Ilyocypris japonica Okubo, 1990

Smith, Robin James, Zhai, Dayou & Chang, Cheon Young, 2019, Ilyocypris (Crustacea: Ostracoda) species in North East Asian rice fields description of one new species, and redescriptions of Ilyocypris dentifera Sars 1903 and Ilyocypris japonica Okubo, 1990, Zootaxa 4652 (1), pp. 56-92 : 56-92

Ilyocypris japonica Okubo, 1990

( Figs 1–4 A–I, 5A & B, 6A, 7 & 17)

1989 Ilyocypris sp. A.—Okubo & Ida: 105, pl. 4g–l, fide Okubo 1990.

1990 Ilyocypris japonica sp. nov. —Okubo: 40, fig. 1f–i.

1992 Ilyocypris haterumensis sp. nov. —Okubo & Terauchi: 101, fig. 1a–f, fide Okubo 2004.

? 2002 Ilyocypris dentifera Sars, 1903 —Nakao & Tsukagoshi: 71, figs 2a–d, tables 2–5, herein.

2003 Ilyocypris japonica Okubo, 1990 — Yamaguchi & Endo: Fig. 4g , table 1.

2004 Ilyocypris japonica Okubo, 1990 — Okubo: 17–18, figs 4w–aa.

2007 Ilyocypris japonica Okubo, 1990 —Yamada: 46, figs 2i & 3n, tables 1 & 2.

2008 Ilyocypris japonica —Tinn & Oakley : Fig. 1 .

? 2008 Ilyocypris dentifera Sars, 1903 —Nakao & Tsukagoshi: 251, 263, plate 1a–d, tables 1, 12–14, herein.

2009 Ilyocypris japonica Okubo, 1990 — Hayashi et al.: 77.

2010 Ilyocypris japonica —Kaji & Tsukagoshi : Table 1 .

2011 Ilyocypris haterumensis Okubo, 1992 —Martens & Savatenalinton: Table 2.

2011 Ilyocypris japonica Okubo, 1990 —Martens & Savatenalinton: Table 2.

2012 I. haterumensis Okubo 1992 —Karanovic: 204, 207.

2012 Ilyocypris japonica Okubo 1990 a—Karanovic: 205, 208.

2012 Ilyocypris japonica Okubo, 1990 — Sidorov & Semenchenko: 233.

2012 Ilyocypris japonica Okubo, 1990 — Hayashi et al.: 61.

2013 I. haterumensis Okubo, 1992 —Karanovic & Lee: 41, 58, 64.

2013 I. japonica Okubo, 1990 —Karanovic & Lee: 41, 58, 64, appendix.

2013 I. haterumensis—Zhai & Xiao: 468.

2013 Ilyocypris japonica Okubo, 1990 —Martens et al.: No page numbers.

2013 Ilyocypris haterumensis Okubo, 1992 —Martens et al.: No page numbers.

2015 I. haterumensis Okubo, 1992 —D’Ambrosio et al.: 65.

2016b Ilyocypris japonica— Smith et al.: Fig. 2i .

2016a Ilyocypris japonica Okubo, 1990 —Smith et al.: 484–488, 492–495, fig. 6, tables 1 & 2.

2017 I. japonica—Ghaouaci et al.: 145.

2017 I. haterumensis—Ghaouaci et al.: 145.

2018 Ilyocypris japonica Okubo, 1990 —Smith et al.: Appendix.

2019 Ilyocypris japonica Okubo, 1990 —Meisch et al.: 71.

Diagnosis. Carapace anterior margin slightly more inflated than posterior margin, dorsal margin sloping down posteriorly. Surface covered in many well-developed small pits, and a small number of tiny spines near posterior and anterior margins (sometimes missing). Up to six tubercles sometimes present, rounded to angular. Anterior inner calcified lamellae of both valves with lists. Swimming setae of antenna very long, extending significantly beyond end of claws. Sixth limb with five segments (second endopodal segment divided). Seventh limb with one seta on basis, two setae on third segment (= second endopodal segment), and small, hook-like setules distally on same segment. Anterior end of Zenker organ large and inflated, much larger than posterior end. Inner lobe of hemipenis long and thin, with inflated, rounded tip, and noticeably longer than outer lobe, middle and outer lobes overlapping, copulatory process slender, with curved outer edge and sharply pointed tip.

