Fish community structure and dynamics are insufficient to mediate coral resilience
Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).CAS
PubMed
Article
Google Scholar
Hatcher, B. G. Coral reef primary productivity: a beggar’s banquet. Trends Ecol. Evol. 3, 106–111 (1988).CAS
PubMed
Article
Google Scholar
Hatcher, B. G. Coral reef primary productivity. A hierarchy of pattern and process. Trends Ecol. Evol. 5, 149–155 (1990).CAS
PubMed
Article
Google Scholar
Lewis, S. M. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol. Monogr. 56, 183–200 (1986).Article
Google Scholar
Carpenter, R. C. Partitioning herbivory and its effects on coral reef algal communities. Ecol. Monogr. 56, 345–364 (1986).Article
Google Scholar
McCook, L. J. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367 (1999).Article
Google Scholar
Meyer, J. L., Schultz, E. T. & Helfman, G. S. Fish schools: an asset to corals. Science 220, 1047–1049 (1983).CAS
PubMed
Article
Google Scholar
Allgeier, J. E., Layman, C. A., Mumby, P. J. & Rosemond, A. D. Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems. Glob. Change Biol. 20, 2459–2472 (2014).Article
Google Scholar
Shantz, A. A., Ladd, M. C., Schrack, E. & Burkepile, D. E. Fish-derived nutrient hotspots shape coral reef benthic communities. Ecol. Appl. 25, 2142–2152 (2015).PubMed
Article
Google Scholar
Folke, C. et al. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst. 35, 557–581 (2004).Article
Google Scholar
Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).CAS
PubMed
Article
Google Scholar
McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).CAS
PubMed
Article
Google Scholar
Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).CAS
PubMed
Article
Google Scholar
Hughes, T. P. et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17, 360–365 (2007).CAS
PubMed
Article
Google Scholar
Graham, N. A. J. et al. Managing resilience to reverse phase shifts in coral reefs. Front. Ecol. Environ. 11, 541–548 (2013).Article
Google Scholar
Holbrook, S. J., Schmitt, R. J., Adam, T. C. & Brooks, A. J. Coral reef resilience, tipping points and the strength of herbivory. Sci. Rep. 6, 35817 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).CAS
PubMed
Article
Google Scholar
Holling, C. S. Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4, 1–23 (1973).Article
Google Scholar
Mumby, P. J. et al. Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311, 98–101 (2006).CAS
PubMed
Article
Google Scholar
Green, A. L. & Bellwood, D. R. Monitoring Functional Groups of Herbivorous Reef Fishes as Indicators of Coral Reef Resilience. A Practical Guide for Coral reef Managers in the Asia Pacific Region (IUCN, 2009).Bozec, Y. M., O’Farrell, S., Bruggemann, J. H., Luckhurst, B. E. & Mumby, P. J. Tradeoffs between fisheries harvest and the resilience of coral reefs. Proc. Natl Acad. Sci. USA 113, 4536–4541 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
Bruno, J. F., Cote, I. M. & Toth, L. T. Climate change, coral loss, and the curious case of the parrotfish paradigm: why don’t marine protected sreas improve reef resilience? Ann. Rev. Mar. Sci. 11, 307–334 (2019).PubMed
Article
Google Scholar
Brandl, S. J. et al. Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Front. Ecol. Environ. 17, 445–454 (2019).Article
Google Scholar
Mora, C. A clear human footprint in the coral reefs of the Caribbean. Proc. Biol. Sci. 275, 767–773 (2008).PubMed
PubMed Central
Google Scholar
Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).CAS
PubMed
Article
Google Scholar
Allgeier, J. E., Layman, C. A., Mumby, P. J. & Rosemond, A. D. Biogeochemical implications of biodiversity and community structure across multiple coastal ecosystems. Ecol. Monogr. 85, 117–132 (2015).Article
Google Scholar
Mellin, C., Bradshaw, C. J., Fordham, D. A. & Caley, M. J. Strong but opposing beta-diversity–stability relationships in coral reef fish communities. Proc. Biol. Sci. 281, 20131993 (2014).CAS
PubMed
PubMed Central
Google Scholar
Nash, K. L. et al. Herbivore cross-scale redundancy supports response diversity and promotes coral reef resilience. J. Appl. Ecol. 53, 646–655 (2016).Article
