Loxoconcha kamiyai, Ozawa & Ishii, 2008

Ozawa, Hirokazu & Ishii, Tohru, 2008, Taxonomy and sexual dimorphism of a new species of Loxoconcha (Podocopida: Ostracoda) from the Pleistocene of the Japan Sea, Zoological Journal of the Linnean Society 153 (2), pp. 239-251 : 241-249

LOXOCONCHA KAMIYAI SP. NOV.

( FIG. 2)

Loxoconcha sp. 1 Ozawa, 1996: 112 , pl. 6, fig. 10.

Etymology: In honour of Dr Takahiro Kamiya (Kanazawa University, Japan), an expert in the phylogeny, speciation and copulatory behaviour of Loxoconcha from the western Pacific region.

Types: Holotype, female, right valve, MPC-03671, from sample C505 ( Fig. 2A). Paratypes, female, right valve, MPC-03672, from sample C304 ( Fig. 2E); male, right valve, MPC-03673, from sample C402 ( Fig. 2C); female, left valve, MPC-03674, from sample C501 ( Fig. 2F); female, left valve, MPC-03675, from sample C506 ( Fig. 2B); male, left valve, MPC-03676, from sample C506 ( Fig. 2D, J); male right valve, MPC- 03677, from sample C304 ( Fig. 2G) .

Type locality: Sakuramachi , Oyabe City, Toyama Prefecture, central Japan (36°41.1′N, 136°52.1′E) of Ozawa & Kamiya (2001) from the early Pleistocene Omma Formation, central Japan ( Fig. 1 ).

Diagnosis: Carapace subrhomboidal in lateral view, and medium-sized. Dorsal and ventral margins slightly curved, slightly concave in ventral margin at one-third of carapace length. Valve surface covered with round fossae in anterior and ventral areas, and numerous fine pits in marginal areas, but sparse and smooth surface areas observed at median part, in and around adductor muscle field. Round fossae arranged in concentric rows running subparallel to antero-ventral, mid-ventral and postero-ventral margins. Two weak radial ridges in mid-anterior and antero-ventral areas extending anteriorly. Three weak crests in postero-dorsal corner, mid-posterior area and postero-ventral corner.

Description: Valves subrhomboidal in lateral view, and medium-sized ( Fig. 2). Dorsal and ventral margins slightly curved, slightly concave in ventral margin at one-third of carapace length. Greatest length near mid-height, and greatest height near mid-length. Anterior margin obliquely rounded. Posterior margin truncated obliquely in upper half and lower half, making blunt angle slightly above mid-height.

Valve surface covered with round fossae in anterior and ventral areas, and numerous fine pits in marginal areas ( Fig. 2A–D). Round fossae arranged in concentric rows running subparallel to anteroventral, mid-ventral and postero-ventral margins. Sparse ornamentation and smooth surface areas at median part, in and around adductor muscle field. Two weak radial ridges in mid-anterior and antero-ventral areas extending anteriorly. Three weak crests found in postero-dorsal corner, mid-posterior area and postero-ventral corner, respectively. Eye tubercle round and not distinct. Carapace surface covered with a total of 85 pore systems in the adult, comprising 68 normal pore systems having sieve plates 0.01–0.02 mm in diameter, and 17 marginal pore systems c. 0.005 mm in diameter; a total of 75 pore systems are found in the A- 1 juvenile ( Fig. 3 ; Table 1 ).

Hingement: gongylodont; right valve with single tooth surrounded by horseshoe-shaped depression in anterior element; numerous fine teeth in median element; few small teeth and one large horseshoeshaped tooth in posterior element, with large socket opening ventrally ( Fig. 2E–G). Hinge line slightly curved. Muscle scars: four adductor scars; two separate frontal scars; two subrounded mandible scars. Vestibules present along anterior and posterior · margins, relatively deep along antero-ventral margin ( Fig. 2E–G). Marginal infoldment moderately broad, especially in anterior half.

