009) for the list of material from South Africa.

For descriptions of European populations see Alonso (1996), Smirnov (1971), Flössner (1972, 2000), Sinev (1997, 2000), Hudec (2010); for full description of South African population see Sinev (2009). Thoracic limbs and dorsal pores of European populations of B. affinis were never fully studied, so full description of these structures of parthenogenetic female is provided in addition to diagnosis.

Diagnosis. Female. Length of adult 0.65–0.1.1 mm. Body ( Fig. 1A , 2 A–F) oval or slightly ovoid; maximum height at the midline or behind it; height/length ratio about 0.6 in adults. Postero-dorsal angle of valves ( Fig. 1B, C ) with 7–10 groups of setulae, with 5–8 setulae in each. Morphology of ventral margin of valves ( Fig. 2E, G ) and head shield typical for the genus ( Fig. 1D ). Main head pores with PP 1.5–2 in adults ( Fig. 1E , 3A, B ). Lateral head pores located about 1 IP distance from midline, at level of anterior major head pore or before it. Labrum ( Fig. 1F ) typical for the genus. Postabdomen ( Fig. 1G , 2H ) subrectangular, with parallel margins, weakly narrowing at the end. Length about 2.5 height. Ventral margin straight. Dorsal margin weakly convex to straight in postanal portion and weakly concave in anal one, with distal part about 2.5 times longer than preanal one, with postanal portion 2.5–2.8 times longer than anal one. Postanal margin ( Fig. 1H ) with 11–13 massive denticles, each with 2–6 spinules along anterior margin; size of denticles increasing distally. Postabdominal claw ( Fig. 1I , 2I ) with basal spine about 0.3 length of the claw. Antennule ( Fig. 1J ) typical for the genus. Antenna ( Fig. 1K , 2J ) with basal and distal segments of both branches of similar length, middle segment being shortest. Spine on basal segment of exopodite longer than middle segment. Spines on apical segments shorter than apical segments. Limb I ( Fig. 4A,B ) with claw-like IDL seta 1. Seta e of endite 2 being 1.5–1.7 times longer than seta f.

Male. Length of adult 0.63–0.73 mm. Body low ovoid ( Fig. 1M , 5A ), with maximum height at the third quarter of the body, height/length ratio about 0.54. Postabdomen ( Fig. 1N , 5B ) of moderate size, with parallel margins in basal half of postanal portion, evenly narrowing in distal part of postanal portion. Length about 2.5 height. Ventral margin straight. Posteroventral angle straight, ventral part of distal margin straight. No protrusion at the base of postabdominal claw. The sperm ducts open at distal margin above the base of claw. Posterodorsal angle rounded. Postanal portion of dorsal margin consisting of two almost straight parts of equal length, with obtuse angle between them; anal portion concave. Preanal angle weakly defined; postanal angle not defined. Distal portion of postabdomen 2.5–3 times longer than preanal one, postanal portion 2.5 times longer than anal one. Postabdominal claw ( Fig. 1O , 5C ) weakly curved, shorter than in female, as long or slightly shorter than preanal margin. Basal spine about 0.25 length of claw. Thoracic limb I ( Fig. 4M , 5 E–F) with IDL seta 1 thin, about 1/2 length of IDL seta 2, located laterally. Anterior face of the limb under the copulatory brush with row of 5–8 stiff setulae of moderate length; outer face of endite 3 with row of 5–8 shorter setulae; there is a wide gap between these two rows.

Description of dorsal pores and thoracic limbs of parthenogenetic female. Posterior dorsal pore ( Fig. 1E , 3 A–E) as elongated longitudinal depression at the dorsal midline of carapace, of about 10 µm length in adults; a small gland-like structure under it beneath the cuticle ( Fig. 1E ). SEM examination reveals two very small apertures located at the middle of the posterior dorsal pore ( Fig. 3 D–E), one before another in some specimens, on same level in others.

Limb I of moderate size ( Fig. 4A,B ). Epipodite oval, without a projection. Accessory seta long, only slightly shorter than ODL seta, with long setulae in distal part. ODL with one seta. IDL with three setae and several clusters of hard setules. IDL seta 1 large and broad, claw-like, strongly curved, slightly longer than seta 2; IDL setae 2 and 3 with thin setulae in distal part; seta 3 slightly shorter than ODL seta; seta 2 about 2/3 the length of seta 3. Endite 3 with four setae subequal in length. Endite 2 with two long distally setulated setae (e–f), a shorter seta near their base (d) and a naked inner seta (2), and small sensillum on anterior face of limb; seta e long, two times longer than seta f, about 2/3 lengths of limb itself. Endite 1 with two 2-segmented setae (g–h), both setulated in distal part, a flat plumose seta pointed the limb base, and a naked inner seta (3). Inner seta 3 two times longer than inner seta 2. Seven–eight rows of thin long setulae on ventral face of limb. Two ejector hooks, one slightly shorter than other. Maxillar process elongated, with short setulated seta in distal part.

