Alona nigra Smirnov, 1996

Kotov, Alexey A., Sinev, Artem Y. & Berrios, Viviana Lorena, 2010, The Cladocera (Crustacea: Branchiopoda) of six high altitude water bodies in the North Chilean Andes, with discussion of Andean endemism 2430, Zootaxa 2430 (1), pp. 1-66 : 33-40

Alona nigra Smirnov, 1996

( Figures 15–18 )

Alona nigra Smirnov, 1996b, p. 14 –15, figs 97–106.

Material studied here. 32 parthenogenetic females, 4 ephippial females, 1 adult male, 1 juvenile male of instar II from locality 3; 24 parthenogenetic females from locality 4.

Emended diagnosis. Parthenogenetic female. Body regular ovoid, of moderate height, in adults height/ length ratio about 0.7, maximum height at the middle; body moderately compressed laterally. Dorsal margin convex, postero-dorsal and postero-ventral angles broadly rounded. Postero-dorsal angle with about 100 setules organised into groups of 12–18 setules in each. Ventral margin with about 55 setae. Head shield with broadly rounded posterior margin, rostrum short and rounded. Three disconnected major head pores. PP = 0.3–0.5 IP. Minute lateral head pores located about 1.5 IP distance from midline, at level of middle major head pore. Labrum of moderate size, labral keel of moderate width, with convex anterior margin and a rounded apex. Pre-ultimate abdominal segment with five-six transverse rows of long setules. Postabdomen of moderate width, with parallel margins in postanal portion, length about 2.5–2.6 height. Dorsal margin almost straight in postanal portion, anal margin concave; distal part of postabdomen two times longer than preanal one, with postanal portion about 1.5 times longer than anal one. Postanal portion of distal margin almost straight, anal portion weakly concave. Preanal angle well-defined, postanal angle not defined, distal margin convex, dorso-distal angle broadly rounded. Postanal margin with 11–13 well-developed marginal denticles, frequently with one-two spinules on anterior margin, near them 11–12 lateral fascicles of setules, distalmost seta of each fascicle largest, in distalmost fascicles 1.5 times longer than a marginal denticles. Postabdominal claw slightly longer than preanal portion of postabdomen. Basal spine about 0.2 of length of claw. Antenna I short and wide, with nine terminal aestetascs. Antennal formula setae 0–0–3/1–1–3, spines 1–0–1/0–0–1. Seta arising from basal segment of endopod longer than endopod. Spine on basal segment of exopod longer than middle segment. Apical spines 1.5 times longer than apical segments. Limb I with accessory seta 1.5 times shorter than ODL seta. IDL with three setae, seta 1 well-developed, about 1/3 length of seta 3. Exopodite of limb III with seven setae, seta 5 being longest. Exopodite IV with six setae. Exopodite V with four setae, filter plate V absent. Epipodites IV and V without projections. Limb VI absent.

Male. Body low oval, height/length ratio about 0.64, maximum height at the middle. Body moderately compressed laterally. Dorsal margin convex, postero-dorsal and postero-ventral angles broadly rounded. Postabdomen short and wide, narrowing distally, dorso-distal angle not defined. Preanal angle not defined, postanal angle weakly-defined. Distal part of postabdomens 1.8 times longer than preanal one. Gonopore openings located almost at the end of postabdomen. Wide clusters of short setules in place of marginal denticles. Postabdominal claw very short, 2.5 times shorter than preanal portion of postabdomen, with blunt apex bearing small spine, basal spine long, sinuous, about 1/3 of claw length. Antenna I with ten terminal and two lateral aestetascs, male seta arising at 1/4 length from tip, about 1/4 of antenna I length. Limb I with V-shaped copulatory hook. IDL seta 1 two times smaller than in female, setae 2 and 3 subequal in length, three times shorter and thinner than in female, male seta large, hook-like, 1.5 times longer than seta 3.

Size up to 0.65 mm in females and up to 0.42 mm in males.

Redescription. Parthenogenetic female. In lateral view body regularly ovoid, of moderate height, maximum height at middle of body ( Figs 15A–B ). In adults height/ length ratio about 0.7, in juveniles – about 0.63 in of instar I, about 0.65 in instar II ( Figs. 15C–D ). Dorsal margin uniformly curved, postero-dorsal and postero-ventral angles broadly rounded, posterior margin uniformly curved, ventral margin in general straight ( Fig. 15E ). Antero-ventral angle rounded. Both head and valves without any sculpture.

