Global decline in capacity of coral reefs to provide ecosystem services

Abstract

•Coral reef habitat, biodiversity, fisheries, effort, and food-web impacts are evaluated•Global coverage of living coral has declined by half since the 1950s•Catch of coral reef associate fishes per unit effort has decreased by 60% since 1950•Coral reefs’ capacity to provide ecosystem services has declined by half since the 1950s Coral reef ecosystems are important for tropical and subtropical coastal communities, small-island developing states, and Indigenous peoples because they provide ecosystem services such as food provision, livelihood opportunities, carbon sequestration, and protection from storms. We have derived global estimates of key ecosystem services provided by coral reefs: catches of coral-reef-associated fishes, abundance of coral-reef-associated fishes, coral-reef-associated biodiversity, and consumption of coral-reef-associated fishes by Indigenous peoples. Our study indicates that the capacity of coral reefs to provide ecosystem services that are relied on by millions of people worldwide has declined by half since the 1950s. Achieving climate-change-emissions targets and reducing local impacts can reduce stress on coral reefs, allowing them and the ecosystem services that they provide to persist. Coral reefs worldwide are facing impacts from climate change, overfishing, habitat destruction, and pollution. The cumulative effect of these impacts on global capacity of coral reefs to provide ecosystem services is unknown. Here, we evaluate global changes in extent of coral reef habitat, coral reef fishery catches and effort, Indigenous consumption of coral reef fishes, and coral-reef-associated biodiversity. Global coverage of living coral has declined by half since the 1950s. Catches of coral-reef-associated fishes peaked in 2002 and are in decline despite increasing fishing effort, and catch-per-unit effort has decreased by 60% since 1950. At least 63% of coral-reef-associated biodiversity has declined with loss of coral extent. With projected continued degradation of coral reefs and associated loss of biodiversity and fisheries catches, the well-being and sustainable coastal development of human communities that depend on coral reef ecosystem services are threatened. Coral reefs worldwide are facing impacts from climate change, overfishing, habitat destruction, and pollution. The cumulative effect of these impacts on global capacity of coral reefs to provide ecosystem services is unknown. Here, we evaluate global changes in extent of coral reef habitat, coral reef fishery catches and effort, Indigenous consumption of coral reef fishes, and coral-reef-associated biodiversity. Global coverage of living coral has declined by half since the 1950s. Catches of coral-reef-associated fishes peaked in 2002 and are in decline despite increasing fishing effort, and catch-per-unit effort has decreased by 60% since 1950. At least 63% of coral-reef-associated biodiversity has declined with loss of coral extent. With projected continued degradation of coral reefs and associated loss of biodiversity and fisheries catches, the well-being and sustainable coastal development of human communities that depend on coral reef ecosystem services are threatened. Coral reefs are biodiversity hotspots that provide millions of people with ecosystem services such as food provision, livelihood opportunities, carbon sequestration, and buffering against extreme climate events.3Cinner J.E. Huchery C. MacNeil M.A. Graham N.A.J. McClanahan T.R. Maina J. Maire E. Kittinger J.N. Hicks C.C. Mora C. et al.Bright spots among the world’s coral reefs.Nature. 2016; 535: 416-419Crossref PubMed Scopus (280) Google Scholar, 4Hicks C.C. Cohen P.J. Graham N.A.J. Nash K.L. Allison E.H. D’Lima C. Mills D.J. Roscher M. Thilsted S.H. Thorne-Lyman A.L. MacNeil M.A. Harnessing global fisheries to tackle micronutrient deficiencies.Nature. 2019; 574: 95-98Crossref PubMed Scopus (191) Google Scholar, 5Woodhead A.J. Hicks C.C. Norström A.V. Williams G.J. Graham N.A.J. Coral reef ecosystem services in the Anthropocene.Funct. Ecol. 2019; 33: 1023-1034Google Scholar, 6Bruno J.F. Selig E.R. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons.PLoS ONE. 2007; 2: e711Crossref PubMed Scopus (831) Google Scholar, 7Hughes T.P. Barnes M.L. Bellwood D.R. Cinner J.E. Cumming G.S. Jackson J.B.C. Kleypas J. van de Leemput I.A. Lough J.M. Morrison T.H. et al.Coral reefs in the Anthropocene.Nature. 