Palaeontologia Electronica palaeo-electronica.org Late Pleistocene-Holocene amphibians from Okinawajima Island in the Ryukyu Archipelago, Japan: Reconfirmed faunal endemicity and the Holocene range collapse of forest-dwelling species Yasuyuki Nakamura and Hidetoshi Ota ABSTRACT Amphibian fossils excavated from two Late Pleistocene-Holocene fissures in the southern part of Okinawajima Island in the Ryukyu Archipelago were identified through detailed comparisons with skeletal specimens of extant taxa. The identified species (eight frogs and two newts) were confined to extant elements on the island and were mostly endemic to either the island or the central part of the archipelago including it. Previous Late Pleistocene records of extralimital frogs (two mainland Japanese spe- cies [Glandirana rugosa and Rana tagoi] and one Southeast Asian frog currently natu- ralized in the Ryukyus [Polypedates leucomystax]) from one of the study sites (the Minatogawa Fissure) are therefore considered misidentifications. This may also be the case with Fejervarya kawamurai, a synanthropic frog currently widely distributed in East Asia, including the Central Ryukyus. Of the species obtained from the Late Pleis- tocene deposits at these sites, five frogs (Limnonectes namiyei, Babina holsti, Odor- rana ishikawae, O. narina, and Rana ulma) are forest-dwellers currently confined to the northern forested area of Okinawajima. Additionally, none of these species were detected in the middle Holocene deposits from one of the sites, the Sashiki Fissure. Our findings indicate that the southern limestone area of Okinawajima in the Late Pleistocene harbored a dense and humid forest with diverse lotic habitats, similar to the northern forested area of the island at present, and that these environmental condi- tions were lost by the midpoint of the Holocene Period. Yasuyuki Nakamura. Tropical Biosphere Research Center, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan. [email protected] Hidetoshi Ota. Institute of Natural and Environmental Sciences, University of Hyogo, and the Museum of Nature and Human Activities, Yayoi-gaoka 6, Sanda, Hyogo 669-1546, Japan. [email protected] Keywords: Biogeography; frogs; limestone; newts; paleoenvironment PE Article Number: 18.1.1A Copyright: Palaeontological Association January 2015 Submission: 6 August 2014. Acceptance: 19 December 2014 Nakamura, Yasuyuki and Ota, Hidetoshi. 2015. Late Pleistocene-Holocene amphibians from Okinawajima Island in the Ryukyu Archipelago, Japan: Reconfirmed faunal endemicity and the Holocene range collapse of forest-dwelling species. Palaeontologia Electronica 18.1.1A: 1-26. palaeo-electronica.org/content/2015/935-okinawan-amphibians NAKAMURA & OTA: OKINAWAN AMPHIBIANS INTRODUCTION are currently strictly confined to the northern for- ested hilly area of the island is astonishing (Ota, Original anthropological excavation at the 2003). This is because the habitat requirements of Minatogawa Fissure on Okinawajima Island of the these frogs (dense forest for adults and shallow Ryukyu Archipelago from 1968 to 1974 resulted in streams under forest cover for juvenile growth; the discovery of a number of Late Pleistocene e.g., Utsunomiya et al., 1983) are quite incompati- human bones (Kaifu and Fujita, 2012; and litera- ble with the inherent properties of the Pleistocene ture cited therein) and numerous associated limestone substrate that predominates in the remains of other terrestrial vertebrates (e.g., Hase- southern part of Okinawajima — high porosity gawa, 1980; Kawamura, 1989; Matsuoka, 2000). (Maekado, 1989) and karstic topography, which The amphibian fossil assemblage was reported to can absorb surface freshwater habitats (Nishijima contain a total of 10 or 11 (if “Rhacophorus sp.” et al., 1974; Tachihara, 2003). In fact, the southern was counted) anurans and one newt species part of the island, particularly the limestone areas, (Hasegawa, 1980). However, the assemblage has lack such lotic habitats and therefore the four often been regarded as unusual because the pres- extant frogs and two newts in the region (Fejer- ence of some of the component species exhibited varya kawamurai, Ryukyu Narrow-mouthed Toad an obvious discrepancy with a biogeographers’ Microhyla okinavensis, Ryukyu