Galaxea, Journal of Studies 14: 73-95（2012）

Original paper

Low species diversity of hermatypic corals on an isolated reef, , in the northwestern Pacifi c

Hajime KAYANNE1, *, Chuki HONGO2, Ken OKAJI3, Yoichi IDE4, Takeshi HAYASHIBARA5, Hidekazu YAMAMOTO6, Nobuo MIKAMI7, Kiyoshi ONODERA8, Takaaki OOTSUBO8, Hiroyuki TAKANO9, Makoto TONEGAWA9, and Shogo MARUYAMA9

1 Department of Earth and Planetary Science, the University of , Hongo, Tokyo 113-0033, 2 Department of Physics and Earth Sciences, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan 3 Coralquest Inc., Atsugi, Kanagawa 243-0014, Japan 4 Oceanic Planning Corporation, Imazu, Fukuoka 819-0165, Japan 5 Oceanic Resources Division, National Research Institute of Far Seas Fisheries, Fukuura, Yokohama 236-8648, Japan 6 ECOH Corporation, Kita-Ueno, Tokyo 110-0014, Japan 7 Fisheries Infrastructure Department, Fisheries Agency, Kasumigaseki, Tokyo 100-8907, Japan 8 Tokyo Port Offi ce, Kanto Regional Development Bureau, Ministry of Land, Infrastructure, Transport and Tourism, Shin-kiba, Tokyo 136-0082, Japan 9 Keihin River Offi ce, Kanto Regional Development Bureau, Ministry of Land, Infrastructure, Transport and Tourism, Tsurumi, Yokohama 230-0051, Japan

* Corresponding author: H. Kayanne E-mail: [email protected]

Communicated by Yasufumi Iryu (Geology and Physical Geography Editor)

Abstract Ninety-three coral species have been identifi ed diversity and isolation from other islands. The island is at Okinotorishima (Okinotori Island), an isolated table located in a subtropical gyre and is isolated from major reef located in the center of the . The species currents. Thus, only coral larvae with a long competency composition of the island is similar to that of other islands period (as long as 70 days) can settle at the island from in the northwestern Pacifi c, but the number of species is surrounding islands. This unique species composition small in comparison with surrounding islands. The coral seems to have been maintained for at least the last 7600 fauna at the island is characterized by a unique species years, since the last stage of sea level rise in the post- composition that is independent of the Ryukyu Islands, glacial period (Holocene). mainland Japan, Palau, and the Mariana Islands. No endemic species were found, but the dominant Acropora Keywords Okinotorishima, Northwestern Pacifi c, Coral species (A. aculeus, A. sp. aff. divaricata, and A. globiceps) fauna, Isolated reef, Biogeography were morphologically different from corresponding species at the Ryukyu Islands. The relatively low species diversity at the island despite the close proximity to an area of high diversity is explained by its small habitat 74 Kayanne et al.: Corals in Okinotorishima