Head of moderate size, triangle-round in lateral view, rostrum short, pointing downward. Eye and ocellus large, of subequal size. Distance from tip of rostrum to ocellus similar with that between ocellus and eye. Head shield with maximum width behind mandibular articulation, without any prominent sculpture ( Fig. 16A ). Rostrum short, more narrow than in most other species of the genus, broadly rounded. Posterior margin of head shield broadly rounded, slightly wavy. Three disconnected major head pores ( Figs 16A–B ), comparative size of pores variable. PP about 0.3–0.5 IP. Lateral head pores minute, located about 1.5 IP distance from midline, at the level of middle major head pores.

Labrum of moderate size. Distal labral plate without setulation. Labral keel wide (heigh less than 1.5 width), with rounded apex ( Figs 16C–E ). Anterior margin of keel convex, slightly undulated, posterior margin without any setules.

Valve subovoid. Ventral margin almost straight, with about 55 setae, first 15 setae long, about ten next setae short, other setae of moderate length ( Fig. 15E ). A row of about hundred setules along the posterior margin ( Fig. 15F ), at some distance from one on inner side of carapace, these setules not organized into groups. Postero-dorsal angle bears about hundred short setules organised in groups of 12–18 setules in each, distalmost seta in each group being longest and thickest.

Thorax and abdomen subequal in length, dorsal surface of abdominal segments not saddle-shaped. No abdominal projections. Penultimate abdominal segment with five-six transverse rows of long setules ( Fig. 15G ).

Postabdomen of moderate width, with parallel margins in postanal portion, convex distal margin and broadly rounded dorso-distal angle, length about 2.5–2.6 height ( Figs 15H–I ). Ventral margin almost straight. Inflated basis of claws bordered from distal margin by clear incision. Dorsal margin with distal part two times longer than preanal one, with postanal portion about 1.5 times longer than anal one. Postanal portion of distal margin almost straight, anal portion weakly concave. Preanal angle well-defined, postanal angle not defined. Preanal margin weakly convex. Postabdomen with 11–13 well-developed marginal denticles, frequently with one-two spindles near base on anterior margin ( Fig. 15J ), and with three-five groups of marginal setules on anal margin and eleven-twelve lateral fascicles of setules on anal and postanal margin, distalmost seta of each fascicle largest, in postanal portion, longest setule in each fascicles 1.5 times longer than a marginal denticles. Additional row of three-five fascicles between lateral fascicles and marginal setules in preanal region. Postabdominal claw slightly longer than preanal portion of postabdomen. Basal spine about 0.2 of length of claw ( Fig. 15K ), 2-3 setules basally to it on postabdominal claw.

Antenna I relatively short and wide, not reaching tip of rostrum, with three clusters of short setules at anterior face ( Fig. 16F ). Antennular sensory seta slender, two times shorter than antenna I, arising at 2/3 distance from the base. Nine terminal aesthetascs, two longest of them about 1/2 length of antenna I. All aesthetascs projecting beyond anterior margin of head shield.

Antenna II short and massive ( Figs. 16G–H ). Antennal formula, setae 0–0–3/1–1–3, spines 1–0–1/0–0–1. Basal segment robust, branches short and broad, basal segments of both branches 1.5 times longer than others. One of terminal setae shorther than two others. Seta arising from proximal segment of endopod longer than endopod. Seta arising from middle segment of endopod of similar size with apical setae. Spine on basal segment of exopod longer than middle segment. Apical spine 1.5 times longer than apical segments.

Thoracic limbs. Five pairs.

Limb I of moderate size ( Figs. 17A–B ). Epipodite was not found, accessory seta of moderate length. ODL ( Fig. 17A ), with a long seta, armed with minute setules in distal part; IDL with three setae and four-five clusters of small setules on ventral face, setae 2 and 3 with subequal in length, similar in length to ODL seta, both with thin setules in distal part, seta 1 of about 1/3 length of ODL seta. Endite 3 with three posterior setae (a– c), and anterior seta 1 shorter than others. On endite 2 there are three setae (d–f), setae e–f robust, armed with robust setules in distal part, seta d shorter than ODL setae, and similar to endite 3 setae. Endite 1 with two 2- segmented setae (g–h), both setulated in distal part, without a flat seta shifted to limb base, present in some other species. A small senssillum on anterior face of limb on both endites 1 and 2. Five rows of thin long setules on ventral face of limb. Two ejector hooks, one of them somewhat larger than the other. Maxillar process with a short seta.

Limb II ( Figs. 17C ) with exopodite elongated, supplied with a short, naked seta ( Fig. 17D ). Eight scraping setae (1–8), increasing in length distally, scrapers 3 and 5 armed with more robust setules than others. Distal armature of gnathobase with four setae. Filter plate with seven setae, the distalmost one considerably shorter.

