Directing coral larval settlement in coral aquaculture for reef restoration

directing-coral-larval-settlement-in-coral-aquaculture-for-reef-restoration
Directing coral larval settlement in coral aquaculture for reef restoration
  • Eddy, T. D. et al. Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4, 1278–1285. https://doi.org/10.1016/j.oneear.2021.08.016 (2021).

    Google Scholar 

  • Fabricius, K. E. et al. The seven sins of climate change: A review of rates of change, and quantitative impacts on ecosystems and water quality in the Great Barrier Reef. Mar. Pollut. Bull. 219, 118267. https://doi.org/10.1016/j.marpolbul.2025.118267 (2025).

    Google Scholar 

  • Zaneveld, J. R. et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7, 11833. https://doi.org/10.1038/ncomms11833 (2016).

    Google Scholar 

  • Souter, D. et al. Status of coral reefs of the world: 2020 report. Global Coral Reef Monitoring Network (GCRMN) and International Coral Reef Initiative (ICRI); https://doi.org/10.59387/WOTJ9184 (2021).

  • Okamoto, M., Nojima, S., Fujiwara, S. & Furushima, Y. Development of ceramic settlement devices for coral reef restoration using in situ sexual reproduction of corals. Fish. Sci. 74, 1245–1253. https://doi.org/10.1111/j.1444-2906.2008.01649.x (2008).

    Google Scholar 

  • Todinanahary, G. G. B. et al. Community-based coral aquaculture in Madagascar: A profitable economic system for a simple rearing technique?. Aquaculture 467, 225–234. https://doi.org/10.1016/j.aquaculture.2016.07.012 (2017).

    Google Scholar 

  • Rinkevich, B. Restoration strategies for coral reefs damaged by recreational activities: The use of sexual and asexual recruits. Restor. Ecol. 3, 241–251. https://doi.org/10.1111/j.1526-100X.1995.tb00091.x (1995).

    Google Scholar 

  • Boström-Einarsson, L. et al. Coral restoration – a systematic review of current methods, successes, failures and future directions. PLoS ONE 15, e0226631. https://doi.org/10.1371/journal.pone.0226631 (2020).

    Google Scholar 

  • Banaszak, A. T. et al. Applying coral breeding to reef restoration: Best practices, knowledge gaps, and priority actions in a rapidly-evolving field. Restor. Ecol. 31, e13913. https://doi.org/10.1111/rec.13913 (2023).

    Google Scholar 

  • Petersen, D. et al. The application of sexual coral recruits for the sustainable management of ex situ populations in public aquariums to promote coral reef conservation—SECORE Project. Aquat. Conserv. 16, 167–179. https://doi.org/10.1002/aqc.716 (2006).

    Google Scholar 

  • Pollock, F. J. et al. Coral larvae for restoration and research: a large-scale method for rearing Acropora millepora larvae, inducing settlement, and establishing symbiosis. PeerJ 5, e3732. https://doi.org/10.7717/peerj.3732 (2017).

    Google Scholar 

  • Randall, C. J. et al. Sexual production of corals for reef restoration in the Anthropocene. Mar. Ecol. Prog. Ser. 635, 203–232. https://doi.org/10.3354/meps13206 (2020).

    Google Scholar 

  • Harrison, P., & Wallace, C. In Reproduction, dispersal and recruitment of scleractinian corals. Ecosystems of the World, Vol. 25 (ed Dubinsky, Z.) 133–196. (Coral Reefs, Elsevier, 1990).

  • Negri, A., Webster, N., Hill, R. & Heyward, A. Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar. Ecol. Prog. Ser. 223, 121–131. https://doi.org/10.3354/meps223121 (2001).

    Google Scholar 

  • Petersen, L.-E. et al. Mono- and multispecies biofilms from a crustose coralline alga induce settlement in the scleractinian coral Leptastrea purpurea. Coral Reefs 40, 381–394. https://doi.org/10.1007/s00338-021-02062-5 (2021).

    Google Scholar 

  • Webster, N. S. et al. Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl. Environ. Microbiol. 70, 1213–1221. https://doi.org/10.1128/AEM.70.2.1213-1221.2004 (2004).