Kajika Frog Buer- view of the archipelago and the intrinsic character- geria japonica, Okinawa Green Tree Frog Rhaco- istics of the Pleistocene limestone substrate of the phorus viridis viridis, Sword-tailed Newt Cynops southern part of the island, where the fissure is ensicauda, and Anderson’s Crocodile Newt Echi- located (e.g., Ota, 2003). notriton andersoni) are mostly lentic breeders. From the biogeographical viewpoint, the fossil Hasegawa (1980) left several questions unan- occurrence of two ranid species (Wrinkled Frog swered because he simply listed the taxa identified Glandirana rugosa and Tago’s Brown Frog Rana in the Minatogawa Fissure without providing infor- tagoi) known only from mainland Japan and adja- mation to verify his species identification. In addi- cent islets (Maeda and Matsui, 1999; Frost, 2014) tion, the lack of a follow-up study has prevented us remarkably contradict the highly endemic nature of from ascertaining the exact state of the Late Pleis- the current terrestrial vertebrate fauna of the Cen- tocene amphibian fauna of the island as well as its tral Ryukyus (i.e., the Amami and Okinawa Island biogeographical/paleoenvironmental significance. Groups and some nearby islands). This current Here we report on Late Quaternary amphibian fos- state unequivocally reflects the long-standing isola- sils recovered from two limestone fissures located tion of this region from nearby landmasses, partic- in the southern limestone area of Okinawajima. ularly the more northern areas of Japan (e.g., One of the sites is the Minatogawa Fissure, which Okada and Koba, 1931; Ota, 1998; Matsui, 2005; was recently re-excavated in an anthropological Motokawa, 2009). Indeed, the extant indigenous survey. Both of the limestone fissures yielded an amphibian fauna of the Central Ryukyus (11 out of abundance of Late Pleistocene amphibian fossils, 14 species are endemic) does not share its compo- and middle Holocene amphibian remains were dis- nent species with mainland Japan, except for the covered at one of the sites. These fossils are ade- Marsh Frog Fejervarya kawamurai (formerly known quate to document snapshots of Late Quaternary as Rana or Fejervarya limnocharis), a widely dis- local amphibian fauna and provide information tributed dicroglossid frog that ranges from Honshu about changes in the paleoenvironmental condi- (mainland Japan) through the Central Ryukyus and tions in the area. Taiwan to Central-South China (Djong et al., 2011). To explain the biogeographical peculiarity of the MATERIAL AND METHODS Central Ryukyu populations, some researchers argue that the species reached this location Geological Settings through relatively recent oversea dispersals from Okinawajima (ca. 1200 km2) is a narrow the Eurasian Continent (Toda et al., 1997; Toda, island oriented on a NE-SW axis with a maximum 1999) (see Discussion). length of 100 km (Figure 1). The island consists of From a paleoenvironmental perspective, the two geologically contrastive components: the fossil occurrence of five obligate forest-dwelling northern part is comprised mainly of pre-Neogene frog species (Namiye’s Frog Limnonectes namiyei, strata (e.g., Fujita, 1989) and the southern part is Holst’s Frog Babina holsti, Ishikawa’s Frog Odor- composed of the Plio-Pleistocene Shimajiri Group rana ishikawae, Okinawa Tip-nosed Frog O. (siltstone associated with tuff), Pleistocene Chinen narina, and Ryukyu Brown Frog Rana ulma) that 2 PALAEO-ELECTRONICA.ORG FIGURE 1. Maps of the Ryukyu Archipelago (1, 2) and Okinawajima Island (3). The map of Okinawajima shows topography, distribution of the Pleistocene limestone, and study sites. Geological data were obtained from Kizaki (1985). Formation (calcareous sandstone and sandy lime- rhacophorine frog believed to have been intro- stone), and Pleistocene Ryukyu Group limestone duced to the Ryukyus in the mid-20th century (see (e.g., Sagae et al., 2012). The Ryukyu Group dis- Discussion); presumably this frog corresponds to tributed in the southern part is divided into three “Rhacophorus sp.” in Hasegawa (1980). Although sections: the Itoman Formation (Early Pleisto- we were unable to examine the amphibian fossils cene), Naha Formation (Early to Middle Pleisto- discussed by Hasegawa (1980) and Nokariya cene), and