A review on ecological response of coral reefs to global warming and oceanic acidification
-
摘要:
生物礁是由珊瑚虫、藻类等造礁生物组成、具有抗浪结构的海相碳酸盐岩,是全球主要碳库之一,也是观察热带海洋影响中-高纬度环境过程的重要窗口。近二、三十年以来,伴随着海洋水体的显著酸化和增温,全球热带海洋生物礁的主体——珊瑚礁系统遭受了不同程度的影响。其中,对于高温强迫而言,海水温度上升诱发珊瑚白化、抑制珊瑚的自我修复;海洋酸化可以显著改变珊瑚钙化率、抑制珊瑚幼虫发育、引发珊瑚礁的溶解;两大因素均可改变珊瑚礁的群落结构。针对这些环境要素的改变,珊瑚自身可以通过共生藻的种类转换以及调控基因表达等手段在一定程度上抵抗高温胁迫;但若温室气体的排放不受控制,绝大多数珊瑚礁到21世纪末都将遭受灾难性打击。为应对未来不同场景下的珊瑚礁变化,还需要对高温、酸化等关键因子响应特征进行更深入的研究;珊瑚礁长序列研究有可能为珊瑚的长周期演化特征提供关键认识,也为现代观测提供有益补充。
Abstract:Tropical reefs are anti-wave structures composed of corals, algae and other reef-building organisms. They are one of the world's major carbon banks and an important window to observe the linkages and interactions between the mid- to high-latitude environmental processes and tropical oceans. In the past decades, with the significant acidification and warming of global oceans, the tropical coral reefs are seriously under threat. Ocean acidification is a factor which may significantly affect coral calcification rates, inhibit the development of coral larvae, and trigger the dissolution of coral reefs. And high temperature may cause the rising of sea temperature, coral bleaching and inhibit the self-repair of coral reefs. In addition, both of the two factors may induce changes in the community structure of coral reefs. In response to the changes in these environmental factors, corals can resist heat stress to a certain extent by changing the types of symbiotic algae and regulating gene expression. However, if the emission of greenhouse gases is not properly controlled in the near future, most coral reefs on the Earth may face complete elimination by the end of this century. A more comprehensive understanding of coral reefs’ response to the key factors in the climate system change, including higher temperature and acidification, is required to cope better with changes of coral reefs in different possible scenarios in the future. The study of reef depositional sequences may provide key insights into the long-term evolving patterns of coral reefs, and serve as a valuable supplement for modern observations.
-
Key words:
- coral reefs /
- climate changes /
- global warming /
- ocean acidification /
- response mechanism
-
图 1 2015—2016年白化事件中全球珊瑚礁的白化程度统计[9]
Figure 1.
图 2 海表温度上升对珊瑚礁群落的影响[3]
Figure 2.
图 3 海洋酸化对珊瑚礁的影响[3]
Figure 3.
图 4 海底火山通风口处CO2排放量对生物礁群落的影响[82]
Figure 4.
-
[1] IPCC. Climate Change 2013: The Physical Science Basis[M]. Cambridge, United Kingdom: Cambridge University Press, 2013.
[2] IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects[M]. Cambridge: Cambridge University Press, 2014.
[3] Hoegh-Guldberg O, Andréfouët S, Fabricius K E, et al. Vulnerability of coral reef ecosystems in the tropical pacific to climate change[M]//Bell J D, Johnson J E, Hobday A. Vulnerability of tropical pacific fisheries and aquaculture to climate chang. Noumea: Secretariat of the Pacific Community, 2011: 251-296.
