Research progress on sexual reproduction of scleractinian corals
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摘要: 造礁珊瑚的有性繁殖是维持珊瑚礁生态系统结构和功能的关键生物学过程,直接决定珊瑚种群的动态更新与遗传多样性,对于珊瑚礁生态系统的稳定与演化具有重要意义。本文综述造礁珊瑚有性繁殖的研究进展,包括:(1)珊瑚的繁殖类型;(2)珊瑚的性腺发育;(3)珊瑚的排卵与受精;(4)珊瑚的胚胎发育;(5)珊瑚幼虫的固着过程;(6)珊瑚幼体的发育。现有进展表明,珊瑚有性繁殖过程受内源生物机制与外源环境因子协同调控,但其具体分子机制及过程仍不明了。未来需高度关注环境因子对造礁珊瑚排卵时间的影响、诱导珊瑚幼虫固着的机制、早期共生关系的建立与可塑性,以及建立分子辅助育种方法筛选耐热型珊瑚等方面。Abstract: Sexual reproduction in scleractinian corals is a fundamental biological process that sustains the structure and function of coral reef ecosystems. It directly determines population dynamics and genetic diversity, thereby playing a crucial role in the stability and evolution of coral reefs. This review summarizes recent advances in the study of coral sexual reproduction, including: (1) reproductive strategies, (2) gonadal development, (3) spawning and fertilization, (4) embryogenesis, (5) larval settlement, and (6) juvenile development. Current research indicates that coral sexual reproduction is jointly regulated by endogenous biological mechanisms and exogenous environmental factors; however, the detailed molecular mechanisms underlying these processes remain largely unclear. Future studies should focus on elucidating the environmental regulation of spawning timing, mechanisms inducing larval settlement, establishment and plasticity of early symbiotic relationships, and the development of molecular-assisted breeding strategies for selecting thermotolerant coral strains.
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图 1 摩羯鹿角珊瑚(Acropora cervicornis)不同时相配子的显微结构(图片改自Vargas-Ángel等[27])
A−D和E−H分别依次为第Ⅰ、Ⅱ、Ⅲ、Ⅳ时相的卵母细胞及精巢。cgb:刺丝囊;g:肠系膜;gvc:消化循环腔;m:中胶层;no:凹痕;sc:波浪形边缘
Fig. 1 Micrographs of A. cervicornis during Gonadal Development (modified from Vargas-Ángel et al.[27])
A−D and E−H represent oocytes and spermaries at stages Ⅰ, Ⅱ, Ⅲ, and Ⅳ, respectively. cgb: cnidoglandular band; g: gastrodermis; gvc: gastrovascular cavity; m: mesoglea; no: notches; sc: scalloping
图 2 肉质扁脑珊瑚的胚胎及幼虫发育过程[69]
a. 卵母细胞;b. 2细胞期;c. 4细胞期;d. 8细胞期;e. 16细胞期;f. 32细胞期;g. 桑葚胚期(64细胞期);h. 桑葚胚期(128细胞期);i. 囊胚早期;j. 囊胚晚期;k. 原肠胚早期;l. 原肠胚中期;m. 浮浪幼虫早期;n1, n2. 浮浪幼虫中期;o. 浮浪幼虫晚期。所有标尺都为 200 μm
Fig. 2 The early development of P.carnosus[69]
a. Oocytes; b. 2-cell stage; c. 4-cell stage; d. 8-cell stage; e. 16-cell stage; f. 32-cell stage; g. morula stage (64-cell stage); h. morula stage (128-cell stage); i. early blastula stage; j. later blastula stage; k. early gastrula stage; l. middle gastrula stage; m. early planula stage; n1, n2. middle planula stage; o. later planula stage. All rulers indicate 200 μm
图 5 丛生盔形珊瑚的幼虫发育(改自Wei等[84])
a. 幼虫在69 h时出现试探附着行为,b. 排卵后5 d观察到幼虫附着成功,有6个明显的肠系膜,c. 第9 d观察到共生虫黄藻和体壁,d、e. 1个月后观察到12个触手和6个隔片,f、g. 后续幼体触手不断增长
Fig. 5 G. fascicularis post-settlement development (modified from Wei et al.[84])
a. Larvae started settling at 69 h; b. larvae settled successfully at 5 d, with 6 mesenteries; c. zooxanthellae and the body wall were observed at 9 d; d, e. after 1 month, 12 tentacles and 6 septa were evident; f, g. the juvenile tentacles continued to elongate
表 1 生物化学因素与物理因素对珊瑚幼虫固着过程的影响[86–87]
Tab. 1 Effects of biochemical and physical factors during larval settlement[86–87]
影响因素 幼虫行为 生物化
学因素壳状珊瑚藻(Crustose Coralline Algae, CCA)及其代谢产物 诱导或排斥幼虫固着、不同种
幼虫对CCA的选择存在差异微生物膜及其代谢产物 诱导或排斥幼虫固着 物理因素 环境光和附着基的颜色 影响固着深度、方向、位置 附着基的材质和结构 影响附着率 沉积物 影响附着率及对附着基的选择 温度 影响附着率及寻找合适
附着基的时间水流 影响幼虫的扩散能力和
珊瑚连通性压强 影响固着深度 -
[1] Jones R, Ricardo G F, Negri A P. Effects of sediments on the reproductive cycle of corals[J]. Marine Pollution Bulletin, 2015, 100(1): 13−33. doi: 10.1016/j.marpolbul.2015.08.021 [2] Randall C J, Negri A P, Quigley K M, et al. Sexual production of corals for reef restoration in the Anthropocene[J]. Marine Ecology Progress Series, 2020, 635: 203−232. doi: 10.3354/meps13206 [3] Richmond, R. H. Reproduction and recruitment in corals[M]//Birkeland, C. Life and Death of Coral Reefs. New York: Springer, 1997: 175–197. [4] Hughes T P, Tanner J E. Recruitment failure, life histories, and long-term decline of caribbean corals[J]. Ecology, 2000, 81(8): 2250−2263. doi: 10.1890/0012-9658(2000)081[2250:RFLHAL]2.0.CO;2 [5] Guest J, Heyward A, Omori M, et al. Rearing coral larvae for reef rehabilitation[J]. Reef Rehabilitation Manual, 2010: 73−92. [6] Omori M, Fujiwara S. Manual for Restoration and Remediation of Coral Reefs[M]. Japan: Nature Conservation Bureau and Ministry of the Environment, 2004. [7] Heyward A J, Negri A