Systematics
Class Branchiopoda Latreille, 1817
Order Anomopoda Sars, 1865
Family Chydoridae Dybowski & Grochowski, 1894 emend. Frey, 1967
Subfamily Aloninae Dybowski & Grochowski, 1894 emend. Frey, 1967
Genus
Alona Baird, 1843
Alona kaingang Sousa, Elmoor-Loureiro & Santos
(Figs. 1, 2, 3, and 4)
Type material
Holotype. Undissected, adult parthenogenetic female in a tube with 90 % ethanol deposited at the Museum of Zoology of the University of São Paulo under access number MZUSP 29593. The label of the holotype is “Alona kaingang n. sp., 1 parth. ♀ from Mostardas—Lagoa de São Simão, RS, Brazil, Holotype.”
Paratypes. Two undissected adult parthenogenetic females in tubes with 90 % ethanol, deposited at the Museum of Zoology of the University of São Paulo under access number MZUSP 29594. One adult parthenogenetic female and one adult male, undissected in tubes with 90 % ethanol, deposited at the National Museum of Rio de Janeiro under access numbers MNRJ 23739 and MNRJ 23740. Eight specimens selected as paratypes (access number EL02477), and several unstudied individuals (access numbers EL02165 and EL02166) are deposited at the Laboratório de Biodiversidade Aquática, Universidade Católica de Brasília.
Type locality
Pond in São Simão, Mostardas, Rio Grande do Sul state, Brazil (30° 57′ 06″ S, 50° 42′ 29″ W).
Etymology
The name kaingang refers to indigenous people who inhabited the southern portion of South America before the European colonization. The kaingang people were distributed in Southeastern and Southern Brazil, where the new species occurs.
Material examined
Twenty-three adult parthenogenetic females and five males from the pond in São Simão, Mostardas, Rio Grande do Sul state, Brazil (30° 57′ 06″ S, 50° 42′ 29″ W). Material collected by Lourdes M. A. Elmoor-Loureiro on 01.i.2002. Four adult parthenogenetic females from the Limnology Laboratory cultivation facility, Instituto de Ciências da Natureza, Universidade Federal de Alfenas; specimens collected at Furnas Reservoir, Minas Gerais state, Brazil (21° 03′ 24″ S, 46° 00′ 18″ W), leg. M. J. Santos-Wisniewski (EL02167). Four adult parthenogenetic females from a marginal pond in São Simão Reservoir, Minas Gerais state, Brazil (18° 48′ 50″ S, 50° 22′ 58″ W); material collected by José Roberto Debastiani-Júnior (EL02173).
Diagnosis
Female. Of small size, length 0.33–0.40 mm. Body ovoid with dorsal margin strongly arched. In dorsal view, it shows weak lateral compression, dorsal keel absent. Head. Head shield with posterior margin rounded, rostrum short, three main head pores subequal in size, narrowly connected, postpore distance (PP) less than 0.2 interpore distance (IP). Lateral pores tiny, inserted midway between the main pores and the head shield margin. Labral keel wide, apex obtuse, without setae or denticles. Carapace. No striations or longitudinal lines. Ventral margin with 40–50 setae arranged in three groups. Posteroventral corner without denticles, with numerous spinules. Antennules. About 2–2.5 times as long as wide, four rows of setules on antennular body, distalmost row shorter than the others. Antennular sensory seta slender and long, about 1.5 times smaller than antennular body. Nine terminal aesthetascs of different sizes. Antenna. Antennal formula: spines 001/101, setae 113/003. Spine on first endopodite segment not exceeding the length of the second segment. Apical setae of endopodite and exopodite with lateral spinules. Postabdomen. Of moderate size (about 2–2.4 times as long as wide). Pre-anal margin longer than anal margin and shorter than postanal margin. Anal margin inserted in a depression, with distinct angles. Lateral fascicles arranged in five to seven groups, first spines of each group thick and exceeding margin of postabdomen. Six to seven clusters of marginal denticles. Postabdominal setae with proximal portion naked, distal portion with short setules armed bilaterally. Terminal claw. Longer than anal margin, with one row of spinules on its base. Basal spine. Long, without spinules or setules. Limb I. First endite with two marginal setae, IDL with three setae; setae 2–3 bisegmented, long and with strong proximal spines. Limb II. Exopodite elongated, with setae present; scrapers 3, 5, 6, 7, and 8 with robust denticulation. Limb III. Exopodite with seven marginal setae; first seta longer than the