[4] Hoegh-Guldberg O, Mumby P J, Hooten A J, et al. Coral reefs under rapid climate change and ocean acidification [J]. Science, 2007, 318(5857): 1737-1742. doi: 10.1126/science.1152509
[5] Pandolfi J M. Incorporating uncertainty in predicting the future response of coral reefs to climate change [J]. Annual Review of Ecology, Evolution, and Systematics, 2015, 46: 281-303. doi: 10.1146/annurev-ecolsys-120213-091811
[6] Hughes T P, Barnes M L, Bellwood D R, et al. Coral reefs in the Anthropocene [J]. Nature, 2017, 546(7656): 82-90. doi: 10.1038/nature22901
[7] Frölicher T L, Fischer E M, Gruber N. Marine heatwaves under global warming [J]. Nature, 2018, 560(7718): 360-364. doi: 10.1038/s41586-018-0383-9
[8] Smale D A, Wernberg T, Oliver E C J, et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services [J]. Nature Climate Change, 2019, 9(4): 306-312. doi: 10.1038/s41558-019-0412-1
[9] Hughes T P, Anderson K D, Connolly S R, et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene [J]. Science, 2018, 359(6371): 80-83. doi: 10.1126/science.aan8048
[10] Weis V M. Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis [J]. Journal of Experimental Biology, 2008, 211(19): 3059-3066. doi: 10.1242/jeb.009597
[11] Oakley C A, Davy S K. Cell biology of coral bleaching[M]//Van Oppen M J H, Lough J M. Coral Bleaching. Cham: Springer, 2018: 189-211.
[12] Bieri T, Onishi M, Xiang T T, et al. Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching [J]. PLoS One, 2016, 11(4): e0152693. doi: 10.1371/journal.pone.0152693
[13] Nielsen D A, Petrou K, Gates R D. Coral bleaching from a single cell perspective [J]. The ISME Journal, 2018, 12(6): 1558-1567. doi: 10.1038/s41396-018-0080-6
[14] Tong H Y, Cai L, Zhou G W, et al. Temperature shapes coral-algal symbiosis in the South China Sea [J]. Scientific Reports, 2017, 7: 40118. doi: 10.1038/srep40118
[15] Baker A C. Reef corals bleach to survive change [J]. Nature, 2001, 411(6839): 765-766. doi: 10.1038/35081151
[16] Baker A C, Starger C J, McClanahan T R, et al. Corals' adaptive response to climate change [J]. Nature, 2004, 430(7001): 741. doi: 10.1038/430741a
[17] Jones A M, Berkelmans R, Van Oppen M J H, et al. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization [J]. Proceedings of the Royal Society B: Biological Sciences, 2008, 275(1641): 1359-1365. doi: 10.1098/rspb.2008.0069
[18] Silverstein R N, Cunning R, Baker A C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals [J]. Global Change Biology, 2015, 21(1): 236-249. doi: 10.1111/gcb.12706
[19] Oliver T A, Palumbi S R. Do fluctuating temperature environments elevate coral thermal tolerance? [J]. Coral Reefs, 2011, 30(2): 429-440. doi: 10.1007/s00338-011-0721-y
[20] Palumbi S R, Barshis D J, Traylor-Knowles N, et al. Mechanisms of reef coral resistance to future climate change [J]. Science, 2014, 344(6186): 895-898. doi: 10.1126/science.1251336
[21] Bay R A, Palumbi S R. Rapid acclimation ability mediated by transcriptome changes in reef-building corals [J]. Genome Biology and Evolution, 2015, 7(6): 1602-1612. doi: 10.1093/gbe/evv085
[22] Mayfield A B, Fan T Y, Chen C S. Physiological acclimation to elevated temperature in a reef-building coral from an upwelling environment [J]. Coral Reefs, 2013, 32(4): 909-921. doi: 10.1007/s00338-013-1067-4
[23] Ainsworth T D, Heron S F, Ortiz J C, et al. Climate change disables coral bleaching protection on the Great Barrier Reef [J]. Science, 2016, 352(6283): 338-342. doi: 10.1126/science.aac7125
[24] Tanzil J T I, Brown B E, Tudhope A W, et al. Decline in skeletal growth of the coral Porites lutea from the Andaman Sea, south Thailand between 1984 and 2005 [J]. Coral Reefs, 2009, 28(2): 519-528. doi: 10.1007/s00338-008-0457-5
[25] Cantin N E, Cohen A L, Karnauskas K B, et al. Ocean warming slows coral growth in the central Red Sea [J]. Science, 2010, 329(5989): 322-325. doi: 10.1126/science.1190182
[26] Steiner Z, Turchyn A V, Harpaz E, et al. Water chemistry reveals a significant decline in coral calcification rates in the southern Red Sea [J]. Nature Communications, 2018, 9: 3615. doi: 10.1038/s41467-018-06030-6
[27] McCulloch M T, D’Olivo J P, Falter J, et al. Coral calcification in a changing world and the interactive dynamics of pH and DIC upregulation [J]. Nature Communications, 2017, 8: 15686. doi: 10.1038/ncomms15686
[28] Burt J A, Bauman A G. Suppressed coral settlement following mass bleaching in the southern Persian/Arabian Gulf [J]. Aquatic Ecosystem Health & Management, 2019, 23(2): 166-174.