    Google Scholar 

  • Morse, D. E., Morse, A. N. C., Raimondi, P. T. & Hooker, N. Morphogen-based chemical flypaper for Agaricia humilis coral larvae. Biol. Bull. 186, 172–181. https://doi.org/10.2307/1542051 (1994).

    Google Scholar 

  • Tebben, J. et al. Chemical mediation of coral larval settlement by crustose coralline algae. Sci. Rep. 5, 10803. https://doi.org/10.1038/srep10803 (2015).

    Google Scholar 

  • Abdul Wahab, M. A. et al. Hierarchical settlement behaviours of coral larvae to common coralline algae. Sci. Rep. 13, 5795. https://doi.org/10.1038/s41598-023-32676-4 (2023).

    Google Scholar 

  • Jorissen, H. et al. Coral larval settlement preferences linked to crustose coralline algae with distinct chemical and microbial signatures. Sci. Rep. 11, 14610. https://doi.org/10.1038/s41598-021-94096-6 (2021).

    Google Scholar 

  • Randall, C. J. et al. Larval precompetency and settlement behaviour in 25 Indo-Pacific coral species. Commun. Biol. 7, 1–15. https://doi.org/10.1038/s42003-024-05824-3 (2024).

    Google Scholar 

  • Whitman, T. N. et al. Settlement of larvae from four families of corals in response to a crustose coralline alga and its biochemical morphogens. Sci. Rep. 10, 16397. https://doi.org/10.1038/s41598-020-73103-2 (2020).

    Google Scholar 

  • Babcock, R. & Mundy, C. Coral recruitment: consequences of settlement choice for early growth and survivorship in two scleractinians. J. Exp. Mar. Biol. Ecol. 206, 179–201. https://doi.org/10.1016/S0022-0981(96)02622-6 (1996).

    Google Scholar 

  • Ricardo, G. F. et al. Impacts of water quality on Acropora coral settlement: The relative importance of substrate quality and light. Sci. Total Environ. 777, 146079. https://doi.org/10.1016/j.scitotenv.2021.146079 (2021).

    Google Scholar 

  • Fong, J. et al. Effects of material type and surface roughness of settlement tiles on macroalgal colonisation and early coral recruitment success. Coral Reefs 43, 1083–1096. https://doi.org/10.1007/s00338-024-02526-4 (2024).

    Google Scholar 

  • Fong, J. et al. The interplay of temperature, light, and substrate type in driving growth and reproduction of an important tropical crustose coralline alga. J. Appl. Phycol. 36, 3133–3145. https://doi.org/10.1007/s10811-024-03312-z (2024).

    Google Scholar 

  • Hoog Antink, M. M. et al. Porous ceramics with tailored pore size and morphology as substrates for coral larval settlement. Ceram. Int. 44, 16561–16571. https://doi.org/10.1016/j.ceramint.2018.06.078 (2018).

    Google Scholar 

  • Lee, C. S., Walford, J. & Goh, B. P. L. Adding coral rubble to substrata enhances settlement of Pocillopora damicornis larvae. Coral Reefs 28, 529–533. https://doi.org/10.1007/s00338-009-0467-y (2009).

    Google Scholar 

  • Leonard, C. et al. Performance of innovative materials as recruitment substrates for coral restoration. Restor. Ecol. 30, e13625. https://doi.org/10.1111/rec.13625 (2022).

    Google Scholar 

  • Mallela, J., Milne, B. C. & Martinez-Escobar, D. A comparison of epibenthic reef communities settling on commonly used experimental substrates: PVC versus ceramic tiles. J. Exp. Mar. Biol. Ecol. 486, 290–295. https://doi.org/10.1016/j.jembe.2016.10.028 (2017).

    Google Scholar 

  • Ramsby, B. D. et al. Developing seeding devices and rapid deployment methods for upscaling coral reef restoration. Restor. Ecol. 34, e70206. https://doi.org/10.1111/rec.70206 (2025).

    Google Scholar 

  • Whitman, T. N. et al. Seeded Acropora digitifera corals survive best on wave-exposed reefs with grazing from small fishes. Restor. Ecol. 33, e70016. https://doi.org/10.1111/rec.70016 (2025).