Sexual dimorphism distinct ( Fig. 2A–F). Carapace of male more slender in lateral view. Dorsal margin slightly rounded in female, in lateral view. The anterior element in the hingement of female (0.04 mm in width) is twice as wide as that of male (0.02 mm in width).

Dimensions (mm): Holotype, L = 0.65, H = 0.43 (female, right valve, MPC-03671). Paratypes, L = 0.63, H = 0.41 (female, right valve, MPC-03672); L = 0.68, H = 0.39 (male, right valve, MPC-03673); L = 0.61, H = 0.42 (female, left valve, MPC-03674); L = 0.61, H = 0.40 (female, left valve, MPC-03675); L = 0.73, H = 0.40 (male, left valve, MPC-03676); L = 0.68, H = 0.40 (male, right valve, MPC-03677).

Occurrence: Pliocene and Pleistocene, on the Japan Sea coast, Japan ( Fig. 1 ); early and late Pliocene Ogikubo Formation, late Pliocene Yabuta, Sasaoka and Junicho formations, and early Pleistocene Omma, Nishiyama, Haizume, Daishaka, Kawachi, Kaidate and Shichiba formations.

Remarks: This species is similar to Loxocorniculum mutsuense defined by Ishizaki (1971: pl. 5, fig. 11; pl. 6, figs 3, 6, 7; pl. 7, fig. 5) from Recent sediments in Aomori Bay, north-eastern Japan, in general external carapace ornamentation and lateral outline. However, it differs from Loxocorniculum mutsuense in the lack of one normal pore system in the median area ( Fig. 3 ; Table 1 ), its rounded outline in lateral view and the nature of the valve surface. Reticulations covering the whole carapace surface and two radial ridges in the mid-anterior and antero-ventral parts are weaker, and are not distinct in the present species. Three radial ridges in the posterior area are weaker in this species. A horn-like protuberance in the posterodorsal corner is not developed in the present species. Sparse ornamentations and smooth surface areas at the median part, in and around the adductor muscle field, are observed in the present species, but not in Loxocorniculum mutsuense .

The present species is also similar to Loxoconcha pentoekensis Kingma, 1948 , figured by Zhao & Whatley (1989: pl. 2, figs 9, 10), from Pliocene and Pleistocene strata in eastern Java, Indonesia, in general external carapace ornamentation. However, it differs from Loxoconcha pentoekensis by its slightly curved dorsal outline in lateral view and the nature of the valve surface. Two weak radial ridges in the mid-anterior and antero-ventral parts and three weak radial crests in the posterior area are found in the present species. A large ear-like protuberance in the postero-dorsal corner is not developed. Sparse ornamentations and smooth surface areas at the median part are found.

Loxoconcha kamiyai has some variability in (1) development of rounded fossae in the anterior marginal and posterior marginal areas, (2) development of two antero-radial ridges and three weak posterocrests, (3) areas of sparse ornamentation and smooth surface parts in the median area, and (4) areas covered by fine pits and fossae in anterior, ventral and posterior margins.

DISCUSSION

PHYLOGENETIC RELATIONSHIP BASED ON THE DISTRIBUTION OF PORE SYSTEMS

The number, distribution and differentiation of pore systems on the carapace during ostracod ontogeny were studied to determine the phylogenetic relationships among ostracod species. The reconstruction of ostracod phylogeny by analysing pore systems was first proposed by Tsukagoshi (1990) for the 14 species in the genus Cythere O. F. Müller, 1785 . This work was followed by Irizuki (1993), who studied 21 species in eight genera of hemicytherinae ostracods, and Ishii et al. (2005), who investigated 17 species in the genus Loxoconcha . Kamiya (1997) named the phylogenetic reconstruction method proposed by Tsukagoshi (1990) ‘differentiation of distributional pattern of pore systems (DDP) analysis’. The distribution of pore systems in Loxoconcha kamiyai was examined with this method and the results were compared with the pore system data for other Loxoconcha species published by Ishii et al. (2005).