[29] Hughes T P, Kerry J T, Baird A H, et al. Global warming impairs stock–recruitment dynamics of corals [J]. Nature, 2019, 568(7752): 387-390. doi: 10.1038/s41586-019-1081-y
[30] Loya Y, Sakai K, Yamazato K, et al. Coral bleaching: the winners and the losers [J]. Ecology Letters, 2001, 4(2): 122-131. doi: 10.1046/j.1461-0248.2001.00203.x
[31] Harii S, Hongo C, Ishihara M, et al. Impacts of multiple disturbances on coral communities at Ishigaki Island, Okinawa, Japan, during a 15 year survey [J]. Marine Ecology Progress Series, 2014, 509: 171-180. doi: 10.3354/meps10890
[32] Van Oppen M J H, Blackall L L. Coral microbiome dynamics, functions and design in a changing world [J]. Nature Reviews Microbiology, 2019, 17(9): 557-567. doi: 10.1038/s41579-019-0223-4
[33] McDevitt-Irwin J M, Baum J K, Garren M, et al. Responses of coral-associated bacterial communities to local and global stressors [J]. Frontiers in Marine Science, 2017, 4: 262. doi: 10.3389/fmars.2017.00262
[34] Keith S A, Baird A H, Hobbs J P A, et al. Synchronous behavioural shifts in reef fishes linked to mass coral bleaching [J]. Nature Climate Change, 2018, 8(11): 986-991. doi: 10.1038/s41558-018-0314-7
[35] Richardson L E, Graham N A J, Pratchett M S, et al. Mass coral bleaching causes biotic homogenization of reef fish assemblages [J]. Global Change Biology, 2018, 24(7): 3117-3129. doi: 10.1111/gcb.14119
[36] Wilson S K, Robinson J P W, Chong-Seng K, et al. Boom and bust of keystone structure on coral reefs [J]. Coral Reefs, 2019, 38(4): 625-635. doi: 10.1007/s00338-019-01818-4
[37] Hughes T P, Kerry J T, Baird A H, et al. Global warming transforms coral reef assemblages [J]. Nature, 2018, 556(7702): 492-496. doi: 10.1038/s41586-018-0041-2
[38] Stuart-Smith R D, Brown C J, Ceccarelli D M, et al. Ecosystem restructuring along the Great Barrier Reef following mass coral bleaching [J]. Nature, 2018, 560(7716): 92-96. doi: 10.1038/s41586-018-0359-9
[39] Van Woesik R, Sakai K, Ganase A, et al. Revisiting the winners and the losers a decade after coral bleaching [J]. Marine Ecology Progress Series, 2011, 434: 67-76. doi: 10.3354/meps09203
[40] Graham N A J, Jennings S, MacNeil M A, et al. Predicting climate-driven regime shifts versus rebound potential in coral reefs [J]. Nature, 2015, 518(7537): 94-97. doi: 10.1038/nature14140
[41] Tambutté E, Venn A A, Holcomb M, et al. Morphological plasticity of the coral skeleton under CO2-driven seawater acidification [J]. Nature Communications, 2015, 6: 7368. doi: 10.1038/ncomms8368
[42] Crook E D, Cohen A L, Rebolledo-Vieyra M, et al. Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification [J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(27): 11044-11049. doi: 10.1073/pnas.1301589110
[43] Fantazzini P, Mengoli S, Pasquini L, et al. Gains and losses of coral skeletal porosity changes with ocean acidification acclimation [J]. Nature Communications, 2015, 6: 7785. doi: 10.1038/ncomms8785
[44] Mollica N R, Guo W F, Cohen A L, et al. Ocean acidification affects coral growth by reducing skeletal density [J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(8): 1754-1759. doi: 10.1073/pnas.1712806115
[45] Foster T, Falter J, McCulloch M, et al. Ocean acidification causes structural deformities in juvenile coral skeletons [J]. Science Advances, 2016, 2(2): e1501130. doi: 10.1126/sciadv.1501130
[46] Al-Horani F A, Al-Moghrabi S M, De Beer D. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis [J]. Marine Biology, 2003, 142(3): 419-426. doi: 10.1007/s00227-002-0981-8