    Google Scholar 

  • Nordborg, F. M. et al. Standard operating procedure: Optimised larval settlement in a high throughput coral aquaculture facility. SOP prepared for the Reef Restoration and Adaptation Program. Australian Institute of Marine Science, Townsville QLD, 41 pp. https://gbrrestoration.org/wp-content/uploads/2025/07/SOP-Mass-settlement-of-coral-larvae.pdf (2024).

  • Ramsby, B. D. et al. Low light intensity increased survival of coral spat in aquaculture. Coral Reefs 43, 627–640. https://doi.org/10.1007/s00338-024-02489-6 (2024).

    Google Scholar 

  • Heyward, A. J. & Negri, A. P. Natural inducers for coral larval metamorphosis. Coral Reefs 18, 273–279. https://doi.org/10.1007/s003380050193 (1999).

    Google Scholar 

  • Harrington, L., Fabricius, K., De’ath, G. & Negri, A. Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85, 3428–3437. https://doi.org/10.1890/04-0298 (2004).

    Google Scholar 

  • Sharp, K. H. et al. Induction of larval settlement in the reef coral Porites astreoides by a cultivated marine Roseobacter strain. Biol. Bull. 228, 98–107. https://doi.org/10.1086/BBLv228n2p98 (2015).

    Google Scholar 

  • Tran, C. & Hadfield, M. G. Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar. Ecol. Prog. Ser. 433, 85–96. https://doi.org/10.3354/meps09192 (2011).

    Google Scholar 

  • O’Brien, P. A. et al. Light and dark biofilm adaptation impacts larval settlement in diverse coral species. Environ. Microbiome 20, 11. https://doi.org/10.1186/s40793-025-00670-0 (2025).

    Google Scholar 

  • Turnlund, A. C. et al. Understanding the role of micro-organisms in the settlement of coral larvae through community ecology. Mar. Biol. 172, 43. https://doi.org/10.1007/s00227-025-04607-6 (2025).

    Google Scholar 

  • Alker, A. T. et al. Linking bacterial tetrabromopyrrole biosynthesis to coral metamorphosis. ISME Commun. 3, 98. https://doi.org/10.1038/s43705-023-00309-6 (2023).

    Google Scholar 

  • Sneed, J. M., Sharp, K. H., Ritchie, K. B. & Paul, V. J. The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals. Proc. R. Soc. B 281, 20133086. https://doi.org/10.1098/rspb.2013.3086 (2014).

    Google Scholar 

  • Tebben, J. et al. Induction of larval metamorphosis of the coral Acropora millepora by Tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLoS ONE 6, e19082. https://doi.org/10.1371/journal.pone.0019082 (2011).

    Google Scholar 

  • Petersen, L. E. et al. Photodegradation of a bacterial pigment and resulting hydrogen peroxide release enable coral settlement. Sci. Rep. 13, 3562. https://doi.org/10.1038/s41598-023-30470-w (2023).

    Google Scholar 

  • Moeller, M., Nietzer, S. & Schupp, P. J. Neuroactive compounds induce larval settlement in the scleractinian coral Leptastrea purpurea. Sci. Rep. 9, 2291. https://doi.org/10.1038/s41598-019-38794-2 (2019).

    Google Scholar 

  • Erwin, P. M. & Szmant, A. M. Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide. Coral Reefs 29, 929–939. https://doi.org/10.1007/s00338-010-0634-1 (2010).

    Google Scholar 

  • Iwao, K., Fujisawa, T. & Hatta, M. A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21, 127–129. https://doi.org/10.1007/s00338-002-0219-8 (2002).

    Google Scholar 

  • Shikina, S. et al. Involvement of GLWamide neuropeptides in polyp contraction of the adult stony coral Euphyllia ancora. Sci. Rep. 10, 9427. https://doi.org/10.1038/s41598-020-66438-3 (2020).

    Google Scholar 

  • Takahashi, T. & Hatta, M. The importance of GLWamide neuropeptides in cnidarian development and physiology. J. Amino Acids 2011, 424501. https://doi.org/10.4061/2011/424501 (2011).

    Google Scholar 

  • Takahashi, T. et al. Systematic isolation of peptide signal molecules regulating development in hydra: LWamide and PW families. Proc. Natl. Acad. Sci. U.S.A. 94, 1241–1246. https://doi.org/10.1073/pnas.94.4.1241 (1997).