fi ll a gap in our understanding of the biogeography of Introduction corals in the northwestern Pacifi c and would provide in- sight into the processes that form and maintain coral fauna Okinotorishima (Okinotori Island; 20°25′N, 136°05′E) at isolated islands. Here we report the fi rst full list of coral is a small table reef located in the center of the Philippine species for Okinotorishima together with their distribution Sea, northwestern Pacifi c (Fig. 1). Although it is located patterns on the reef, which are presented in a habitat map. close to the Coral Triangle, which has the highest diversity The coral fauna is then compared with the fauna at sur- of hermatypic corals (hereafter corals) with 605 species rounding islands and faunal similarities and characteristics (Veron et al. 2009), the island is isolated from other are discussed with regard to larval competency periods islands. It is 675 km southeast of Okidaitojima and 700 km and oceanic currents. southwest of Minami-iwojima. Over long time scales, some coral species will go ex- An isolated reef that is far from larval source reefs is tinct and others will recruit to a study area. The bio geo- separated from connectivity, and therefore there is a graphical representativeness of a site needs to be evaluated limited chance that larvae will recruit from other reefs by examining the presence or absence of specifi c species (Maragos and Jokiel 1986; Glynn and Ault 2000). The within a certain temporal scale. Therefore, we analyzed probability that coral larvae will recruit to a remote island core records to evaluate the historical diversity of corals is constrained by the competency period of the larvae and throughout the Holocene (the last 10,000 years) and com- the ocean currents that deliver them (Harii et al. 2002, pared these data with the list of living corals. 2007). Okinotorishima is located in a subtropical gyre and no strong currents reach the island; therefore, it can take a long time for larvae to reach the island. Moreover, the Study site and methods island is small and receives severe waves, and thus the diversity of habitats for corals is small. Considering these Study site features, the biodiversity of corals at this island is expected Okinotorishima, the southernmost island of Japan, is a to be small despite its close proximity to the zone with the small table reef that spans 4.5 km east-west and 1.7 km highest coral diversity in the world. north-south (Fig. 1). It is located on a submerged arc that Unfortunately, a complete list of the coral species found comprises the Kyushu-Palau ridge. A volcanic island at the island has not yet been reported. Several studies of formed on the ridge before the Miocene (24 million years corals and coral reefs have been conducted by the gov- ago) and subsequently became submerged (Kobayashi ernments of Japan and Tokyo, but lists of corals have only 2004), allowing for the growth of coral. The outer slope of been published as internal reports in Japan and species the island is steep, with a 45° angle descending down to identifi cation has not been examined in detail. Therefore, the ocean fl oor to depths of 3000 to 5000 m. the coral fauna of Okinotorishima remains un known. In The reef has a fl at surface (a reef fl at) with a shallow the most comprehensive map of coral bio geo graphy in the (maximum depth 5.5 m) that is surrounded by a Indo-Pacifi c (Veron 1993), the area around Okinotorishima reef crest which reaches to the low water level and be- is described as having a low diversity, with 40 to 50 comes dry during spring low . Two (Kita- genera, which is smaller than the diversity of the sur- kojima and Higashi-kojima) on the reef fl at are exposed rounding islands: 74 for the Ryukyus (Nishihira and Veron above the high level. The geology of the islets is 1995), 62 for Palau (Yukihira et al. 2007), 49 for Ogasa- described as foraminifera and coral limestone standing on wara (Tachikawa et al. 1991), and 57 for the Mariana the reef fl at (Tayama 1952), which implies that they are Islands (Randall 1995). However, the number of genera Pleistocene or Holocene limestone remnants. Three and species at Okinotorishima was not based on precise additional islets that extended above the high tide level data. were previously described but they have since been lost A full list of the coral species at Okinotorishima would because of severe erosion. Kayanne et al.: Corals in Okinotorishima 75

Fig. 1 Location of Okinotorishima. Isolines are numbers of genera. Site numbers in brackets correspond to the numbers in Table 2

The island is situated at the center of the northwestern specimens were identifi ed using available references Pacifi c subtropical gyre, facing the northeast trade wind (Nishi hira and Veron 1995; Veron and Stafford-Smith from November to February and the southeast trade wind 2000) and compared with previous coral lists to reexamine from May to August. Surface seawater temperature around their identifi cation (Hayashibara et al. 2006). We also the island varied from 24.7 to 29.7℃ (monthly averages) made a detailed survey of the corals at the island and between May 2007 and April 2008, and the underwater observed 67 species from 20 genera and 9 families. More light intensity at 5 m depth around noon in fair weather recently, the Fisheries Agency, Japan, conducted a coral was as high as 1000 μmol m－2 s－1 in May 2007 (Nakamura mass culture project at this island and described additional et al. 2011). coral species (Nakamura et al. 2011). Previous lists were The North Equatorial Current fl ows westward along examined for the validity of the specimens and descrip- 10-15°N latitude and turns north to become the warm tions. Kuroshio Current, which then fl ows along the east coast Coral species composition was compared with sur- of and west of the Ryukyu Islands. These major round ing islands in the northwestern Pacifi c using lists currents fl ow far from Okinotorishima. based on monographs for Japan (mainland and Ryukyu Islands: Nishihira and Veron 1995), Taiwan (Dai 1991; Methods Dai and Horng 2009b,a), Palau (Yukihira et al. 2007), and Collection and identifi cation of coral specimens. The the Mariana Islands (Randall 1995, 2003). Similarities Ministry of Land, Infrastructure, Transport and Tourism, and dissimilarities in coral species composition among 17 Japan, has conducted a series of annual fi eld surveys of sites were examined using multivariate analysis (cluster- the distribution of corals on the reef at Okinotorishima ing technique). Species data were converted to binary data since 1988 and has produced lists of observed corals. (present or absent). The data were compiled into a matrix Coral specimens were haphazardly collected from dif- and “present” and “absent” data in the matrix were as- ferent habitats that were defi ned by reef topography in signed the numbers “1” and “0,” respectively, for sub- June 2000 and May 2006. Collected specimens were sequent calculations. The overall degree of similarity in bleached using household bleach and dried. In total, 89 species composition between a pair of sites was expressed 76 Kayanne et al.: Corals in Okinotorishima