Limb II subtriangular ( Fig. 4D ). Exopodite elongated, of irregular shape, with slender seta as long as exopodite itself and cluster of very long setulae in distal part. Eight scraping spines, three basalmost spines subequal in length, others increasing in length distally. Size of denticles on basal part of spines decreasing from basal to distal spines. Distal armature of gnathobase with four elements. Filter plate II with seven setae, the posteriormost member shorter than others.

Limb III ( Fig. 4 E-G). Epipodite oval, without projection. Exopodite of irregular shape, with seven setae. Seta 3 being longest, setae 6 about 1/2 length of seta 3, seta 7 two times shorter than seta 6, other setae very short. Setae 1–5 plumose, seta 6 with three rows of hard setulae in distal part, seta 7 with thin short setulae in distal portion. Distal endite with 3 setae evenly decreasing in size basally, two distalmost members (1–2) scraping, slender, sharp, with denticles in distal part; short bottle-shaped sensillum located between their bases; seta 3 flattened, bilaterally armed with long setulae. Basal endite with 4 plumose setae increasing in size basally. Four pointed soft setae increasing in size basally, a small bottle-shaped sensillum near the distalmost seta. Distal armature of gnathobase with four elements; the first one elongated, narrowing distally sensillum, second strongly geniculated seta, third and fourth—spines. Filter plate III with seven setae.

Limb IV ( Fig. 4H, I ). Pre-epipodite setulated; epipodite oval, with projection shorter than exopodite itself. Exopodite subquadrangular, with six setae. Seta 1 and 2 being longest, equal in length; seta 3 slightly shorter, seta 4 about 2/3 length of seta 1, bending toward inner portion of limb; setae 5–6 subequal in length, slightly shorter than seta 4. Setae 1–4 plumose, setae 5–6 with very short thin setulae in distal portion. Inner portion of limb IV with four setae and bottle-shaped sensillum. Scraping seta (1) slender, three flaming-torch seta decreasing in size basally, with 7–9 long setulae each. Small sensillum between the base of middle and basal flaming-torch setae. Three soft setae slightly increasing in size basally. Gnathobase with one long 2-segmented setae, a small hillock distally and a sensillum. Filter plate IV with five setae.

Limb V ( Fig. 4J, K ). Pre-epipodite setulated; epipodite oval, with projection as long as epipodite itself. Exopodite divided into two lobes, with four plumose setae: setae 1–3 long, evenly decreasing in size, seta 4 four times shorter than seta 1. Inner lobe broad, rounded with setulated inner margin. At inner face, two setae densely setulated in distal part, one of them very long, as long as exopodite seta 1, the other two times shorter. Filter plate V with three setae, two broad-based sensilla-like structures between inner face setae and filter plate.

Limb VI ( Fig. 4L ) as elongated oval lobe with setulated margin.

Notes on South African populations. Morphology of studied females from South African populations fully agrees with the previous data (see Sinev 2009), and did not differ in any details rom that of Palaearctic populations. Morphology of males from South African populations was studied for the first time; it fully agrees with that of Palaearctic populations ( Fig. 5 A–F). Length of males from South African populations was 0.63–0.69 mm, height 0.35–0.39 mm, within the range of size of Palaearctic populations.

Differential diagnosis. B. affinis differs from B. lepida in a claw-like IDL seta I, from B. martensi and B. elliptica in female postabdomen with parallel margins, from B. sibirica in the absence of denticles on posteroventral margin of valves, and from B. kendallensis in smaller IP/PP ratio. It differs from B. ossiani , B. sibirica and B. kendallensis in shape of male postabdomen, with a right ventrodistal angle, and in IDL of male thoracic limb I with seta 1 being thin and located laterally.