Minatogawa Formation (presumably (1983b), we investigated unsorted fossils collected Late Pleistocene) (see Sagae et al., 2012). in the recent (1998–2001) anthropological excava- tion at the fissure (see Hashimoto et al., 2002 for Study Sites details). These fossils were collected by water The amphibian fossils examined here were screening. Part of the fossils were reported to con- derived from two limestone fissures located in the tain one vertebra of Limnonectes namiyei, one southern part of Okinawajima Island (Figure 1). right ilium of Babina holsti, one vertebra of Odor- Minatogawa Fissure (26° 07' 46" N, 127° 45' 34" rana narina, 41 miscellaneous bones of unidenti- E; elevation: 20 m a.s.l). The Minatogawa Fissure fied anurans, and 79 precaudal/caudal vertebrae of in Nagamou, Yaese Town, is located on a bank of unidentified newts (Nohara and Irei, 2002). How- the Yuhi River (0.5 km from the mouth of the river), ever, we did not confirm these records except for on the southeastern coast of the island. It is a crev- B. holsti because most of the fossils discussed by ice formed in the Minatogawa Formation of the Nohara and Irei (2002) could not be identified (pre- Ryukyu Group (e.g., Tsuchi, 1982). As mentioned sumably, they are included in the studied material). above, Hasegawa (1980) reported 11 or 12 spe- The age of the Minatogawa fossils examined cies of amphibians and their relative quantities here is estimated as the latest Late Pleistocene. An (Table). Of these, Glandirana rugosa (as Rana Accelerator Mass Spectrometry (AMS) 14C age of rugosa) and Rana tagoi are known as mainland 13,460 ± 110 BP (ca. 15,670 cal. BP: calibrated Japanese species and there is no other record using Fairbanks0107 [Fairbanks et al., 2005]) was from the island or the Central Ryukyus (see reported by Hashimoto et al. (2002) for a sample of above). Additionally, Nokariya (1983b) mentioned sediment humates from deposits located at the the fossil occurrence of Polypedates leucomystax base of the fissure, from which all the amphibian (as Rhacophorus leucomystax), a Southeast Asian fossils were derived. The fossils examined here 3 NAKAMURA & OTA: OKINAWAN AMPHIBIANS TABLE. Amphibian taxa and abundance (in minimum number of individuals [MNI]) from two Late Pleistocene-Holo- cene fissures in Okinawajima, and a comparison with the results of Hasegawa (1980). - indicates absence of the fossil, * denotes extralimital taxa (mainland Japanese species: Glandirana rugosa and Rana tagoi; Southeast Asian species: Polypedates leucomystax), and ** denotes a taxon mentioned by Nokariya (1983b). Species Hasegawa (1980) This study Minatogawa Fissure Minatogawa Fissure Sashiki Fissure (Late Pleistocene) (Late Pleistocene) Lower unit Upper unit (Late Pleistocene) (middle Holocene) Anura Fejervarya kawamurai “rare” - - - Limnonectes namiyei “rare” 1 1 - Babina holsti “rare” 2 6 - Glandirana rugosa* “abundant” - - - Odorrana ishikawae “common” - 7 - O. narina “abundant” 40 5 - Rana tagoi* “rare” - - - R. ulma “abundant” 49 152 - Microhyla okinavensis “rare” - - 2 Buergeria japonica - 1 - 1 Rhacophorus viridis viridis “rare” 1 6 1 Rhacophorus sp. (or Polypedates “rare” - - - leucomystax*)** Caudata Cynops ensicauda “common” 20 51 1 Echinotriton andersoni - 1 92 - are housed at the Yaese Town Museum of History effort for stratigraphic control at the excavation site and Folklore, Yaese Town, Okinawa Prefecture, was limited due to the infill, particularly in the lower Japan (YMHF-MA; we provisionally assigned the unit, which had collapsed and was largely abbreviation for the institution and the collection exposed. Fossils were gathered using dry or wet number). screening (1 mm mesh). Some of the fossils were Sashiki Fissure (26º 09’ 82” N, 127º 48’ 32” E; collected by Mr. Mitsuru Moriguchi and courteously elevation: 160 m a.s.l.). The Sashiki Fissure provided for this study. (Moriguchi, 2003; “Chinen Fissure” in Azuma, The sediments of the lower unit had a height 2007) in Sashiki-Tedokon, Nanjo City, lies ca. 6 km of approximately 2.2 m and were composed of dark northeast of the Minatogawa Fissure (Figure 1) brown clayey soil with limestone debris. The exact and is situated on an uplifted terrace of the Naha amount of the sediments we examined is unknown, Formation on