second, fifth, and seventh setae less than half length of sixth seta, fourth setae geniculated. Limb IV. Exopodite with six marginal plumose setae; fourth seta thick and more than half length of fifth seta; sixth seta half as long as fifth seta. Limb V. Exopodite with slight depression in middle portion, with four plumose setae; seta 3 smaller than setae 1 and 2; Gnathobase without elements or setae. Male. Body elongated, smaller than female (length 0.27–0.30 mm). Ventral margin armed with 40 setae followed by fine spinules. Posteroventral corner without denticles. Head with short rostrum. Main pores nearly connected. Lateral pore inserted between distal and median pores. Antennules. With three rows of short setules on the antennular body. Nine (juvenile) to 11 (adult) aesthetascs present: seven to nine terminal and two lateral. Male seta short, thick, about 4.6 times shorter than length of antennular body. Postabdomen. Narrowing toward distal portion, anal angle not defined. Marginal clusters of spinules present, at least five postanal fascicles. Gonopores opening ventrally, subapically to terminal claw. Terminal claw. Smaller than that of female, tip blunt, with slender spinules implanted at base. Basal spine about one-third length of terminal claw. Limb I. With copulatory hook U-shaped; copulatory brush seta slender; IDL with three setae. Seta 1 long, thick, subequal in size to setae 2 and 3.
Description of adult parthenogenetic female
Habitus (Fig. 1(a–c)). Compared to other species of the genus, it is a small-sized animal (0.33–0.40 mm), colorless, and transparent. Carapace ovoid in lateral view, about 1.5 times as long as high, dorsal margin strongly arched. In dorsal view, it shows weak lateral compression. Dorsal keel absent.
Head (Fig. 1(a, e, f)). Ocellus as large as eye. Head shield about 1.7 times as long as wide, with posterior margin rounded. Rostrum short, blunt, projected toward ventral margin. Three main head pores of subequal size, narrowly connected (Fig. 4(a)), PP less than 0.2 IP. Lateral pores tiny, inserted midway between main pores and head shield margin. Labrum (Fig. 1(g–i)). Labral keel wide in lateral view, anterior margin slightly convex, apex obtuse, lateral projections not observed, without setae or denticles. In some specimens, the margin is subquadrangular (Fig. 1(h)) or with a small depression near the apex (Fig. 1(i)). Mandible (Fig. 1(j)). Well developed in relation to body size (Fig. 1(a)). First maxilla (Fig. 2(a)). Relatively well developed, with two long setulose setae.
Carapace (Figs. 1(c, d) and 4(b)). No striations or longitudinal lines (Fig. 4(b)), punctuated ornamentation observed in optical microscopy. Ventral margin straight, with 40–50 setae arranged in three groups, proximal group long, middle group short, posterior group increasing in size toward posteroventral corner. These setae are followed by spinules not arranged in groups, proximalmost spinule projecting beyond margin.
Antennules (Fig. 2(b)). Reaching the tip of the rostrum, setae sometimes exceeding it, about 2–2.5 times longer than wide, four rows of setules on antennular body, distalmost row shorter than the others. Antennular sensory seta slender and long, about 1.5 times smaller than antennular body, inserted at two thirds of antennule length, counting from the base. Nine terminal aesthetascs of different sizes. None of these aesthetascs exceed the length of the antennules.
Antenna (Figs. 2(c, d) and 4(e)). Coxal setae not studied. Basipodite thick, with many spinules and one long spine. First exopodite segment with long thick spinules near the base (3–4) and terminal portion. Second exopodite segment with long thick spinules on the terminal portion. Endopodite segments with short spinules. Antennal formula: spines 001/101, setae 113/003. Seta on first exopodite segment thick and plumose (Fig. 4(c, d)), not reaching mid length of terminal setae. Seta on second exopodite bisegmented, long, with many setules. Spine on first endopodite segment without denticles, reaching but not exceeding distal end of second segment. Apical spines of endopodite and exopodite of different sizes, with denticles (Fig. 4(e)). Two apical setae of endopodite and exopodite with spinules, which are larger on the first segment.
Abdomen. About two times shorter than thorax. Two or three abdominal setae (Fig. 1(a)).
