1.Alvarez-Filip, L., Dulvy, N. K., Gill, J. A., Côté, I. M. & Watkinson, A. R. Flattening of Caribbean coral reefs: Region-wide declines in architectural complexity. Proc. R. Soc. B Biol. Sci. 276, 3019–3025 (2009).
Google Scholar
2.Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).ADS
CAS
PubMed
Google Scholar
3.Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).ADS
CAS
PubMed
Google Scholar
4.Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).ADS
CAS
PubMed
Google Scholar
5.Loya, Y. et al. Coral bleaching: The winners and the losers. Ecol. Lett. 4, 122–131 (2001).
Google Scholar
6.Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. A., Grottoli, A. G. & Middlebrook, R. Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Funct. Ecol. 23, 539–550 (2009).
Google Scholar
7.Depczynski, M. et al. Bleaching, coral mortality and subsequent survivorship on a West Australian fringing reef. Coral Reefs 32, 233–238 (2013).ADS
Google Scholar
8.Edmunds, P. J. Implications of high rates of sexual recruitment in driving rapid reef recovery in Mo’orea, French Polynesia. Sci. Rep. 8, 16615. https://doi.org/10.1038/s41598-018-34686-z (2018).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
9.Richmond, R. H., Tisthammer, K. H. & Spies, N. P. The effects of anthropogenic stressors on reproduction and recruitment of corals and reef organisms. Front. Mar. Sci. 5, 266. https://doi.org/10.3389/fmars.2018.00226 (2018).Article
Google Scholar
10.Oliver, E. C. J. et al. Marine heatwaves. Ann. Rev. Mar. Sci. 13, 313–342 (2021).PubMed
Google Scholar
11.Rinkevich, B. The contribution of photosynthetic products to coral reproduction. Mar. Biol. 101, 259–263 (1989).CAS
Google Scholar
12.Lesser, M. P. Using energetic budgets to assess the effects of environmental stress on corals: Are we measuring the right things?. Coral Reefs 32, 25–33 (2013).ADS
Google Scholar
13.Muscatine, L., McCloskey, L. & Marian, R. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26, 601–611 (1981).ADS
CAS
Google Scholar
14.Rodrigues, L. J. & Grottoli, A. G. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 52, 1874–1882 (2007).ADS
Google Scholar
15.Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl. Acad. Sci. USA 118, e2022653118. https://doi.org/10.1073/pnas.2022653118 (2021).CAS
Article
PubMed
PubMed Central
Google Scholar
16.Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).ADS
CAS
PubMed
Google Scholar
17.Schoepf, V. et al. Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B 282, 20151887. https://doi.org/10.1098/rspb.2015.1997 (2015).Article
PubMed
PubMed Central
Google Scholar
18.Leuzinger, S., Willis, B. L. & Anthony, K. R. N. Energy allocation in a reef coral under varying resource availability. Mar. Biol. 159, 177–186 (2012).
Google Scholar
19.Oren, U., Benayahu, Y., Lubinevsky, H. & Loya, Y. Colony integration during regeneration in the stony coral Favia favus. Ecology 82, 802–813 (2001).
Google Scholar
20.Fisch, J., Drury, C., Towle, E. K., Winter, R. N. & Miller, M. W. Physiological and reproductive repercussions of consecutive summer bleaching events of the threatened Caribbean coral Orbicella faveolata. Coral Reefs 38, 863–876 (2019).ADS
Google Scholar
21.Ward, S., Harrison, P. & Hoegh-Guldberg, O. Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. Proc. 9th Int. Coral Reef Symp. 1123–1128 (2002).22.Levitan, D. R., Boudreau, W., Jara, J. & Knowlton, N. Long-term reduced spawning in Orbicella coral species due to temperature stress. Mar. Ecol. Prog. Ser. 515, 1–10 (2014).ADS
Google Scholar
23.Johnston, E. C., Counsell, C. W. W., Sale, T. L., Burgess, S. C. & Toonen, R. J. The legacy of stress: Coral bleaching impacts reproduction years later. Funct. Ecol. 34, 2315–2325 (2020).
