Holocene key coral species in the Northwest Pacific: indicators of reef formation and reef ecosystem responses to global climate change and anthropogenic stresses in the near future

Quaternary Science Reviews 35 (2012) 82e99

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Holocene key coral species in the Northwest Pacific: indicators of reef formation and reef ecosystem responses to global climate change and anthropogenic stresses in the near future Chuki Hongo* Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies (NIES), 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan

a r t i c l e i n f o

a b s t r a c t

Article history: Received 21 August 2011 Received in revised form 6 January 2012 Accepted 11 January 2012 Available online 1 February 2012

The geological record of key coral species that contribute to reef formation and maintenance of reef ecosystems is important for understanding the ecosystem response to global-scale climate change and anthropogenic stresses in the near future. Future responses can be predicted from accumulated data on Holocene reef species identified in drillcore and from data on raised reef terraces. The present study analyzes a dataset based on 27 drillcores, raised reef terraces, and 134 radiocarbon and UeTh ages from reefs of the Northwest Pacific, with the aim of examining the role of key coral species in reef growth and maintenance for reef ecosystem during Holocene sea-level change. The results indicate a latitudinal change in key coral species: arborescent Acropora (Acropora intermedia and Acropora muricata) was the dominant reef builder at reef crests in the tropics, whereas Porites (Porites australiensis, Porites lutea, and Porites lobata) was the dominant contributor to reef growth in the subtropics between 10,000 and 7000 cal. years BP (when the rate of sea-level rise was 10 m/ka). Acropora digitifera, Acropora hyacinthus, Acropora robusta/ A. abrotanoides, Isopora palifera, Favia stelligera, and Goniastrea retiformis from the corymbose and tabular Acropora facies were the main key coral species at reef crests between 7000 and 5000 cal. years BP (when the rate of sea-level rise was 5 m/ka) and during the following period of stable sea-level. Massive Porites (P. australiensis, P. lutea, and P. lobata) contributed to reef growth in shallow lagoons during the period of stable sea level. Key coral species from the corymbose and tabular Acropora facies have the potential to build reefs and maintain ecosystems in the near future under a global sea-level rise of 2e6 m/ka, as do key coral species from the arborescent Acropora facies and massive Porites facies, which show vigorous growth and are tolerant to relatively deep-water, low-energy environments. However, these species are likely to experience severe mortality in upcoming decades due to natural and anthropogenic stresses. Consequently, this damage will lead to a collapse in reef formation and the maintenance of reef ecosystems in the near future. This study emphasizes the need for research into the conservation of key coral species. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Key coral species Sea level Global warming Anthropogenic stress Species diversity Northwest Pacific

1. Introduction Key coral species (e.g., Smith et al., 2008; Hennige et al., 2010) or key species (e.g., Idjadi et al., 2006; Hongo and Kayanne, 2010a,b) contribute to the variability in physical conditions, resources, and habitats required by many other organisms; consequently, coral reefs are one of the most important life-supporting systems on Earth (Huston, 1994). However, coral reef formations and species diversity have shown great losses worldwide (Gardner et al., 2003; Bruno and Selig, 2007; Wilkinson and Souter, 2008; Alvarez-Filip et al., 2011), influenced by recent climate change and human impacts; e.g.,

* Tel.: þ81 29 850 2416; fax: þ81 29 850 2219. E-mail address: [email protected]. 0277-3791/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.quascirev.2012.01.011

overfishing, increased sediment runoff, coral disease, hurricanes, and coral bleaching (e.g., Hughes et al., 2003; Bruno et al., 2009; Maina et al., 2011). Consequently, knowledge of temporal and spatial pattern of coral reef in the near future is significant concerns. Various scientific approaches, based on ecology and biology, have been employed to study the conservation and restoration of coral reefs, leading to the direct transplantation of juvenile corals at sites worldwide in recent decades (Edwards and Clark, 1998; Lindahl, 2003; Soong and Chen, 2003; Dizon and Yap, 2006). However, previous studies have reported conflicting results in terms of the key coral species for reef conservation (Rinkevich, 2005; Omori, 2011); consequently, the optimal coral species for future reef ecosystems remain poorly understood. Geological knowledge regarding the growth patterns and internal facies of coral reefs has shown a marked improvement in the past

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

40 years (e.g., Macintyre and Glynn, 1976; Konishi et al., 1978; Marshall and Davies, 1982; Cabioch et al., 1995, 1999; Kan et al., 1995; Montaggioni and Faure, 1997; Shen et al., 2010). During the last postglacial period, reef formation occurred in response to sea-level rise at rate of 5e10 m/ka (e.g., Montaggioni and Braithwaite, 2009). The amount of global sea-level rise until 2099 is projected to be 0.18e0.59 m, equivalent to a rate of 2e6 m/ka (Meehl et al., 2007). Although other environmental factors (e.g., increasing sea-surface temperature and ocean acidification) will affect coral reefs (e.g., Pandolfi et al., 2011), this projection indicates the potential for reef formation worldwide. Consequently, it is important to identify key coral species that are indicators of the building and maintenance of reef ecosystems in response to the future sea-level rise, in order to evaluate and project the magnitude of reef formation and species diversity. Species-level records from fossil corals indicate that few species (Acropora palmata and Acropora cervicornis) contributed to reef formation in the Caribbean during the Quaternary (Blanchon et al., 2002; Gischler and Hudson, 2004; Hubbard et al., 2005; Macintyre, 2007). Perry et al. (2008) reported that Acropora pulchra, Montipora mollis, and Turbinaria frondens were the main reef builders at a turbid reef (Paluma Shoal) on the Great Barrier Reef, Australia, during the past 1200 years. Hongo and Kayanne (2010b, 2011) reported that the active role of a small number of coral species was the most important factor in reef formation and the maintenance of coral reef ecosystems at sites in the Northwest Pacific during the Holocene. These species are characterized by a rigid growth form that is strongly resistant to wave action and by a high growth rate that enables vigorous upward reef growth. The distribution of key coral species is an important aspect of research into reef restoration and conservation, yet little is known of the temporal and spatial patterns of such species. Coral reefs in the Northwest Pacific are of particular interest because this region ranges from the Coral Triangle to areas of low species diversity, such as along the Kuroshio (Veron, 1995). The aim of the present study is to compare the key coral species and reef growth during the period of post-glacial sea-level change at different sites within the Northwest Pacific (Fig. 1), to identify geographical variations in key coral species with the aim of predicting their survival and development in the future, and to suggest suitable approaches to conservation and restoration planning in the near future. The dataset examined in this study includes 27 drillcores and the records of raised reef terrace constrained by 134 dates (87 radiocarbon ages and 47 UeTh ages). The data have been collected from reefs in the Northwest Pacific, as follows: Nakaguma reef at Kikai Island (Konishi et al., 1978, 1983, 1985; Webster et al., 1998), Shidooke reef at Kikai Island (Sasaki et al., 1998; Ota et al., 2000; Sugihara et al., 2003; Hongo, 2010), Kurohana reef at Yoron Island (Yonekura et al., 1994; Hongo and Kayanne, 2011), Ibaruma reef at Ishigaki Island (Hongo and Kayanne, 2009), and Ngemelis reef at the Palau Islands (Kayanne et al., 2002; Hongo and Kayanne, 2011). Data were excluded from Luzon in the Philippines (Shen et al., 2010), Tonaki Island (Kan et al., 1997), Kume Island (Takahashi et al., 1988), and other reefs (e.g., Kan and Hori, 1993; Kan et al., 1995; Yamano et al., 2001; Kan and Kawana, 2006) because the coral records at these sites were restricted to the genera level. 2. Regional setting and dataset 2.1. Kikai Island Kikai Island (28 200 N, 130 000 E; Fig. 1a) in the central Ryukyu Islands is influenced by the warming western boundary current (Kuroshio Current). The mean sea-surface temperature is 20.5e28.5  C (Japan Meteorological Agency; see http://www.data. kishou.go.jp/kaiyou/db/kaikyo/dbindex.html). The tide is semi-