Postabdomen (Fig. 2(e–g)). Moderate size, relatively wide, about 2–2.4 times as long as wide, ventral margin slightly rounded, with at least three rows of spinules. Pre-anal margin longer than anal margin and shorter than postanal margin. Anal margin concave, clearly inserted in a depression and with two distinct angles (Fig. 4(f–g)), with many spinules forming groups (Fig. 4(g)). Postanal margin rounded, not projected. Lateral fascicles arranged in five to seven groups, first spines of each group thick and exceeding margin of postabdomen. Six to seven clusters of marginal denticles, distal ones with two to three marginal denticles (apparently fused when observed in optical microscopy but superimposed in layers when observed in SEM (Fig. 4(f)); proximal denticles may be separated; length of the marginal denticles on the postanal margin of the postabdomen about two times longer than the width of the base of the denticles. Postabdominal seta (Fig. 2(e)). Approximately half as long as postabdomen, proximal portion naked. Short setules armed bilaterally, inserted toward distal portion. Terminal claw (Fig. 2(e–g)). Implanted at projected basis from the postabdomen, longer than anal margin, uniformly curved, with one row of spinules on the base (Fig. 4(i)); pecten armed with rows of internal and external spinules; inner row composed of robust spinules; outer row with spinules increasing in size toward distal region (Fig. 4(h)). Basal spine long, about two times as long as width of claw at its base, without spinules or setules.
Five pairs of limbs
Limb I (Fig. 3(a, b)). Epipodite not studied. Outer distal lobe (ODL) with thin seta, serrulate in distal part, about same size as the longest IDL seta. Accessory seta relatively small, setulated, and implanted near base of ODL. IDL with three groups of spinules on its face, three setae present; seta 3 smaller than the others, naked. Setae 2–3 bisegmented, long, and with strong proximal spines and narrow distal portion with short denticles. Third endite with four setae, one of them thinner than the others (1); inner seta densely setulated, longer than the other two (a, b). Second endite with one row of spinules; three setae of different sizes, seta 4 (e) about 2.7 times longer than seta 3 (f) and about 4.3 times longer than seta 5 (d); setae 3–4 (d–f) with thick spinules on the lateral face, seta 4 (e) with spinules not exceeding median portion; seta 5 (d) about half length of seta 3 (f). First endite with two marginal setae (g, h), bisegmented, similar in size and slightly setulated. No specialized elements on endites. Ejector hooks similar in size. Ventral face of limb with seven rows of setules organized in clusters, decreasing toward distal portion. Gnathobase thick, corresponding to a densely setulated seta.
Limb II (Fig. 3(c, d)). Exopodite elongated, with tiny proximal spinules, and distally setulated. Seta on exopodite present, setulated, about two to three times smaller than the exopodite itself. Endite armed with eight scrapers gradually decreasing in size toward the gnathobase, sixth and eighth scrapers smaller than seventh. Scrapers 1, 2, and 4 armed with fine denticulation, other scrapers with robust denticulation. Proximal portion of gnathobase wide, apex armed with fine spinules followed by long setules (in the populations from Minas Gerais state, these appear shorter, thinner, and more numerous), distal portion armed with sensillum and three elements, first element geniculated and setulated. Filter comb with seven setae, first seta short and densely setulated; other setae long, with setules and implanted from median portion.
Limb III (Fig. 3(e, f)). Epipodite round, without evident projections (in the populations from Minas Gerais state, long projections were observed). Exopodite subquadrangular, with seven marginal setae arranged in 2 + 5. First seta longer than second; third seta about 1.8 times longer than sixth seta; fourth seta geniculated; fifth and seventh setae less than half length of sixth seta; all setae are plumose, except the seventh. Distal endite with three setae, two scraper-like of different sizes, third seta geniculated and armed with many setules implanted bilaterally; four plumose setae, increasing in size towards the gnathobase. Basal endite with four soft setae, increasing in size towards the base. Gnathobase armed with four elements, first a cylindrical sensillum, second a strong geniculated seta, setulated on the base, third and fourth elements with acute tip and without setules. Filter comb with seven long setae.
Limb IV (Fig. 3(g, h)). Pre-epipodite round, densely setulated, epipodite oval with short projections. Exopodite round with six marginal plumose setae; setae 1 and 2 subequal in size, third seta longer than all others, fourth seta thick exceeding the half length of fifth seta; sixth seta half as long as fifth seta. Distal endite with four setae, one scraper-like and three flaming-torch-like, decreasing in size toward the base. Basal endite with three soft setae, increasing in size toward the base. Gnathobase armed with one globular sensillum and a setulated seta implanted on robust base. Filter plate with five slender setae.