the Chinen Peninsula. This fissure is but it was at least double the amount of the upper a sinkhole (ca. 8 m in depth) that was exposed by unit (see below). Most of the fossils from the lower limestone mining (Figure 2). Our excavation at the unit have been dated to the Late Pleistocene fissure was conducted from 2004–2008. Because because a fragment of charcoal collected 1 m from the remnant infill consisted of two discrete compo- the bottom produced an AMS 14C age of 31,745 ± nents, we treated the sediments separately as fol- 216 cal. BP (Conventional Radiocarbon Age: lows: the “lower unit” formed at the base and the 26,480 ± 150 BP; δ 13C [measured using AMS]: - “upper unit” deposited on a shelf (Figure 2). Our 27.96 ± 0.89 ‰; sample number: IAAA-80231; cali- 4 PALAEO-ELECTRONICA.ORG FIGURE 2. Photograph of the Sashiki Fissure (left) and schematic figure showing the structure of the fissure (right). In the right figure, broken lines represent the outline of the fissure behind rock, shaded areas represent studied sed- iments, and open circles represent the locations of the dating samples. bration curve used: Fairbanks0107, same hereaf- ered a metacarpal fragment of the extinct Ryukyu ter; this and the following radiometric dates were Deer Cervus astylodon and numerous fossils of the measured by the Institute of Accelerator Analysis Okinawa Spiny Rat Tokudaia muenninki, the Ltd. [IAA], Kawasaki, Japan). However, a land snail Amami Woodcock Scolopax mira, and the Oki- (Cyclophorus turgidus) shell from the bottom of the nawa Rail Gallirallus okinawae, which are not cur- sediment yielded a relatively younger age of rently found on this part of the island. Those 28,729 ± 185 cal. BP (24,000 ± 120 BP; -7.21 ± remains were derived from various sized animals, 0.46 ‰; IAAA-80228). A C. turgidus shell from the and small vertebrates including amphibians were top of the remnant sediments of the unit (2.2 m mostly represented by several parts of cranial and from the bottom) yielded an AMS 14C age of 7,445 postcranial skeletons. Thus, these fossils, together ± 26 cal. BP (6,540 ± 40 BP; -8.52 ± 0.62 ‰; IAAA- with those obtained from the upper unit (see 80227), but no vertebrate fossils were discovered below), may suggest that the fissure acted as a pit- in this area of the sediments. These somewhat fall for small animals and a sink for surface debris. inverted estimates suggest that the matrix may The upper unit sediments were comprised of have been disturbed, but could partially be approximately 0.4 m3 (1 m high, 1 m deep, and 0.4 explained by the difference in the chemical proper- m wide) of light brown clayey soil on the floor of the ties of the dating samples (i.e., terrestrial plant and shelf (Figure 2). The AMS 14C ages of Cyclophorus land snail shell) or by sample pollution from mod- turgidus shells derived from the bottom (3,904 ± 40 ern carbonate. Although the sediments lack any cal. BP [3,600 ± 30 BP; -9.26 ± 0.32 ‰; IAAA- sign of human occupation, the inferred depositional 80229]) and the top (5,558 ± 43 cal. BP [4,810 ± 40 ages postdate human arrival on the island (prior to BP; -10.42 ± 0.87 ‰; IAAA-80230]) generally fall 37 ka; Kaifu and Fujita, 2012). Additionally, Azuma within the range of the middle Holocene. As in the (2007) reported a radiocarbon age of the fissure case of the lower unit, these inverted estimates deposits of 22,941 ± 434 cal. BP, using Cyclopho- suggest that there was some disturbance of the rus shells presumably derived from this unit, but matrix or pollution of the samples. the details of the dating are uncertain. In contrast with the lower unit, the sediments The fossils obtained from the fissure, which of the upper unit produced a number of different were presumably derived from the lower unit sedi- marine fish bones that may be interpreted as leav- ments defined here, included terrestrial crabs, land ings of early human inhabitants (although such snails, and some vertebrates (Moriguchi, 2003; remains may have been left by roosting seabirds, Naruse et al., 2004; Azuma, 2007). We also recov- such as ospreys or boobies). However, neither arti- 5 NAKAMURA & OTA: OKINAWAN AMPHIBIANS facts nor present-day debris were discovered. SYSTEMATIC PALEONTOLOGY There were also several fossils of other