Fig. 2 Study site overlaid with surveyed grids (red squares) and transects (yellow and light blue lines)

using the Bray-Curtis coeffi cient (Bray and Curtis 1957). non-overlapping images from each transect were imported A cluster analysis was performed using the group average into a coral cover analysis program, CPCe (National Coral method and the software R-2.13.0. Reef Institute, USA), and 50 grid points were projected Habitat map. A satellite image (IKONOS) of the island onto each image. Percent coral cover was determined that was taken in July 2007 was overlaid with a 250 using point sampling techniques (Kohler and Gill 2006). ×250 m grid. Fourteen grids (total area 875,000 m2) were Relative abundance of each species was marked as selected as representative areas for the different habitats abundant, common, uncommon and rare based on the grid available based on our fi eld survey and previous surveys; and transect survey. these grids were examined in detail (Fig. 2). In addition, Core analysis. Three cores were recovered from the reef 21 transects (total 6800 m) were established to compensate crest and the shallow lagoon along the east-west transect for gaps in the grid survey. In the selected grids and (OK-1, 2, and 3 in Fig. 5), which represent the major transects, the coverage of corals belonging to the dominant habitat of Okinotorishima. The lengths of the cores were species or genus and the coverage of turf algae were 20.1 (OK-1), 26.2 (OK-2), and 20.1 m (OK-3). The cores recorded with their landform and sediment type. The were slabbed and their lithological characteristics were coverage of corals was visually determined throughout described. Fossil corals in the cores were identifi ed to each selected grid and in 1-m-wide strips that were spaced species, or at least to genera. In total, seven samples were at 10-m intervals along each transect. Coral coverage was analyzed by Teledyne Inc. to obtain radiocarbon ages. The recorded at four levels: ＞20%, 20-5%, ＜5%, and 0%. mineralogy of the dated samples was analyzed by X-ray The visual method was evaluated using a point-counting diffraction (XRD) with a PANalytical X’Pert diffraction method with 1400 points within a 0.4×0.6 m quadrat. system to confi rm that there were no alterations to the The coverage of corals that was determined by this quadrat calcite. The dates were calibrated to calendar years using survey matched the results of the grid and transect survey. the calibration program CALIB Rev.5.0 (Stuiver and Reimer To compensate for gaps in the transect survey, a manta 1993; Stuiver et al. 2005) and the marine calibration data tow survey was conducted over the reef fl at and on the set Marine 04 (Hughen et al. 2004), assuming a marine outer slope all around the island to observe coral coverage reservoir effect of 400 years (Stuiver and Braziunas 1993; (total distance 23,170 m). Additional survey was con- Stuiver and Reimer 1993). ducted on the western outer slope in 2012. Five 20 m transects were located horizontally at a depth of 8 m. Photographs of the bottom in a 0.4×0.6 m area were taken along the transects at 1-m intervals. The 20 Kayanne et al.: Corals in Okinotorishima 77

families were identifi ed. The numbers of genera and Results species at Okinotorishima were smaller than at other islands in the northwestern Pacifi c (Table 2). List of coral species The major coral groups consisted of Acroporidae and The coral species identifi ed at Okinotorishima are listed Faviidae corals. The dominant species in the genus Acropora in Table 1. Ninety-three species from 25 genera and 11 were A. aculeus, A. sp. aff. divaricata, and A. globiceps.

Table 1 List of coral species at Okinotorishima (Okinotori Island) 78 Kayanne et al.: Corals in Okinotorishima