[47] Ries J B. A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification [J]. Geochimica et Cosmochimica Acta, 2011, 75(14): 4053-4064. doi: 10.1016/j.gca.2011.04.025
[48] Venn A, Tambutté E, Holcomb M, et al. Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater [J]. PLoS One, 2011, 6(5): e20013. doi: 10.1371/journal.pone.0020013
[49] McCulloch M, Falter J, Trotter J, et al. Coral resilience to ocean acidification and global warming through pH up-regulation [J]. Nature Climate Change, 2012, 2(8): 623-627. doi: 10.1038/nclimate1473
[50] Biscéré T, Zampighi M, Lorrain A, et al. High pCO2 promotes coral primary production [J]. Biology Letters, 2019, 15(7): 20180777. doi: 10.1098/rsbl.2018.0777
[51] Cooper T F, O'Leary R A, Lough J M. Growth of Western Australian corals in the Anthropocene [J]. Science, 2012, 335(6068): 593-596. doi: 10.1126/science.1214570
[52] Morita M, Suwa R, Iguchi A, et al. Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates [J]. Zygote, 2009, 18(2): 103-107.
[53] Nakamura M, Morita M. Sperm motility of the scleractinian coral Acropora digitifera under preindustrial, current, and predicted ocean acidification regimes [J]. Aquatic Biology, 2012, 15(3): 299-302. doi: 10.3354/ab00436
[54] Albright R, Mason B, Miller M, et al. Ocean acidification compromises recruitment success of the threatened caribbean coral Acropora palmata [J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(47): 20400-20404. doi: 10.1073/pnas.1007273107
[55] Albright R, Mason B. Projected near-future levels of temperature and pCO2 reduce coral fertilization success [J]. PLoS One, 2013, 8(2): e56468. doi: 10.1371/journal.pone.0056468
[56] Albright R, Langdon C. Ocean acidification impacts multiple early life history processes of the caribbean coral Porites astreoides [J]. Global Change Biology, 2011, 17(7): 2478-2487. doi: 10.1111/j.1365-2486.2011.02404.x
[57] Nakamura M, Ohki S, Suzuki A, et al. Coral larvae under ocean acidification: survival, metabolism, and metamorphosis [J]. PLoS One, 2011, 6(1): e14521. doi: 10.1371/journal.pone.0014521
[58] Caroselli E, Gizzi F, Prada F, et al. Low and variable pH decreases recruitment efficiency in populations of a temperate coral naturally present at a CO2 vent [J]. Limnology and Oceanography, 2019, 64(3): 1059-1069. doi: 10.1002/lno.11097
[59] Heyward A J, Negri A P. Natural inducers for coral larval metamorphosis [J]. Coral Reefs, 1999, 18(3): 273-279. doi: 10.1007/s003380050193
[60] Morse J W, Andersson A J, Mackenzie F T. Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and “ocean acidification”: role of high Mg-calcites [J]. Geochimica et Cosmochimica Acta, 2006, 70(23): 5814-5830. doi: 10.1016/j.gca.2006.08.017
[61] Kuffner I B, Andersson A J, Jokiel P L, et al. Decreased abundance of crustose coralline algae due to ocean acidification [J]. Nature Geoscience, 2008, 1(2): 114-117. doi: 10.1038/ngeo100
[62] Vásquez-Elizondo R M, Enríquez S. Coralline algal physiology is more adversely affected by elevated temperature than reduced pH [J]. Scientific Reports, 2016, 6: 19030. doi: 10.1038/srep19030
[63] Cornwall C E, Comeau S, McCulloch M T. Coralline algae elevate pH at the site of calcification under ocean acidification [J]. Global Change Biology, 2017, 23(10): 4245-4256. doi: 10.1111/gcb.13673
[64] Cornwall C E, Comeau S, DeCarlo T M, et al. Resistance of corals and coralline algae to ocean acidification: physiological control of calcification under natural pH variability [J]. Proceedings. of the Royal Society B:Biological Sciences, 2018, 285(1884): 20181168.