83

diurnal with a range of 2.4 m at sprig tide, and the mean low-water spring tide is 1.2 m below mean sea level (MSL) at Amami port (28 190 N, 129 320 E) on Amami Island (Japan Meteorological Agency; see http://www.data.kishou.go.jp/kaiyou/db/tide/suisan/). This island is situated in the Asian monsoon region, with southerly winds predominating in summer and stronger northerly winds in winter. According to Veron (1992), Kikai Island belongs to the Amami geographic region (28 N), which contains 220 coral species. Kikai Island is part of an active island arc system and is characterized by raised reefs. Over the past 125,000 years, the island has been uplifted by w220 m, at a rate of less than 2 mm/year (Konishi et al., 1974). Four raised reef terraces (Terraces IeIV) were developed during the Holocene due to global sea-level change coupled with regional tectonic uplift of the island (Ota et al., 1978). Terrace I is the highest of the Holocene reef terraces, located less than 10e11 m above the present MSL (Sasaki et al., 1998; Webster et al., 1998; Ota et al., 2000; Sugihara et al., 2003). However, this terrace is rarely exposed because of extensive cultivation on the island. Terraces IIeIV are well exposed around the entire coastline of the island, and they retain a reef flat and distinct spur and groove systems (Sasaki et al., 1998; Webster et al., 1998; Ota et al., 2000; Sugihara et al., 2003; Hongo, 2010). Terraces IIeIV are located at approximately 4e5, 2e3, and 1e2 m above the present MSL, respectively (e.g., Webster et al., 1998; Sugihara et al., 2003; Hongo, 2010). A fifth reef terrace is currently being formed by the present-day reef. Nakaguma reef is 400 m wide and consists of Holocene reef terraces (Fig. 2a). It is situated on the northwest coast of the island and is affected by monsoonal winds during winter, making it a moderate-energy reef. Bio-lithological descriptions and radiometric dating of the reef have been based on 13 Holocene cores (NG-1 to -13; 8.5e25.0 m long; 72e77 mm in inner diameter and 84e88 mm in outer diameter) (Konishi et al., 1978, 1983, 1985). Cores were recovered using a rotary system with an oil-feed drilling system (OP-1 type) during 1977e1982 (Konishi et al., 1978, 1983). The drill system comprised a boring machine, a drilling pump, and drilling strings. The piston displacement of the engine was 5500 W. The maximum output of the water pump was 6.0  102 m3/min, and the average recovery of Holocene reefs was 31%e93% (Konishi et al., 1983; Table 1). Moreover, observations of Holocene reef terraces have revealed the detailed spatial and temporal distribution of corals (Konishi et al., 1978; Webster et al., 1998). Shidooke reef, located east of Kikai Island, is 800 m wide and consists of Holocene reef terraces (Fig. 2b, c). This reef is a typical high-energy reef, exposed throughout the year to large waves originating from Pacific swell and monsoonal winds during summer. Three Holocene cores (SD-1 to -3; 20.0e27.0 m long) were recovered from this reef during 1996e1997 (Ota, 1998; Ota et al., 2000). Previous studies have examined Holocene reef terraces at this site (Sasaki et al., 1998; Ota et al., 2000; Sugihara et al., 2003; Hongo, 2010). 2.2. Yoron Island Yoron Island (27 020 N, 128 260 E ; Fig. 1b), located north of Okinawa Island, has a sea-surface temperature (SST) of 21.0e28.5  C (Japan Meteorological Agency; see http://www.data.kishou.go.jp/ kaiyou/db/kaikyo/dbindex.html). The tide is semi-diurnal with a range of 1.6 m at spring tide, and the mean low-water spring tide is 0.8 m below MSL at Chabana port (27 030 N, 128 250 E) on the island (Japan Coast Guard, 2007). The island is home to w200 coral species (Nishihira and Veron, 1995). Kurohana reef (Fig. 2d) is located on northeast coast of Yoron Island. The reef faces the open ocean and is affected by monsoonal winds, making it a high-energy reef. The reef consists of distinctly zoned landforms comprising a reef flat (shallow lagoon and reef

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C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Fig. 1. Map showing the location of the Northwest Pacific reefs considered in this study. Gray arrows indicate the schematic paths of the Kuroshio Current and the North Equatorial Current. The detailed maps show (a) Kikai Island in the northern Ryukyu Islands, (b) Yoron Island in the central Ryukyu Islands, (c) Ishigaki Island in the southern Ryukyu Islands, and (d) the Palau Islands. Solid lines show the locations of transects along which the altitude of raised reef terraces or water depth was surveyed. Black circles show the locations of drilling sites.

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Fig. 2. Topographic profiles and sedimentary facies of Holocene reefs at (a) Nakaguma reef at Kikai Island, (b) Shidooke reef at Kikai Island, (c) Holocene raised reef terraces of Shidooke reef at Kikai Island, (d) Kurohana reef at Yoron Island, (e) Ibaruma reef at Ishigaki Island, and (f) Ngemelis reef at the Palau Islands. Four sedimentary facies (corymbose and tabular Acropora facies, arborescent Acropora facies, massive Porites facies, and detritus facies) are identified in this study. Detailed descriptions of the facies are provided in Table 3. MSL and MLWL indicate mean sea level and mean lowest water level, respectively.

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in inner diameter and 55 mm in outer diameter) were obtained from four holes (YR-II, YR-III, YR-IV, and YR-V) drilled at Kurohana reef (Yonekura, 1986; Yonekura et al., 1994). Three of the cores (YR-II, YR-III, and YR-V) were recovered from the reef crest, while YR-IV was recovered from the shallow lagoon. Cores were recovered using a rotary system with a gasoline-feed drilling system (HIPAC-CDS-2) during 1983e1984 (Ishii and Kayanne, 1986). The drill system comprised a boring machine, a drilling pump, and drilling strings. The piston displacement of the engine was 2900 W, and the maximum output of the water pump was 3.4  102 m3/min. The double core barrel ensured high recovery, with the average recovery of Holocene reefs being 79%e99% (Hongo and Kayanne, 2011; Table 1).

f

2.3. Ishigaki Island

Fig. 2. (continued). Table 1 Details of drilling cores recovered from study sites in the Northwest Pacific. Core ID

Length (m)

Kikai Island NG-1 9.5 NG-2 11.0 NG-3 9.4 NG-4 10.8 NG-5 17.7 NG-6 8.5 NG-7 8.7 NG-8 23.6 NG-9 11.5 NG-10 18.8 NG-11 25.0 NG-12 11.7 NG-13 25.0 SD-1 20.0 SD-2 27.0 SD-3 26.2 Yoron Island YR-II 1.8 YR-III 3.2 YR-IV 1.5 YR-V 3.8 Ishigaki Island IB-1 13.0 IB-2 22.0 IB-3 25.0 IB-4 2.7 Palau Islands PL-I 25.0 PL-II 25.0 PL-III 30.0

Thickness of Holocene sequence (m)

Altitude from MSL (m)

Recovery (%)*

9.3 11.0 9.4 10.8 16.0 8.5 8.7 20.5 11.5 18.8 23.5 11.7 19.7 >18.0 >24.0 25.9

þ2.8 þ2.7 þ2.6 þ2.5 þ2.1 þ1.9 þ0.3 0.3 0.3 1.8 1.8 7.4 9.4 þ2.2 þ4.0 þ2.2

63 31 84 82 92 93 89 74 70 76 63 85 42 N/A N/A N/A

1.8 3.2 1.5 3.8

0.4 0.5 1.3 0.5

99 79 93 98

10.5 21.1 22.4 2.7

3.4 1.0 0.8 0.7

100 95 92 96

15.0 16.0 23.0

1.2 1.4 1.5

77 64 61

Note that asterisk indicate the number is for Holocene reefs.

crest) and reef slope (Yonekura et al., 1994; Nakai, 2007). The shallow lagoon (2e5 m deep) is situated between the reef crest and the shore. The reef crest, which forms a topographic high along the reef margin, is 100e150 m wide and is emergent during low tide. The reef slope is characterized by spur and groove systems that extend 250 m seaward to a water depth of 20 m. Holocene drillcores (1.8e3.4 m long; 42 mm

Ishigaki Island (24 250 N, 124100 E; Fig. 1c) is located w430 km southwest of Okinawa Island. The monthly average SST is 23.5e29.0  C in summer (Japan Meteorological Agency; see http:// www.data.kishou.go.jp/kaiyou/db/kaikyo/dbindex.html) and the tide is semi-diurnal, with a range of 2.1 m at spring tide; the mean low-water spring tide is 1.1 m below MSL at Ishigaki port on Ishigaki Island (Japan Meteorological Agency; see http://www.data.kishou.go. jp/kaiyou/db/tide/suisan/). The island is home to 363 coral species (Veron, 1992). Ibaruma reef (Fig. 2e) occurs along the eastern side of Ishigaki Island, enclosing a shallow lagoon that is up to 1000 m wide. This reef is a high-energy reef and is exposed throughout the year to large waves originating from Pacific swell and monsoonal winds during summer (Hongo and Kayanne, 2009). Four Holocene cores (IB-1 to -4; 2.7e25.0 m long; 50e55 mm in inner diameter and 66 mm in outer diameter) were recovered from Ibaruma reef: two from the reef crest and two from the shallow lagoon (Hongo and Kayanne, 2009). The cores were recovered using a rotary system with an oil- or gasolinefeed drilling system in 1989 and 2006 (Hongo and Kayanne, 2009). The drill system comprised a boring machine, a drilling pump, and drilling strings. The piston displacement of the engine was 5500 W, and the maximum output of the water pump was 6.0  102 m3/min. The average recovery of Holocene reefs was 92%e100% (Hongo and Kayanne, 2009; Table 1). 2.4. Palau Islands The Palau Islands consist of volcanic and limestone islands. The Ngemelis barrier reef (7 240 N, 134 210 E; Fig. 1d) is located west of Babeldaob Island, which is subjected to seasonal winds, including a northeast trade wind from November to May, and a southesouthwest wind from June to October (Wolanski and Furukawa, 2007). The reef is protected by trade winds, making it a moderateto low-energy reef (Kayanne et al., 2002; Hongo and Kayanne, 2011). The average SST in this area is 28e30  C (Morimoto et al., 2002). The tide is semi-diurnal with a range of 1.5 m at spring tide, and the mean low-water spring tide is 1.1 m below MSL (NOAA, 2002). The Palau Islands are situated in an area with high species diversity, including w400 species of coral (Yukihira et al., 2007). The Ngemelis barrier reef (1e3 km wide) is a topographically well-developed barrier reef that comprises a distinct lagoon, a reef flat, and a reef slope. The lagoon, 15 km wide and with a maximum depth of 50 m, separates the island from the reef flat (Kayanne et al., 2002), which is w1600 m wide and located 1 m below MSL (Kayanne et al., 2002; Hongo and Kayanne, 2011). Three deep cores (PL-I to -III; 66 mm in inner diameter and 88 mm in outer diameter) were recovered from Ngemelis reef in 1991 (Kayanne et al., 2002). PL-I and PL-II were recovered from the reef crest and sand flat, respectively, whereas PL-III was recovered from a patch reef in the lagoon (Fig. 2f). These cores are 25e30 m long, penetrating the