Type locality. A type locality was not explicitly designated by Okubo (1990). The type material was collected from “paddy fields near Tsukuda Station of the Japan Railway, Gumma Prefecture” ( Okubo 1990), approximate coordinates (herein given) 36.5610º N, 139.0427º E.

Type material (as designated by Okubo 1990). Holotype: male (FO-652). Allotype: female (FO-654). Paratypes: male (FO-651), male (FO-655). Numbers were provisional. Location of type material not stated and currently unknown.

Material examined. See Table 1 .

Description. Male carapace length 659–823 µm, height 367–431 µm, height/length 0.50–0.56. Female carapace length 722–927 µm, height 405–500 µm, height/length 0.54–0.56. Anterior margin approximately evenly curved, more inflated than posterior margin ( Figs 1 & 2 ). Dorsal margin noticeably sloping down posteriorly, ventral margin distinctly concave. Maximum height at anterior end of hinge. Well-defined bifurcated sulcus near dorsal margin above and slightly anterior of adductor muscle scars. Both valves without outer lists ( Fig. 1M ). With or without tubercles; when present, one rounded to angular tubercle each side of sulcus (posterior one called lateral tubercle by some authors), one in mid-position of sulcus, one towards postero-ventral region, and two tubercles in central ventral region ( Fig. 2J & K ). Six adductor muscle scars, location visible externally as pit below posterior part of sulcus. Surface of carapace covered with well defined pits, and small spines near anterior and posterior margins. Anterior inner calcified lamellae of both valves with lists. Inner side of lists uneven and with striae. Postero-ventral region of calcified inner lamella of left valve with shallow depression, internally roughened, but not with well-defined marginal ripplets. Dorsal view more rounded posteriorly than anteriorly, maximum width posterior of midlength. Males generally smaller and slightly more elongate than females. Dorsal view of male similar to female, but with more rounded posterior margin and slightly more compressed.

Antennule ( Fig. 3A ) with seven articulated segments. First segment with two long sub-apical setae on ventral margin and one medium-length seta on dorsal margin. Second segment with relatively long apical-dorsal seta. Third segment with one short apical-dorsal seta and one short apical-ventral seta. Fourth segment with two long apicaldorsal setae, and two shorter apical-ventral setae. Fifth segment with two long apical-dorsal setae, and two shorter, stout, apical-ventral setae. Sixth segment with four long setae and relatively long alpha seta. Terminal segment apically with two short setae, one of which quite stout, one long seta and relatively short aesthetasc ya.

Male antennae with fourth segment undivided ( Figs 3B & 4B ). Swimming setae very long, extending considerably beyond end of claws; shorter accompanying seta also long, reaching to mid-point of claws. G3 reduced to short seta, but extending slightly beyond end of terminal segment. Claw z1 small and slender, not reaching to end of claw G2. Female antenna claw G2 long, longer than G1 ( Fig. 4A ). Claw Gm ca. 80% length of claw GM.

Mandibular coxa small, with well-developed teeth on endite ( Fig. 3D ). Mandibular palp four-segmented ( Fig. 3C ). S1 seta on first segment longer than S2, alpha seta small and slender. Second segment with two setae on outer edge, and 3+1+beta setae on inner edge. Beta seta short, stubby and hirsute. Third segment with four setae on outer apical corner, three setae on inner apical corner, and one apical seta between other two groups. Terminal segment with three stout apical setae, two thinner and shorter apical setae and one seta protruding from area proximal of segment mid-length, towards outer edge.

Maxillula palp first segment with three sub-equal, medium-length setae on outer apical corner, one shorter seta positioned on apical edge offset from apical corner, and one sub-apical seta in mid-width position ( Fig. 3E ). Second segment wider than long, apically with three claw-like setae and three shorter setae.