    Google Scholar 

  • Kundu, S. et al. Biomimetic chemical microhabitats enhance coral settlement. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2025.03.019 (2025).

    Google Scholar 

  • Fujiwara, S. et al. Effect of substratum structural complexity of coral seedlings on the settlement and post-settlement survivorship of coral settlers. Oceans 4, 1. https://doi.org/10.3390/oceans4010001 (2023).

    Google Scholar 

  • Levenstein, M. A. et al. Millimeter-scale topography facilitates coral larval settlement in wave-driven oscillatory flow. PLoS ONE 17, e0274088. https://doi.org/10.1371/journal.pone.0274088 (2022).

    Google Scholar 

  • Nozawa, Y. Effective size of refugia for coral spat survival. J. Exp. Mar. Biol. Ecol. 413, 145–149. https://doi.org/10.1016/j.jembe.2011.12.008 (2012).

    Google Scholar 

  • Randall, C. J., Giuliano, C., Heyward, A. J. & Negri, A. P. Enhancing coral survival on deployment devices with microrefugia. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.662263 (2021).

    Google Scholar 

  • Petersen, D., Laterveer, M. & Schuhmacher, H. Innovative substrate tiles to spatially control larval settlement in coral culture. Mar. Biol. 146, 937–942. https://doi.org/10.1007/s00227-004-1503-7 (2005).

    Google Scholar 

  • Whalan, S. et al. Larval settlement: the role of surface topography for sessile coral reef invertebrates. PLoS ONE 10, e0117675. https://doi.org/10.1371/journal.pone.0117675 (2015).

    Google Scholar 

  • Foster, T. & Gilmour, J. P. Seeing red: Coral larvae are attracted to healthy looking reefs. Mar. Ecol. Prog. Ser. 559, 65–71. https://doi.org/10.3354/meps11902 (2016).

    Google Scholar 

  • Mason, B., Beard, M. & Miller, M. W. Coral larvae settle at a higher frequency on red surfaces. Coral Reefs 30, 667–676. https://doi.org/10.1007/s00338-011-0739-1 (2011).

    Google Scholar 

  • Bridge, T. C. L. et al. A tenuis relationship: traditional taxonomy obscures systematics and biogeography of the Acropora tenuis species complex. Zool. J. Linn. Soc. 202, zlad062. https://doi.org/10.1093/zoolinnean/zlad062 (2024).

    Google Scholar 

  • Grasso, L. C. et al. The biology of coral metamorphosis: molecular responses of larvae to inducers of settlement and metamorphosis. Dev. Biol. 353, 411–419. https://doi.org/10.1016/j.ydbio.2011.02.010 (2011).

    Google Scholar 

  • Leitz, T., Morand, K. & Mann, M. Metamorphosin A: A novel peptide controlling development of the lower metazoan Hydractinia echinata (Coelenterata, Hydrozoa). Dev. Biol. 163, 440–446. https://doi.org/10.1006/dbio.1994.1160 (1994).

    Google Scholar 

  • Brunner, R. Investigating receptors and signalling pathways of coral settlement and metamorphosis using proteomics, transcriptomics and phylogenetics [PhD, James Cook University]. James Cook University Research Repository; https://doi.org/10.25903/ggd7-xe43 (2023).

  • Di Mauro, V. et al. Ecotoxicological effects of four commonly used organic solvents on the scleractinian coral Montipora digitata. Toxics 11, 4. https://doi.org/10.3390/toxics11040367 (2023).

    Google Scholar 

  • Abdul Wahab, M. A. et al. Standard operating procedure: Coral spawning, larval culturing and the production of coral spats in aquaculture for reef restoration. SOP prepared for the Reef Restoration and Adaptation Program. 36 (Australian Institute of Marine Science, Townsville, QLD, 2022)

  • Karacan, I. et al. The synthesis of hydroxyapatite from artificially grown Red Sea hydrozoan coral for antimicrobacterial drug delivery system applications. J. Aust. Ceram. Soc. 57, 399–407. https://doi.org/10.1007/s41779-020-00554-1 (2021).

    Google Scholar 

  • R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; https://www.R-project.org/ (2023).