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Pleistocene reef. Cores were recovered using a rotary system with an oil-feed drilling system (Toho D-O type; Hongo and Kayanne, 2011). The drill system comprised a boring machine, a drilling pump, and drilling strings. The piston displacement of the engine was 5590 W, and the maximum output of the water pump was 6.0  102 m3/min. The core barrel and casing ensured high performance and high recovery, with an average recovery of Holocene reefs of 61%e77% (Kayanne et al., 2002; Hongo and Kayanne, 2011; Table 1).

terraces at Nakaguma and Shidooke reefs, Kikai Island. The facies is characterized by common corals dominated by corymbose and tabular Acropora (e.g., A. digitifera, A. robusta/A. abrotanoides, and A. hyacinthus). These corals are found under high-energy conditions at the reef crest and the upper reef slope around the present study sites (Sugihara et al., 2003; Nakamura and Nakamori, 2006; Nakai, 2007), and at Indo-Pacific reefs (Done, 1982; Montaggioni and Faure, 1997; Cabioch et al., 1999; Montaggioni and Braithwaite, 2009).

2.5. Species composition and ages

3.1.2. Arborescent Acropora facies The arborescent Acropora facies, which is restricted to the lower unit of the reef crest section and to patch reefs in the lagoon at the Palau Islands (cores PL-I and PL-III), is characterized by arborescent Acropora (A. muricata/Acropora intermedia). These corals are present at the inner reef slope and under low-energy wave conditions near the present study sites (Nakamori, 1986; Nakai, 2007; Yukihira et al., 2007), and in the Indo-Pacific Ocean (Done, 1982; Montaggioni and Braithwaite, 2009; Hongo and Kayanne, 2010b).

Previous studies have reported data on the species composition and ages of fossil corals from reefs in the Northwest Pacific (Konishi et al., 1978, 1983, 1985; Yonekura et al., 1994; Sasaki et al., 1998; Webster et al., 1998; Ota et al., 2000; Kayanne et al., 2002; Sugihara et al., 2003; Hongo and Kayanne, 2009, 2011; Hongo, 2010). The species record of fossil corals from Yoron Island, Ishigaki Island, and the Palau Islands was determined by criteria of reliability (Hongo and Kayanne, 2009, 2011), but the criteria employed for corals from Kikai Island remain unknown (Sasaki et al., 1998; Webster et al., 1998; Ota et al., 2000). Forty-nine coral samples from Kikai Island (Konishi et al., 1978, 1983, 1985; Sugihara et al., 2003), 10 from Yoron Island (Yonekura, 1986; Yonekura et al., 1994), 9 from Ishigaki Island (Hongo and Kayanne, 2009), and 19 from the Palau Islands (Kayanne et al., 2002) were subjected to radiocarbon dating as part of the present study. Moreover, 47 230Th/234U ages have been reported from Kikai Island (Sasaki et al.,1998; Ota et al., 2000). The radiocarbon and UeTh ages are listed in Tables 2 and 3, respectively. From this database, only in situ and unaltered aragonite corals were selected for this study. The radiocarbon ages were determined using liquid scintillation counting methods (e.g., Togashi and Matsumoto, 1983), except for the age data from Sugihara et al. (2003), which were measured by AMS (accelerator mass spectrometry). All of the radiocarbon ages were calibrated to calendar years using the calibration program CALIB 6.0 (Stuiver and Reimer, 1993) and using the marine calibration dataset Marine09 (Reimer et al., 2009). The marine reservoir correction (DR) value was assumed to be 5  15 for Kikai Island (Yoshida et al., 2010), 38  10 for Yoron Island (Yoshida et al., 2010), 35  25 for Ishigaki Island (Hideshima et al., 2001), and 101  44 for the Palau Islands (Yoneda et al., 2007). The 230Th/234U ages were determined by the a-spectrometric method based on a five-step screening protocol (Omura et al., 1995). The errors for 14C and 230Th/234U ages are given by 2s and 1s, respectively. The average reef-growth curve was calculated for the periods between dated samples. 3. Results

3.1.3. Massive Porites facies The massive Porites facies occurs in the lower unit of the Holocene Nakaguma reef at Kikai Island (cores NG-1, -5, -8, -10, and -11), the upper unit of the shallow lagoon section at Shidooke reef at the same island (core SD-1), the upper unit of the shallow lagoon section at Yoron Island (core YR-IV), and the upper unit of the shallow lagoon section and the patch reef section in the lagoon at the Palau Islands (cores PL-II and PL-III). This facies consists of in situ massive Porites that is interpreted to have grown in a shallow lagoon or on a reef slope under deep-water/low-energy conditions near the present study sites (Kayanne et al., 2002; Nakai, 2007; Hongo and Kayanne, 2010a,b) and at other reefs (Marshall and Davies, 1982; Montaggioni, 2005). 3.1.4. Detritus facies The detritus facies occurs in the middle unit of Nakaguma reef and the lower unit of Shidooke reef at Kikai Island (cores NG-2 to -13, and SD-1 to -3), the lower unit of the reef crest and the shallow lagoon section at Yoron Island (cores YR-III, -IV, and -V), all of the shallow lagoon section (cores IB-1 and -2) and the lower unit of the reef crest section at Ishigaki Island (core IB-3), and the lower unit of the shallow lagoon section at the Palau Islands (core PL-II). This facies consists of allochthonous coral fragments and other calcareous organisms (gastropods, bivalves, calcareous algae, foraminifera tests, and echinoid debris). The depositional environment is interpreted to have been a lagoon and shallow lagoon subjected to low-energy conditions, located near the present study sites (Nakai, 2007; Nakamura and Nakamori, 2009; Hongo and Kayanne, 2010a,b) and at other reefs (Montaggioni, 2005).

3.1. Internal composition and facies of reefs 3.2. Key coral species Four facies were observed in the analyzed cores and at outcrops. The internal structures and detailed descriptions of the reefs are provided in Fig. 2 and Table 4. Below, each of the facies is summarized in turn. 3.1.1. Corymbose and tabular Acropora facies The corymbose and tabular Acropora facies are dominant in the upper unit of Nakaguma and Shidooke reefs at Kikai Island (cores NG-3 to -12, SD-2, and SD-3), Holocene raised reef terraces on Kikai Island, the upper unit of the reef crest section at Yoron Island (cores YR-II, -III, and -V), the upper unit of the reef crest section at Ishigaki Island (cores IB-3 and IB-4), and the upper unit of the reef crest section at the Palau Islands (core PL-I). Analyses of outcrops indicate that this facies is also dominant at the surface of Holocene reef

Among the Holocene reefs, 16 genera and 40 species were identified as key coral species from the cores and outcrop records. A detailed description of the key coral species and facies is provided in Table 4, and a list of key coral species is given in Table 5. The following paragraphs summarize the key coral species in each of the facies. In the corymbose and tabular Acropora facies, 15 genera and 32 key coral species were identified in the cores and outcrops. In particular, A. digitifera and A. hyacinthus were widely distributed in Holocene reefs of the Northwest Pacific. Holocene reefs in this region also contain abundant A. robusta/A. abrotanoides, Isopora palifera, Goniastrea retiformis, and Favia stelligera (Table 5). In the arborescent Acropora facies, the key coral species from Holocene reefs are

Reef location and cited reference

Sample ID

Laboratory codea

Altitude from MSL (m)

Core and terrace No.

Sample

Aragonite contentb

Measured 14C age (years BP  1s)

d13C (&)

Conventional 14 C age (years BP)

Calibrated 14C age (cal. years BP  2s)e

LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL

3.3 2.7 2.6 2.5 2.1 1.6 1.5 0.8 0.4 2.5 1.0 1.2 5.9 2.0 10.4 12.8 13.5 1.7 0.5 1.3 1.4 3.2 4.9 0.2 6.4 0.4 20.6 0.5 9.1 1.9 19.8 20.3 21.8 9.4 13.4 24.4 25.0 27.4

Terrace-III Terrace-III Terrace-III Terrace-III Terrace-III Terrace-IV Terrace-IV Core-NG-1 Core-NG-2 Core-NG-3 Core-NG-3 Core-NG-4 Core-NG-4 Core-NG-5 Core-NG-5 Core-NG-5 Core-NG-5 Core-NG-6 Core-NG-6 Core-NG-6 Core-NG-6 Core-NG-6 Core-NG-6 Core-NG-7 Core-NG-7 Core-NG-8 Core-NG-8 Core-NG-9 Core-NG-9 Core-NG-10 Core-NG-10 Core-NG-11 Core-NG-11 Core-NG-13 Core-NG-13 Core-NG-13 Core-NG-13 Core-NG-13

Favites sp. Montipora sp. Goniastrea sp. Favia sp. Favites sp. Goniastrea sp. Favites sp. Acropora sp. Favia sp. Acropora sp. Favites sp. Favites sp. Goniastrea sp. Favites sp. Montipora sp. ? Acropora sp. Montipora sp. ? Goniastrea sp. Leptoria sp. Montastrea sp. Goniastrea sp. Montipora sp. ? Acropora sp. Favites sp. Goniastrea sp. Favites sp. Porites sp. Goniastrea sp. Acropora sp. Montipora sp. ? Acropora sp. Porites sp. Porites sp. Favia sp. Favia sp. Montipora sp. Montipora sp. Montipora sp.