Fifth limb with two a setae on dorsal margin, and approximately 17 setae along dorsal and anterior edge of basis ( Fig. 3F ). Branchial plate with six rays. Palp (endopodite) of female two-segmented, terminating with three setae of differing lengths. Palps of male symmetrical, with slender elongate hooks ( Fig. 3G ).

Sixth limb five-segmented ( Fig. 3H ). First segment (= protopodite) with short d1 seta. Second, third and fourth segments (= first, second and third endopodal segments respectively) with short e, f and g setae respectively. Terminal segment (= fourth endopodal segment) with relatively long h1 seta, short h3 and well-developed h2 claw, 1.9x length of anterior sclerotized margin of first endopodal segment (indicated with black triangle on Fig. 3H ).

Seventh limb with four segments ( Fig. 4C ). One seta (d1) on basal segment. Second segment with one apical seta (e). Third segment with two setae on outer edge (f and g) (junior synonym I. haterumensis figured with one), and group of hook-like setules apically. Fourth segment with two long and one medium-length setae apically.

Caudal ramus typical of genus, ramus curved ( Fig. 3I ). Claw Gp approximately same length as Ga, seta sp long.

Female reproductive organ with one flattened lobe, sub-angular towards anterior and posterior corners ( Fig. 4D ). Organ delicate and easily distorted or damaged during dissections.

Hemipenes with outer lobe rounded distally, overlapping middle lobe ( Figs 4 E–I, black triangle indicates overlap, 5A & B). Middle lobe sub-quadrate to triangular, with thick base, widening distally, distal inner corner sharply angled, outer edge angled to rounded. Inner lobe long and thin, protruding beyond outer lobe, terminating with bul- bous end; distally variable, ranging from narrow and hook-like to slightly thicker and bulbous. Copulatory process slender, with curved outer edge and sharply pointed tip.

Zenker organ with proximal end significantly inflated compared with posterior end, and with 15–17 internal rosettes ( Fig. 6A ). Spermatozoa lengths ranging from 1007 to 1232 µm with an average of 1139 µm ( Smith et al. 2016a).

Intraspecific variation. 13% of specimens studied have tubercles present on each valve (see description for more details) ( Table 1 ), ranging from slightly to well developed, rounded to angular ( Figs 1 & 2 ). The inner and middle lobes of the hemipenis are somewhat variable in shape; some specimens have a middle lobe that is slightly wider distally than others, and the outer corner ranges from quite angular to rounded ( Fig. 4E, G & I ). The male copulatory process is slightly narrower distally in some specimens compared with others. Sizes of individuals were variable, even within one sample, with some adult specimens noticeably larger (approximately 20% longer and 14% higher) than other adults ( Fig. 7 ). The hemipenis morphology of the two size types are very similar ( Fig. 5A & B ), so we conclude that they are the same species (see Discussion). The roughened surface of the postero-ventral region of the calcified inner lamella of the left valve varies in extent, extending higher up the posterior margin in some specimens.

Remarks. The locations of the type specimens of Ilyocypris japonica and its junior synonym Ilyocypris haterumensis Okubo, 1992 (in Okubo & Terauchi 1992) were not mentioned in the original publications and enquires were unsuccessful in determining their whereabouts. The material must therefore be considered lost, and only the figures in Okubo (1990; 2004) and Okubo & Terauchi (1992) are available for identification of this species.

In the original description of I. haterumensis it was noted that it was similar to I. japonica , but the middle lobe of the hemipenis was slightly different, and this was used to justify the erection of a new species ( Okubo & Terauchi 1992). However, it was later synonymised with I. japonica by Okubo (2004), but without an explanation. The middle lobe of the hemipenis of I. japonica is somewhat variable in shape ( Figs 4E, G & I ) and the figured middle lobe of I. haterumensis does fit into this range. In the figures of I. haterumensis provided by Okubo & Terauchi (1992) the seventh limb has one seta on the third segment, and the sp seta on the caudal ramus is short, while I. japonica has two setae on the same seventh limb segment, and the sp seta on the caudal ramus is noticeably longer. These discrepancies cannot be checked because of the lack of type material. We therefore follow Okubo (2004), who observed specimens of both species and considered that the two names are synonyms. We assume that the discrepancies are due to errors, damage or abnormalities with the specimen of I. haterumensis figured by Okubo & Terauchi (1992). This is supported by our material, some of which has a very similar hemipenis morphology to that of I. haterumensis (i.e. a very similar middle lobe morphology), but two setae on the third segment of the seventh limb and a long sp seta on the caudal ramus.