On the basis of the DDP results for its adult and A- 1 juvenile stages, Loxoconcha kamiyai is judged to be the species most closely related to Loxocorniculum mutsuense , in the family Loxoconchidae . Both species have the same total number of normal and radial pore systems on the carapace at the A- 1 juvenile stage (75 pore systems per valve, Table 1 ). The difference in total number of pore systems in the adult stage is just one normal pore system between the two species ( Table 1 ), which is missing on the central area in Loxoconcha kamiyai ( Fig. 3 ). Furthermore, only these two species have seven marginal pore systems at the postero-ventral to mid-posterior margins at the adult and A- 1 juvenile stages; the other 16 species, including Loxoconcha japonica Ishizaki, 1968 , have just five marginal pore systems in the postero-marginal areas at the adult and A- 1 juvenile stages (T. Ishii, unpubl. data). This character is unique among the species of Loxoconcha from Japan (T. Ishii, unpubl. data), and strongly suggests a very close phylogenetic position between these two species within the genus Loxoconcha . This assessment is also supported by similar surface ornamentations, such as the existence of two radial ridges in the anterior area.

Loxoconcha species from Japan can be divided into two groups (A and B) on the basis of the distributional patterns of their pore systems ( Ishii et al., 2005), especially the pore pattern below the eye tubercle (PBE analysis of Ishii et al., 2005). This division reflects phylogenetically related groups within the genus. PBE analysis in this study reveals the L-shaped pore pattern of Ishii et al. (2005) below the eye-tubercle in Loxoconcha kamiyai (see v, w, x, y and z in Fig. 4 ); it differs from their ‘upside-down L-shape’ pattern. We therefore consider that this species belongs to their Group A, which also includes Loxocorniculum mutsuense ( Fig. 5 ). This result for Loxoconcha kamiyai corresponds well with the phylogenetic relationships of the species in the genus Loxoconcha from Japan proposed by Ishii et al. (2005).

The genus Loxocorniculum was established by Benson & Coleman (1963) primarily on the basis of modern specimens of Loxocorniculum fischeri (Brady, 1869) from the Caribbean Sea near Panama. It is characterized by a horn-like protuberance on the postero-dorsal corner of the carapace. However, except for the horn-like protuberance, the appearance of the carapace of the species in this genus, including Loxocorniculum mutsuense Ishizaki, 1971 from Japan, is very similar to that of the genus Loxoconcha as noted by Ishii et al. (2005). The phylogenetic independence of Loxocorniculum in Japan as a genus distinct from Loxoconcha has been debated. Therefore, we tentatively include Loxocorniculum mutsuense , proposed as a new, extant species from Japan by Ishizaki (1971), in the genus Loxoconcha following the opinion of Ishii et al. (2005).

MODE OF LIFE AND MICROHABITAT

Loxoconcha kamiyai has a round carapace outline in lateral view and a ‘rugby-ball’ shape in posterior view with a convex ventral area ( Fig. 2A–D, K). These morphological characters are common in phytal-dwelling ostracods, including Loxoconcha species , in relation to their microhabitats and life style – e.g. Loxoconcha japonica Ishizaki, 1968 and Loxocorniculum mutsuense live on the leaf surfaces of marine plants such as Zostera ( Kamiya, 1988) . This clearly differs from the bottom-dwelling species that inhabit the surface of the sand bottom, which show an elongate outline in lateral view and a triangular shape in posterior view with a flat ventral plane, e.g. Loxoconcha uranouchiensis Ishizaki, 1968 ( Kamiya, 1988) . Although it became extinct during the Pleistocene, Loxoconcha kamiyai is therefore inferred to have been a phytal-dwelling species on the basis of its carapace shape.