  • Brooks, M. E. et al. GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9, 378–400. https://doi.org/10.32614/RJ-2017-066 (2017).

    Google Scholar 

  • Hartig, F. DHARMa: residual diagnostics for hierarchical (multi-level / mixed) regression models. R package version 0.4.7; https://github.com/florianhartig/dharma (2024).

  • Wickham, H. ggplot2: Elegant graphics for data analysis. R package version 3.5.2. (Springer-Verlag, New York, 2016).

  • Bartoń, K. MuMIn: Multi-model inference. R package version 1.47.5 (2023).

  • Müller, W. A. & Leitz, T. Metamorphosis in the Cnidaria. Can. J. Zool. 80, 1755–1771. https://doi.org/10.1139/z02-130 (2002).

    Google Scholar 

  • Ishii, Y. et al. Gene expression alterations from reversible to irreversible stages during coral metamorphosis. Zoolog Lett. 8, 4. https://doi.org/10.1186/s40851-022-00187-1 (2022).

    Google Scholar 

  • Schindler, S. & Bechtold, T. Mechanistic insights into the electrochemical oxidation of dopamine by cyclic voltammetry. J. Electroanal. Chem. 836, 94–101. https://doi.org/10.1016/j.jelechem.2019.01.069 (2019).

    Google Scholar 

  • Amar, K. O., Chadwick, N. E. & Rinkevich, B. Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny. BMC Evol. Biol. 8, 126. https://doi.org/10.1186/1471-2148-8-126 (2008).

    Google Scholar 

  • Doropoulos, C., Evensen, N. R., Gómez-Lemos, L. A. & Babcock, R. C. Density-dependent coral recruitment displays divergent responses during distinct early life-history stages. R. Soc. Open Sci. 4, 170082. https://doi.org/10.1098/rsos.170082 (2017).

    Google Scholar 

  • Jiang, L. et al. Gregarious larval settlement mediates the responses of new recruits of the reef coral Acropora austera to ocean warming and acidification. Front. Mar. Sci. https://doi.org/10.3389/fmars.2022.964803 (2022).

    Google Scholar 

  • Puill-Stephan, E., van Oppen, M. J. H., Pichavant-Rafini, K. & Willis, B. L. High potential for formation and persistence of chimeras following aggregated larval settlement in the broadcast spawning coral. Acropora millepora. Proc. R. Soc. B 279, 699–708. https://doi.org/10.1098/rspb.2011.1035 (2012).

    Google Scholar 

  • Raymundo, L. & Maypa, A. Recovery of the Apo Island Marine Reserve, Philippines, 2 years after the El Niño bleaching event. Coral Reefs 21, 3. https://doi.org/10.1007/s00338-002-0237-6 (2002).

    Google Scholar 

  • Rinkevich, B. Coral chimerism as an evolutionary rescue mechanism to mitigate global climate change impacts. Glob. Change Biol. 25, 1198–1206. https://doi.org/10.1111/gcb.14576 (2019).

    Google Scholar 

  • Shefy, D., Shashar, N. & Rinkevich, B. Exploring traits of engineered coral entities to be employed in reef restoration. J. Mar. Sci. Eng. 8, 1038. https://doi.org/10.3390/jmse8121038 (2020).

    Google Scholar 

  • Vidal-Dupiol, J. et al. Frontloading of stress response genes enhances robustness to environmental change in chimeric corals. BMC Biol. 20, 167. https://doi.org/10.1186/s12915-022-01371-7 (2022).

    Google Scholar 

  • Carleton, J. H. & Sammarco, P. W. Effects of substratum irregularity on success of coral settlement: Quantification by comparative geomorphological techniques. Bull. Mar. Sci. 40, 85–98 (1987).

    Google Scholar 

  • Scardino, A. J., Harvey, E. & De Nys, R. Testing attachment point theory: Diatom attachment on microtextured polyimide biomimics. Biofouling 22, 55–60. https://doi.org/10.1080/08927010500506094 (2006).

    Google Scholar 

  • Nishikawa, A., Katoh, M. & Sakai, K. Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar. Ecol. Prog. Ser. 256, 87–97. https://doi.org/10.3354/meps256087 (2003).

    Google Scholar