Table 2 Numbers of genera and species at 17 sites in the markers, no differences were detected between the sam- northwestern Pacifi c ples from Okinotorishima and Okinawa (Hayashibara et al. in prep.). Acropora sp. aff. divaricata at Okinotorishima had a different colony shape from A. divaricata in the Ryukyu Islands. The form of the corallites and the detailed struc- ture of the coenosteum agreed with the description of A. divaricata (Wallace 1999). However, although colonies at Okinotorishima showed variation in shape, they did not present all of the features of A. divaricata, whose branches anastomose to form a network. For this reason, Hayashi- bara et al. (2006) hypothesized that the specimens from Okinotorishima were from a different species and treated them as A. sp.4? Here, we labeled the specimens as A. sp. aff. divaricata. Although there was a close relationship between the specimens during a genetic comparison, there Acropora tenuis and A. donei comprised the second most was a distinguishable level of difference in their mito- abundant group. Interestingly, A. hyacinthus, A. muricata, chondrial DNA (Hayashibara et al. in prep.). and A. gemmifera were not in the majority group, yet they The specimens of A. globiceps from Okinotorishima are dominant reef components in the western Pacifi c. closely resembled the morphology of A. humilis in the Moreover, A. humilis, A. monticulosa, and A. digitifera, Ryukyu Islands; however, their caespito-corymbose col- which are dominant reef builders on reef crests in the ony shape, columnar branches, and small axial corallites northwestern Pacifi c, were not found at Okinotorishima. matched the description of A. globiceps (Wallace 1999). The genera Stylophora, Seriatopora, and Pachyseris and Although this species has only been recorded from the the families Oculinidae and Pectiniidae have not been south-central Pacifi c (Wallace 1999), one of the authors, recorded at the island, but they are all common in the T. Hayashibara, confi rmed that this species is distributed Ryukyu Islands. Only one Fungia species, Fungia in . Although the specimens from Okinotorishima scutaria, was found. Only two species, Lobophyllia hem- and Guam did not differ genetically, A. humilis from prichii and L. corymbosa, were present from the Family Okinawa did differ from A. globiceps in the non-coding Mussidae, and only Merulina ampliata and Scapophyllia region of the mitochondrial DNA by one base (Hayashi- cylindrica were present from the Family Merulinidae. bara et al. in prep.).

Ecomorphic features of some Acropora species Cluster analysis The species composition at Okinotorishima was essen- The cluster analysis produced four groups among the tially similar to other islands in the northwestern Pacifi c. 17 sites (Fig. 3 and in ESM Table 1). Group 1 only in- However, the three dominant species of Acropora (A. cluded one site (1: Okinotorishima). Group 2 was com- aculeus, A. sp. aff. divaricata, and A. globiceps) were posed of nine sites (2: Southern Mariana Islands, 3: North- mor phologically different from corresponding species in ern Mariana Islands, 4: Palau Islands, 5: Ogasawara Is- the Ryukyu Islands (Hayashibara et al. 2006). land, 6: Taiwan, 7: Yaeyama Islands, 8: Okinawa Islands, At Okinotorishima, A. aculeus had larger branches and 9: Miyako Islands and 10: Amami Islands). Group 3 con- corallites and a more irregular colony shape than in the sisted of fi ve sites (11: Tanagashima, 12: Tosa Shimizu, Ryukyus, and the colonies extended brown tentacles dur- 13: Amakusa, 14: Shirahama, and 15: Kushimoto), and ing the daytime. However, from the results of genetic Group 4 had two sites (16: Izu Penisula and 17: Tateyama). comparisons using mitochondrial and nuclear molecular Group 2 was located in tropical and subtropical areas, Kayanne et al.: Corals in Okinotorishima 79 while Groups 3 and 4 were located in temperate areas of in other areas. Along the northern and eastern rims of the Japan. Group 1 (Okinotorishima) was located in an iso- island, the reef crest is as wide as 200 to 300 m, with less lated area in the Philippine Sea. than 5% coral coverage. The surface of the reef crest is reef rock covered with turf algae and it is exposed during Habitat map low water in the spring. The surface landform of Okinotorishima consists of an The shallow lagoon contains patch reefs that are up to outer slope, a reef crest, and a shallow lagoon. The outer 10 m wide and 1 to 5 m high from the lagoon bottom. reef descends steeply to the ocean fl oor. Coral coverage Patch reefs were generally densely covered with corals, exceeds 20% along the northern slope but is only 5 to 20% with coral coverage exceeding 20%, particularly in the central and western patches. The dominant inhabitants of patch reefs were encrusting Faviidae (genus Cyphastrea and Echinopora), especially on the sides of the reefs. In the central part of the island, bush-like A. aculeus was dominant on the top portions of some patch reefs and corymbose A. sp. aff. divaricata and A. globiceps were also abundant. The patch reefs in the southwestern corner of the island were densely inhabited with corymbose Pocillopora damicornis. The bottom of the shallow lagoon was covered with sand and gravel, with less than 5% coral coverage. Massive Porites and Leptoria were scattered in the shallow lagoon where reef rock was ex- posed without gravel cover. Corymbose, encrusting and massive types of corals are dominant on the outer slope. Acropora robusta, Isopora palifera, Favia laxa, Favia rotundata and Montastrea annuligera were only found from the outer slope.