100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100%

3790  70 3400  70 3490  60 3650  70 3360  50 3190  50 2410  50 3530  80 3900  80 4100  80 4690  90 3780  80 5540  90 3020  80 7460  90 7460  90 8070  90 3320  100 3980  90 4610  90 4740  100 5080  120 4890  80 3050  80 5270  80 1750  80 8530  100 2160  110 5120  80 1750  80 6730  90 8190  150 8620  130 450  110 1670  110 8390  160 9030  130 8720  180

N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A

3390 3000 3090 3250 2960 2790 2010 3130 3500 3700 4290 3380 5140 2620 7060 7060 7670 2920 3580 4210 4340 4680 4490 2650 4870 1350 8130 1760 4720 1350 6330 7790 8220 50 1270 7990 8630 8320

3240  190 2780  180 2880  150 3060  200 2730  130 2520  160 1560  140 2940  200 3380  200 3620  210 4410  280 3220  210 5480  190 2310  240 7550  160 7550  160 8140  190 2630  270 3470  220 4280  260 4500  290 4940  340 4640  200 2360  250 5160  240 880  180 8660  270 1300  240 5020  220 880  180 6790  240 8250  310 8740  330 modern 840  210 8540  400 9250  280 8870  450

NZA NZA NZA NZA NZA NZA NZA NZA NZA NZA NZA

4.3 4.2 3.9 3.2 2.6 2.3 2.2 2.1 1.6 0.7 0.3

Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-III Terrace-III Terrace-III Terrace-IV Terrace-IV

Acropora robusta Acropora gemmifera Acropora gemmifera Acropora gemmifera Acropora formosa Acropora robusta Acropora gemmifera Acropora digitifera Acropora palifera Pocillopora damicornis Acropora gemmifera

100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100%

5670 3810 5900 4260 4890 5990 3270 3360 3030 2540 1610

N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A

5270 3410 5500 3860 4490 5590 2870 2960 2630 2140 1210

5620  150 3270  160 5880  190 3810  180 4670  160 6030  170 2590  170 2710  170 2320  210 1710  160 770  120

          

60 60 70 60 60 60 60 60 70 60 60

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Kikai Island Nakaguma reef (28 200 2600 N, 129 580 0500 E) Konishi et al. (1978) 77051206 77051202 77051207 77051204 77051209 77051212 77051211 Konishi et al. (1983, 1985) KL-37 KL-257 KL-23 KL-24 KL-30 KL-26 KL-39 KL-28 KL-35 KL-32 KL-19 KL-258 KL-20 KL-259 KL-21 KL-22 KL-40 KL-27 KL-38 KL-36 KL-25 KL-29 KL-33 KL-34 KL-375 KL-368 KL-376 KL-378 KL-379 KL-524 KL-377 Shidooke reef (28 210 1100 N, 130 010 4500 E) Sugihara et al. (2003) NZA7025 NZA7023 NZA7024 NZA7022 NZA7026 NZA7027 NZA7021 NZA8625 NZA7020 NZA7018 NZA7019 Yoron Island

88

Table 2 Radiocarbon ages of fossil corals from Holocene reef cores and Holocene raised reef terraces of the Northwest Pacific.

Kurohana reef (27 030 5300 N, 128 270 0000 E) Yonekura (1986); Yonekura et al. (1994)

Ishigaki Island Ibaruma reef (24 300 1100 N, 124 170 2100 E) Hongo and Kayanne (2009)

Acropora hyacinthus ? Isopora palifera Acropora digitifera Acropora hyacinthus I. palifera Acropora digitifera I. palifera ? I. palifera ? Corymbose Acropora sp. Corymbose Acropora sp.

>99% >99% >99% >99% >99% >99% >99% >97% >99% >99%

2875 2860 3300 3600 4670 4760 3230 4960 4880 5260

         

80 60 90 80 90 90 90 80 80 100

N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A

2475 2460 2900 3200 4270 4360 2830 4560 4480 4860

1.6 2.7 5.3 6.9 7.5 10.8 17.2 20.3 6.4

Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-3 Core-IB-1

Acropora digitifera Favia stelligera Acropora sp. Acropora digitifera Acropora sp. Montastrea curta Favites sp. Acropora digitifera Acropora sp.

>97% >99% 100% 100% >96% 100% >95% N/A >98%

4180 4370 5080 5330 5620 5920 6630 7000 6040

        

80 60 50 60 60 70 70 60 60

0.4 0.7 0.5 1.0 2.2 0.8 0.2 0.9 0.9

4600 4770 5490 5730 6000 6320 7040 7400 6430

        

JGS-438 JGS-415 JGS-412 JGS-416 JGS-417

1.8 2.5 4.4 6.8 12.0

Core-PL-I Core-PL-I Core-PL-I Core-PL-I Core-PL-I

>99% >99% >99% >99% >99%

N/A N/A N/A N/A N/A

0.8 2.3 0.1 0.4 0.3

3950 5870 6600 6720 6860

    

PL-I-79 PLeIIe11 PLeIIe33 PLeIIe49 PLeIIe58

JGS-413 JGS-432 JGS-414 JGS-429 JGS-430

15.1 2.0 5.0 9.3 12.2

Core-PL-I Core-PL-II Core-PL-II Core-PL-II Core-PL-II

>99% >99% >99% >99% >99%

N/A N/A N/A N/A N/A

1.2 1.3 0.8 0.9 0.0

7830  90 modern 2700  60 4400  110 5580  70

8180  200 modern 2280  210 4440  340 5860  210

PLeIIe78

JGS-418

15.3

Core-PL-II

>99%

N/A

0.9

6870  90

7280  200

PLeIIIe6 PLeIIIe8 PLeIIIe11 PLeIIIe17 PLeIIIe25 PLeIIIe34 PLeIIIe41

JGS-421 JGS-442 JGS-422 JGS-423 JGS-424 JGS-425 JGS-426

3.0 3.9 5.9 9.6 13.8 17.6 22.6

Core-PL-III Core-PL-III Core-PL-III Core-PL-III Core-PL-III Core-PL-III Core-PL-III

>99% >99% >99% >99% >99% >99% >99%

N/A N/A N/A N/A N/A N/A N/A

0.0 0.4 1.0 0.1 1.3 0.5 1.3

520  60 570  60 4440  70 4970  90 5610  80 6390  80 7380  80

modern modern 4480  240 5160  270 5890  230 6750  230 7750  170

PLeIIIe45

JGS-427

24.6

Core-PL-III

Massive Porites sp. Algal crust Acropora digitifera Acropora digitifera Acropora sp. cf. A. muricata/ A. intermedia Massive Porites sp. Massive Porites sp. Massive Porites sp. Montipora sp. Acropora sp. cf. A. muricata/A. intermedia Acropora sp. cf. A. muricata/A. intermedia Massive Porites sp. Massive Porites sp. Massive Porites sp. Massive Porites sp. Branching Porites sp. Massive Porites sp. Acropora sp. cf. A. muricata/ A. intermedia Massive Porites sp.

>99%

N/A

1.3

7530  80

7880  200

JGS-145 JGS-360c JGS-146 JGS-362c JGS-147 JGS-148 JGS-158 JGS-365c JGS-363c JGS-246

IB-3-8 IB-3-18 IB-3-32 IB-3-39 IB-3-44 IB-3-59 IB-3-97 IB-3-1950 IB-1-300

Beta-184774d Beta-209307d Beta-209308d Beta-209309d Beta-209310d Beta-209311d Beta-209312d Beta-184775 Beta-184771d

PL-I-3 PL-I-8 PL-I-26 PL-I-43 PL-I-67

0.7 0.9 2.2 0.9 2.0 3.6 0.9 2.3 2.7 3.0

2090 2080 2570 2970 4320 4470 2530 4700 4610 5080

         

200 180 220 210 260 260 210 210 200 250

80 60 50 60 60 70 80 70 60

4750 5020 5820 6100 6400 6750 7500 7820 6880

        

230 190 140 160 140 190 150 150 180

60 90 90 80 80

3810 6160 7000 7120 7280

    

210 220 240 210 190

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Palau Island Ngemelis reef (7 210 4900 N, 134 190 0500 E) Kayanne et al. (2002)

Core-YR-II Core-YR-II Core-YR-II Core-YR-III Core-YR-III Core-YR-III Core-YR-V Core-YR-V Core-YR-V Core-YR-V

YReIIe1 YReIIe2 YReIIe3 YReIIIe1 YReIIIe2 YReIIIe3 YR-V-1 YR-V-2 YR-V-3 YR-V-4

a

The laboratory code is the following: LLRL (Low Level Radioactivity Laboratory, Kanazawa University, Japan), NZA (Institute of Geological and Nuclear Sciences, New Zealand), JGS (Geological Survey of Japan), and Beta (Beta Analytic Inc., USA). b 100% in aragonite content indicated “unaltered corals” from cited references (Konishi et al., 1978, 1983, 1985; Sugihara et al., 2003). c The data of aragonite content was from Dr. Hajime Kayanne (per. comm.). d Data of aragonite content from Ibaruma reef are performed in the present study. e Calibrated 14C age are performed in the present study.