GEOGRAPHICAL AND GEOLOGICAL DISTRIBUTION OF TWO SPECIES AND THEIR ORIGIN AND EXTINCTION–SURVIVAL

Based on the oldest fossil record, Loxoconcha kamiyai and Loxocorniculum mutsuense first appeared in Japan during the Pliocene, around 3 Myr ago. The oldest record of Loxoconcha kamiyai is from the Pliocene Ogikubo Formation at the Japan Sea side of central Japan ( Fig. 1 ; c. 3.5 Ma, fide Nagamori, Furukawa & Hayatsu, 2003). The oldest record of Loxocorniculum mutsuense is from the Pliocene Ananai Formation on the Pacific side of southwestern Japan ( Fig. 6; Ishizaki, 1983; c. 3 Ma, fide Iwai et al., 2006). Therefore, it is still difficult to specify which is the ancestral species on the sole basis of their fossil records. The genus Loxoconcha has southern origins, and shows high species diversity in areas affected by the modern warm Kuroshio Current along the western Pacific coasts and in East and Southeast Asia. So Loxocorniculum mutsuense , first appearing along Pacific coasts during the Pliocene, might be the probable ancestral species of Loxoconcha kamiyai , distributed only along Japan Sea coasts.

According to its geographical and geological occurrences ( Fig. 1 ), Loxoconcha kamiyai is judged to be a formerly endemic species restricted to the Pliocene– Pleistocene of the Japan Sea. Therefore, its origin appears to be along the coasts of the Japan Sea, and this species would have been extinct for the last 0.5 Myr, based on the youngest fossil record from the Shichiba Formation in central Japan ( Fig. 1 ; age fide Kato et al., 1995). The period of extinction of this species is the same as those of 23 now extinct, formerly endemic species in the Japan Sea in three families, the Hemicytheridae , Cytheruridae and Eucytheridae , as reported by Ozawa & Kamiya (2005b), Ozawa (2006) and H. Ozawa (unpubl. data). These 23 species would have become extinct because of low-salinity water at the Japan Sea surface during glacial and corresponding low sea-level periods since the early Pleistocene related to glacio-eustatic sealevel changes. These species probably only inhabited open-marine environments in shallow areas, and could not have lived in low-salinity areas such as the brackish inner bay ( Ozawa & Kamiya, 2005b).

As for these 23 species, the palaeo-occurrence of Loxoconcha kamiyai is also inferred to have been restricted to shallow, open, marine environments on the basis of its fossil occurrence with shallow, openmarine ostracods from Pleistocene strata ( Ozawa, 1996). It would also have become extinct during the Pleistocene because of its narrow ecological niche and salinity tolerance.

Loxocorniculum mutsuense first appeared along the Pacific coast around 3 Myr ago and migrated into the Japan Sea around 2 Myr ago in view of its oldest fossil record on the Japan Sea coast from the Pliocene Sasaoka Formation in northern Japan ( Fig. 5 ; age fide Yamada, Irizuki & Tanaka, 2002). Its first appearance in the Japan Sea is more than 1 Myr later than that of Loxoconcha kamiyai . Therefore, the origin of Loxocorniculum mutsuense appears to be the Pacific coast in or around Japan.

Thereafter, this species expanded its range, probably by floating on the leaves of marine plants, and became widely distributed on the coasts of the Pacific Ocean, Japan Sea, Yellow Sea and Bo-Hai Sea coasts until today ( Figs 6, 7 ). Loxocorniculum mutsuense is found in both open-marine and inner-bay environments ( Ishizaki, 1971; Zhou, 1995), where it was able to survive because of its wide salinity tolerance. This ecological tolerance may have allowed this species to have a wider distribution in East Asia than Loxoconcha kamiyai .

SEXUAL DIMORPHISM IN HINGEMENT

These two species in the family Loxoconchidae , Loxoconcha kamiyai and Loxocorniculum mutsuense , commonly show a unique and remarkable sexual dimorphism in the adult stage, especially in the anterior element of the hingement ( Figs 8 , 9 ). On the right valve, the anterior hingement element of the adult male is commonly smaller and rounder than that of the adult female. Its shape is very similar to the small, round anterior element of its A- 1 juvenile stage. The anterior element of the female hingement is larger and more rectangular than that of either the male or the A- 1 juvenile stage ( Figs 8 , 9 ).