Limb III with exopodite trapezium-shaped, with seven setae ( Fig. 17E : 1–7). Seta 5 being longest, setae 1 and 2 about 1/3 and 1/4 length of seta 5, respectively, other setae shorter, seta 4 geniculated. Setae 1 and 2 armed with short setules in distal part. Distal endite with three setae ( Fig. 17E : 1–3), two distalmost members slender, sharp, with distal parts unilaterally armed with sharp denticles; basalmost seta 3 much shorter, bilaterally armed with long setules. Basal endite marginally with four stiff setae ( Fig. 17F : 4-7), increasing in size in basal direction. Four soft posterior setae (a–d) increasing in size basally, a small sensillum near the base of distalmost seta. Gnathobase not clearly separated from basal endite. Distal armature of gnathobase with four elements: the first one elongated, cylindrical sensillum, second thin, geniculate seta, others two sharp spines. Filter plate III with seven setae.

Limb IV with e xopodite rounded, supplied with six plumose setae ( Fig. 17G : 1–6). Seta 4 longest, setae 5–6 and 2 of about 2/3 length of seta 4, setae 3 and 1 of about 1/3 length of seta 4. Inner-distal portion of limb IV with four marginal setae ( Fig. 17G : 1–4), distalmost seta slender, sharp, armed with sharp denticles, three flaming-torch setae of similar shape, armed with long setules, decreasing in size basally. Three soft setae ( Fig. 17G : a–c) increasing in size basally. Gnathobase with a large sensillum, a 2-segmented seta, and pair of small hillocks distally. Filter plate with five setae.

Limb V ( Fig. 17H ) with setulated pre-epipodite, epipodite was not found; exopodite oval, not divided into two lobes, with four plumose setae, decreasing in size basally, seta 1 four times shorter than seta 4. Inner limb portion an oval lobe, with setulated inner margin. At inner face, two setae (1–2), 1 two times longer than 2. Filter plate absent.

Ephippial female ( Fig. 18A ). Body subrectangular, dorsal and posterior margins of valves almost straight, postero-dorsal angle expressed, ephippium dark brown, almost black.

Male. Body shape of instar II juvenile male ( Fig. 18B ) of same shape as juvenile female of same instar. Adult male is very small in comparison with the adult female, with lower body ( Fig. 18G ). General shape low oval, body height/body length about 0.64. Both eye and ocellus significantly larger than in female, ocellus larger than eye.

Postabdomen of instar II juvenile male more narrow, than that of female, with subrectangular distal portion ( Fig. 18C ). Gonopore openings located close to the end of postabdomen. Marginal denticles same as in female. Postabdominal claw 1.5 times shorter than preanal portion of postabdomen, basal spine same as in female. In adult male postabdomen short and wide, narrowing distally, dorso-distal angle not defined ( Fig. 18H ). Preanal angle not defined, postanal angle weakly-defined. Distal part of postabdomen 1.8 times longer than preanal. Gonopore openings located almost at the end of postabdomen. Wide clusters of short setules in place of marginal denticles, in five distalmost clusters setules much thicker than in others. Lateral fascicles of setules similar to these of female, but 1.5 times narrower. Postabdominal claw very short, 2.5 times shorter than preanal portion of postabdomen, with blunt apex bearing characteristic small spine, basal spine long, slightly sinuous, about 1/3 of claw length ( Fig. 18I ).

Antenna I of instar II juvenile male broader than in female, with 9 terminal aesthetascs and an anlage of male seta ( Fig. 18D ). In adult male, antenna I of same length, but broader than in female, with 10 terminal aesthetascs of similar length and two long lateral aestetascs, male seta arising at 1/4 length from tip, about 1/4 of antenna I length ( Fig. 18J ).

Limb I of instar II juvenile male with U-shaped copulatory hook ( Fig. 18E ), ventral face of limb with an anlage of copulatory brush seta and a peculiar hillock above it, not present in adult male ( Fig. 18F ). IDL with anlage of male seta, seta 1 same as in female, seta 2 and 3 much shorter than in female. In adult male, copulatory hook V-shaped, its free arm (= terminal part) little longer than basal one ( Figs. 18K–L ). A group of five long setules located under copulatory brush, at some distance of it a row of about 11–12 short, robust setules on ventral face of limb. IDL seta 1 two times smaller than in female, setae 2 and 3 subequal in length, three times shorter and thinner than in female, male seta large, hook-like, 1.5 times longer than seta 3.

Size. Juvenile females of instar I 0.38–0.41 mm (height 0.24–0.26 mm); juvenile females of instar II 0.45–0.48 mm (height 0.29–0.32 mm); adult females 0.55–0.65 mm (height 0.38–0.46 mm). Single studied juvenile male of instar II 0.42 mm (height 0.27 mm), single studied adult male 0.42 mm (height 0.26 mm).