89

Reef location and cited reference

Sample ID

KS-45 AO432 KS-41 KS-44 KN-04 KS-65 KS-59 KS-61 KN-01 KN-08 KN-09 KN-07 KN-02 KN-06 KN-03 KS-50 AO445 AO437 KS-49 AO438 AO441 KS-48 AO439 KS-64 KS-66 KS-52 KS-53 KS-63 KS-62 a b

Th/234U ages of fossil corals from Holocene reef cores and Holocene raised reef terraces of the Northwest Pacific.

Altitude above MSL (m)

Core and terrace No.

Sample

Aragonite contenb

238

LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL

4.0 3.8 3.8 3.8 3.8 3.7 3.2 3.0 3.0 2.5 1.9 1.8 1.0 1.0 0.8 0.7

Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-II Terrace-III Terrace-III Terrace-III Terrace-III Terrace-IV Terrace-IV Terrace-IV Terrace-IV

Goniastrea sp. Acropora sp. Acropora sp. Acropora sp. Goniastrea sp. Goniastrea sp. Goniastrea sp. Goniastrea sp. Pavona sp. Acropora sp. Acropora sp. Acropora sp. Acropora sp. Acropora sp. Goniastrea sp. Goniastrea sp.

100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100%

2.858 3.628 3.436 3.356 2.730 3.032 2.764 2.593 3.395 3.910 3.741 3.817 3.836 4.002 2.756 2.760

LLRL LLRL

4.0 3.9

Terrace-II Terrace-II

100% 100%

LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL LLRL

3.9 3.6 3.6 2.6 2.2 2.1 0.8 0.7 0.9 1.8 3.8 6.6 7.9 11.1 20.6 2.9 1.7 0.0 2.6 8.5 13.1 17.7 19.1 20.1 2.5 6.8 6.8 10.5 15.9

Pavona minuta Gardineroseris planulata Acropora gemmifera Acropora gemmifera Acropora digitifera Acropora digitifera Acropora palifera Acropora robusta Acropora gemmifera Acroproa robusta Acropora digitifera Acropora robusta Acropora digitifera Acropora digitifera Acropora digitifera Favia pallida Porites sp. Acropora robusta Acropora robusta Acropora gemmifera Acropora digitifera Acropora gemmifera Galaxea sp. Porites sp. Favia pallida Favites halicora ? Leptoria phrygia Porites sp. Porites sp. Platygyra sinensis Porites sp.

100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100% 100%

Laboratory codea

Terrace-II Terrace-II Terrace-II Terrace-II Terrace-III Terrace-III Terrace-IV Terrace-IV Core-SD-3 Core-SD-3 Core-SD-3 Core-SD-3 Core-SD-3 Core-SD-3 Core-SD-3 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-2 Core-SD-1 Core-SD-1 Core-SD-1 Core-SD-1 Core-SD-1

The laboratory code is the following: LLRL (Low Level Radioactivity Laboratory, Kanazawa University, Japan). 100% in aragonite content indicated "unaltered corals" from cited references (Sasaki et al., 1998; Ota et al., 2000).

U (ppm)

               

234

U/238U (activity ratio)

Th/232Th (activity ratio)

230

Th/234U (activity ratio)

>20 >30 >25 >40 >40 >35 >19 >20 >35 >25 >15 >15 >15 >15 >10 >10

0.0642 0.0461 0.0455 0.0583 0.0621 0.0579 0.0501 0.0651 0.0499 0.0359 0.0349 0.0265 0.0259 0.0235 0.0369 0.0284

3.316  0.024 3.359  0.029

1.141  0.007 1.148  0.007

>70 >40

0.0479  0.0009 0.0574  0.0012

5320  110 6400  140

3.975  3.812  3.749  3.931  3.257  3.954  4.067  3.654  4.107  3.719  3.900  4.265  3.598  2.600  2.567  3.688  3.734  4.028  3.797  4.157  3.834  2.996  2.536  2.431  3.179  2.925  2.994  2.828  2.999 

1.130  1.135  1.148  1.139  1.133  1.148  1.139  1.144  1.146  1.146  1.146  1.132  1.153  1.143  1.148  1.153  1.142  1.153  1.154  1.144  1.145  1.136  1.150  1.145  1.145  1.148  0.134  1.135  1.144 

0.0567  0.0483  0.0495  0.0520  0.0393  0.0281  0.0236  0.0420  0.0457  0.0483  0.0532  0.0588  0.0569  0.0696  0.0870  0.0520  0.0569  0.0561  0.0588  0.0669  0.0725  0.0822  0.0845  0.0871  0.0544  0.0649  0.0639  0.0707  0.0818 

6330 5360 5500 5780 4340 3090 2590 4650 5060 5370 5920 6560 6340 7810 9860 5780 6350 6250 6560 7510 8160 9290 9560 9870 6070 7270 7150 7950 9240

0.035 0.029 0.036 0.034 0.020 0.026 0.029 0.025 0.030 0.027 0.028 0.027 0.024 0.018 0.017 0.026 0.025 0.028 0.029 0.029 0.026 0.022 0.017 0.015 0.021 0.020 0.020 0.019 0.021

1.131 1.149 1.149 1.148 1.134 1.150 1.141 1.149 1.140 1.147 1.145 1.143 1.131 1.145 1.132 1.140

0.008 0.007 0.008 0.007 0.006 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.006 0.008 0.007 0.007 0.007 0.006 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007

>30 >10 >40 >44 >20 >30 >70 >60 >30 >20 >60 >20 >20 >20 >20 >70 >110 >120 >90 >80 >90 >110 >80 >130 >60 >190 >130 >90 >170

               

Age (years  1s)

0.008 0.008 0.007 0.008 0.007 0.007 0.008 0.008 0.009 0.007 0.008 0.007 0.007 0.007 0.008 0.008

0.021 0.032 0.025 0.029 0.021 0.022 0.021 0.019 0.033 0.031 0.030 0.027 0.029 0.028 0.021 0.020

               

230

0.0011 0.0010 0.0010 0.0012 0.0012 0.0011 0.0010 0.0011 0.0010 0.0009 0.0007 0.0006 0.0007 0.0006 0.0009 0.0007

0.0011 0.0010 0.0010 0.0011 0.0008 0.0006 0.0006 0.0009 0.0009 0.0010 0.0009 0.0009 0.0010 0.0013 0.0014 0.0009 0.0010 0.0010 0.0010 0.0011 0.0013 0.0014 0.0013 0.0013 0.0010 0.0011 0.0011 0.0013 0.0013

7190 5110 5050 6510 6940 6460 5560 7290 5550 3960 3850 2920 2850 2570 4080 3130

               

                            

130 110 110 140 140 130 110 130 120 100 80 70 80 60 100 80

130 120 110 120 90 70 70 100 100 120 110 110 110 150 170 110 120 110 120 130 150 170 150 160 110 130 130 150 160

(234U/238U)0 (activity ratio)

1.134 1.152 1.151 1.151 1.137 1.153 1.143 1.152 1.142 1.148 1.147 1.145 1.132 1.146 1.133 1.141

               

0.008 0.008 0.008 0.008 0.008 0.007 0.008 0.008 0.009 0.007 0.008 0.007 0.007 0.007 0.008 0.008

1.143  0.007 1.151  0.007 1.132  1.137  1.150  1.141  1.135  1.149  1.140  1.145  1.148  1.148  1.149  1.135  1.155  1.146  1.152  1.155  1.145  1.156  1.157  1.147  1.149  1.140  1.154  1.149  1.148  1.151  1.137  1.138  1.148 

0.008 0.008 0.008 0.007 0.006 0.007 0.007 0.007 0.007 0.007 0.007 0.006 0.006 0.008 0.008 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007 0.007

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Kikai Island Shidooke reef (28 220 0500 N, 130 010 5800 E) Sasaki et al. (1998) TM-05 KS-34 KS-33 KS-36 KS-35 AO419 AO417 TM-06 KS-38 KS-47 TM-04 TM-02 AO418 TM-03 TM-07 TM-01 Shidooke reef (28 210 0700 N, 130 010 3900 E) Ota et al. (2000) AO435 KS-42

230

90

Table 3 Uraniumethorium isotopic compositions and a-spectrometric

Table 4 Summary of sedimentary facies and key species at Holocene reefs of the Northwest Pacific. Reef location Kikai Island Nakaguma reef (28 200 2600 N, 129 580 0500 E)

Core

Facies

Distribution

Age (14C/230Ue234Th)