verte- Class AMPHIBIA de Blainville, 1816 brates, particularly those that are presently absent Order ANURA Fischer von Waldheim, 1813 in the southern part of the island, such as the Family DICROGLOSSIDAE Anderson, 1871 Ryukyu Long-furred Rat Diplothrix legata. We Genus LIMNONECTES Fitzinger, 1843 therefore regarded the fossils from the unit as Limnonectes namiyei (Stejneger, 1901)—Namiye’s being representative middle Holocene fauna, pre- Frog sumably associated with early civilization. The Figure 3.1–3.4 amphibian fossils from this fissure are located in the Fujukan, University Museum of the University Occurrence (MNI). Minatogawa: 1; Sashiki (lower of the Ryukyus, Nishihara Town, Okinawa Prefec- unit): 1. ture, Japan (RUMF). Referred material. Minatogawa: 1 female humerus (left: YMHF-MA 001); Sashiki (lower unit): Identification 1 ilium (left: RUMF-GF-04000). A common limitation of accuracy in the identi- Humerus. A left humerus lacking the proximal part fication of amphibian fossils lies in the frequent of the shaft, the distal half of the distal condylar insufficiency of characters for the phylogenetic part, and the crista ventralis (YMHF-MA 001: Fig- analysis that can be extracted from available bone ure 3.1–3.3), is referred to this large-sized frog. fragments. Therefore, as practiced in some previ- The identification is based on the absence of the ous studies on the Quaternary paleoherpetology, crista medialis and the crista lateralis, and the pos- our identification was based on overall similarity session of a stout and scarcely waisted shaft, a through direct comparisons with the skeletal speci- massive distal condylar part, a well-concaved fos- mens of extant taxa. We used specimens repre- sula dividens, a very weak spina tuberculi medialis senting all extant anuran species of Japan (except (sensu Bolkay [1919, p. 330–331], which refers to Glandirana susurra, which is confined to an off- a ridge on the shaft extending distally from the shore island of northern Honshu [Sekiya et al., tuberculum mediale of the caput humeri), and a 2012]) and of all three salamander (newt) species pointed proximal tip of the olecranon scar (in dorsal known from the Ryukyu Archipelago (Appendix). view). The gender (female) is inferred from the Specimens of other extant anurans and salaman- slender overall shape. Practical observations on ders from adjacent areas, such as those from the humerus of this species by Nokariya (1984) are Korean Peninsula, were also examined. Addition- confined to the presence of the fossula dividens ally, literature information on the osteology of Japa- and the crista paraventralis (the crest was mistak- nese anurans (Nokariya, 1983a, b, 1984) was enly referred to as the “spina tuberculi medialis” in consulted. Because all fossils were from relatively his publication; see Nokariya and Hasegawa recent geological ages (see above), present geo- [1979, figure 2]). graphic distributions of the extant taxa were con- Ilium. A left ilium lacking the anterior part of the ilial sidered in selecting the comparative materials, and shaft (RUMF-GF-04000: Figure 3.4) is referred to we believe possible effect of such an a-priori this species. Nokariya’s (1984) observations on the assumption on the accuracy in identification is neg- ilium of this species note a well-developed crista ligibly small. dorsalis and the tuber superior that is separated We concentrated our identification of anuran from the acetabular margin. The following combi- fossils on the humeri and ilia, which are dominant nation of character states may be useful to discrim- elements in the fossils discussed here and are use- inate the ilium from those of other Japanese ful for species-level identification. Morphological anurans examined: a thin, high (the height [from comparisons were conducted using a binocular the ventral edge of the ilial shaft, same hereafter] is microscope (Nikon SMZ-10). The minimum num- higher than that of the acetabulum), and anteriorly ber of individuals (MNI) was calculated for each tapered crista dorsalis with an angulated postero- taxon from each site/excavation unit. Osteological dorsal corner; a straight posterior edge of the crista terminology follows Bolkay (1919, 1933) and dorsalis that forms at a sharp angle with the ante- Sanchiz (1998) for anurans, and Estes (1981) and rior edge of the pars ascendens; the tuber superior Duellman and Trueb (1986) for salamanders. The that is mediolaterally thin, subround in shape, and higher group taxonomy of amphibians follows that defined by a weakly ridged margin; a straight ante- of Frost (2014). rior edge of the pars ascendens; and a distinct supracetabular fossa. 