[65] Doropoulos C, Ward S, Diaz-Pulido G, et al. Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions [J]. Ecology Letters, 2012, 15(4): 338-346. doi: 10.1111/j.1461-0248.2012.01743.x
[66] Webster N S, Uthicke S, Botté E S, et al. Ocean acidification reduces induction of coral settlement by crustose coralline algae [J]. Global Change Biology, 2013, 19(1): 303-315. doi: 10.1111/gcb.12008
[67] Albright R. Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals [J]. Journal of Marine Biology, 2011, 2011: 473615.
[68] Kline D I, Teneva L, Okamoto D K, et al. Living coral tissue slows skeletal dissolution related to ocean acidification [J]. Nature Ecology & Evolution, 2019, 3(10): 1438-1444.
[69] Eyre B D, Andersson A J, Cyronak T. Benthic coral reef calcium carbonate dissolution in an acidifying ocean [J]. Nature Climate Change, 2014, 4(11): 969-976. doi: 10.1038/nclimate2380
[70] Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, et al. Coral and mollusc resistance to ocean acidification adversely affected by warming [J]. Nature Climate Change, 2011, 1(6): 308-312. doi: 10.1038/nclimate1200
[71] Eyre B D, Cyronak T, Drupp P, et al. Coral reefs will transition to net dissolving before end of century [J]. Science, 2018, 359(6378): 908-911. doi: 10.1126/science.aao1118
[72] Cyronak T, Eyre B D. The synergistic effects of ocean acidification and organic metabolism on calcium carbonate (CaCO3) dissolution in coral reef sediments [J]. Marine Chemistry, 2016, 183: 1-12. doi: 10.1016/j.marchem.2016.05.001
[73] Albright R, Takeshita Y, Koweek D A, et al. Carbon dioxide addition to coral reef waters suppresses net community calcification [J]. Nature, 2018, 555(7697): 516-519. doi: 10.1038/nature25968
[74] Albright R, Caldeira L, Hosfelt J, et al. Reversal of ocean acidification enhances net coral reef calcification [J]. Nature, 2016, 531(7594): 362-365. doi: 10.1038/nature17155
[75] Comeau S, Edmunds P J, Spindel N B, et al. Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations [J]. Limnology and Oceanography, 2014, 59(3): 1081-1091. doi: 10.4319/lo.2014.59.3.1081
[76] Comeau S, Cornwall C E, McCulloch M T. Decoupling between the response of coral calcifying fluid pH and calcification to ocean acidification [J]. Scientific Reports, 2017, 7: 7573. doi: 10.1038/s41598-017-08003-z
[77] Bove C B, Ries J B, Davies S W, et al. Common caribbean corals exhibit highly variable responses to future acidification and warming [J]. Proceedings of the Royal Society B: Biological Sciences, 2019, 286(1900): 20182840. doi: 10.1098/rspb.2018.2840
[78] Comeau S, Cornwall C E, DeCarlo T M, et al. Resistance to ocean acidification in coral reef taxa is not gained by acclimatization [J]. Nature Climate Change, 2019, 9(6): 477-483. doi: 10.1038/s41558-019-0486-9
[79] Comeau S, Carpenter R C, Nojiri Y, et al. Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification [J]. Proceedings of the Royal Society B: Biological Sciences, 2014, 281(1790): 20141339. doi: 10.1098/rspb.2014.1339
[80] Clements C S, Hay M E. Biodiversity enhances coral growth, tissue survivorship and suppression of macroalgae [J]. Nature Ecology & Evolution, 2019, 3(2): 178-182.