Google Scholar
24.Szmant, A. M. & Gassman, N. J. The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8, 217–224 (1990).ADS
Google Scholar
25.Jones, A. M. & Berkelmans, R. Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium Type-D. J. Mar. Biol. 2011, 185890. https://doi.org/10.1155/2011/185890 (2011).Article
Google Scholar
26.Figueiredo, J. et al. Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31, 613–619 (2012).ADS
Google Scholar
27.Hagedorn, M. et al. Potential bleaching effects on coral reproduction. Reprod. Fertil. Dev. 28, 1061–1071 (2016).CAS
Google Scholar
28.Michalek-Wagner, K. & Willis, B. L. Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability. Coral Reefs 19, 231–239 (2001).
Google Scholar
29.Howells, E. J. et al. Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories. Mar. Pollut. Bull. 105, 532–539 (2016).CAS
PubMed
Google Scholar
30.Godoy, L. et al. Southwestern Atlantic reef-building corals Mussismilia spp. are able to spawn while fully bleached. Mar. Biol. 168, 15. https://doi.org/10.1007/s00227-021-03824-z (2021).CAS
Article
Google Scholar
31.Veron, J. E. Acropora hyacinthus. in Corals of the World, vol. 1–3. (ed. Veron, J. E.) 404–405 (Australian Institute of Marine Sciences, 2000).32.Pratchett, M. S., McCowan, D., Maynard, J. A. & Heron, S. F. Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French polynesia. PLoS ONE 8, e70443. https://doi.org/10.1371/journal.pone.0070443 (2013).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
33.Speare, K. E., Adam, T. C., Winslow, E. M., Lenihan, H. S. & Burkepile, D. E. Size-dependent mortality of corals during marine heatwave erodes recovery capacity of a coral reef. Glob. Change Biol. https://doi.org/10.1111/gcb.16000 (2021). Article
Google Scholar
34.Holbrook, S. J. et al. Recruitment drives spatial variation in recovery rates of resilient coral reefs. Sci. Rep. 8, 7338. https://doi.org/10.1038/s41598-018-25414-8 (2018).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
35.Carroll, A., Harrison, P. & Adjeroud, M. Sexual reproduction of Acropora reef corals at Moorea, French polynesia. Coral Reefs 25, 93–97 (2006).ADS
Google Scholar
36.Tsounis, G. et al. Anthropogenic effects on reproductive effort and allocation of energy reserves in the Mediterranean octocoral Paramuricea clavata. Mar. Ecol. Prog. Ser. 449, 161–172 (2012).ADS
Google Scholar
37.Wall, C. B., Ritson-Williams, R., Popp, B. N. & Gates, R. D. Spatial variation in the biochemical and isotopic composition of corals during bleaching and recovery. Limnol. Oceanogr. 64, 2011–2028 (2019).ADS
CAS
PubMed
PubMed Central
Google Scholar
38.Jung, E. M. U., Stat, M., Thomas, L., Koziol, A. & Schoepf, V. Coral host physiology and symbiont dynamics associated with differential recovery from mass bleaching in an extreme, macro-tidal reef environment in northwest Australia. Coral Reefs 40, 893–905 (2021).
Google Scholar
39.Tremblay, P., Gori, A., Maguer, J. F., Hoogenboom, M. & Ferrier-Pagès, C. Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Sci. Rep. 6, 38112. https://doi.org/10.1038/srep38112 (2016).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
40.Baumann, J., Grottoli, A. G., Hughes, A. D. & Matsui, Y. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J. Exp. Mar. Bio. Ecol. 461, 469–478 (2014).CAS
Google Scholar
41.Grottoli, A. G. et al. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob. Chang. Biol. 20, 3823–3833 (2014).ADS
PubMed
Google Scholar
42.Graham, E. M., Baird, A. H., Connolly, S. R., Sewell, M. A. & Willis, B. L. Rapid declines in metabolism explain extended coral larval longevity. Coral Reefs 32, 539–549 (2013).ADS
Google Scholar
43.Michalek-Wagner, K. & Willis, B. L. Impacts of bleaching on the soft coral Lobophytum compactum. II. Biochemical changes in adults and their eggs. Coral Reefs 19, 240–246 (2001).