Coral communities in reef cores Fig. 3 Dendrogram from average linkage clustering of Core analyses and radiocarbon dating showed that the coral composition at 17 sites in the northwestern Pacifi c upper 10 m of the cores were from the Holocene. They

Fig. 4 Habitat map of Okinotorishima. Percent cover of living corals are shown by colors for each habitat 80 Kayanne et al.: Corals in Okinotorishima

Fig. 5 Internal structure of sample cores and recovered fossil corals of the Holocene coral reef at Okinotorishima Kayanne et al.: Corals in Okinotorishima 81 contained rich unaltered corals overlying Pleistocene the Yaeyama Islands (site no. 7) to Tateyama (site no. 17), limestone with altered corals. Detailed internal structures basically matched the grouping by Veron and Minchin for the cores are shown in Figure 5. (1992), which detected two main clusters: the Ryukyu Core OK-1: this western reef crest consisted of A. Islands, with reef communities, and mainland Japan, with globiceps, Montastrea curta, Favia stelligera, Pocillopora non-reef communities. The decrease in temperature with verrucosa, Millepora sp., massive Porites sp., corymbose latitude is the major constraint that leads to a decreasing types of Acropora spp., and fragments of Montipora, number of species. Species composition at islands in the Cyphastrea, Favia sp. cf. pallida, massive Porites, and northwestern Pacifi c, from Southern Mariana (site no. 2) Pocillopora verrucosa. Core OK-2: this shallow lagoon to Taiwan (site no. 6), was categorized together with the core was divided into two units. The lower part between Ryukyu Islands. The results showed that the community 13 and 10 m in depth mainly consisted of massive Porites composition on reefs in the tropical and subtropical north- and a few Cyphastrea fragments. The upper part between western Pacifi c (Mariana Islands, Palau Islands, Ogasa- 10 m in depth and the core top was mainly composed of wara, Taiwan, and Ryukyu Islands) clustered together into detritus. This detritus was composed of coral gravels one group (Group 2), with the exception of Okinotori- (Cyphastrea, Pocillopora, massive Porites, and corymbose shima. The island’s species composition was dissimilar to Acropora) and calcareous sand (e.g., Halimeda fragments that of the surrounding tropical and subtropical reefs, and adhering foraminifera). Core OK-3: this eastern reef although the island is located in a tropical area. This crest was very similar to OK-1. It consisted of A. globiceps, indicates that the species composition at the island was M. curta, F. stelligera, Pocillopora damicornis, P. ver- infl uenced by more than just sea surface temperature. rucosa, Millepora sp., massive Porites sp., Montipora sp., The uniqueness of the species composition was also corymbose types of Acropora spp., and fragments of manifested by the abundance of Acropora. Although three Pocil lopora eydouxi and P. verrucosa. Acropora species (A. aculeus, A. sp. aff. divaricata, and Radiocarbon dates for six coral samples ranged from A. globiceps) were relatively more abundant than other 4300 to 7600 cal. years BP. The oldest Holocene age Acropora species at Okinotorishima, they are absent or (7600 cal. years BP) was obtained from the bottom of core are only minor species in the Ryukyus (Hayashibara et al. OK-3. The uppermost portions of the reef crest were dated 2006). On the other hand, although A. hyacinthus and A. to 3930 and 4300 cal. years BP at OK-1 and OK-3, re- muricata are the most abundant species at many locations spectively. in the Ryukyu and Amami Islands, they were rarely observed at Okinotorishima. Acropora digitifera and A. nasuta, which are also dominant species in Okinawa, Discussion were not found at Okinotorishima. The small size and the high wave energy of Okino- Low species diversity at Okinotorishima torishima are major factors affecting the low species rich- The number of species, 93 species in 25 genera, at ness. The outer slope, reef crest, and patch reefs in the Okinotorishima (Table 1) was small when compared with shallow lagoon were the only habitats available at this Palau (209 species in 62 genera) and the Yaeyama Islands island (Fig. 4). All of the habitats receive high wave (368 species in 74 genera) to the west and Ogasawara energy, and typical low energy habitats, such as deep (180 species in 49 genera) and the Mariana Islands (205 and inner reef fl ats, were not available. Species of species in 57 genera) to the east in the northwestern Pa- Pectinidae, Fungiidae, and Merulinidae prefer protected cifi c (Table 2). The species richness is rather smaller than environments, which may explain the relatively