Distribution and ecology. B. affinis is distributed in the whole Palaearctic region, from Iceland and Spain to Kamchatka peninsula and Japan; rather rare in West Siberia and Yakutia, areas of primary distribution of B. sibirica , common in other regions ( Sinev et al., 2020). B. affinis is also recorded from South Africa. Records of B. affinis from Afrotropical and Oriental region lack detailed description and should be re-evaluated ( Sinev 2009, 2016; Van Damme & Eggermont 2011). B. affinis is an eurybiotic species living in littoral both in the bottom sediments and among vegetation. In Europe, reported from lakes, ponds, reservoirs, river floodplains in lowlands and mountains (up to the elevation of 3000 m.a.s.l), at pH 4.0–10.2, calcium (Ca2+) concentrations 0.7–112 mg L- 1, conductivity 54–2050 μS cm ̅1, salt water tolerant up to 5.25 ‰ ( Bledzki & Rybak 2016), encountered in hypogean waters ( Brancelj & Sket 1990).

Figures

FIGURE 1. Biapertura affinis (Leydig, 1860) from Glubokoe Lake, Moscow Area, Russia.A–K, adult parthenogenetic female. A, lateral view. B–C, posteroventral angle of valves. D, head shield. E, head pores. F, labrum. G, postabdomen. H, postanal margin of postabdomen. I, postabdominal claw. J, antennule. K, antenna. L, ephippial female. M–O, adult male. M, lateral view. N, postabdomen. O, postabdominal claw. (A–L, orig.; M–O, after Sinev et al. 2020)

FIGURE 2. Biapertura affinis (Leydig, 1860) from Glubokoe Lake, Moscow Area, Russia. A–B, lateral view. C, dorsolateral view. D, dorsal view. E, ventral view. F, frontal view. G, ventral part of valve. H, postabdomen. I, postabdominal claw. J, antenna.

FIGURE 3. Biapertura affinis (Leydig, 1860) from Glubokoe Lake, Moscow Area, Russia, parthenogenetic female.A–B, head pores. C–E, posterior dorsal pores.

FIGURE 4. Biapertura affinis (Leydig, 1860) from Glubokoe Lake, Moscow Area, Russia. A–L, thoracic limbs of adult parthenogenetic female. A, limb I. B, IDL and ODL of limb I. C. inner setae of endites 1–2 of limb I. D, limb II. E, exopodite of limb III. F–G, inner and outer parts of inner portion of limb III. H, exopodite of limb IV. I, inner portion of limb IV. J–K, limb V and its gnathobase filter plate. L, limb VI. M, copulatory hook and IDL of thoracic limb I of adult male. (A–L, orig.; M, after Sinev et al., 2020)

FIGURE 5. Biapertura affinis (Leydig, 1860) from Klein Vaal River, Transvaal Province, Republic of South Africa, adult male. A, lateral view. B, postabdomen. C, distal portion of postabdomen. D, antennule. E, copulatory hook of thoracic limb I. F, IDL of thoracic limb I.

FIGURE 6. Biapertura kendallensis (Henry, 1919) from Ryan’s II Billabong, Bonegilla, east of Wodonga, Victoria, Australia. A–B, juvenile females of instar I and II. C–K, adult parthenogenetic female. C, lateral view. D, ventral margin of valves. E, setae of anterior group. F, setae of posterior group. G, posterior margin of valves. H, posteroventral angle of valves. I–J, head shields. K, head pores. L, ephippial female. M–N, juvenile males of instar I and II. O, adult male.

FIGURE 7 Biapertura kendallensis (Henry, 1919) from near Ryan’s II Billabong, Bonegilla, east of Wodonga, Victoria,Australia. A, juvenile female of instar I. B–I, adult parthenogenetic female. B, lateral view. C–D, same specimen in lateral and dorsolateral view. E, anterior portion of ventral margin of valves. F, head pores. G, postabdomen. H, postanal margin of postabdomen. I, postabdominal claw.

FIGURE 8. Biapertura kendallensis (Henry, 1919) from near Ryan’s II Billabong, Bonegilla, east of Wodonga, Victoria, Australia.A–B, antenna of adult female. C–F, ephippial female. C–D, same specimen in lateral and dorsolateral view. E, ephippium. F, head pores.

FIGURE 9. Biapertura kendallensis (Henry, 1919) from near Ryan’s II Billabong, Bonegilla, east of Wodonga, Victoria, Australia. A–H parthenogenetic female. A–B, labrum. C–D. postabdomens. E, postanal margin of postabdomen. F, postabdominal claw. G, antennule. H, antenna. I, postabdomen of juvenile male of instar I. J–L, juvenile male of instar II. J, postabdomen. K, postabdominal claw. L, antennule. M–P, adult male. M, postabdomen. N, postanal margin of postabdomen. O, postabdominal claw. P, antennule.