6 PALAEO-ELECTRONICA.ORG FIGURE 3. Fossils referred to Limnonectes namiyei (1–4) and Babina holsti (5–11). 1–3, left female humerus lacking the proximal and distal parts and the crista ventralis (YMHF-MA 001) in ventral (1), medial (2) and dorsal (3) views; 4, left ilium lacking the anterior part (RUMF-GF-04000) in lateral view; 5–7, right female humerus (one of six registered as RUMF-GF-04003) in ventral (5), medial (6) and dorsal (7) views; 8–10, right male humerus lacking the proximal part (one of two registered as RUMF-GF-04004) in ventral (8), medial (9), and dorsal (10) views; and 11, right ilium lacking the anterior part (one of nine registered as RUMF-GF-04005) in lateral view. Abbreviations: acet, acetabulum; acet.m, acetabular margin; cr.dors, crista dorsalis; cr.lat, crista lateralis; cr.med, crista medialis; cr.par, crista paraven- tralis; cr.ven, crista ventralis; e.cap, eminentia capitata; ep.rad, epicondylus radialis; ep.ul, epicondylus ulnaris; fo.div, fossula dividens; il.sh, ilial shaft; ol.sc, olecranon scar; p.asc, pars ascendens; stm, spina tuberculi medialis; supr.fo, supracetabular fossa; tub.sup, tuber superior. Scale bars equal 5 mm. 7 NAKAMURA & OTA: OKINAWAN AMPHIBIANS Family RANIDAE Rafinesque, 1814 3.11) are: an elliptical and swell-like tuber superior Genus BABINA Thompson, 1912 without ridging in the margin; the tuber superior Babina holsti (Boulenger, 1892)—Holst’s Frog that is in contact with the acetabular margin (contra Figure 3.5–3.11 Nokariya, 1984); a thin and high (the height is higher than that of the acetabulum) crista dorsalis Occurrence (MNI). Minatogawa: 2; Sashiki (lower with a gently round posterodorsal corner; the pars unit): 6. ascendens with a posteriorly curved anterior edge; Referred material. Minatogawa: 2 female humeri and a distinct supracetabular fossa. (right: YMHF-MA 002) and 2 ilia (right: YMHF-MA Remarks. While the ilia and female humeri of this 003); Sashiki (lower unit): 6 female humeri (1 right species are morphologically indistinguishable from and 5 left: RUMF-GF-04003), 2 male humeri (1 those of Babina subaspera (the sibling species right and 1 left: RUMF-GF-04004), and 9 ilia (6 endemic to the Amami Island Group: Maeda and right and 3 left: RUMF-GF-04005). Matsui, 1999), fossils of these elements are Humerus. Nokariya’s (1984) observations on the referred on the basis of the species’ exclusive humerus of this large-sized frog note a laterally occurrence on the island. Male humeri of B. holsti projected epicondylus radialis, a small and ridge- differ from those of B. subaspera by having less- like crista lateralis (female only), and a proximally developed crista lateralis and crista medialis. positioned waisted part of the shaft (female only). The other diagnostically useful character states of Genus ODORRANA Fei, Ye, and Huang, 1990 the humerus are: a robust and strongly waisted Odorrana ishikawae (Stejneger, 1901)—Ishikawa’s shaft; a high crista ventralis with a straight ventral Frog edge that is parallel to the dorsal edge of the shaft Figure 4.1–4.7 (in mediolateral views); the distal edge of the crista Occurrence (MNI). Sashiki (lower unit): 7. ventralis that forms an oblique angle with the ven- Referred material. 10 female humeri (5 right and 5 tral outline of the shaft (in mediolateral views); the left: RUMF-GF-04009), 3 male humeri (2 right and distance between the ventrodistal corner of the 1 left: RUMF-GF-04010), and 5 ilia (4 right and 1 crista ventralis and the eminentia capitata, which is left: RUMF-GF-04011). only 2.5 times longer than the length of the emi- Humerus. The humerus of this large-sized frog nentia capitata; the crista paraventralis that (Figure 4.1–4.6) differs from those of other anurans extends proximally to the level of the ventrodistal examined (except O. splendida, see below) in hav- corner of the crista ventralis; the proximal part of ing a series