small that previously inferred (Veron 1993). number of coral species from these families. The coral fauna at Okinotorishima was characterized The low species diversity can also be partially attributed by a unique species composition. In the cluster analysis to the island’s isolation, which limits coral recruitment (Fig. 3), species composition at the sites in Japan, from from other islands. This point is discussed further in the 82 Kayanne et al.: Corals in Okinotorishima following section. is exposed to a weak current of about 0.1 m s－1 that runs from the southeast to the northwestern in the subtropical Larval dispersal potential and low diversity Pacifi c; this is an Ekman current that is induced by the The biodiversity of hermatypic corals is maintained by northeastern trade wind (Maximenko et al. 2009). The connectivity among reefs through the dispersal of coral other currents observed in this region are mesoscale ed- larvae (Roberts 1997). Larval dispersal is controlled by dies that are several hundred kilometers in diameter, have the period during which larvae can settle after spawning maximum velocities of 0.2 m s－1, and move from east to or release (settlement-competency period) and the speed west (Kobashi and Kawamura 2002; Qiu and Chen 2010). and direction of ocean currents (Harii et al. 2007). The Therefore, the most probable route of larval transportation competency period varies among coral species, ranging by these currents originates in the southeast, where the from a few hours to more than 100 days with an average Mariana Islands are located at a distance of 1400 km. If of several days (Harrison and Wallace 1990). In general, we take 0.2 m s－1 as the maximum current speed from corals can disperse several tens of kilometers, and thus the Mariana to Okinotorishima, it would take 70 days for lar- species diversity of corals in a group of islands or reefs vae to settle. The larval competency period of the dominant that are distributed within this distance is maintained corals is as long as 100 days; therefore, these species have because of tight connectivity among locations. However, the potential to travel this distance. On the other hand, the Okinotorishima is separated from other islands and only competency periods of corals that were not observed at larvae with long competency periods will be able to recruit Okinotorishima might be shorter than this threshold to the island. period. Some of the common species at Okinotorishima are known to have longer competency periods. The compe- Historical species composition during the last 7600 tency period of A. tenuis, one of the common species in years Okinotorishima, is longer than 70 days (Richmond 1987; On the basis of identifi ed fossil corals, the species com- Nishikawa and Sakai 2003; Nishikawa et al. 2003; Harii position at Okinotorishima has been maintained through- et al. 2010). Pocillopora damicornis is known to have a out the past 7600 years at least within a generic level, long competency period that is longer than 100 days since the last stage of sea level rise that was followed by (Richmond 1987; Harii et al. 2002). The abundant and stabilization in the post-glacial period (Holocene). All of common Pocillopora species are P. verrucosa, P. eydouxi the fossil corals that were extracted from the cores (P. and P. elegans, which competency periods have not been verrucosa, P. damicornis, P. eydouxi, A. globiceps, cor- reported, but the similar characteristics of their larvae ymbose types of Acropora, M. curta, F. stelligera, Cypha- with zooxanthellae to P. damicorns infers the potential of strea spp., Favia sp., massive Porites sp., Millepora sp., their long competency periods. The abundances of these and Montipora sp.) are distributed in the present-day species at Okinotorishima are explained by their long reefs. Furthermore, the fossil corals in these cores gen- competency periods and their higher recruitment potential erally corresponded to the dominant species on the pre- to this remote reef. On the other hand, some brooding sent reef. Therefore, the unique composition of coral spe- corals such as Heliopora coerulea (Harii et al. 2002) and cies has been maintained by the dispersal potential thresh- Stylophora pistillata (Nishikawa et al. 2003) settle soon old and the low habitat diversity at this small isolated reef, after the release of matured larvae and they lose their at least during the Holocene. settlement potential within 20 days after release. The The species composition in the east Pacifi c region has shorter competency periods of these two corals are con- supported the unique coral fauna at Okinotorishima. East