FIGURE 10. Biapertura kendallensis (Henry, 1919) from near Ryan’s II Billabong, Bonegilla, east of Wodonga, Victoria, Australia. A–L, thoracic limbs of adult parthenogenetic female. A, limb I. B, IDL and ODL of limb I. C, inner setae of endites 1–2 of limb I. D, limb II. E, exopodite of limb III. F–G, inner and outer parts of inner portion of limb III (gnathobase filter plate not shown). H, exopodite of limb IV. I, inner portion of limb IV. J–K, limb V and its gnathobase filter plate. L, limb VI. M, anlage of copulatory hook and IDL of thoracic limb I of juvenile male of instar I male. N, anlage of copulatory hook and IDL of thoracic limb I of juvenile male of instar II male. O–Q thoracic limb I of adult male. O, general view. P, copulatory brush and endite 3 (setae a–b not shown); Q, copulatory hook and IDL.

FIGURE 11. Biapertura elliptica (Sinev, 1997) from pool near Lake Albina, Kosciuszko National Park, New South Wales, Australia (type locality). A–B, juvenile females of instar I and II. C–P, adult parthenogenetic female. C, lateral view. D, ventral margin of valves. E–F, posteroventral angle of valves. G–H, head shield. I, head pores. J–K, labral keel. L–M, postabdomen. N, postanal margin of postabdomen. O, postabdominal claw. P, antenna.

FIGURE 12. Biapertura elliptica (Sinev, 1997) from pool near Lake Albina, Kosciuszko National Park, New South Wales, Australia (type locality). A–I, adult parthenogenetic female. A–B, lateral view. C, ventrolateral view. D, dorsal view. E–F, head pores. G, dorsal pores. H, postabdomen. I, postabdominal claw and distal portion of postabdomen.

FIGURE 13. Biapertura elliptica (Sinev, 1997) from pool near Lake Albina, Kosciuszko National Park, New South Wales, Australia (type locality). A–D, adult parthenogenetic female. A, posteroventral angle of valves. B–C, antenna. D, thoracic limbs.

FIGURE 14. Biapertura elliptica (Sinev, 1997) from pool near Lake Albina, Kosciuszko National Park, New South Wales, Australia (type locality). A–L, adult parthenogenetic female. A, antennule. B–L, thoracic limbs. B, limb I. С, IDL and ODL of limb I. В. inner setae of endites 1–2 of limb I. E, limb II. F, exopodite of limb III. G, distal endite of inner portion of limb III. H, exopodite of limb IV. I, inner portion of limb IV. J–K, limb V and its gnathobase filter plate. L, limb VI.

FIGURE 15. Biapertura martensi (Sinev, 2009). A–F, adult parthenogenetic female. A, lateral view. B, posteroventral angle of valves. C, head pores. D, postabdomen. E, antenna. F, IDL of thoracic limb. Biapertura lepida (Birge, 1892). G–N, adult parthenogenetic female. G, lateral view. H, posteroventral angle of valves. I, head pores. J, postabdomen. K, postanal margin of postabdomen. L, postabdominal claw. M, antenna. N, IDL of thoracic limb I. (A–F, after Sinev, 2009; G–N, after Sinev, 2013).

FIGURE 16. Biapertura ossiani herricki (Sinev, 2013).A–I, adult parthenogenetic female.A, lateral view. B–C, posteroventral angle of valves. D, head pores. E, postabdomen. F, postanal margin of postabdomen. G, postabdominal claw. H, antenna. I, IDL of thoracic limb. J, ephippial female. K–M, adult male. K, lateral view. L, postabdomen. M, copulatory hook and IDL of thoracic limb I. Biapertura ossiani ossiani (Sinev 1998). N–O, adult male. N, lateral view. O, postabdomen. (A–M, after Sinev, 2013; N–O, after Sinev, 1998).

FIGURE 17. Biapertura sibirica (Sinev, Karabanov & Kotov, 2020). A–J, adult parthenogenetic female. A, lateral view. B–D, posteroventral angle of valves. E, head pores. F, postabdomen. G, postanal margin of postabdomen. H, postabdominal claw. I, antenna. J, IDL of thoracic limb I. K–N, adult male. K, lateral view. L, postabdomen. M, distal portion of postabdomen. N, copulatory hook and IDL of thoiracic limb I. (After Sinev et al. 2020.)