of character states: a robust shaft that the epicondylus ulnaris that protrudes medially is strongly waisted at the point proximal to the con- (more than the distal part in dorsoventral views); dylar part (in dorsoventral views); a weakly curved and a tapered and round outline of the proximal ventral edge of the crista ventralis, which is not par- part of the olecranon scar (in dorsal view). The allel to the dorsal margin of the shaft (in mediolat- crista lateralis and the crista medialis of male eral views); the distal edge of the crista ventralis humeri inflect dorsally, with the former extending that forms an oblique angle with the ventral outline laterally beyond the level of the lateral edge of the of the shaft (in mediolateral views); a distinct crista epicondylus radialis, and the latter extending medi- paraventralis that extends proximally beyond the ally beyond the level of the medial edge of the epi- level of the ventrodistal corner of the crista ventra- condylus ulnaris (Figure 3.8–3.10). These crests lis; a developed spina tuberculi medialis; a are ridge-like in the female (Figure 3.5–3.7) and depressed and flattened shaft at the area interven- extend proximally to the level of the crista ventralis ing between the spina tuberculi medialis and the forming angulated ridges of the shaft (as a conse- crista ventralis; a usually distinct and shallowly quence, the cross-section of the narrowest part of concaved fossula dividens; a scarcely protruded the shaft forms a semicircle). The fossula dividens epicondylus radialis; the distal part of the epicondy- scarcely concaves in the female and some males lus ulnaris that protrudes medially (more than the while it concaves deeply in some males; and the proximal part in dorsoventral views); and a gently spina tuberculi medialis is weak in the female and round outline of the proximal part of the olecranon some males, but developed in other males (Figure scar (in dorsal view). In the female, the crista medi- 3.8–3.10). alis and the crista lateralis are ridge-like (Figure Ilium. Nokariya’s (1984) observations on the ilium 4.1, 4.3), while in the male, the former is developed of this species note a well-developed crista dorsa- but the medial extent is less than the level of the lis and tuber superior. The other diagnostic combi- medial edge of the epicondylus ulnaris, and the lat- nations of the character states on the ilium (Figure ter is much less developed than the former with a 8 PALAEO-ELECTRONICA.ORG FIGURE 4. Fossils referred to Odorrana ishikawae (1–7) and Odorrana narina (8–14), 1–3, right female humerus (one of 10 registered as RUMF-GF-04009) in ventral (1), medial (2), and dorsal (3) views; 4–6, right male humerus (one of three registered as RUMF-GF-04010) in ventral (4), medial (5), and dorsal (6) views; 7, right ilium lacking the anterior part with part of the ischium (one of five registered as RUMF-GF-04011) in lateral view; 8–10, right female humerus (one of eight registered as RUMF-GF-04014) in ventral (8), medial (9), and dorsal (10) views; 11–13, right male humerus lacking the proximal part of the shaft and the distal part of the epicondylus ulnaris (RUMF-GF-04015) in ventral (11), medial (12), and dorsal (13) views; and 14, pelvic girdle (fused right and left ilia [lacking anterior parts] with the ischium and the pubis: RUMF-GF-04016) in right lateral view. Abbreviations are the same as Figure 3. Arrows indicate the proximal ends of the crista paraventralis. Scale bars equal 5 mm. 9 NAKAMURA & OTA: OKINAWAN AMPHIBIANS laterally convex edge (Figure 4.4, 4.6). Nokariya fossula dividens; a scarcely protruded epicondylus (1984) did not provide useful observations on the radialis; the proximal part of the epicondylus humerus of this species. ulnaris that protrudes medially (more than the dis- Ilium. The ilium of this species (Figure 4.7) differs tal part in dorsoventral views); and a gently round from that of the other anurans examined (except O. outline of the proximal part of the olecranon scar splendida) in having a series of character states: (in dorsal view). The crista medialis and the crista the tuber superior that is separated from the ace- lateralis are fringe-like in the female (Figure 4.8, tabular margin (Nokariya, 1984); a comma shaped 4.10), while