Google Scholar
Thibaut, L. M., Connolly, S. R. & Sweatman, H. P. Diversity and stability of herbivorous fishes on coral reefs. Ecology 93, 891–901 (2012).PubMed
Article
Google Scholar
Zhang, S. Y. et al. Is coral richness related to community resistance to and recovery from disturbance? PeerJ 2, e308 (2014).PubMed
PubMed Central
Article
Google Scholar
Clements, C. S. & Hay, M. E. Biodiversity enhances coral growth, tissue survivorship and suppression of macroalgae. Nat. Ecol. Evol. 3, 178–182 (2019).PubMed
PubMed Central
Article
Google Scholar
Bellwood, D. R., Hoey, A. S., Ackerman, J. L. & Depczynski, M. Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob. Change Biol. 12, 1587–1594 (2006).Article
Google Scholar
Burkepile, D. E. & Hay, M. E. Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc. Natl Acad. Sci. USA 105, 16201–16206 (2008).CAS
PubMed
PubMed Central
Article
Google Scholar
Mumby, P. J. Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28, 761–773 (2009).Article
Google Scholar
Cheal, A. J., Emslie, M., MacNeil, M. A., Miller, I. & Sweatman, H. Spatial variation in the functional characteristics of herbivorous fish communities and the resilience of coral reefs. Ecol. Appl. 23, 174–188 (2013).PubMed
Article
Google Scholar
Cheal, A. J. et al. Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29, 1005–1015 (2010).Article
Google Scholar
Bellwood, D. R., Hughes, T. P., Folke, C. & Nystrom, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).CAS
PubMed
Article
Google Scholar
Mouillot, D. et al. Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc. Natl Acad. Sci. USA 111, 13757–13762 (2014).CAS
PubMed
PubMed Central
Article
Google Scholar
Graham, N. A., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).CAS
PubMed
Article
Google Scholar
Steneck, R. S., Mumby, P. J., Macdonald, C., Rasher, D. B. & Stoyle, G. Attenuating effects of ecosystem management on coral reefs. Sci. Adv. 4, eaao5493 (2018).PubMed
PubMed Central
Article
Google Scholar
Williams, I. D., Polunin, N. V. C. & Hendrick, V. J. Limits to grazing by herbivorous fishes and the impact of low coral cover on macroalgal abundance on a coral reef in Belize. Mar. Ecol. Prog. Ser. 222, 187–196 (2001).Article
Google Scholar
Harvey, C. J. et al. The importance of long-term ecological time series for integrated ecosystem assessment and ecosystem-based management. Prog. Oceanogr. 188, 102418 (2020).Article
Google Scholar
Robinson, J. P. W. et al. Productive instability of coral reef fisheries after climate-driven regime shifts. Nat. Ecol. Evol. 3, 183–190 (2019).PubMed
Article
Google Scholar
MacNeil, M. A. et al. Water quality mediates resilience on the Great Barrier Reef. Nat. Ecol. Evol. 3, 620–627 (2019).PubMed
Article
Google Scholar
Kayal, M. et al. Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS ONE 7, e47363 (2012).CAS
PubMed
PubMed Central
Article
Google Scholar
Adjeroud, M. et al. Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28, 775–780 (2009).Article
Google Scholar
Adam, T. C. et al. How will coral reef fish communities respond to climate-driven disturbances? Insight from landscape-scale perturbations. Oecologia 176, 285–296 (2014).PubMed
Article
Google Scholar
Munsterman, K. S., Allgeier, J. E., Peters, J. R. & Burkepile, D. E. A view from both ends: shifts in herbivore assemblages impact top-down and bottom-up processes on coral reefs. Ecosystems 24, 1702–1715 (2021).Article
Google Scholar
Newman, M. J., Paredes, G. A., Sala, E. & Jackson, J. B. Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecol. Lett. 9, 1216–1227 (2006).PubMed
Article
Google Scholar
McClanahan, T. R. et al. Critical thresholds and tangible targets for ecosystem-based management of coral reef fisheries. Proc. Natl Acad. Sci. USA 108, 17230–17233 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
Suchley, A., McField, M. D. & Alvarez-Filip, L. Rapidly increasing macroalgal cover not related to herbivorous fishes on Mesoamerican reefs. PeerJ 4, e2084 (2016).PubMed
PubMed Central
Article
Google Scholar