Google Scholar
44.Harii, S., Nadaoka, K., Yamamoto, M. & Iwao, K. Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar. Ecol. Prog. Ser. 346, 89–96 (2007).ADS
CAS
Google Scholar
45.Wallace, C. C. Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar. Biol. 88, 217–233 (1985).
Google Scholar
46.Ziegler, R. & Ibrahim, M. M. Formation of lipid reserves in fat body and eggs of the yellow fever mosquito, Aedes aegypti. J. Insect Physiol. 47, 623–627 (2001).CAS
PubMed
Google Scholar
47.Baliña, S., Temperoni, B., Greco, L. S. L. & Tropea, C. Losing reproduction: effect of high temperature on female biochemical composition and egg quality in a freshwater crustacean with direct development, the red cherry shrimp, Neocaridina davidi (Decapoda, Atyidae). Biol. Bull. 234, 139–151 (2018).PubMed
Google Scholar
48.Levitan, D. R. The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Integr. Comp. Biol. 46, 298–311 (2006).PubMed
Google Scholar
49.Caballes, C. F., Pratchett, M. S., Kerr, A. M. & Rivera-Posada, J. A. The role of maternal nutrition on oocyte size and quality, with respect to early larval development in the coral-eating starfish, Acanthaster planci. PLoS ONE 11, e0158007. https://doi.org/10.1371/journal.pone.0158007 (2016).CAS
Article
PubMed
PubMed Central
Google Scholar
50.Madin, J. S. et al. The Coral Trait Database, a curated database of trait information for coral species from the global oceans. Sci. Data 4, 160017. https://doi.org/10.1038/sdata.2016.17 (2017).Article
Google Scholar
51.Foster, T. & Gilmour, J. Egg size and fecundity of biannually spawning corals at Scott Reef. Sci. Rep. 10, 12313. https://doi.org/10.1038/s41598-020-68289-4 (2020).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
52.Harriott, V. J. Reproductive ecology of four scleratinian species at Lizard Island, Great Barrier Reef. Coral Reefs 2, 9–18 (1983).ADS
Google Scholar
53.Vargas-Ángel, B., Colley, S. B., Hoke, S. M. & Thomas, J. D. The reproductive seasonality and gametogenic cycle of Acropora cervicornis off Broward County, Florida, USA. Coral Reefs 25, 110–122 (2006).ADS
Google Scholar
54.Hall, V. R. & Hughes, T. P. Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77, 950–963 (1996).
Google Scholar
55.Brandt, M. E. The effect of species and colony size on the bleaching response of reef-building corals in the Florida Keys during the 2005 mass bleaching event. Coral Reefs 28, 911–924 (2009).ADS
Google Scholar
56.Sakai, K., Singh, T. & Iguchi, A. Bleaching and post-bleaching mortality of Acropora corals on a heat-susceptible reef in 2016. PeerJ 2019, e8138. https://doi.org/10.7717/peerj.8138 (2019).Article
Google Scholar
57.Nozawa, Y. & Lin, C. H. Effects of colony size and polyp position on polyp fecundity in the scleractinian coral genus Acropora. Coral Reefs 33, 1057–1066 (2014).ADS
Google Scholar
58.Álvarez-Noriega, M. et al. Fecundity and the demographic strategies of coral morphologies. Ecology 97, 3485–3493 (2016).PubMed
Google Scholar
59.Bena, C. & Van Woesik, R. The impact of two bleaching events on the survival of small coral colonies (Okinawa, Japan). Bull. Mar. Sci. 75, 115–125 (2004).