in the male, the former extends medi- tuber superior that is usually anteroposteriorly lon- ally beyond the level of the medial edge of the epi- ger than the height with a gently curved postero- condylus ulnaris, and the latter forms a straight- dorsal corner; a ridged margin of the tuber edged ridge of the shaft (Figure 4.11, 4.13). superior; a thick and low crista dorsalis (the height Nokariya (1984) did not provide useful observa- is less than that of the acetabulum); the crista dor- tions on the humerus of this species. salis that is anteriorly tapered with a straight dorsal Ilium. Nokariya (1984) noted that the tuber supe- edge; a medial inclination of the crista dorsalis, rior of this species is separated from the acetabular except the posterior end; the pars ascendens with margin. Other informative character states on the a posteriorly curved anterior edge; and a fused ilium (Figure 4.14) are: the tuber superior that is supracetabular fossa. well-defined and encircled by a ridged margin; a Remarks. The Amamioshima Island (Amami parallelogram- or drop-shaped tuber superior with Island Group) population of this species has been a weakly angulated posterodorsal corner and described as O. splendida (see Kuramoto et al., straight, steep posterior edge; the tuber superior 2011). These sibling species resemble each other that is higher than the anteroposterior length; the osteologically, while O. ishikawae has more robust crista dorsalis that is thick, low (the height is less humeri and a more developed crista medialis in than that of the acetabulum), and weakly tapered male humeri. The species-level identification of the anteriorly with a straight dorsal edge; a medial incli- fossil ilia discussed here is based on the species’ nation of the crista dorsalis (except the posterior exclusive occurrence on the island. end); the pars ascendens with a posteriorly curved anterior edge; and a fused supracetabular fossa. Odorrana narina (Stejneger, 1901)—Okinawa Tip- Remarks. It is difficult to discriminate the humerus nosed Frog and the ilium of O. narina from those of allied spe- Figure 4.8–4.14 cies of the Ryukyus (O. amamiensis, O. suprana- Occurrence (MNI). Minatogawa: 40; Sashiki rina, and O. utsunomiyaorum) based solely on the (lower unit): 5. morphological characters. The species-level identi- Referred material. Minatogawa: 45 female humeri fication of the fossils discussed here is based on (21 right and 24 left: YMHF-MA 004), 32 male the species’ exclusive occurrence on the island. humeri (16 right and 16 left: YMHF-MA 005), and Genus RANA Linnaeus, 1758 53 ilia (22 right and 31 left: YMHF-MA 006); Rana ulma Matsui, 2011 (formerly known as R. Sashiki (lower unit): 8 female humeri (4 right and 4 okinavana Boettger, 1895: see Matsui, 2007)— left: RUMF-GF-04014), 1 male humerus (right: Ryukyu Brown Frog RUMF-GF-04015), 1 pelvic girdle (RUMF-GF- Figure 5.1–5.7 04016), and 1 ilium (left: RUMF-GF-04017). Humerus. The humerus of this middle-sized frog Occurrence (MNI). Minatogawa: 49; Sashiki (Figure 4.8–4.13) can be distinguished from that of (lower unit): 152. other anurans examined (except allied species, Referred material. Minatogawa: 89 female humeri see below) by having a series of character states: (41 right and 48 left: YMHF-MA 007), 1 male a slender shaft with an almost uniform diameter humerus (left: YMHF-MA 008), and 17 ilia (8 right throughout the length; a straight ventral edge of the and 9 left: YMHF-MA 009); Sashiki (lower unit): crista ventralis that is often nearly parallel to the 176 female humeri (108 right and 68 left: RUMF- dorsal edge of the shaft (in mediolateral views); the GF-04019), 87 male humeri (44 right and 43 left: distal edge of the crista ventralis that forms an RUMF-GF-04020), and 93 ilia (46 right and 47 left: oblique angle with the ventral outline of the shaft RUMF-GF-04021). (in mediolateral views); a distinct crista paraventra- Humerus. Correct observations on the humerus of lis that extends proximally to the level of the ventro- this tiny, slender-bodied frog by Nokariya (1984; as distal corner of the crista ventralis; a weak spina Rana [Rana] okinavana) are confined to a weak tubercli medialis; a distinct and shallowly concaved crista paraventralis and a distinct fossula dividens. 10