These morphological characters of Loxoconcha kamiyai are seen in specimens from different geological ages and separate geographical areas, i.e. in fossil specimens from the Omma Formation near the Noto Peninsula ( Figs 1 , 2; 1.7–1.4 Ma; age fide Takata, 2000) and the Kaidate Formation on Sado Island ( Figs 1 , 8 ; 0.9 Ma, fide Kato et al., 1995). The same character is found in Loxocorniculum mutsuense from different geological ages and in fossil specimens from areas such as the Omma Formation near the Noto Peninsula ( Fig. 6; 1.7–1.4 Ma) (H. Ozawa, unpubl. data) and the Kaidate Formation on Sado Island ( Figs 6, 9 ; 0.9 Ma), and also on modern specimens from Aomori Bay in northern Japan ( Fig. 7 , a; Ishizaki, 1971) and the Seto Inland Sea, south-western Japan ( Fig. 7 , h; Okubo, 1980).

Ishizaki (1971) only briefly mentioned this sexual dimorphism in modern specimens of Loxocorniculum mutsuense from Aomori Bay. He referred to a ‘hinge structure delicate in male but stronger (bold) in female; with prominent tooth within anterior socket of right valve’ (p. 90) in his systematic description of that species. However, he did not show clear illustrations of these dimorphic characters for comparison. Furthermore, Okubo (1980) redescribed Loxocorniculum mutsuense from the Seto Inland Sea, with a carapace sketch from an internal view of the female right valve. His illustration ( Okubo, 1980: 425, fig. 17b) shows the large anterior tooth of the hingement on the female of this species. However, he did not refer to this character or the morphology of the male’s hingement in the text of his description.

We therefore conclude that this dimorphic morphology is a stable character within each species, and not a geographical or geological variation within one species.

Taking the female’s hingement as a standard, the male’s morphological characters in these loxoconchid species can be explained as a kind of heterochrony, i.e. paedomorphosis. These paedomorphic examples of podocopid hingements have been found in two different species in 11 pairs of five families – the Cytheridae , Leptocytheridae , Hemicytheridae , Cytheruridae and Loxoconchidae within the superfamily Cytheroidea – from the Miocene to the present ( Tsukagoshi, 1994; Tsukagoshi & Kamiya, 1996). However, this is the first report of the remarkable morphological difference in the anterior hingement element between the male and female together with the A- 1 juvenile within the same species in other families of ostracods.

Perhaps this is because few publications show clear illustrations of the hingements of males and females together with A- 1 juveniles, especially for ostracod taxa having hingements of complicated rather than simple morphology, e.g. adont and lophodont types. We know of only one example for comparison with the number of teeth per one gongylodont hingement in the adult male, female and A- 1 juvenile: Loxoconcha uranouchiensis ( Kamiya, 1992) . It may be expected that sexual dimorphism and paedomorphosis of the complicated-type hingement will be found in other species or families of Cytheroidea and in podocopid ostracods if hingements of males, females and A- 1 juveniles are examined by SEM.

It is still unclear why only two species of this species-group having seven radial pore systems at the posterior margin in the genus Loxoconcha show sexual dimorphism and paedomorphosis in the anterior element of the hingement. The sexual dimorphism of the hingement appears not to be directly related to its functional morphology for copulatory behaviour in these phytal species. The anterior element of the hingement is located on the inner area of the carapace at the anterodorsal margin; this is furthest from the copulatory organ that stretches out from the posteroventral area when the ostracods copulate.