Ilyocypris japonica is morphologically very similar to Ilyocypris mongolica Martens, 1991 . Ilyocypris mongolica differs from I. japonica in the following characters: it is slightly more rectangular in lateral view, with a shallower sloping dorsal margin; the pitting on the carapace is coarser; the inner lists on the calcified inner lamella are closer to the inner edge; and the copulatory process, although similar, is differently shaped ( Figs 4J & K , 5C , 8 ). The middle lobe of the hemipenis is also generally larger distally than that of I. japonica , but the variation of this character in I. japonica is quite large, so that the largest example is similar to that of I. mongolica . These morphological differences are small, but due to the different geographical (and climatic) distributions and habitats of the two species (see Distribution section below), we provisionally treat them as two separate species.

Contrary to our results, a cladistic study by Karanovic & Lee (2013) of 21 Ilyocypris species indicated that I. japonica and I. mongolica are only distantly related (see cladistic diagram Fig. 15 of Karanovic & Lee 2013). However, characters for some species were incorrectly coded in the study of Karanovic & Lee (2013) (e.g. for I. japonica characters 3, 11, 12, and 14 were incorrectly coded), and this undoubtedly accounts for the discrepancy between their cladistic results and our detailed morphological analysis. A corrected cladistic analysis of Ilyocypris species is not given herein, as an informative analysis is hindered by the lack of comprehensive descriptions for many species.

The record of I. dentifera reported from the brackish part of the Obitsu River estuary in Japan by Nakao & Tsukagoshi (2002; 2008) is possibly a misidentification of I. japonica . See under I. dentifera below for more details.

Distribution. In Japan I. japonica is known from Gunma, Okinawa and Shiga Prefectures ( Okubo & Ida 1989; Okubo 1990; Okubo & Terauchi 1992; herein) ( Fig. 9 ). The records of I. japonica reported herein from Gyeongsangnam-do and Gyeongsangbuk-do in the south east of South Korea are the first for that country (see Table 1 for more details). Its distribution corresponds to temperate to cold Köppen climatic zones with hot summers, and no dry season (zones Dfa and Cfa; Peel et al. 2007). The morphologically similar species I. mongolica , in contrast, is known from Mongolia and Inner Mongolia, China ( Martens 1991; Van der Meeren et al. 2010; Zhai & Zhao 2014), corresponding to Köppen climatic zones of arid, cold steppe (BSk), arid, cold desert (BWk) and cold, dry winters, with warm summers (Dwb) ( Peel et al. 2007) ( Fig. 9 ).

Ecology. This species can be abundant in rice fields in Japan, found in the top few millimetres of mud in the oxygenated zone. In Japan it has only been found in rice fields, but in Korea it was also collected from a lotus field ( Table 1 ). This species has so far only been found from mid May through to late July ( Okubo 1990; herein), although its appearance and disappearance in rice fields is probably strongly influenced by the rice-growing cycle rather than the seasons per se. Ilyocypris mongolica , on the other hand, has not been reported from rice fields, but from a puddle, lakes, and a saline ditch on the flood plain of a river ( Martens 1991; Van der Meeren et al. 2010; Zhai & Zhao 2014).