Key species

Reference

Corymbose and tabular Acropora facies

Upper unit of Holocene section (restricted to the top 2e3 m of coreNG-3, NG-4, NG-5, NG-6, NG- 7, NG-8, NG-9, NG-10, NG-11, and NG-12) Lower unit of Holocene section (restricted to the partial core NG-1, NG-5, NG-8, NG-10, and NG-11)

4940 cal. years BPePresent

Acropora hyacinthus, Acropora monticulosa, and Acropora humilis group, and Isopora palifera

Konishi et al. (1983); Webster et al. (1998)

8740e7510 cal. years BP

Porites lutea, Porites lobata or Porites australiensis with associated Leptoria phygia, Goniastrea sp, Favia pallida, Favites sp., Platygyra sp., Montipora sp., and Montastrea sp. Corals fragments (braching Acropora) and detritus (echinoid debris and calcareous algae)

Massive Porites facies

Detritus facies

Shidooke reef: Site 2 (28 210 1200 N, 130 010 4600 E)

Shidooke reef: Site 3 (28 210 0700 N, 130 010 3900 E)

Shidooke reef: Site 4 (28 200 5900 N, 130 010 3100 E)

3240e2730 cal. years BP

Surface of Holocene section (Terrace IV) Surface of Holocene section (Terrace II)

2520e1560 cal. years BP 7290e3270 years ago

Surface of Holocene section (Terrace III) Surface of Holocene section (Terrace IV) Surface of Holocene section (Terrace II)

5550e2320 years ago 4650e770 years ago 7290e3270 years ago

Surface of Holocene section (Terrace III) Surface of Holocene section (Terrace IV) Upper unit of reef crest section (restricted to the core SD-2 and SD-3)

5550e2320 years ago 4650e770 years ago 6560e5060 years (UeTh age)

Massive Porites facies Detritus facies

Upper unit of shallow lagoon section (restricted to the core SD-1) Lower unit of reef crest and shallow lagoon section (restricted to the core SD-1, SD-2, and SD-3)

6070e5320 years (UeTh age) 9870e6560 years (UeTh age)

Corymbose and tabular Acropora facies

Surface of Holocene section (Terrace II)

7290e3270 years ago

Surface of Holocene section (Terrace III)

5550e2320 years ago

Outcrop

Corymbose and tabular Acropora facies

Outcrop

Corymbose and tabular Acropora facies

Outcrop

Core

Outcrop

Corymbose and tabular Acropora facies

Corymbose and tabular Acropora facies

7510e4940 cal. years BP

Acropora hyacinthus, Acropora monticulosa, and Acropora humilis group, I. palifera, Montipora sp. with associated Pocillopora verrucosa, Goniastrea retiformis, Leptoria phygia, Favites sp., and Platygyra sp.

Konishi et al. (1978); Webster et al. (1998)

Acropora digitifera, Acropora hyacinthus, Acropora robusta, I. palifera, G. retiformis, and Favia stelligera

Sasaki et al. (1998)

Pocillopora verrucosa, Pocillopora eydouxi, Acropora hyacinthus, Acropora gemmifera, Acropora digitifera, Pavona minuta, G. retiformis, Favites chinensis, Favites abdita, Echinopora gemmacea, Leptoria phrygia, Platygyra daedalea, F. stelligera, and Montastrea curta

Sugihara et al. (2003)

Acropora digitifera, Acropora gemmifera, and Acropora hyacinthus with associated I. palifera, Acropora robusta, Favia speciosa, Favia pallida, Favites chinensis, G. retiformis, Pavona minuta, Pocillopora verrucosa, and Pocillopora damicornis Porites and Acropora muricata

Ota et al. (2000)

Corals fragments (branching Acropora, Seriatopora hystrix, and massive Porites) and detritus (calcareous and siliceous sediments) Acropora digitifera, Acropora robusta, F. stelligera, G. retiformis, Cyphastrea chalcidicum, Pavona minuta, I. palifera, and Porites sp. Acropora digitifera, Acropora gemmifera, Acropora robusta, F. stelligera, G. retiformis,

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Shidooke reef: Site 1 (28 220 0500 N, 130 010 5800 E)

Middle unit of Holocene section (restricted to the partial coreNG-2, NG-3, NG-4, NG-5, NG-6, NG- 7, NG-8, NG-9, NG-10, NG-11, NG-12, and NG-13) Surface of Holocene section (Terrace III)

Hongo (2010)

(continued on next page)

91

92

Table 4 (continued ) Reef location

Yoron Island Kurohana reef (27 030 5300 N, 128 270 0000 E)

Ishigaki Island Ibaruma reef (24 300 1100 N, 124 170 2100 E)

Core

Core

Core

Distribution

Age (14C/230Ue234Th)

Surface of Holocene section (Terrace IV)

4650e770 years ago

Corymbose and tabular Acropora facies Massive Porites facies Detritus facies

Upper unit of reef crest section (restricted to the core YR-II, YR-III, and YR-V) Upper unit of shallow lagoon section (restricted to the core YR-IV) Lower unit of reef crest and shallow lagoon section (restricted to the core YR-III, YR-IV and YR-V)

5080e2090 cal. years BP

Corymbose and tabular Acropora facies

unknown

Key species

Reference

Pavona minuta, Montastrea curta, and Favites chinensis Acropora digitifera, Acropora robusta, F. stelligera, G. retiformis, Favites chinensis, Platygyra sinensis, Platygyra ryukyuensis, and Porites sp. Acropora digitifera, Acropora hyacinthus, I. palifera, Montipora sp., P. damicornis with associated Cyphastrea sp. Porites sp.

Yonekura et al. (1994); Hongo and Kayanne (2011)

older than 4320 cal. years BP

Coral fragment (Acropora digitifera, Acropora, P. damicornis, and I. palifera) and detritus (calcareous algae)

Upper unit of reef crest section (restricted to the core IB-3 and IB-4)

7200e4750 cal. years BP

Hongo and Kayanne (2009)

Detritus facies

Lower unit of reef crest and shallow lagoon section (restricted to the core IB-1, IB-2, and IB- 3)

7820e7200 cal. years BP

Acropora digitifera, Acropora hyacinthus with associated I. palifera, Montastrea curta, G. retiformis, Platygyra ryukyuensis, Cyphastrea sp., Millepora platyphylla, Favia stelligera, Favia sp., Favites sp., and Pocillopora sp. Acropora digitifera, Favites sp, and detritus (calcareous algae, foraminifera, gastropods, and echinoid debris)

Corymbose and tabular Acropora facies Arborescent Acropora facies

Upper unit of reef crest section (restricted to the core PL-I)

7120e3810 cal. years BP

Acropora digitifera, Acropora robusta/Acropora abrotanoides

Kayanne et al. (2002); Hongo and Kayanne (2011)

Lower unit of reef crest and lagoon (restricted to the core PL-I and PL-III)

8180e7120 cal. years BP

Upper unit of lagoon and shaloow lagoon section (restricted to the core PL-II and PL-III) Lower unit of shallow lagoon section (restricted to the core PL-II)

5160 cal. years BPePresent

Acropora muricata/Acropora intermedia with associated Porites sp., P. damicornis, and Lobophyllia sp. Porites sp.

Massive Porites facies Detritus facies

7280e2280 cal. years BP

Coral fragment (arborescent Acropora, Goniastrea, and Montipora) and detritus (calcareous algae, foraminifera, gastropods, and bivalves)

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

Palau Island Ngemelis reef (7 210 4900 N, 134 190 0500 E)

Facies

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Table 5 List of key species at Holocene reefs of the Northwest Pacific. Reef site/Key species

Nakaguma reef, Kikai island

Corymbose and tabular Acropora facies Acropora digitifera Acropora gemmifera Acropora humilis C Acropora hyacinthus C Acropora monticulosa C Acropora robusta/A. abrotanoides Cyphastrea chalcidicum Cyphastrea sp. Echinopora gemmacea Favia pallida Favia sp. Favia speciosa Favia stelligera Favites abdita Favites chinensis 6 Favites sp. Goniastrea retiformis 6 Isopora palifera C Leptoria phygia 6 Millepora platyphylla Montastrea curta Montipora sp. C Pavona minuta Platygyra daedalea Platygyra ryukyuensis Platygyra sinensis Platygyra sp. 6 Pocillopora damicornis Pocillopora eydouxi Pocillopora sp. Pocillopora verrucosa 6 Porites sp. Arborescent Acropora facies Acropora muricata/A. intermedia Lobophyllia sp. P. damicornis Porites sp. Massive Porites facies Acropora muricata 6 Favia pallida Favites sp. 6 Goniastrea sp. 6 Leptoria phygia 6 Montastrea sp. 6 Platygyra sp. 6 Porites australiensis C Porites lobata C Porites lutea C Porites sp. (massive)

Shidooke reef (site 1), Kikai island

Shidooke reef (site 2), Kikai island

Shidooke reef (site 3), Kikai island

Shidooke reef (site 4), Kikai island

Kurohana reef, Yoron island

Ibaruma reef, Ishigaki island

Ngemelis reef, Palau islands

C

C C

C C

C C

C

C

C

C

C

C

C

C

6

C

C

C

C C

C C C C C

C

6

6 6

6

C C

6 6

C C

C

C

6

C

C

6 6

6 6 6 6 6

C

6

C C

C

6 6

6

C C C

C C

C

6 C C

6 6 6

C

C

C

C

Note that circle and triangle indicate key coral species and associated key coral species, respectively.