A kind of sexual dimorphism and paedomorphosis of the inner marginal area of the ostracod carapace has also been reported in a freshwater podocopid, Vestalenula cornelia Smith, Kamiya & Horne, 2006 in the Family Darwinulidae ( Smith et al., 2006) , although in this case it is not on the hingement. According to that study, the sexual dimorphism in Vestalenula cornelia is found along the ventral edge of the valve. The male has two internal tooth-shaped structures on the left valve, while the female has a single internal tooth on the left valve. Furthermore, the female has a keel-shaped structure on the right valve, which is lacking in the male. It is interesting that the A- 1 juvenile of this species has a similar arrangement to that of the male with a similar carapace length–height and lateral outline ( Smith et al., 2006). Thus, this male also exhibits paedomorphic morphology.

We propose a speculative hypothesis for this interesting problem on the basis of these two paedomorphic examples. We suggest that the adult males of marine podocopid ostracods may have originated from the adult female by paedomorphosis in ancient times, i.e. the early Palaeozoic. The gongylodont hingement, characteristic of the family Loxoconchidae , is generally considered to be one of the most complicated and evolved hingements among all families of podocopid ostracods since the late Cretaceous (e.g. Horne, 2003). Thus, this most evolved hingement in loxoconchid ostracods in the late Cenozoic would have by chance exhibited atavistic features. These may have been common in the ancient and primitive ancestors of marine ostracods, although most podocopid ostracods had already lost these characters by the early Cenozoic. This kind of sexual dimorphism in ostracod hingements may be much easier to find in more complicated hingements than in simpler and more primitive hingements such as the adont or lophodont types.

Non-marine ostracods are considered to have originated and diversified from marine ostracods several times during the Palaeozoic (e.g. Horne, 2003). Therefore, the sexual dimorphism and paedomorphosis in the hingement of a marine species, Loxoconcha kamiyai , and in structures on the internal ventral margin of a freshwater species, Vestalenula cornelia , may be an interesting perspective for discussing the origin of male ostracods and the history of their sexual dimorphism together with paedomorphosis for geologically long periods (i.e. since the Palaeozoic). It will be necessary to collect data regarding sexually dimorphic characters on the carapaces of many ostracod taxa with heterochronic morphology since the early Palaeozoic, by examining the excellent fossil records from marine and non-marine environments worldwide.

Figures

Figure 1. Geographical and geological occurrences of Loxoconcha kamiyai sp. nov. based on original data, except for data from the Omma Formation cited from Ozawa (1996). Fm: Formation.

Figure 3. Distributional pattern of pore systems in adult left valve of Loxoconcha kamiyai sp. nov. Position of one missing pore system of this species is determined by comparison with the distributional pattern of pore systems of Loxocorniculum mutsuense Ishizaki, 1971 (Ishii et al., 2005).

Figure 4. Patterns of normal pore systems below the eye tubercle by PBE analysis of Ishii et al. (2005) for the adult left valve of Loxoconcha kamiyai sp. nov., based on Figure 3. Pore systems with italic letters (v–z) are the same as those of Ishii et al. (2005), respectively. etb: eye tubercle.

Figure 5. Results of DDP analysis for 17 loxoconchid species and Loxoconcha kamiyai sp. nov., modified from Ishii et al. (2005). Numbers indicate total numbers of pore systems for each lineage and stage. Trees drawn by hand.

Figure 7. Recent geographical occurrences of Loxocorniculum mutsuense Ishizaki, 1971, based on data from previous studies.

Figure 8. Comparison of lateral view (adult female, A-1 juvenile, adult male) of inner right valve of Loxoconcha kamiyai sp. nov. A, lateral view from inside. B, close-up view of anterior hingement element. C, sketch of anterior hingement element (= B). Upper row: adult female; middle row: A-1 juvenile; lower row: adult male. All specimens from the early Pleistocene Kaidate Formation, central Japan.

Figure 9. Comparison of lateral view (adult female, A-1 juvenile, adult male) for right valve of Loxocorniculum mutsuense Ishizaki, 1971. A, external lateral view. B, internal lateral view. C, close-up view of anterior hingement element. Upper row: adult female; middle row: A-1 juvenile; lower row: adult male. All specimens from the early Pleistocene Kaidate Formation, central Japan.