2017; 546: 82-90Crossref PubMed Scopus (818) Google Scholar, 8Eddy T.D. Cheung W.W.L. Bruno J.F. Historical baselines of coral cover on tropical reefs as estimated by expert opinion.PeerJ. 2018; 6: e4308Crossref PubMed Scopus (13) Google Scholar, 9Jackson J.B.C. Kirby M.X. Berger W.H. Bjorndal K.A. Botsford L.W. Bourque B.J. Bradbury R.H. Cooke R. Erlandson J. Estes J.A. et al.Historical overfishing and the recent collapse of coastal ecosystems.Science. 2001; 293: 629-637Crossref PubMed Scopus (4555) Google Scholar, 10Díaz, S., Settele, J.E.S. and Brondízio, E.S. (2019). Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, H.T. Ngo, M. Guèze, J. Agard, A. Arneth, P. Balvanera, K.A. Brauman, S.H.M. Butchart, K.M.A. Chan, L.A. Garibaldi, K. Ichii, J. Liu, S.M. Subramanian, G.F. Midgley, P. Miloslavich, Z. Molnár, D. Obura, A. Pfaff, S. Polasky, A. Purvis, J. Razzaque, B. Reyers, R. Roy Chowdhury, Y.J. Shin, and I.J. Visseren-Hamakers, K.J. Willis, and C.N. Zayas, eds. (Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services).Google Scholar, 11Worm B. Barbier E.B. Beaumont N. Duffy J.E. Folke C. Halpern B.S. Jackson J.B.C. Lotze H.K. Micheli F. Palumbi S.R. et al.Impacts of biodiversity loss on ocean ecosystem services.Science. 2006; 314: 787-790Crossref PubMed Scopus (2967) Google Scholar, 12Sheppard C. Dixon D.J. Gourlay M. Sheppard A. Payet R. Coral mortality increases wave energy reaching shores protected by reef flats: Examples from the Seychelles.Estuar. Coast. Shelf Sci. 2005; 64: 223-234Crossref Scopus (245) Google Scholar, 13Ferrario F. Beck M.W. Storlazzi C.D. Micheli F. Shepard C.C. Airoldi L. The effectiveness of coral reefs for coastal hazard risk reduction and adaptation.Nat. Commun. 2014; 5: 3794Crossref PubMed Scopus (403) Google Scholar, 14Quataert E. Storlazzi C. van Rooijen A. Cheriton O. van Dongeren A. The influence of coral reefs and climate change on wave-driven flooding of tropical coastlines.Geophys. Res. Lett. 2015; 42: 6407-6415Crossref Scopus (146) Google Scholar, 15Perry C.T. Alvarez-Filip L. Graham N.A.J. Mumby P.J. Wilson S.K. Kench P.S. Manzello D.P. Morgan K.M. Slangen A.B.A. Thomson D.P. et al.Loss of coral reef growth capacity to track future increases in sea level.Nature. 2018; 558: 396-400Crossref PubMed Scopus (156) Google Scholar, 16Woodhead A.J. Graham N.A.J. Robinson J.P.W. Norström A.V. Bodin N. Marie S. Balett M.-C. Hicks C.C. Fishers perceptions of ecosystem service change associated with climate-disturbed coral reefs.People Nat. 2021; 3: 639-657Crossref Scopus (2) Google Scholar The capacity of coral reefs to provide these services can change on millennial timescales with natural fluctuations in environmental conditions or on decadal timescales due to anthropogenic stressors such as overfishing, pollution, habitat destruction, and climate change.7Hughes T.P. Barnes M.L. Bellwood D.R. Cinner J.E. Cumming G.S. Jackson J.B.C. Kleypas J. van de Leemput I.A. Lough J.M. Morrison T.H. et al.Coral reefs in the Anthropocene.Nature. 2017; 546: 82-90Crossref PubMed Scopus (818) Google Scholar,17Newton K. Côté I.M. Pilling G.M. Jennings S. Dulvy N.K. Current and future sustainability of island coral reef fisheries.Curr. Biol. 2007; 17: 655-658Abstract Full Text Full Text PDF PubMed Scopus (287) Google Scholar, 18Maire E. Cinner J. Velez L. Huchery C. Mora C. Dagata S. Vigliola L. Wantiez L. Kulbicki M. Mouillot D. How accessible are coral reefs to people? A global assessment based on travel time.Ecol. Lett. 2016; 19: 351-360Crossref PubMed Scopus (69) Google Scholar, 19Hughes T.P. Baird A.H. Dinsdale E.A. Moltschaniwskyj N.A. Pratchett M.S. Tanner J.E. Willis B.L. Assembly rules of reef corals are flexible along a steep climatic gradient.Curr. Biol. 2012; 22: 736-741Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar Understanding the impacts of these stressors on the ocean’s capacity to provide ecosystem services is important for transitioning to a sustainable blue economy,20Cisneros-Montemayor A.M. Moreno-Báez M. Reygondeau G. Cheung W.W.L. Crosman K.M. González-Espinosa P.C. Lam V.W.Y. Oyinlola M.A. Singh G.G. Swartz W. et al.Enabling conditions for an equitable and sustainable blue economy.Nature. 