Differential diagnosis. Alona nigra can be differentiated from the majority of other species of Alona s. lat. belonging to a small set of species with disconnected major head pores. There are only three other known species with this peculiarity (1) paleotropical A. cambouei Guerne & Richard, 1893 , (2) Mediterranean A. nuragica Margaritora, 1971 , and (3) Australian A. setuloides Smirnov & Timms, 1983 . No other species with disconnected head pores are known from America. A. cambouei differs from A. nigra in (1) smaller size (less than 0.5 mm), (2) narrow postabdomen with parallel margins, (3) prominent, sharp distal angle, and (4) smaller size of the antennal spines (see Sinev 2001c). A. nuragica differs from A. nigra in (1) tapering postabdomen with more numerous denticles and lateral fascicles and (2) lateral pores as small round cavities ( Alonso 1996). A. setuloides differs from A. nigra in (1) lower body (height/length ratio about 0.5), (2) longer postabdomen with obtuse distal angle and straight distal margin, and (3) the spine on basal segment of exopodite of antenna II being shorter than middle segment ( Smirnov & Timms 1983). Also, Alona nigra differs from these species in a densely setulated penultimate abdominal segment. The male of A. nigra clearly differs from males of these species in (1) shape of postabdomen and (2) very small postabdominal claw with the spine at the apex.

Comments. Type locality of this species is Lake Uru-Uru , Oruro Department, Bolivia (3686 m.a.s.l.). Holotype: female MGU 3579 . Paratypes: females MGU 3571 , 35 73, 3574, 3575, 3581, 3587, 3589, 3594, 3595.

Our specimens completely fit the initial description of the species ( Smirnov 1996b). Complete description of appendages was not provided in the initial description.

A. nigra shares numerous affinities with the A. pulchella -group, phylogenetic position of which, according to Van Damme & Dumont (2008a) is uncertain, intermediate between Hexalona - and Cornatellabranches. These similarities include: (1) morphology of IDL setae, (2) absence of third seta on endite 1 of limb I, (3) exopodite IV with plumose setae 1–2, (4) absence of filter plate V and (5) absence of limb VI. Male antenna of A. nigra bears two lateral aesthetascs, which are not present in any groups of Hexalona. The aforementioned A. cambouei is also a member of this group. On the other hand, species of the pulchella -group have more narrow and long postabdomen with parallel margins and prominent distal angle, posteroventral margin of valves with setules not differentiated into groups, small accessory seta of limb I, and more broad rostrum. The morphology of male postabdomen of A. nigra also significantly differs from that of pulchella -group.

There are two characters rare for Alona s. lat – disconnected major head pores and densely setulated middle abdominal segment. There are only three species with such morphology of head pores (see above), and only one, A. setosocaudata Vasiljeva & Smirnov, 1969 , with densely setulated abdomen (see Sinev & Kotov 2001).

In our opinion, pulchella -group and related species, like A.nigra and A. setulosa (see Sinev, 2009b) belong to the Hexalona -branch of Alona -like animals, having two most important features of Hexalona – seven setae on exopodite III and well-developed first IDL seta. Common features between pulchella -group and Coronatella -branch (see Van Damme & Dumont, 2008a) are mostly reductions of limb structures, which independently appears in several unrelated groups of Aloninae (see Kotov, 2000b).

Distribution. So far, Alona nigra was found only in saline lakes of the Andes ( Bolivia and North Chile); this species seems to be an endemic of the Andes .

Figures

FIGURE 15. Alona nigra, parthenogenetic female from Salar de Lagunillas, Chile. A–B. Large adult; C–D. Juvenile; E. Armature of valve free margin; F. Posterior margin; G. Abdomen; H–I. Postabdomen; J. dorso-distal angle of postabdomen; K. Postabdominal claw. Scale bars 0.1 mm.

FIGURE 16. Alona nigra, parthenogenetic female from Salar de Lagunillas, Chile. A. Head shield; B. Dorsal head pores; C–E. Labrum; F. Antenna I; G–H. Antenna II. Scale bars 0.1 mm.

FIGURE 17. Alona nigra, thoracic appendages of parthenogenetic female from Salar de Lagunillas, Chile. A–B. Limb I, outer (posterior) and inner (anterior) view; C–D. Limb II and its distal portion; E–F. Limb III and its basal endite; G. Limb IV; H. Limb V. Scale bars 0.1 mm.

FIGURE 18. Alona nigra, gamogenetic specimens from Salar de Lagunillas, Chile. A. Ephippial female; B–F. Juvenile male II, its postabdomen, antenna I; distal portion of limb I and copulatory brush on limb I; G–L. adult male, its postabdomen, postabdominal claw, antenna I, limb I and its distal portion. Scale bars 0.1 mm.