A. muricata/A. intermedia and those associated with Pocillopora damicornis, Lobophyllia sp., and Porites sp. in the Palau Islands (Table 5). In the massive Porites facies, 8 genera and 11 key coral species were identified from Holocene reefs. Massive Porites (P. australiensis, P. lutea, and P. lobata) are the main key coral species (Table 5). 4. Discussion 4.1. Response of facies and key coral species to sea-level change during the past 10 ka Environmental conditions (e.g., hydrodynamic conditions and SST) control the species composition of corals. For example, as wave energy increases, branching corals change from delicate to more robust forms (Geister, 1977; Montaggioni and Braithwaite,

2009). Corals in high-energy reefs (e.g., in windward locations or under shallow-water conditions) generally consist of tabular and robust forms. In contrast, corals in low-energy reefs (e.g., in leeward locations, closed bays, or deep-water) are composed of delicate branching or massive corals. However, reef crests in leeward sites, which face the open ocean, are characterized by moderate-energy reef, and reef-building corals are generally concentrated in this zone. Indeed, tabular corals (e.g., A. digitifera and A. hyacinthus) are dominant in both leeward and windward reef crests at Ishigaki Island (Hongo and Kayanne, 2009). These findings indicate that the magnitude of hydrodynamic energy, related to sea-level change (i.e., changes induced by varying water depth), has a greater influence on coral species composition than do wind or swell. Moreover, no significant variation in Holocene wind directions has been reported for the present study area (e.g., Bush, 2002).

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SST also influences the species composition of corals. Veron and Minchin (1992) showed that a decrease in species diversity was correlated with decreasing SST in present-day Japan. Moreover, the average SST at the Palau Islands is the highest among the present study sites, and the species diversity is high at these islands (Yukihira et al., 2007). However, key coral species are widely distributed throughout the Northwest Pacific, but such corals are generally absent in the temperate zone (Veron, 2000; Yamano et al., 2011). These findings indicate that SST affects only the limit of species diversity or the latitudinal limit of the distribution. Moreover, Holocene paleo-SSTs at low- and mid-latitudes in the Northwest Pacific have similar present-day mean SSTs in all cases (Shen et al., 2005; Sun et al., 2005; Morimoto et al., 2007).

Holocene trends in reef growth and facies distributions derived from cores and raised reef terraces were driven mainly by sea-level change. Indeed, previous studies have reported that sea-level change is one of most important controlling factors of reef growth throughout the Caribbean and Indo-Pacific regions (e.g., Cabioch et al., 1995; Grossman and Fletcher, 2004; Hubbard et al., 2005; Macintyre, 2007; Montaggioni and Braithwaite, 2009). Sea-level curves have been reconstructed for the Northwest Pacific based on biological markers (Fig. 3; Chappell and Polach,1991; Yokoyama et al., 1996; Hongo and Kayanne, 2010a), showing a rapid rise (10 m/ka) between 10,000 and 7000 cal. years BP, continued rise at a lower rate (5 m/ka) between 7000 and 5000 years BP, and a subsequent period of stabilization (Fig. 3).

a Kikai Island 10000 5

b Yoron Island Age [cal. years BP] 6000 4000

8000

2000

10000 5

0

-5

-5

-10

-10

-15

-15

Depth [m]

MSL 0

Depth [m]

MSL 0

-20

Age [cal. years BP] 6000 4000

2000

0

-20 -25

-25 -30

Pre-Holocene substrate

-30

Reef terrace

Ota et al. (2000) Konishi et al. (1978)

Sugihara et al. (2003) Sasaki et al. (1998)

-35 -40

8000

-35

Core NG-5 core SD-1 core

9870 years ago

c Ishigaki Island 10000 5

8000

Age [cal. years BP] 6000 4000

NG-6 core SD-2 core

SD-3 core

YR-II core

-40

d Palau Island 2000

10000 5

0

MSL 0

MSL 0

-5

-5

-10

-10

-15

-15

8000

Age [cal. years BP] 6000 4000

YR-III core

YR-V core

2000

0

-20 -25

Depth [m]

Depth [m]

8180 cal. years BP

7820 cal. years BP Pre-Holocene substrate

-20 -25

-30

-30

-35

-35 IB-3 core

-40

Sea level curve Chappell and Polach (1991); Yokoyama et al. (1996) Hongo and Kayanne (2010a)

Pre-Holocene substrate

PL-I core

PL-II core

PL-III core

-40

Reef growth curve Corymbose and tabular Acropora facies

Massive Porites facies

Arborescent Acropora facies

Detritus facies

Fig. 3. Sea-level and reef-growth curves for study sites in the Northwest Pacific. Sea-level curves are derived from Chappell and Polach (1991), Yokoyama et al. (1996), and Hongo and Kayanne (2010a). Average reef-growth curves are calculated for the time periods between dated samples. Radiometric counter errors for 14C ages and 230Th/234U ages are given as 2s and 1s, respectively. Each plot is positioned in terms of the present-day mean sea level (MSL). Data for the Kikai Island are plotted at 1.8 m/ka from the original curve as a correction for tectonic uplift (Ota et al., 2000).

C. Hongo / Quaternary Science Reviews 35 (2012) 82e99

At the present study sites, upward reef growth began soon after inundation of the substrate at between 10,000 and 8000 years ago, as indicated by initial reef growth at 9870 years ago (UeTh ages) from the SD-2 core at Shidooke reef at Kikai Island, at 9250 cal. years BP from the NG-13 core at Nakaguma reef at Kikai Island, at 7820 cal. years BP from the IB-3 reef-crest core at Ishigaki Island, and at 8180 cal. years BP from the PL-I reef-crest core at the Palau Islands (Fig. 3). However, the timing at Yoron Island remains unknown because the base of Holocene reef was not recovered in the cores. The obtained sea-level curve shows a rapid rise between 10,000 and 7000 years ago, followed by stabilization. This period is marked by a latitudinal change in the key coral species at the present study

95

sites. In the Palau Islands, buildup facies (arborescent Acropora facies) at the reef crest developed upward at a rate equivalent to that of sea-level rise (10 m/ka) until 7120 years ago (Figs. 3 and 4). During this period, arborescent Acropora (A. muricata/A. intermedia) were the key coral species, due to their rapid growth rate (w0.1 m/year; Gomez et al., 1985), continuous growth, and rapid exploitation of the habitat. Reef in the shallow lagoon at the Palau Islands (PL-II core) consisted of transported gravel and sand from the reef crest. On the reef crest at Ishigaki Island, the detritus facies accumulated rapidly at around 7200 years ago (between 7500 and 6750 years ago), at a rate equivalent to that of sea-level rise, and burial of the shallow lagoon began after the period of upward reef growth. The

Fig. 4. Temporal and spatial patterns of sedimentary facies and key coral species at study sites in the Northwest Pacific. During the period of rapid sea-level rise (10 m/ka) between 10000 and 7000 years ago, arborescent Acropora (A. muricata/A. intermedia) from the arborescent Acropora facies and massive Porites (P. australiensis, P. lutea, and P. lobata) from the massive Porites facies were the dominant contributors to reef growth at the reef crest in tropical and subtropical regions, respectively. Reef detritus also contributed to reef development during this period. During the period of sea-level rise (5 m/ka) between 7000 and 5000 years ago, the key species were completely replaced by A. digitifera, A. hyacinthus, A. robusta/A. abrotanoides, I. palifera, F. stelligera, and G. retiformis from the corymbose and tabular Acropora facies throughout the Northwest Pacific. The key coral species continued to contribute to reef growth during the period of sea-level stabilization between 5000 years ago and the present. In the lagoon section of the present study, the detritus facies was replaced by massive Porites (P. australiensis, P. lutea, and P. lobata) during the period of sea-level stabilization, and the corals continued to contribute to reef growth until the present. The key coral species of the corymbose and tabular Acropora facies on the reef crest are likely to contribute to reef growth and the maintenance of reef ecosystems in response to future sea-level rise at a rate of 2e6 m/ka. Moreover, key coral species from the arborescent Acropora facies and massive Porites facies will fulfill this role in the near future when the key coral species of the corymbose and tabular Acropora facies decline due to global climate change and anthropogenic stresses.