sistent with their absence at Okinotorishima. Pacifi c reefs (e.g., Costa Rica, Panamá, and Galápagos Okinotorishima is situated in the center of a subtropical Island) are generally composed of Pocillopora and Porites gyre and is isolated from the major currents of the North (Glynn et al. 1994; Glynn and Ault 2000). Acropora is a Equatorial Current and the Kuroshio Current. The island dominant reef builder in the northwestern Pacifi c, but it is Kayanne et al.: Corals in Okinotorishima 83 not distributed in east Pacifi c reefs. This pattern is also mainly explained by the competency period of coral References larvae and ocean currents, although other factors are also involved, such as vicariance. Bray JR, Curtis JT (1957) An Ordination of the Upland Forest Most of the fossil corals are identifi ed as generic level Communities of Southern Wisconsin. Ecol Monogr 27: or a group of the same ecomorphic species. Moreover, 326-349 post-depositional taphomony has degraded the original Dai CF (1991) Reef environment and coral fauna of southern assemblage. Even with these problems, however, the re- Taiwan. Res Bull 354: 1-28 Dai CF, Horng S (2009a) Scleractinia fauna of Taiwan. II. The constructed generic-level assemblage of the fossil corals robust group. National Taiwan University Press, Taipei is consistent with the present coral fauna. Dai CF, Horng S (2009b) Scleractinia fauna of Taiwan. I. The complex group. National Taiwan University Press, Taipei Glynn PW, Ault JS (2000) A biogeographic analysis and review Conclusion of the far eastern Pacifi c coral reef region. Coral Reefs 19: 1-23 We reexamined the previous lists and specimens of Glynn PW, Colley SB, Eakin CM, Smith DB, Cortes J, Gassman corals and conducted additional survey to compile the list NJ, Guzman HM, Delrosario JB, Feingold JS (1994) Reef of coral fauna, which shows 93 species within 25 genera coral reproduction in the Eastern Pacifi c - Costa-Rica, are present in Okinotorishima, southernmost island of Panama, and Galapagos-Islands (Ecuador) 2. Poritidae. Japan. The survey has been spatially dense over a small Mar Biol 118: 191-208 island and the list provides a sound basis for future re- Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative search and any changes in ecosystem in Okinotorishima, contribution of dinofl agellate photosynthesis and stored and biogeographical studies in the northwestern Pacifi c. lipids to the survivorship of symbiotic larvae of the reef- building corals. Mar Biol 157: 1215-1224 However, additional species might be found from the Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal deep outer slope, where relatively small survey efforts changes in settlement, lipid content and lipid composition have been done. The low species diversity is explained of larvae of the spawning hermatypic coral Acropora by its low environmental diversity and isolated location, tenuis. Mar Ecol Prog Ser 346: 89-96 which permits the recruitment of coral larvae with long Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M competency period. However, the competency period has (2002) Larval survivorship, competency periods and set- been known only for few species and more information tlement of two brooding corals, Heliopora coerulea and for the other species is necessary for further discussion. Pocillopora damicornis. Mar Biol 141: 39-46 Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Acknowledgements Coral reefs. Elsevier, Amsterdam, pp 133-207 Hayashibara T, Seno K, Yoneyama S (2006) Reef-building corals We are grateful to K. Shimoike and M. Kitano for their on Okino-torishima. Tokyo Metropolitan Reserch on Fish- involvement in the fi eld survey and coral identifi cation, to eries Science 1: 87-95 Hughen KA, Baillie MGL, Bard E, Beck JW, Bertrand CJH, H. Fukami for allowing us to refer to unpublished in- Blackwell PG, Buck CE, Burr GS, Cutler KB, Damon PE, formation from genetic analyses, and to T. Tozuka for his Edwards RL, Fairbanks RG, Friedrich M, Guilderson TP, comments on ocean currents. This research was conducted Kromer B, McCormac G, Manning S, Ramsey CB, Reimer by the Ministry of Land, Infrastructure, Transport and PJ, Reimer RW, Remmele S, Southon JR, Stuiver M, Tourism, the Fisheries Agency, and the Tokyo Metropoli- Talamo S, Taylor FW, van der Plicht J, Weyhenmeyer CE tan Government. The analysis was partly supported by the (2004) Marine04 marine radiocarbon age calibration, 0- Ocean Policy Research Foundation and the University of 26 cal kyr BP. Radiocarbon 46: 1059-1086 Tokyo Ocean Alliance. Kobashi F, Kawamura H (2002) Seasonal variation and instab- 84 Kayanne et al.: Corals in Okinotorishima