Figures

FIGURE 1. Ilyocypris japonica Okubo, 1990. Japanese specimens. A, female left valve, external view (LBM 1430009143, sample 6; see Table 1). B, female right valve, external view (LBM 1430009143, sample 6). C, female left valve, internal view (LBM 1430009143, sample 6). D, female right valve, internal view (LBM 1430009143, sample 6). E, female left valve, internal view, detail of postero-ventral margin (LBM 1430009143, sample 6). F, female right valve, internal view, detail of antero-ventral margin (LBM 1430009143, sample 6). G, female left valve, internal view, muscle scars (LBM 1430009143, sample 6). H, male right valve, external view (LBM 1430009141, sample 6). I, male carapace, dorsal view, anterior to right (LBM 1430009160, sample 25). J, female carapace, dorsal view, anterior to right (LBM 1430009142, sample 6). K, female carapace, tuberculated form, right lateral view (LBM 1430009159, sample 23). L, female carapace, tuberculated form, dorsal view, anterior to right (LBM 1430009159, sample 23). M, male left valve, ventral view (LBM 1430009141, sample 6). Scale bar = 500 µm for A–D, H–M, 174 µm for E–G.

FIGURE 2. Ilyocypris japonica Okubo, 1990. Korean specimens. A, female left valve, external view (LBM 1430009147, sample 15, see Table 1). B, female right valve, external view (LBM 1430009147, sample 15). C, female left valve, internal view (LBM 1430009147, sample 15). D, female right valve, internal view (LBM 1430009147, sample 15). E, female left valve, internal view, detail of postero-ventral margin (LBM 1430009147, sample 15). F, female right valve, internal view, detail of anteroventral margin (LBM 1430009147, sample 15). G, female left valve, internal view, muscle scars (LBM 1430009147, sample 15). H, male right valve, external view (LBM 1430009146, sample 15). I, male left valve, external view (LBM 1430009146, sample 15). J, female carapace, tuberculated form, right lateral view (LBM 1430009149, sample 16). K, female carapace, tuberculated form, oblique view of right side (LBM 1430009149, sample 16). Scale bar = 500 µm for A–D, H–K, 174 µm for E–G.

FIGURE 3. Ilyocypris japonica Okubo, 1990. A, antennule, male (LBM 1430009154). B, antenna, male (LBM 1430009155). C, mandibular palp, male (LBM 1430009158). D, mandibular coxa, male (LBM 1430009155). E, maxillula palp and endites (setae on endites not drawn), male (LBM 1430009154). F, fifth limb, female (LBM 1430009157). G, fifth limb palp, male (LBM 1430009154). H, sixth limb, male (LBM 1430009154), arrow and dashed line indicate length of first endopodal segment. I, caudal ramus, male (LBM 1430009155). All specimens from sample 22; see Table 1.

FIGURE 4. A–I, Ilyocypris japonica Okubo, 1990. A, detail of female antenna (LBM 1430009156, sample 22; see Table 1). B, detail of male antenna (LBM 1430009155, sample 22). C, seventh limb, male (LBM 1430009154, sample 22). D, outline of female reproductive organ, arrow indicates anterior (LBM 1430009157, sample 22). E, hemipenis (LBM 1430009154, sample 22). F, copulatory process of hemipenis (LBM 1430009154, sample 22). G, hemipenis (LBM 1430009148, sample 15). H, copulatory process of hemipenis (LBM 1430009148, sample 15). I, outlines of the hemipenes of six specimens, some reflected on the vertical axis to facilitate comparisons (left to right LBM 1430009153, sample 22; LBM 1430009152, sample 21; LBM 1430009146, sample 15; LBM 1430009145, sample 10; LBM 1430009140, sample 5; LBM 1430009139, sample 3). J & K, Ilyocypris mongolica. J, hemipenis (LBM 1430009161, sample 17). K, copulatory process of hemipenis (LBM 1430009161, sample 17).

FIGURE 5. Light microscopy photographs of Ilyocypris hemipenes. A, Ilyocypris japonica Okubo, 1990 (LBM 1430009150, sample 18; see Table 1). B, Ilyocypris japonica Okubo, 1990 (LBM 1430009151, sample 18). C, Ilyocypris mongolica Martens, 1991 (LBM 1430009161, sample 17). D, Ilyocypris dentifera Sars, 1903 (LBM 1430009119, sample 6). E, Ilyocypris angulata Sars, 1903 (LBM 1430009112, sample 20). F, Ilyocypris incus sp. nov. (DB40054, sample 14). E has been reflected on the vertical axis to facilitate comparisons.