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lower part of the Holocene section at Shidooke reef (Kikai Island) also consisted of detritus facies, and the accumulation continued until 6560 years ago. Nakaguma reef (Kikai Island) consisted of massive Porites facies during the early stage of reef growth, and the subsequent detritus facies accumulated until 4940 years ago. During the period of rapid sea-level rise at the study sites, the massive Porites facies is limited to the lower section of Nakaguma reef (Fig. 2), because massive Porites (mainly P. australiensis, P. lutea, and P. lobata) is generally restricted to deep-water/low-energy conditions or a turbid water environment (Montaggioni, 2005; Pichon, 2011). The rate of reef growth at Nakaguma reef was relatively slow during this period, because the reef is located in a moderate-energy environment where reef growth is generally inactive (Montaggioni, 2005; Hongo and Kayanne, 2009) and where massive Porites has a slow growth rate (w0.01 m/year; Pichon, 2011); consequently, the relationship between corals and environmental condition cause effect increasing in water depths (i.e., deepwater/low-energy conditions). Furthermore, like Nakaguma reef, the growth rate of Shidooke reef was slower than that of sea-level rise during this period, indicating that reef growth at Kikai Island was influenced by sea-level change in combination with other environmental factors. For example, a decrease in SST generally causes a decline in reef growth (Montaggioni, 2005). Kikai Island is located near the northern limit of coral reefs where the area is generally characterized by low SST in winter. In the present study sites, upward growth facies on the reef crest were completely replaced by a corymbose and tabular Acropora facies that adapted to high-energy conditions in shallow water, as a consequence of reduced accommodation space at around 7000 years ago (Fig. 4) when the rate of sea-level rise decreased to 5 m/ka. In the Palau Islands, this facies appeared at 7120 years ago, and A. digitifera and A. robusta/A. abrotanoides were the key coral species because they are strongly resistant to wave action and live in a shallow-water environment (Cabioch et al., 1999; Sugihara et al., 2003). Reef crests on Ibaruma reef at Ishigaki Island and on Kurohana reef at Yoron Island were the sites of accumulations of’ corymbose and tabular Acropora facies from 7200 to 5080 years ago, respectively. At Nakaguma reef on Kikai Island, the upward facies was also replaced by corymbose and tabular Acropora facies, mainly A. digitifera and A. hyacinthus, until 4940 years ago. At Shidooke reef on Kikai Island, this replacement occurred between 7290 and 6560 years ago. Moreover, data from outcrops and cores from Nakaguma reef and Shidooke reef at Kikai Island indicate that the reef has been continuously composed of key coral species (A. digitifera, Acropora gemmifera, A. hyacinthus, F. stelligera, G. retiformis, and I. palifera) from this facies until the present. In shallow lagoons, the detritus facies was generally replaced by massive Porites facies at 6070 years ago in Shidooke reef (SD-1 core) and at 2280 years ago in the Palau Islands (PL-II core) and on Yoron Island (YR-IV core), because the environment of the shallow lagoon changed to turbid or low-energy conditions. This shift occurred because the reef crest reached sea level between 6000 and 5000 years ago, and a clear reef zonation developed in terms of variations in topography and wave energy from onshore to offshore; consequently, the shallow lagoon was a turbid, low-energy environment. The above history of reef development and associated sea-level changes has been reported from other reefs (e.g., Davies et al., 1985; Cabioch et al., 1995; Montaggioni and Faure, 1997; Grossman and Fletcher, 2004). Although few reefs had been established prior to 10,000 cal. years BP in the Caribbean and Indo-Pacific regions (Fairbanks, 1989; Chappell and Polach, 1991; Montaggioni et al., 1997; Cabioch et al., 2003), many reefs started to grow between 10,000 and 8000 cal. years BP from a pre-Holocene foundation (e.g., Cabioch et al., 1995; Camoin et al., 2004; Hubbard et al., 2005; Kan and Kawana, 2006; Gischler et al., 2008; Kench et al., 2009; Shen

et al., 2010). For example, Montaggioni and Faure (1997) reported that changes in the facies at the reef crest at Mauritius reef were driven by increasing water energy due to decreased accommodation space, and by sea-level change during the Holocene. The burial history of the shallow lagoon in the present study is consistent of the findings of Montaggioni and Faure (1997). 4.2. Future scenario: predictions of reef ecosystems and implications for restoration and conservation Although future sea-level rise, together with global climate change (i.e., increases in sea-surface temperatures, and ocean acidification) and local changes (i.e., increases in turbidity, pollution, and overfishing) will have a negative effect on corals, the present study indicates that a potential future scenario of coral reefs can be constructed from analyses of past and future sea-level trends. Given that key coral species contributed to reef development in the Northwest Pacific during Holocene sea-level rise, it is likely that such species will build coral reefs in response to the projected global sea-level rise of 0.18e0.59 m until 2099, equivalent to a rate of 2e6 m/ka (Meehl et al., 2007). In particular, the first reef builders at the reef crest in this region are A. digitifera, A. hyacinthus, A. robusta/A. abrotanoides, I. palifera, F. stelligera, and G. retiformis from the corymbose and tabular Acropora facies, because these species contributed to reef development during Holocene sea-level rise at a rate of less than 5 m/ka (Fig. 4). Moreover, shallow lagoons in this region will accumulate the transported fragments of these species and other calcareous debris. If these species are faced with mortality due to global warming, increasing sea-surface temperatures, ocean acidification, and/or local stresses (e.g., overfishing, pollution, and habitat destruction), the reefs will be undeveloped. However, other key coral species (mainly P. australiensis, P. lutea, and P. lobata in subtropical areas, and A. muricata and A. intermedia in tropical areas) would engage in reef building at the reef crest in this region, because mortality of the above species would result in an increase in the water depth between the reef top and the sea surface (i.e., accommodation space), suiting species adapted to low-water-energy environments. Moreover, shallow lagoons in this region will be characterized by the continuous accumulation of debris. In Caribbean reefs, A. palmata and A. cervicornis are potential reefbuilders, as these species are dominant in Holocene reefs in this region (e.g., Hubbard et al., 2008). Although sedimentary and biological records have been reconstructed for Holocene reefs in the Indian Ocean, the Great Barrier Reef, and other areas (Montaggioni and Faure, 1997; Cabioch, 2003; Camoin et al., 2004; Kench et al., 2009; Roche et al., 2011), few studies have identified the key coral species during this period of reef growth. The present findings indicate that some of these species will play a significant role as reef builders in the near future. However, the continuity of reef formations and ecosystems in regions with low species diversity (e.g., Caribbean reefs, the Hawaiian Islands, and the eastern Pacific; Veron, 1995, 2000) would be at risk in the near future because the future ecological succession would be unique to reefs of the Northwest Pacific, which contains several hundred species of coral. Furthermore, key coral species have been faced with global mortality in recent decades (Fujioka, 2002; Gardner et al., 2003; Hughes et al., 2003; Aronson et al., 2005; Pandolfi et al., 2011). Given the above findings, planning for reef restoration and conservation is an important issue for reconstructing and maintaining pristine reef ecosystems in the near future. In particular, the geological records described in this study demonstrate the importance of research into key coral species as a means of restoring and conserving reef ecosystems in the near future. For example, key coral species should be assigned priority over other species in terms of the direct

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transplantation of juvenile corals. Moreover, knowledge of the habitat of key coral species should be a basic criterion for designing ecologically and biologically significant areas (EBSA) and marine protected areas (MPAs), which are generally established based upon biological, social, and economic criteria (e.g., McLeod et al., 2009). 5. Conclusion (1) An analysis of 27 Holocene drillcores and raised reef terraces in the Northwest Pacific revealed the dominance of four sedimentary facies: corymbose and tabular Acropora facies, arborescent Acropora facies, massive Porites facies, and detritus facies. A number of key coral species contributed to reef development during Holocene sea-level change. Arborescent Acropora (A. intermedia and A. muricata) and massive Porites (P. australiensis, P. lutea, and P. lobata) were reef builders at the reef crest during a period of abrupt sea-level rise by 10 m/ka (between 10,000 and 7000 cal. years BP), whereas A. digitifera, A. hyacinthus, A. robusta/A. abrotanoides, I. palifera, F. stelligera, and G. retiformis from the corymbose and tabular Acropora facies were involved in reef-building at reef crests between 7000 and 5000 cal. years BP (sea-level rise of 5 m/ka) and during the ensuing period of stable sea level between 5000 years ago and the present. Massive Porites (P. australiensis, P. lutea, and P. lobata) contributed to reef development in lagoons during the period of stable sea-level. (2) The key coral species of the corymbose and tabular Acropora facies are potential reef builders in the future under the scenario of a global sea-level rise of 2e6 m/ka. Although corals are faced with global-scale mortality in the near future, the key coral species of the arborescent Acropora facies and the massive Porites facies have the potential to be reef-builders in the Northwest Pacific. However, reefs in the Caribbean, the Hawaiian Islands, and the east Pacific face a bleak future because these areas are characterized by low species diversity, suggesting a lack of relief species that would contribute to reefbuilding and maintenance of reef ecosystems. (3) Future sea-level rise, together with an increase in sea-surface temperature, ocean acidification, and anthropogenic stresses, will have a negative effect on corals and reef ecosystems. Moreover, other environmental factors (e.g., wave energy, intensity of typhoons, and turbidity) will also affect corals; consequently, it is need to focus on the relation between corals and such factors. Furthermore, it is important that research into direct transplantation and the designation of marine protected areas focuses on key coral species that will contribute to maintaining pristine reef ecosystems worldwide in the near future. Acknowledgments This work was financially supported by the Tokyo Geographical Society, a Grant-in-Aid for Scientific Research on Innovative Areas (Coral Reef Science for Symbiosis and Coexistence of Human and Ecosystem under Combined Stresses; No. 20121006) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, and the Environmental Research and Technology Development Fund (S9) of the Ministry of the Environment, Japan. Editorin-Chief Dr. Colin MurrayeWallace and an anonymous reviewer are thanked for their constructive criticism of the manuscript. References Alvarez-Filip, L., Gill, J.A., Dulvy, N.K., Perry, A.L., Watkinson, A.R., Côté, I.M., 2011. Drivers of region-wide declines in architectural complexity on Caribbean reefs. Coral Reefs 30, 1051e1060.

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