P. Turbulence, cleavage, and the naked embryo: a case for coral clones[J]. Science, 2012, 335(6072): 1064−1064. doi: 10.1126/science.1216055 [8] Humphrey C, Weber M, Lott C, et al. Effects of suspended sediments, dissolved inorganic nutrients and salinity on fertilisation and embryo development in the coral Acropora millepora (Ehrenberg, 1834)[J]. Coral Reefs, 2008, 27(4): 837−850. doi: 10.1007/s00338-008-0408-1 [9] Riegl B, Purkis S J, Keck J, et al. Monitored and modeled coral population dynamics and the refuge concept[J]. Marine Pollution Bulletin, 2009, 58(1): 24−38. doi: 10.1016/j.marpolbul.2008.10.019 [10] Harrison P L, Wallace C C. Reproduction, dispersal and recruitment of scleractinian corals[M]//Dubinsky Z. Coral Reefs. Netherlands: Elsevier Science Publishers, 1990, 25: 133−207. [11] Byrne M. Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches[J]. Marine environmental research, 2012, 76: 3−15. doi: 10.1016/j.marenvres.2011.10.004 [12] Baird A H, Guest J R, Willis B L. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals[J]. Annual Review of Ecology, Evolution, and Systematics, 2009, 40: 551−571. doi: 10.1146/annurev.ecolsys.110308.120220 [13] 杨小东. 澄黄滨珊瑚、大管孔珊瑚和丛生盔形珊瑚性腺发育与生长规律的研究[D]. 湛江: 广东海洋大学, 2013.Yang Xiaodong. Study of gonad development and growths of Porites lutea, Goniopora djiboutiensis and Galaxea fascicularis[D]. Zhanjiang: Guangdong Ocean University, 2013. [14] Loya Y, Sakai K. Bidirectional sex change in mushroom stony corals[J]. Proceedings of the Royal Society B: Biological Sciences, 2008, 275(1649): 2335−2343. doi: 10.1098/rspb.2008.0675 [15] Eyal-Shaham L, Eyal G, Ben-Zvi O, et al. A unique reproductive strategy in the mushroom coral Fungia fungites[J]. Coral Reefs, 2020, 39(6): 1793−1804. doi: 10.1007/s00338-020-02004-7 [16] Santiago-Valentín J D, Rodríguez-Troncoso A P, Carpizo-Ituarte E, et al. Reproductive pattern of the reef-building coral Pavona gigantea (Scleractinia: agariciidae) off southwestern Mexico[J]. Ciencias Marinas, 2015, 41(3): 233−246. doi: 10.7773/cm.v41i3.2482 [17] Glynn P W, Gassman N J, Eakin C M, et al. Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador)[J]. Marine Biology, 1991, 109(3): 355−368. doi: 10.1007/BF01313501 [18] Cabral-Tena R A, Tortolero-Langarica J J A, Carricart-Ganivet J P, et al. Sex-associated differences in sclerochronology and sensitivity to thermal stress in Caribbean and eastern Pacific reef-building corals[J]. Marine Ecology Progress Series, 2024, 743: 167−183. doi: 10.3354/meps14661 [19] Cruz-Ortega I, Cabral-Tena R A, Carpizo-Ituarte E, et al. Sensitivity of calcification to thermal history differs between sexes in the gonochoric reef-building corals Dichocoenia stokesi and Dendrogyra cylindrus[J]. Marine Biology, 2020, 167(7): 101. doi: 10.1007/s00227-020-03713-x [20] Shikina S, Chang C F. Sexual reproduction in stony corals and insight into the evolution of oogenesis in Cnidaria[M]//Goffredo S, Dubinsky Z. The Cnidaria, Past, Present and Future: The world of Medusa and Her Sisters. Cham: Springer, 2016: 249−268. [21] Fadlallah Y H. Sexual reproduction, development and larval biology in scleractinian corals[J]. Coral Reefs, 1983, 2(3): 129−150. doi: 10.1007/BF00336720 [22] Harrison P L. Sexual reproduction of scleractinian corals[M]//Dubinsky Z, Stambler N. Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer, 2011: 59-85. [23] Tanner J E. Seasonality and lunar periodicity in the reproduction of Pocilloporid corals[J]. Coral Reefs, 1996, 15(1): 59−66. doi: 10.1007/BF01626077 [24] 韦芬, 崔梦瑶, 余克服, 等. 涠洲岛海域美丽鹿角珊瑚和秘密角蜂巢珊瑚的性腺发育研究[J]. 海洋学报, 2023, 45(12): 92−100.Wei Fen, Cui Mengyao, Yu Kefu, et al. Gonadal development of Acropora formosa and Favites abdita in Weizhou Island[J]. Haiyang Xuebao, 2023, 45(12): 92−100. [25] Gomez E J, Jamodiong E A, Maboloc E A, et al. Gametogenesis and reproductive pattern of the reef-building coral Acropora millepora in northwestern Philippines[J]. Invertebrate Reproduction & Development, 2018, 62(4): 202−208. [26] Fan T Y, Dai C F. Reproductive plasticity in the reef coral Echinopora lamellosa[J]. Marine Ecology Progress Series, 1999, 190: 297−301. doi: 10.3354/meps190297 [27] Vargas-Ángel B, Colley S B, Hoke S M, et al. The reproductive seasonality and gametogenic cycle of Acropora cervicornis off Broward County, Florida, USA[J]. Coral Reefs, 2006, 25(1): 110−122. doi: 10.1007/s00338-005-0070-9 [28] Shikina S, Chung Y J, Wang H M, et al. Localization of early germ cells in a stony