Limb V (Fig. 3(i)). Pre-epipodite round and densely setulated, epipodite with short projections. Exopodite rectangular, not divided in lobes, about twice as long as wide, slight depression in the middle portion; four plumose setae, decreasing in size toward internal lobe; setae 1 and 2 subequal in size, seta 3 markedly smaller than setae 1 and 2; seta 4 about half length of seta 3. Internal lobe wide, oval and with long setules; two setulated setae of similar size on the inner face of the lobe, no elements between these setae. Gnathobase reduced, without elements or setae.
Ephippial female: Unknown.
Description of male
Habitus (Fig. 1(k)). Smaller than female, length 0.27–0.30 mm, about 1.6 times as long as high. Body elongated, weak lateral compression, body less arched than in female. Head with short rostrum, ocellus smaller than eye. Main pores close to each other, nearly connected, lateral pores tiny and arranged in different positions than in females (between distal and median pores; Fig. 1(l)). Carapace without punctuated ornamentations or longitudinal lines (Fig. 4(k)), ventral margin armed with 40 setae followed by fine spinules, the most proximal exceeding the line of posterior margin.
Antennules (Fig. 2(h)). Slightly exceeding the tip of the rostrum, about two times as long as wide, with three rows of short setules on antennular body; seven (juvenile) to nine (adult) aesthetascs of different sizes (none of these aesthetascs exceeds the length of antennules). Two lateral aesthetascs of different sizes, about half as long as antennular body; sensory seta long, about 1.4 times shorter than antennular body. Male seta short, thick, about 4.6 times shorter than length of antennular body, inserted at three thirds of antennular length, counting from base.
Antenna as described for females.
Postabdomen (Fig. 2(i)). Smaller than in female, narrowing distally; anal margin longer than postanal margin, angles not defined; marginal clusters of spinules present (Fig. 4(k)); at least five postanal fascicles, distalmost fascicle exceeding the margin line; anal margin with spinules differentiated in three groups; gonopores opening ventrally, subapically to terminal claw. Terminal claw smaller and thicker than in female, tip not acute (Fig. 4(l)). Slender spinules implanted at the base of terminal claw (as in the female). Basal spine about one-third length of terminal claw.
Limb I (Fig. 3(j)). Smaller than in female, copulatory hook U-shaped. Copulatory brush present, copulatory brush seta slender; IDL with three setae, smaller than corresponding setae of female, seta 1 long, thick, subequal in size to the other two setae, setae 2 and 3 bisegmented and with strong proximal spines (as in female).
Differential diagnosis
Alona kaingang sp. nov. is a member of the pulchella-group because its posteroventral corner of the carapace is armed with many short and thin spinules not arranged in groups, three main head pores, marginal denticles of postabdomen merged and developed, lateral fascicles developed, IDL with three setae, seven setae on the exopodite of limb III, fourth setae of limb III well-developed, gnathobase of limb V reduced, and limb VI absent. Alona kaingang sp. nov. also has the fourth seta on the exopodite of limb III geniculated, like many species of the pulchella-group (except in Alona archeri). As an alternative to identification, the pulchella-group may be separated into two groups based on the morphology of the main head pores: one group contains species with interrupted connection (including those species with main head pore isolated) and the other contains species with complete connection. Thus, A. kaingang sp. nov., having a complete connection between the main head pores, could be differentiated from species belonging to do the first group: Alona capensis (Rüher, 1914), Alona setulosa (Megard, 1967), Alona cambouei (Guerne & Richard, 1893), Alona aguascalientensis Sinev & Silva-Briano, 2013, Alona nigra Smirnov, 1996, Alona setuloides Smirnov & Timms, 1983, Alona azorica Frenzel & Alonso 1989, Alona anastasia Sinev Alonso, Miracle & Suhaquillo, 2012, and Alona nuragica Margaritora, 1971. Regarding species with complete connection between main head pores, A. kaingang sp. nov. is distinguished by the presence of spinules on apical setae of antenna and proximal spines on IDL setae. Besides, A. kaingang sp. nov. has single morphological traits such as the slight depression in the middle portion of the exopodite of the limb V.