Google Scholar
60.Shenkar, N., Fine, M. & Loya, Y. Size matters: Bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294, 181–188 (2005).ADS
Google Scholar
61.Hughes, T. P. et al. Global warming impairs stock–recruitment dynamics of corals. Nature 568, 387–390 (2019).ADS
CAS
PubMed
Google Scholar
62.McClanahan, T. R., Maina, J., Moothien-Pillay, R. & Baker, A. C. Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. Mar. Ecol. Prog. Ser. 298, 131–142 (2005).ADS
Google Scholar
63.Hoogenboom, M. O. et al. Environmental drivers of variation in bleaching severity of Acropora species during an extreme thermal anomaly. Front. Mar. Sci. 4, 376. https://doi.org/10.3389/fmars.2017.00376 (2017).Article
Google Scholar
64.Schoepf, V. et al. Thermally variable, macrotidal reef habitats promote rapid recovery from mass coral bleaching. Front. Mar. Sci. 7, 245. https://doi.org/10.3389/fmars.2020.00245 (2020).Article
Google Scholar
65.Golbuu, Y. et al. Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26, 319–332 (2007).
Google Scholar
66.van Woesik, R. et al. Climate-change refugia in the sheltered bays of Palau: Analogs of future reefs. Ecol. Evol. 2, 2474–2484 (2012).PubMed
PubMed Central
Google Scholar
67.Penin, L., Adjeroud, M., Schrimm, M. & Lenihan, H. S. High spatial variability in coral bleaching around Moorea (French Polynesia): Patterns across locations and water depths. C. R. Biol. 330, 171–181 (2007).PubMed
Google Scholar
68.Penin, L., Vidal-Dupiol, J. & Adjeroud, M. Response of coral assemblages to thermal stress: Are bleaching intensity and spatial patterns consistent between events?. Environ. Monit. Assess. 185, 5031–5042 (2013).PubMed
Google Scholar
69.Brown, B. E., Downs, C. A., Dunne, R. P. & Gibb, S. W. Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242, 119–129 (2002).ADS
Google Scholar
70.Kenkel, C. D. et al. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol. Ecol. 22, 4335–4348 (2013).CAS
PubMed
Google Scholar
71.Burt, J. A. & Bauman, A. G. Suppressed coral settlement following mass bleaching in the southern Persian/Arabian Gulf. Aquat. Ecosyst. Heal. Manag. 23, 166–174 (2020).
Google Scholar
72.Shlesinger, T. & Loya, Y. Breakdown in spawning synchrony: A silent threat to coral persistence. Science 365, 1002–1007 (2019).ADS
CAS
PubMed
Google Scholar
73.Edmunds, P., Gates, R. & Gleason, D. The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar. Biol. 139, 981–989 (2001).
Google Scholar
74.Edmunds, P. J. Spatiotemporal variation in coral recruitment and its association with seawater temperature. Limnol. Oceanogr. 66, 1394–1408 (2021).ADS
Google Scholar
75.Bouwmeester, J. et al. Latitudinal variation in monthly-scale reproductive synchrony among Acropora coral assemblages in the Indo-Pacific. Coral Reefs 40, 1411–1418 (2021).
Google Scholar
76.Edmunds, P. J. MCR LTER: Coral reef: Long-term population and community dynamics: Corals, ongoing since 2005. knb-lter-mcr.4.38. 10.6073/pasta/10ee808a046cb63c0b8e3bc3c9799806 (2020).77.Claar, D. C. & Baum, J. K. Timing matters: Survey timing during extended heat stress can influence perceptions of coral susceptibility to bleaching. Coral Reefs 38, 559–565 (2019).ADS
Google Scholar
78.Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS
PubMed
PubMed Central
Google Scholar
79.Leichter, J., Seydel, K. & Gotschalk, C. MCR LTER: Coral reef: Benthic water temperature, ongoing since 2005. knb-lter-mcr.1035.13. 10.6073/pasta/2087a33cdd16986352bed443fecc7fd7 (2020).80.Bradford, M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).CAS
PubMed
Google Scholar
81.Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356 (1955).
Google Scholar
82.Masuko, T. et al. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal. Biochem. 339, 69–72 (2005).CAS
PubMed
Google Scholar
83.Stimson, J. & Kinzie, R. A. The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J. Exp. Mar. Bio. Ecol. 153, 63–74 (1991).
Google Scholar
84.Szmant-Froelich, A., Rhetter, M. & Riggs, L. Sexual reproduction of Favis fragum (ESPER): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull. Mar. Sci. 37, 880–892 (1985).
Google Scholar More