coral, Euphyllia ancora: potential implications for a germline stem cell system in coral gametogenesis[J]. Coral Reefs, 2015, 34(2): 639−653. doi: 10.1007/s00338-015-1270-6 [29] Shikina S, Chiu Y L, Chen C J, et al. Immunodetection of acetylated alpha‐tubulin in stony corals: evidence for the existence of flagella in coral male germ cells[J]. Molecular Reproduction and Development, 2017, 84(12): 1285−1295. doi: 10.1002/mrd.22927 [30] Chiu Y L, Shikina S, Yoshioka Y, et al. De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: molecular mechanisms underlying scleractinian gametogenesis[J]. BMC Genomics, 2020, 21(1): 732. doi: 10.1186/s12864-020-07113-9 [31] Baird A H, Guest J R. Spawning synchrony in scleractinian corals: comment on Mangubhai & Harrison (2008)[J]. Marine Ecology Progress Series, 2009, 374: 301−304. doi: 10.3354/meps07838 [32] Shlesinger Y, Goulet T L, Loya Y. Reproductive patterns of scleractinian corals in the northern Red Sea[J]. Marine Biology, 1998, 132(4): 691−701. doi: 10.1007/s002270050433 [33] Okubo N, Motokawa T. Embryogenesis in the reef-building coral Acropora spp[J]. Zoological Science, 2007, 24(12): 1169−1177. doi: 10.2108/zsj.24.1169 [34] Chui A P Y, Wong M C, Liu S H, et al. Gametogenesis, embryogenesis, and fertilization ecology of Platygyra acuta in marginal nonreefal coral communities in Hong Kong[J]. Journal of Marine Biology, 2014, 2014: 953587. [35] Guest J R, Baird A H, Goh B P L, et al. Seasonal reproduction in equatorial reef corals[J]. Invertebrate Reproduction & Development, 2005, 48(1/3): 207−218. [36] Baird A H, Guest J R, Edwards A J, et al. An indo-pacific coral spawning database[J]. Scientific Data, 2021, 8(1): 35. doi: 10.1038/s41597-020-00793-8 [37] Hoadley K D, Vize P D, Pyott S J. Current understanding of the circadian clock within Cnidaria[M]//Goffredo S, Dubinsky Z. The Cnidaria, Past, Present and Future: The World of Medusa and Her Sisters. Cham: Springer, 2016: 511−520. [38] Babcock R C, Bull G D, Harrison P L, et al. Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef[J]. Marine Biology, 1986, 90(3): 379−394. doi: 10.1007/BF00428562 [39] Shlesinger T, Loya Y. Breakdown in spawning synchrony: a silent threat to coral persistence[J]. Science, 2019, 365(6457): 1002−1007. doi: 10.1126/science.aax0110 [40] Keith S A, Maynard J A, Edwards A J, et al. Coral mass spawning predicted by rapid seasonal rise in ocean temperature[J]. Proceedings of the Royal Society B: Biological Sciences, 2016, 283(1830): 20160011. doi: 10.1098/rspb.2016.0011 [41] 黄洁英. 三亚鹿回头海域造礁石珊瑚的有性繁殖生物学研究[D]. 北京: 中国科学院, 2011.Huang Jieying. The sexual reproductive biology of hermatypic corals in Luhuitou, Sanya, China[D]. Beijing: University of Chinese Academy of Sciences, 2011. [42] Lin C H, Nozawa Y. The influence of seawater temperature on the timing of coral spawning[J]. Coral Reefs, 2023, 42(2): 417−426. doi: 10.1007/s00338-023-02349-9 [43] Fogarty N D, Marhaver K L. Coral spawning, unsynchronized[J]. Science, 2019, 365(6457): 987−988. doi: 10.1126/science.aay7457 [44] Lin C H, Nozawa Y. Variability of spawning time (lunar day) in Acropora versus merulinid corals: a 7-yr record of in situ coral spawning in Taiwan[J]. Coral Reefs, 2017, 36(4): 1269−1278. doi: 10.1007/s00338-017-1622-5 [45] Levy O, Appelbaum L, Leggat W, et al. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora[J]. Science, 2007, 318(5849): 467−470. doi: 10.1126/science.1145432 [46] Shoguchi E, Tanaka M, Shinzato C, et al. A genome-wide survey of photoreceptor and circadian genes in the coral, Acropora digitifera[J]. Gene, 2013, 515(2): 426−431. doi: 10.1016/j.gene.2012.12.038 [47] Lin C H, Takahashi S, Mulla A J, et al. Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa[J]. Proceedings of the National Academy of Sciences, 2021, 118(34): e2101985118. doi: 10.1073/pnas.2101985118 [48] Kaniewska P, Alon S, Karako-Lampert S, et al. Signaling cascades and the importance of moonlight in coral broadcast mass spawning[J]. eLife, 2015, 4: e09991. doi: 10.7554/eLife.09991 [49] Wolstenholme J, Nozawa Y, Byrne M, et al. Timing of mass spawning in corals: potential influence of the coincidence of lunar factors and associated changes in atmospheric pressure from northern and southern hemisphere case studies[J]. Invertebrate Reproduction & Development, 2018, 62(2): 98−108. [50] Levitan D R, Fogarty N D, Jara J, et al. Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex[J]. Evolution, 2011, 65(5): 1254−1270. doi: 10.1111/j.1558-5646.2011.01235.x [51] Sakai Y, Hatta M, Furukawa S, et al. Environmental factors explain spawning day deviation from full moon in the scleractinian coral Acropora[J]. Biology Letters, 2020, 16(1): 20190760. doi: 10.1098/rsbl.2019.0760 [52] Harrison P L. Sexual reproduction of reef corals and application to coral restoration[M]//Wolanski E, Kingsford M J. Oceanographic Processes of Coral Reefs. 2nd ed. Boca Raton: CRC Press, 2024: 419−437. [53] Gouezo M, Doropoulos C, Fabricius K, et al. Multispecific coral spawning events and extended breeding periods on an equatorial reef[J]. Coral Reefs, 2020, 39(4): 1107−1123. doi: 10.1007/s00338-020-01941-7 [54] Lobov A A, Maltseva A L, Mikhailova N A, et al. The molecular mechanisms of gametic incompatibility in invertebrates[J]. Acta Naturae, 2019, 11(3): 4−15. doi: 10.32607/20758251-2019-11-3-4-15 [55] Buccheri E, Ricardo G F, Babcock R C, et al. Fertilisation kinetics among common Indo-Pacific broadcast spawning corals with distinct and shared functional traits[J]. Coral Reefs, 2023, 42(6): 1351−1363. doi: 10.1007/s00338-023-02431-2 [56] Mumby P J, Sartori G, Buccheri E, et al. Allee effects limit coral fertilization success[J]. Proceedings of the National Academy of Sciences of the United States of America, 2024, 121(52): e2418314121. [57] Nozawa Y, Isomura N, Fukami H. Influence of sperm dilution and gamete contact time on the fertilization rate of scleractinian corals[J]. Coral Reefs, 2015, 34(4): 1199−1206. doi: 10.1007/s00338-015-1338-3 [58] Martignago D C, Godoy L, Amaral A P, et al. Establishment of oxidative stress biomarkers in oocytes from healthy and bleached scleractinian corals[J]. Journal of Experimental Marine Biology and Ecology, 2024, 570: 151963. doi: 10.1016/j.jembe.2023.151963 [59] Paxton C W, Baria M V B, Weis V M, et al. Effect of elevated temperature on fecundity and reproductive timing in the coral Acropora digitifera[J]. Zygote, 2016, 24(4): 511−516. doi: 10.1017/S0967199415000477 [60] Briggs N D, Page C A, Giuliano C, et al. Dissecting coral recovery: bleaching reduces reproductive output in Acropora millepora[J]. Coral Reefs, 2024, 43(3): 557−569. doi: 10.1007/s00338-024-02483-y [61] 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 [62] Puisay A, Hédouin L, Pilon R, et al. How thermal priming of coral gametes shapes fertilization success[J]. Journal of Experimental Marine Biology and Ecology, 2023, 566: 151920. doi: 10.1016/j.jembe.2023.151920 [63] Hagedorn M, Page C A, O’Neil K L, et al. Assisted gene flow using cryopreserved sperm in critically endangered coral[J]. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118(38): e2110559118. [64] Hagedorn M, Carter V L, Henley E M, et al. Producing coral offspring with cryopreserved sperm: a tool for coral reef restoration[J]. Scientific Reports, 2017, 7(1): 14432. doi: 10.1038/s41598-017-14644-x [65] Daly J, Hobbs R J, Zuchowicz N, et al. Cryopreservation can assist gene flow on the great barrier reef[J]. Coral Reefs, 2022, 41(2): 455−462. doi: 10.1007/s00338-021-02202-x [66] Hobbs R J, O'brien J K, Bay L K, et al. A decade of coral biobanking science in Australia-transitioning into applied reef restoration[J]. Frontiers in Marine Science, 2022, 9: 960470. doi: 10.3389/fmars.2022.960470 [67] Bouwmeester J, Daly J, Zuchowicz N, et al. Cryopreservation to conserve genetic diversity of reef-building corals[M]//Van Oppen M J H, Lastra M A. Coral Reef Conservation and Restoration in the Omics Age. Cham: Springer, 2022: 225−240. [68] Daly J, Hobbs R, Zuchowicz N, et al. A semi-automated workflow for the cryopreservation of coral sperm to support biobanking and aquaculture[J]. Journal of Visualized Experiments, 2024(208): e66233. [69] 韦芬, 黄雯, 余克服, 等. 广西涠洲岛黄癣蜂巢珊瑚、肉质扁脑珊瑚的胚胎和幼虫的早期发育[J]. 海洋学报, 2020, 42(4): 87−95.Wei Fen, Huang Wen, Yu Kefu, et al. Embryonic and larval early development of Favia favus and Platygyra carnosus in the Weizhou Island, Guangxi[J]. Haiyang Xuebao, 2020, 42(4): 87−95. [70] Okubo N, Mezaki T, Nozawa Y, et al. Comparative embryology of eleven species of stony corals (Scleractinia)[J]. PLoS One, 2013, 8(12): e84115. doi: 10.1371/journal.pone.0084115 [71] Permata W D, Kinzie Iii R A, Hidaka M. Histological studies on the origin of planulae of the coral Pocillopora damicornis[J]. Marine Ecology Progress Series, 2000, 200: 191−200. doi: 10.3354/meps200191 [72] Babcock R C, Heyward A J. Larval development of certain gamete-spawning scleractinian corals[J]. Coral reefs, 1986, 5(3): 111−116. doi: 10.1007/BF00298178 [73] Hirose M, Hidaka M. Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae[J]. Zoological Science, 2006, 23(10): 873−881. doi: 10.2108/zsj.23.873 [74] 肖宝华, 廖宝林, 杨小东, 等. 肉质扁脑珊瑚的有性繁殖及早期发育[J]. 热带海洋学报, 2017, 36(1): 65−71.Xiao Baohua, Liao Baolin, Yang Xiaodong, et al. Sexual reproduction and early development of Platygyra carnosus[J]. Journal of Tropical Oceanography, 2017, 36(1): 65−71. [75] Technau U. Gastrulation and germ layer formation in the sea anemone Nematostella vectensis and other cnidarians[J]. Mechanisms of Development, 2020, 163: 103628. doi: 10.1016/j.mod.2020.103628 [76] Okubo N, Hayward D C, Forêt S, et al. A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora-morphology, transcriptome, and developmental gene expression[J]. BMC Evolutionary Biology, 2016, 16(1): 48. doi: 10.1186/s12862-016-0615-2 [77] Marlow H Q, Martindale M Q. Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation[J]. Evolution & Development, 2007, 9(4): 355−367. [78] Keshavmurthy S, Fontana S, Mezaki T, et al. Doors are closing on early development in corals facing climate change[J]. Scientific Reports, 2014, 4(1): 5633. doi: 10.1038/srep05633 [79] Humanes A, Noonan S H C, Willis B L, et al. Cumulative effects of nutrient enrichment and elevated temperature compromise the early life history stages of the coral Acropora tenuis[J]. PLoS One, 2016, 11(8): e0161616. doi: 10.1371/journal.pone.0161616 [80] Puisay A, Pilon R, Goiran C, et al. Thermal resistances and acclimation potential during coral larval ontogeny in Acropora pulchra[J]. Marine Environmental Research, 2018, 135: 1−10. doi: 10.1016/j.marenvres.2018.01.005 [81] Petersen L E, Kellermann M Y, Schupp P J. Secondary metabolites of marine microbes: From natural products chemistry to chemical ecology[M]//Jungblut S, Liebich V, Bode-Dalby M. YOUMARES 9 - The Oceans: Our Research, Our Future. Cham: Springer, 2020: 159−180. [82] Randall C J, Giuliano C, Stephenson B, et al. Larval precompetency and settlement behaviour in 25 Indo-Pacific coral species[J]. Communications Biology, 2024, 7(1): 142. doi: 10.1038/s42003-024-05824-3 [83] Mass T, Putnam H M, Drake J L, et al. Temporal and spatial expression patterns of biomineralization proteins during early development in the stony coral Pocillopora damicornis[J]. Proceedings of the Royal Society B: Biological Sciences, 2016, 283(1829): 20160322. doi: 10.1098/rspb.2016.0322 [84] Wei Fen, Cui Mengyao, Huang Wen, et al. Ex situ reproduction and recruitment of scleractinian coral Galaxea fascicularis[J]. Marine Biology, 2023, 170(3): 30. doi: 10.1007/s00227-023-04175-7 [85] Connolly S R, Baird A H. Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals[J]. Ecology, 2010, 91(12): 3572−3583. doi: 10.1890/10-0143.1 [86] Gleason D F, Hofmann D K. Coral larvae: from gametes to recruits[J]. Journal of Experimental Marine Biology and Ecology, 2011, 408(1/2): 42−57. [87] Pysanczyn J W, Williams E A, Brodrick E, et al. The role of acoustics within the sensory landscape of coral larval settlement[J]. Frontiers in Marine Science, 2023, 10: 1111599. doi: 10.3389/fmars.2023.1111599 [88] Whitman T N, Negri A P, Bourne D G, et al. Settlement of larvae from four families of corals in response to a crustose coralline alga and its biochemical morphogens[J]. Scientific Reports, 2020, 10(1): 16397. doi: 10.1038/s41598-020-73103-2 [89] Abdul Wahab M A, Ferguson S, Snekkevik V K, et al. Hierarchical settlement behaviours of coral larvae to common coralline algae[J]. Scientific Reports, 2023, 13(1): 5795. doi: 10.1038/s41598-023-32676-4 [90] Tebben J, Motti C A, Siboni N, et al. Chemical mediation of coral larval settlement by crustose coralline algae[J]. Scientific Reports, 2015, 5(1): 10803. doi: 10.1038/srep10803 [91] Kitamura M, Schupp P J, Nakano Y, et al. Luminaolide, a novel metamorphosis-enhancing macrodiolide for scleractinian coral larvae from crustose coralline algae[J]. Tetrahedron Letters, 2009, 50(47): 6606−6609. doi: 10.1016/j.tetlet.2009.09.065 [92] Turnlund A C. Interactions between coral larval settlement, marine biofilms and crustose coralline algae microbiomes[D]. Brisbane: The University of Queensland, 2024. [93] Bourne D G, Sato Y, Smith H A. Microbes guide corals looking to find a home[J]. Trends in Microbiology, 2024, 32(2): 120−121. doi: 10.1016/j.tim.2023.11.017 [94] Turnlund A C, Vanwonterghem I, Botté E S, et al. Linking differences in microbial network structure with changes in coral larval settlement[J]. ISME Communications, 2023, 3(1): 114. doi: 10.1038/s43705-023-00320-x [95] Kegler P, Kegler H F, Gärdes A, et al. Bacterial biofilm communities and coral larvae settlement at different levels of anthropogenic impact in the Spermonde Archipelago, Indonesia[J]. Frontiers in Marine Science, 2017, 4: 270. doi: 10.3389/fmars.2017.00270 [96] Tebben J, Tapiolas D M, Motti C A, et al. Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium[J]. PLoS One, 2011, 6(4): e19082. doi: 10.1371/journal.pone.0019082 [97] Alker A T, Farrell M V, Demko A M, et al. Linking bacterial tetrabromopyrrole biosynthesis to coral metamorphosis[J]. ISME Communications, 2023, 3(1): 98. doi: 10.1038/s43705-023-00309-6 [98] Sneed J M, Sharp K H, Ritchie K B, et al. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals[J]. Proceedings of the Royal Society B: Biological Sciences, 2014, 281(1786): 20133086. doi: 10.1098/rspb.2013.3086 [99] Petersen L E, Kellermann M Y, Nietzer S, et al. Photosensitivity of the bacterial pigment cycloprodigiosin enables settlement in coral larvae—light as an understudied environmental factor[J]. Frontiers in Marine Science, 2021, 8: 749070. doi: 10.3389/fmars.2021.749070 [100] Petersen L E, Kellermann M Y, Fiegel L J, et al. Photodegradation of a bacterial pigment and resulting hydrogen peroxide release enable coral settlement[J]. Scientific Reports, 2023, 13(1): 3562. doi: 10.1038/s41598-023-30470-w [101] Erwin P M, Szmant A M. Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide[J]. Coral Reefs, 2010, 29(4): 929−939. doi: 10.1007/s00338-010-0634-1 [102] Moeller M, Nietzer S, Schupp P J. Neuroactive compounds induce larval settlement in the scleractinian coral Leptastrea purpurea[J]. Scientific Reports, 2019, 9(1): 2291. doi: 10.1038/s41598-019-38794-2 [103] Yang Qingsong, Zhang Wenqian, Zhang Ying, et al. Promoting larval settlement of coral Pocillopora damicornis by calcium[J]. Coral Reefs, 2022, 41(1): 223−235. doi: 10.1007/s00338-021-02216-5 [104] Strader M E, Davies S W, Matz M V. Differential responses of coral larvae to the colour of ambient light guide them to suitable settlement microhabitat[J]. Royal Society Open Science, 2015, 2(10): 150358. doi: 10.1098/rsos.150358 [105] Mason B, Beard M, Miller M W. Coral larvae settle at a higher frequency on red surfaces[J]. Coral Reefs, 2011, 30(3): 667−676. doi: 10.1007/s00338-011-0739-1 [106] Levenstein M A, Marhaver K L, Quinlan Z A, et al. Engineered substrates reveal species-specific inorganic cues for coral larval settlement[J]. ACS Sustainable Chem. Eng., 2022, 10: 3960−3971. [107] Patterson J T, Flint M, Than J, et al. Evaluation of substrate properties for settlement of Caribbean staghorn coral Acropora cervicornis larvae in a land‐based system[J]. North American Journal of Aquaculture, 2016, 78(4): 337−345. doi: 10.1080/15222055.2016.1185068 [108] Wilson J, Harrison P. Post-settlement mortality and growth of newly settled reef corals in a subtropical environment[J]. Coral Reefs, 2005, 24(3): 418−421. doi: 10.1007/s00338-005-0033-1 [109] Doropoulos C, Roff G, Bozec Y M, et al. Characterizing the ecological trade‐offs throughout the early ontogeny of coral recruitment[J]. Ecological Monographs, 2016, 86(1): 20−44. doi: 10.1890/15-0668.1 [110] Wolanski E, Kingsford M J. Oceanographic Processes of Coral Reefs: Physical and Biological Links in the Great Barrier Reef[M]. 2nd ed. Boca Raton: CRC Press, 2024. [111] Babcock R, Mundy C. Coral recruitment: consequences of settlement choice for early growth and survivorship in two scleractinians[J]. Journal of Experimental Marine Biology and Ecology, 1996, 206(1/2): 179−201. [112] Doropoulos C, Ward S, Marshell A, et al. Interactions among chronic and acute impacts on coral recruits: the importance of size‐escape thresholds[J]. Ecology, 2012, 93(10): 2131−2138. doi: 10.1890/12-0495.1 [113] Penin L, Michonneau F, Baird A H, et al. Early post-settlement mortality and the structure of coral assemblages[J]. Marine Ecology Progress Series, 2010, 408: 55−64. doi: 10.3354/meps08554 [114] Nozawa Y. Micro-crevice structure enhances coral spat survivorship[J]. Journal of Experimental Marine Biology and Ecology, 2008, 367(2): 127−130. doi: 10.1016/j.jembe.2008.09.004 [115] Chamberland V F, Petersen D, Guest J R, et al. New seeding approach reduces costs and time to outplant sexually propagated corals for reef