[81] Meron D, Atias E, Kruh L I, et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma [J]. The ISME Journal, 2011, 5(1): 51-60. doi: 10.1038/ismej.2010.102
[82] Enochs I C, Manzello D P, Donham E M, et al. Shift from coral to macroalgae dominance on a volcanically acidified reef [J]. Nature Climate Change, 2015, 5(12): 1083-1088. doi: 10.1038/nclimate2758
[83] Inoue S, Kayanne H, Yamamoto S, et al. Spatial community shift from hard to soft corals in acidified water [J]. Nature Climate Change, 2013, 3(7): 683-687. doi: 10.1038/nclimate1855
[84] Fabricius K E, Langdon C, Uthicke S, et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations [J]. Nature Climate Change, 2011, 1(3): 165-169. doi: 10.1038/nclimate1122
[85] Barkley H C, Cohen A L, Golbuu Y, et al. Changes in coral reef communities across a natural gradient in seawater pH [J]. Science Advances, 2015, 1(5): e1500328. doi: 10.1126/sciadv.1500328
[86] Kroeker K J, Micheli F, Gambi M C, et al. Divergent ecosystem responses within a benthic marine community to ocean acidification [J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(35): 14515-14520. doi: 10.1073/pnas.1107789108
[87] Fabricius K, De'ath G, Noonan S, et al. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities [J]. Proceedings of the Royal Society B: Biological Sciences, 2014, 281(1775): 20132479. doi: 10.1098/rspb.2013.2479
[88] Smith J N, De’ath G, Richter C, et al. Ocean acidification reduces demersal zooplankton that reside in tropical coral reefs [J]. Nature Climate Change, 2016, 6(12): 1124-1129. doi: 10.1038/nclimate3122
[89] Frieler K, Meinshausen M, Golly A, et al. Limiting global warming to 2°C is unlikely to save most coral reefs [J]. Nature Climate Change, 2013, 3(2): 165-170. doi: 10.1038/nclimate1674
[90] Van Hooidonk R, Maynard J A, Planes S. Temporary refugia for coral reefs in a warming world [J]. Nature Climate Change, 2013, 3(5): 508-511. doi: 10.1038/nclimate1829
[91] Van Woesik R, Köksal S, Ünal A, et al. Predicting coral dynamics through climate change [J]. Scientific Reports, 2018, 8: 17997. doi: 10.1038/s41598-018-36169-7
[92] Kubicek A, Breckling B, Hoegh-Guldberg O, et al. Climate change drives trait-shifts in coral reef communities [J]. Scientific Reports, 2019, 9: 3721. doi: 10.1038/s41598-019-38962-4
[93] DeCarlo T M, Cohen A L, Wong G T F, et al. Mass coral mortality under local amplification of 2 ℃ ocean warming [J]. Scientific Reports, 2017, 7: 44586. doi: 10.1038/srep44586
[94] Quattrini A M, Rodríguez E, Faircloth B C, et al. Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time [J]. Nature Ecology & Evolution, 2020, 4(11): 1531-1538.
[95] Zachos J, Pagani M, Sloan L, et al. Trends, rhythms, and aberrations in global climate 65 Ma to present [J]. Science, 2001, 292(5517): 686-693. doi: 10.1126/science.1059412
[96] Wu S G, Yang Z, Wang D W, et al. Architecture, development and geological control of the Xisha carbonate platforms, northwestern South China Sea [J]. Marine Geology, 2014, 350: 71-83. doi: 10.1016/j.margeo.2013.12.016
[97] Yi L, Jian Z M, Liu X Y, et al. Astronomical tuning and magnetostratigraphy of neogene biogenic reefs in Xisha Islands, South China Sea [J]. Science Bulletin, 2018, 63(9): 564-573. doi: 10.1016/j.scib.2018.04.001