FIGURE 6. Light microscopy photographs of Ilyocypris Zenker organs. Black triangles mark the anterior ends. A, Ilyocypris japonica Okubo, 1990 (LBM 1430009144, sample 9; see Table 1). B, Ilyocypris dentifera Sars, 1903 (LBM 1430009119, sam- ple 6). C, Ilyocypris incus sp. nov. (LBM 1430009131, sample 14).

FIGURE 7. Two male specimens of Ilyocypris japonica from the same sample (Lake Biwa Museum rice field, 14 June 2013, sample 18; see Table 1), showing the two size types, large and small. A (LBM 1430009151) & B (LBM 1430009150), external view of right valves. C (LBM 1430009151) & D (LBM 1430009150), details of surface of valves, locations marked by dotted rectangles on A & B. Scale bar = 500 µm for A & B, 94 µm for C & D.

FIGURE 8. Ilyocypris mongolica Martens, 1991.A, female left valve, external view (LBM 1430009163). B, female right valve, external view (LBM 1430009163). C, female left valve, internal view (LBM 1430009163). D, female right valve, internal view (LBM 1430009163). E, female left valve, internal view, detail of postero-ventral margin (LBM 1430009163). F, female right valve, internal view, detail of antero-ventral margin (LBM 1430009163). G, female left valve, internal view, muscle scars (LBM 1430009163). H, male right valve, external view (LBM 1430009161). I, female carapace, dorsal view, anterior to right (LBM 1430009162). Scale bar = 500 µm for A–D, H–I, 174 µm for E–G. All specimens from sample 17; see Table 1.

FIGURE 9. Distribution maps of Ilyocypris dentifera, I. angulata, I. japonica, I. mongolica, and Ilyocypris incus sp. nov. One additional fossil record of I. dentifera exists from Manitoba, Canada (Klassen et al. 1967), but is not shown on the map. As the records of Ilyocypris dentifera of Kim & Min (1991) probably at least in part refer to different species, their records are not plotted on the map. Records of I. dentifera by Huang (1986) and Huang et al. (2006) are also not plotted as they are likely to also be misidentifications. Other reports with no figures cannot be confirmed but are plotted (see text for more details).? indicates uncertain records. Abbreviations and colours of points refer to Köppen climatic zones, following Peel et al. (2007). Data from: 1, Kaiser et al. (1973). 2, Shinde et al. (2014). 3, Kulkarni et al. (2015). 4, Zhai & Zhao (2014). 5, Chen (1982; 1990). 6, Sars (1903), Chen (1982). 7, Yu et al. (2005). 8, Ma & Yu (2018). 9, Yu (2014). 10, Yu et al. (2009). 11, Victor & Fernando (1980). 12, Zenina & Schornikov (2008). 13, Sidorov & Semenchenko (2012). 14, Lee et al. (2000). 15, This study. 16, Tabuki & Tsuhako (2015). 17, Okubo (1990). 18, Broodbakker (1988). 19, Okubo (2004), this study. 20, Tanaka et al. (2015). 21, Sánchez-Bayo & Goka (2006a; 2006b). 22, Van der Meeren et al. (2010). 23, Martens (1991). 24, Zhai & Zhao (2014). 25, This study. 26, Okubo & Terauchi (1992). 27, This study. 28, Okubo (1990). 29, Nakao & Tsukagoshi (2002; 2008). 30, This study. 31, Okubo (1974).

FIGURE 15. Ilyocypris incus sp. nov. A, antennule, male (DB40054). B, antenna, male (LBM 1430009132). C, mandibular palp, female (LBM 1430009136). D, mandibular coxa, female (LBM 1430009134). E, maxillula palp and endites (setae on endites not drawn), female (LBM 1430009136). F, fifth limb, female (DB40055). G, sixth limb, male (LBM 1430009132), arrow and dashed line indicate length of first endopodal segment. H, fifth limb palp, male (DB40054). All specimens from sample 14; see Table 1.