restoration[J]. Scientific Reports, 2017, 7(1): 18076. doi: 10.1038/s41598-017-17555-z [116] Tebben J, Guest J R, Sin T M, et al. Corals like it waxed: paraffin-based antifouling technology enhances coral spat survival[J]. PLoS One, 2014, 9(1): e87545. doi: 10.1371/journal.pone.0087545 [117] Davies S W, Matz M V, Vize P D. Ecological complexity of coral recruitment processes: effects of invertebrate herbivores on coral recruitment and growth depends upon substratum properties and coral species[J]. PLoS One, 2013, 8(9): e72830. doi: 10.1371/journal.pone.0072830 [118] Toh T C, Ng C S L, Guest J, et al. Grazers improve health of coral juveniles in ex situ mariculture[J]. Aquaculture, 2013, 414−415: 288−293. [119] Craggs J, Guest J, Bulling M, et al. Ex situ co culturing of the sea urchin, Mespilia globulus and the coral Acropora millepora enhances early post-settlement survivorship[J]. Scientific Reports, 2019, 9(1): 12984. doi: 10.1038/s41598-019-49447-9 [120] Nozawa Y, Harrison P L. Effects of elevated temperature on larval settlement and post-settlement survival in scleractinian corals, Acropora solitaryensis and Favites chinensis[J]. Marine Biology, 2007, 152(5): 1181−1185. doi: 10.1007/s00227-007-0765-2 [121] Ross C, Ritson-Williams R, Olsen K, et al. Short-term and latent post-settlement effects associated with elevated temperature and oxidative stress on larvae from the coral Porites astreoides[J]. Coral Reefs, 2013, 32(1): 71−79. doi: 10.1007/s00338-012-0956-2 [122] 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 [123] Cohen A L, McCorkle D C, de Putron S, et al. Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification[J]. Geochemistry, Geophysics, Geosystems, 2009, 10(7): 2009GC002411. doi: 10.1029/2009GC002411 [124] Chan Y L, Stock J H, Watson M W. A dynamic factor model framework for forecast combination[J]. Spanish Economic Review, 1999, 1(2): 91−121. doi: 10.1007/s101080050005 [125] Quigley K M, Marzonie M, Ramsby B, et al. Variability in fitness trade-offs amongst coral juveniles with mixed genetic backgrounds held in the wild[J]. Frontiers in Marine Science, 2021, 8: 636177. doi: 10.3389/fmars.2021.636177 [126] Torda G, Lundgren P, Willis B L, et al. Revisiting the connectivity puzzle of the common coral Pocillopora damicornis[J]. Molecular Ecology, 2013, 22(23): 5805−5820. doi: 10.1111/mec.12540 [127] Hoegh-Guldberg O, Hughes L, McIntyre S, et al. Assisted colonization and rapid climate change[J]. Science, 2008, 321(5887): 345−346. doi: 10.1126/science.1157897 [128] Chan W Y, Chung J, Peplow L M, et al. Maternal effects in gene expression of interspecific coral hybrids[J]. Molecular Ecology, 2021, 30(2): 517−527. doi: 10.1111/mec.15727 [129] Quigley K M, Randall C J, Van Oppen M J H, et al. Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles[J]. Biology Open, 2020, 9(1): bio047316. [130] Kirk N L, Howells E J, Abrego D, et al. Genomic and transcriptomic signals of thermal tolerance in heat‐tolerant corals (Platygyra daedalea) of the Arabian/Persian Gulf[J]. Molecular Ecology, 2018, 27(24): 5180−5194. doi: 10.1111/mec.14934 [131] Fuller Z L, Mocellin V J L, Morris L A, et al. Population genetics of the coral Acropora millepora: toward genomic prediction of bleaching[J]. Science, 2020, 369(6501): eaba4674. doi: 10.1126/science.aba4674 [132] Cleves P A, Tinoco A I, Bradford J, et al. Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor[J]. Proceedings of the National Academy of Sciences, 2020, 117(46): 28899−28905. [133] Rinkevich B, Shaish L, Douek J, et al. Venturing in coral larval chimerism: a compact functional domain with fostered genotypic diversity[J]. Scientific Reports, 2016, 6(1): 19493. doi: 10.1038/srep19493 [134] Huffmyer A S, Drury C, Majerová E, et al. Tissue fusion and enhanced genotypic diversity support the survival of Pocillopora acuta coral recruits under thermal stress[J]. Coral Reefs, 2021, 40(2): 447−458. doi: 10.1007/s00338-021-02074-1 [135] Jiang Lei, Zhang Yuyang, Liu Chengyue, et al. Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification[J]. Frontiers in Marine Science, 2022, 9: 964803. doi: 10.3389/fmars.2022.964803 [136] Edmunds P J. Coral recruitment: patterns and processes determining the dynamics of coral populations[J]. Biological Reviews, 2023, 98(6): 1862−1886. doi: 10.1111/brv.12987 [137] Bockel T, Rinkevich B. Rapid recruitment of symbiotic algae into developing scleractinian coral tissues[J]. Journal of Marine Science and Engineering, 2019, 7(9): 306. doi: 10.3390/jmse7090306 [138] Kenkel C D, Bay L K. Exploring mechanisms that affect coral cooperation: symbiont transmission mode, cell density and community composition[J]. PeerJ, 2018, 6: e6047. doi: 10.7717/peerj.6047 [139] McIlroy S E, Coffroth M A. Coral ontogeny affects early symbiont acquisition in laboratory-reared recruits[J]. Coral Reefs, 2017, 36(3): 927−932. doi: 10.1007/s00338-017-1584-7 [140] Quigley K M, Alvarez Roa C, Beltran V H, et al. Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui: lessons learnt across a decade of stress experiments to enhance coral heat tolerance[J]. Restoration Ecology, 2021, 29(3): e13342. doi: 10.1111/rec.13342 [141] Pochon X, Gates R D. A new Symbiodinium clade (Dinophyceae) from Soritid foraminifera in Hawai’i[J]. Molecular Phylogenetics and Evolution, 2010, 56(1): 492−497. doi: 10.1016/j.ympev.2010.03.040 [142] Adams L M, Cumbo V R, Takabayashi M. Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae[J]. Marine Ecology Progress Series, 2009, 377: 149−156. doi: 10.3354/meps07834 [143] Cumbo V R, Baird A H, Van Oppen M J H. The promiscuous larvae: flexibility in the establishment of symbiosis in corals[J]. Coral Reefs, 2013, 32(1): 111−120. doi: 10.1007/s00338-012-0951-7 [144] Schwarz J A, Krupp D A, Weis V M. Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria[J]. The Biological Bulletin, 1999, 196(1): 70−79. doi: 10.2307/1543169 [145] Williams R B, Cornelius P F S, Hughes R G, et al. Coelenterate biology: recent research on cnidaria and ctenophora[C]//Proceedings of the Fifth International Conference on Coelenterate Biology. Dordrecht: Springer, 1991. [146] Yamashita H, Suzuki G, Kai S, et al. Establishment of coral–algal symbiosis requires attraction and selection[J]. PLoS One, 2014, 9(5): e97003. doi: 10.1371/journal.pone.0097003 [147] Quigley K M, Willis B L, Bay L K. Heritability of the Symbiodinium community in vertically-and horizontally-transmitting broadcast spawning corals[J]. Scientific Reports, 2017, 7(1): 8219. doi: 10.1038/s41598-017-08179-4 [148] Quigley K M, Bay L K, Willis B L. Temperature and water quality-related patterns in sediment-associated Symbiodinium communities impact symbiont uptake and fitness of juveniles in the genus Acropora[J]. Frontiers in Marine Science, 2017, 4: 401. doi: 10.3389/fmars.2017.00401 [149] Yorifuji M, Harii S, Nakamura R, et al. Shift of symbiont communities in Acropora tenuis juveniles under heat stress[J]. PeerJ, 2017, 5: e4055. doi: 10.7717/peerj.4055 [150] Turnham K E, Lewis A M, Kemp D W, et al. Limited persistence of the heat-tolerant zooxanthella, Durusdinium trenchii, in corals transplanted to a barrier reef where it is rare among natal colonies[J]. Coral Reefs, 2025, 44(2): 555−570. doi: 10.1007/s00338-025-02625-w [151] Sun Youfang, Jiang Lei, Gong Sanqiang, et al. Impact of ocean warming and acidification on symbiosis establishment and gene expression profiles in recruits of reef coral Acropora intermedia[J]. Frontiers in Microbiology, 2020, 11: 532447. doi: 10.3389/fmicb.2020.532447 [152] Abrego D, Van Oppen M J H, Willis B L. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny[J]. Molecular Ecology, 2009, 18(16): 3532−3543. doi: 10.1111/j.1365-294X.2009.04276.x [153] Cumbo V R, Van Oppen M J H, Baird A H. Temperature and Symbiodinium physiology affect the establishment and development of symbiosis in corals[J]. Marine Ecology Progress Series, 2018, 587: 117−127. doi: 10.3354/meps12441 [154] Jiang Lei, Sun Youfang, Zhang Yuyang, et al. Impact of diurnal temperature fluctuations on larval settlement and growth of the reef coral Pocillopora damicornis[J]. Biogeosciences, 2017, 14(24): 5741−5752. doi: 10.5194/bg-14-5741-2017 [155] Quigley K M, Baker A C, Coffroth M A, et al. Bleaching resistance and the role of algal endosymbionts[M]//Van Oppen M J H, Lough J M. Coral Bleaching: Patterns, Processes, Causes and Consequences. Cham: Springer, 2018: 111−151. [156] Quigley K M, Alvarez-Roa C, Raina J B, et al. Heat-evolved microalgal symbionts increase thermal bleaching tolerance of coral juveniles without a trade-off against growth[J]. Coral Reefs, 2023, 42(6): 1227−1232. doi: 10.1007/s00338-023-02426-z [157] Maire J, Van Oppen M J H. A role for bacterial experimental evolution in coral bleaching mitigation?[J]. Trends in Microbiology, 2022, 30(3): 217−228. doi: 10.1016/j.tim.2021.07.006 -
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