ility nature of the North Pacifi c Subtropical Countercurrent Richmond RH (1987) Energetics, competence, and long-distance and the Hawaiian Lee Countercurrent. J Geophys Res 107: dispersal of planula larvae of the coral Pocillopora damicornis. 3185, doi:10.1029/2001JC001225 Mar Biol 93: 527-533 Kobayashi K (2004) Origin of the Palau and Yap trench-arc Roberts CM (1997) Connectivity and management of Caribbean systems. Geophys J Int 157: 1303-1315 coral reefs. Science 278: 1454-1457 Kohler KE, Gill SM (2006) Coral Point Count with Excel ex- Stuiver M, Reimer PJ (1993) Extended 14C data base and re vised tensions (CPCe): A Visual Basic program for the deter- CALIB 3.0 14C age calibration program. Radiocarbon 35: mination of coral and substrate coverage using random 215-230 point count methodology. Comput Geosci 32: 1259-1269 Stuiver M, Braziunas TF (1993) Modelling atmospheric 14C in- Maragos JE, Jokiel PL (1986) Reef corals of Johnston Atoll - fl uences and 14C ages of marine samples to 10,000 BC. one of the worlds most isolated reefs. Coral Reefs 4: 141- Radiocarbon 35: 137-189 150 Stuiver M, Reimer PJ, Reimer RW (2005) CALIB 5.0. Maximenko N, Niiler P, Rio MH, Melnichenko O, Centurioni L, Tachikawa H, Suganuma H, Sato F (1991) Hermatypic corals of Chambers D, Zlotnicki V, Galperin B (2009) Mean dy- and Archipelago Research Report, namic topography of the ocean derived from satellite and Tokyo Metropolitan University, Tokyo, pp 285-296 drifting buoy data using three different techniques. J Atmos Tayama R (1952) Coral Reefs of the South Seas. Bull Hydro- Ocean Tech 26: 1910-1919 graphic Offi ce, Maritime Safety Agency of Japan 11: 1- Nakamura R, Ando W, Yamamoto H, Kitano M, Sato A, Naka- 292 mura M, Kayanne H, Omori M (2011) Corals mass-cul- Veron JEN (1993) Corals of Australia and the Indo-Pacifi c. tured from eggs and transplanted as juveniles to their University of Hawaii Press, Honolulu native, remote coral reef. Mar Ecol Prog Ser 436: 161-168 Veron JEN, Devantier LM, Turak E, Green AL, Kininmonth S, Nishihira M, Veron JEN (1995) Hermatypic corals of Japan. Stafford-Smith M, Peterson N (2009) Delineating the Kaiyusha, Tokyo Coral Triangle. Galaxea J Coral Rreef Stud 11: 91-100 Nishikawa A, Sakai K (2003) Genetic variation and gene fl ow of Veron JEN, Minchin PR (1992) Correlations between sea surface broadcast spawning and planula brooding coral, Goniastrea temperature, circulation patterns and the distribution of aspera (Scleractinia) in the Ryukyu Archipelago, southern hermatypic corals of Japan. Cont Shelf Res 12: 835-857 Japan. Zool Sci 20: 1031-1038 Veron JEN, Stafford-Smith M (2000) Corals of the world. Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates Australian Institute of Marine Science, Townsville and gene fl ow of broadcast-spawning (Acropora tenuis) Wallace C (1999) Staghorn Corals of the World. CSIRO Pub- and planula-brooding (Stylophora pistillata) corals. Mar lishing, Collingwood Ecol Prog Ser 256: 87-97 Yukihira H, Shimoike K, Golbuu Y, Kimura T, Vector S, Ohba H Qiu B, Chen SM (2010) Interannual variability of the orth Pa- (2007) Coral reef communities and other marine biotopes cifi c Subtropical Countercurrent and its associated meso- in Palau. In: Kayanne H, Omori M, Fabricius K, Verheiji scale eddy fi eld. J Phys Oceanogr 40: 213-225 E, Colin P, Golbuu S, Yukihira H (eds) Coral reefs of Randall RH (1995) Biogeography of reef-building corals in the Palau. Palau International Coral Reef Center, Palau, pp Mariana and Palau Islands in relation to back-arc rifting 10-29 and the formation of the eastern Philippine Sea. Nat His- tory Res 3: 193-210 Received: 22 June 2012 Randall RH (2003) An annotated checklist of hydrozoan and Accepted: 28 October 2012 scleractinian corals collected from Guam and other Mariana Islands. Micronesica 35-36: 121-137 Ⓒ Japanese Coral Reef Society Kayanne et al.: Corals in Okinotorishima 85 c corals at the site, respectively fi c. 1 and 0 represent presence absence of the speci fi A list of hermatypic corals at the 17 sites in northwest Paci A

Supplementary Table 1 Supplementary Table 86 Kayanne et al.: Corals in Okinotorishima Continued

Supplementary Table 1 Supplementary Table Kayanne et al.: Corals in Okinotorishima 87 Continued

Supplementary Table 1 Supplementary Table 88 Kayanne et al.: Corals in Okinotorishima Continued

Supplementary Table 1 Supplementary Table Kayanne et al.: Corals in Okinotorishima 89 Continued

Supplementary Table 1 Supplementary Table 90 Kayanne et al.: Corals in Okinotorishima Continued

Supplementary Table 1 Supplementary Table Kayanne et al.: Corals in Okinotorishima 91 Continued

Supplementary Table 1 Supplementary Table 92 Kayanne et al.: Corals in Okinotorishima Continued

Supplementary Table 1 Supplementary Table Kayanne et al.: Corals in Okinotorishima 93 Continued

Supplementary Table 1 Supplementary Table 94 Kayanne et al.: Corals in Okinotorishima Continued

Supplementary Table 1 Supplementary Table Kayanne et al.: Corals in Okinotorishima 95 Continued

Supplementary Table 1 Supplementary Table