Ecology and distribution
Alona kaingang sp. nov. has populations occurring in water bodies of the subtropical region of South America. Until now, A. kaingang sp. nov. has been found only in Minas Gerais state (São Simão and Furnas Reservoirs) and Rio Grande do Sul state (São Simão pond), Brazil. However, we expect that its geographical distribution is broader in the subtropical zone, because A. kaingang sp. nov. might be confused with Coronatella rectangula (Sars, 1861). This latter species likely does not occur in the Neotropics (Van Damme and Dumont 2008b), but there are many records in different Brazilian hydrographic regions (see Green 1972; Smirnov and Santos-Silva 1995; Eskinazi-Sant’Anna et al. 2005; Sterza and Fernandes 2006; Rocha et al. 2011), including the Furnas Reservoir (Santos et al. 1994; Viti et al. 2013). The review of Coronatella in Brazil confirmed that C. rectangula does not occur in Brazil, and probably not in the Neotropics (Sousa et al. 2015).
São Simão pond is located on the coastal plain of Rio Grande do Sul state and is part of the coastal wetland complex between the Atlantic Ocean and Patos Lagoon. São Simão pond does not connect with the ocean. The abiotic parameters of the pond water were as follows: pH 6.8–7.1, electrical conductivity 97.3–110 μS.cm−1, total phosphorus 0.104–0.139 mg.L−1, ammoniacal nitrogen 0.051–0.11 mg.L−1, dissolved oxygen 7.2–9.1 mg.L−1, and temperature 17–17.5 °C (data available from State Foundation of Environmental Protection Henrique Luiz Roessler—FEPAM, referring to the year when the type material was collected).
Furnas Reservoir, located in Minas Gerais state, is the largest reservoir in southeastern Brazil, with a total area of approximately 1440 km2. Recent data indicate that water temperature ranges between 24 and 28 °C, pH is approximately 7, electrical conductivity 19–22 μS.cm−1, total nitrogen 210–318 μg.L−1, total phosphorus 13–29 μg.L−1, and dissolved oxygen 8–9 mg.L−1 (Santos et al. 2010).
São Simão Reservoir is located on the boundary between Goiás and Minas Gerais states. Currently, it is being impacted by the uncontrolled increase in urban areas and farmland in its surroundings. This has led to eutrophication of the reservoir (Fonseca 2010).
The biology of A. kaingang sp. nov. is not well known. It inhabits the littoral zones of water bodies, probably among aquatic vegetation. Based on the present records, it should be found in different kinds of ecosystems: reservoirs, wetlands, and coastal lagoons. We believe that this species may occur in habitats with varying degrees of salinity. Alona kaingang sp. nov. is presumed to be an active scraper of substrates, based on the strong scrapers found in the limbs I and II (Fryer 1968; Van Damme et al. 2011).
Identification key for species from the pulchella-group with occurrence in the Neotropics (adult parthenogenetic females)
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1.
Basal spines very short, less 0.1 of the length claw, aesthetascs length about 2.6 times shorter than antennular body…………....A. bromelicola-Central America (Sinev 2002b)
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2.
Labral keel with two rows of short setules………………………..…………….………3
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3.
Postabdomen narrowing distally, basal segment of the apical setae of antenna without spines, one seta markedly longer than the others on the anterior group on the ventral margin of the carapace,.....................Alona anamariae—Endemic from the Central Plateau of Mexico (Sinev and Silva-Briano 2012)
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Postabdomen wide and truncated, basal segment of the apical setae of antenna with spines, setae of the anterior group on the ventral margin of the carapace not differentiated in length.................……………A. setulosa—From North Canada to North Mexico (Sinev, 2009; Sinev and Silva-Briano 2012)
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4.
Abdomen armed with two to three rows of setules...............…………………………………..5
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5.
Main head pores connected……………………………………………………………6
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6.
Antenna, spine on the first segment of the endopodite shorter than second segment…………….7
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7.
Carapace ornamented with longitudinal lines, length of the postabdomen about 2.5 height, postanal margin armed with 5–6 denticles………Alona altiplana—Endemic from Andes (Kotov et al. 2010)
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Carapace without longitudinal lines, length of the postabdomen about 2.8–3 height, postanal margin armed with seven to eight denticles………………………Alona glabra—Common in the Neotropics (Sinev 2001b; Sinev and Silva-Briano 2012)