Rogers, A., Blanchard, J. L. & Mumby, P. J. Vulnerability of coral reef fisheries to a loss of structural complexity. Curr. Biol. 24, 1000–1005 (2014).CAS
PubMed
Article
Google Scholar
Hempson, T. N., Graham, N. A. J., MacNeil, M. A., Hoey, A. S. & Wilson, S. K. Ecosystem regime shifts disrupt trophic structure. Ecol. Appl 28, 191–200 (2018).PubMed
Article
Google Scholar
Mouillot, D. et al. Global marine protected areas do not secure the evolutionary history of tropical corals and fishes. Nat. Commun. 7, 10359 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
Han, X., Adam, T. C., Schmitt, R. J., Brooks, A. J. & Holbrook, S. J. Response of herbivore functional groups to sequential perturbations in Moorea, French Polynesia. Coral Reefs 35, 999–1009 (2016).Article
Google Scholar
Donovan, M. K. et al. Nitrogen pollution interacts with heat stress to increase coral bleaching across the seascape. Proc. Natl Acad. Sci. USA 117, 5351–5357 (2020).CAS
PubMed
PubMed Central
Article
Google Scholar
Holbrook, S. J. et al. Recruitment drives spatial variation in recovery rates of resilient coral reefs. Sci. Rep. 8, 7338 (2018).PubMed
PubMed Central
Article
Google Scholar
Doropoulos, C. et al. Characterising the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecol. Monogr. 86, 20–44 (2016).Article
Google Scholar
Russ, G. R., Questel, S. A., Rizzari, J. R. & Alcala, A. C. The parrotfish–coral relationship: refuting the ubiquity of a prevailing paradigm. Mar. Biol. 162, 2029–2045 (2015).Article
Google Scholar
Chung, A. E. et al. Building coral reef resilience through spatial herbivore management. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00098 (2019).Kelly, E. L. A. et al. A budget of algal production and consumption by herbivorous fish in an herbivore fisheries management area, Maui, Hawaii. Ecosphere 8, e01899 (2017).Article
Google Scholar
Edwards, A. J. Reef Rehabilitation Manual (Coral Reef Targeted Research & Capacity Building for Management Program, 2010).Worm, B. et al. Rebuilding global fisheries. Science 325, 578–585 (2009).CAS
PubMed
Article
Google Scholar
Sale, P. F. et al. Transforming management of tropical coastal seas to cope with challenges of the 21st century. Mar. Pollut. Bull. 85, 8–23 (2014).CAS
PubMed
Article
Google Scholar
Schindler, D. E. & Hilborn, R. Sustainability. Prediction, precaution, and policy under global change. Science 347, 953–954 (2015).CAS
PubMed
Article
Google Scholar
Mumby, P. J. et al. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427, 533–536 (2004).CAS
PubMed
Article
Google Scholar
Walsworth, T. E. et al. Management for network diversity speeds evolutionary adaptation to climate change. Nat. Clim. Change 9, 632–636 (2019).Article
Google Scholar
Cote, I. M. & Darling, E. S. Rethinking ecosystem resilience in the face of climate change. PLoS Biol. 8, e1000438 (2010).PubMed
PubMed Central
Article
Google Scholar
Darling, E. S. & Cote, I. M. Seeking resilience in marine ecosystems. Science 359, 986–987 (2018).CAS
PubMed
Article
Google Scholar
Rassweiler, A. et al. Perceptions and responses of Pacific Island fishers to changing coral reefs. Ambio 49, 130–143 (2020).PubMed
Article
Google Scholar
Moorea Coral Reef LTER & Carpenter, R. MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Benthic Algae and Other Community Components (Environmental Data Initiative, accessed 2019); https://doi.org/10.6073/pasta/37d9c451a908e4a6f8e7ab914b93f44fBrooks, A. MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Fishes (MCR, 2018).de Loma, T. L. et al. A framework for assessing impacts of marine protected areas in Moorea (French Polynesia). Pac. Sci. 62, 431–441 (2008).Article
Google Scholar
Nicholson, M. D. & Jennings, S. Testing candidate indicators to support ecosystem-based management: the power of monitoring surveys to detect temporal trends in fish community metrics. ICES J. Mar. Sci. 61, 35–42 (2004).Article
Google Scholar
Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270 (1984).
Google Scholar
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn (Springer, 2002).R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019). More