2021; 591: 396-401Crossref PubMed Scopus (31) Google Scholar establishing recovery targets,8Eddy T.D. Cheung W.W.L. Bruno J.F. Historical baselines of coral cover on tropical reefs as estimated by expert opinion.PeerJ. 2018; 6: e4308Crossref PubMed Scopus (13) Google Scholar,21Pauly D. Anecdotes and the shifting baseline syndrome of fisheries.Trends Ecol. Evol. 1995; 10: 430Abstract Full Text PDF PubMed Scopus (1524) Google Scholar achieving the United Nations (UN) sustainable development goals (SDGs),22Lam V.W.Y. Allison E.H. Bell J.D. Blythe J. Cheung W.W.L. Frölicher T.L. Gasalla M.A. Sumaila U.R. Climate change, tropical fisheries and prospects for sustainable development.Nat. Rev. Earth Environ. 2020; 1: 440-454Crossref Scopus (40) Google Scholar and anticipating where and how future societies will be impacted under socio-economic and greenhouse-gas-emissions scenarios.22Lam V.W.Y. Allison E.H. Bell J.D. Blythe J. Cheung W.W.L. Frölicher T.L. Gasalla M.A. Sumaila U.R. Climate change, tropical fisheries and prospects for sustainable development.Nat. Rev. Earth Environ. 2020; 1: 440-454Crossref Scopus (40) Google Scholar,23IPCC (2019). Special Report on the Ocean and Cryosphere in a Changing Climate, H.-O. Pörtner, D.C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, and N.M. Weyer, eds. (IPCC).Google Scholar There are an estimated 6 million coral reef fishers worldwide,24Teh L.S.L. Teh L.C.L. Sumaila U.R. A Global Estimate of the Number of Coral Reef Fishers.PLoS ONE. 2013; 8: e65397Crossref PubMed Scopus (125) Google Scholar and coral reef fisheries are valued at USD 6 billion.25Reefs at Risk Revisited Report | World Resources Institute https://www.wri.org/research/reefs-risk-revisited.Google Scholar Coastal Indigenous peoples have essential cultural relationships with coral reef ecosystems, and their consumption of seafood is 15 times higher than that of non-Indigenous populations.2Cisneros-Montemayor A.M. Pauly D. Weatherdon L.V. Ota Y. A Global Estimate of Seafood Consumption by Coastal Indigenous Peoples.PLoS ONE. 2016; 11: e0166681Crossref PubMed Scopus (98) Google Scholar Fish is an important source of nutrition for people in small-island developing states (SIDSs),26Wabnitz C.C.C. Cisneros-Montemayor A.M. Hanich Q. Ota Y. Ecotourism, climate change and reef fish consumption in Palau: Benefits, trade-offs and adaptation strategies.Mar. Policy. 2018; 88: 323-332Crossref Scopus (38) Google Scholar comprising 50%–90% of dietary animal protein in Pacific Island countries and territories,27Bell J.D. Kronen M. Vunisea A. Nash W.J. Keeble G. Demmke A. Pontifex S. Andréfouët S. Planning the use of fish for food security in the Pacific.Mar. Policy. 2009; 33: 64-76Crossref Scopus (315) Google Scholar 50% in west Africa,4Hicks C.C. Cohen P.J. Graham N.A.J. Nash K.L. Allison E.H. D’Lima C. Mills D.J. Roscher M. Thilsted S.H. Thorne-Lyman A.L. MacNeil M.A. Harnessing global fisheries to tackle micronutrient deficiencies.Nature. 2019; 574: 95-98Crossref PubMed Scopus (191) Google Scholar,28The scourge of “hidden hunger”: global dimensions of micronutrient deficiencies https://agris.fao.org/agris-search/search.do?recordID=XF2004414753.Google Scholar and 37% in southeast Asia.22Lam V.W.Y. Allison E.H. Bell J.D. Blythe J. Cheung W.W.L. Frölicher T.L. Gasalla M.A. Sumaila U.R. Climate change, tropical fisheries and prospects for sustainable development.Nat. Rev. Earth Environ. 2020; 1: 440-454Crossref Scopus (40) Google Scholar,29Teh L.S.L. Teh L.C.L. Sumaila U.R. Quantifying the overlooked socio-economic contribution of small-scale fisheries in Sabah, Malaysia.Fish. Res. 2011; 110: 450-458Crossref Scopus (41) Google Scholar In these regions, fish are an important source of micronutrients, such as iron, zinc, and omega-3 fatty acids.4Hicks C.C. Cohen P.J. Graham N.A.J. Nash K.L. Allison E.H. D’Lima C. Mills D.J. Roscher M. Thilsted S.H. Thorne-Lyman A.L. MacNeil M.A. Harnessing global fisheries to tackle micronutrient deficiencies.Nature. 2019; 574: 95-98Crossref PubMed Scopus (191) Google Scholar There is increased recognition and need to contextualize efforts and challenges with ensuring protection and restoration of tropical marine ecosystems, notably coral reefs. In recent studies, this has included global analyses of Indigenous-led initiatives to support sovereignty and nature conservation in traditional territories30Garnett S.T. Burgess N.D. Fa J.E. Fernández-Llamazares Á. Molnár Z. Robinson C.J. Watson J.E.M. Zander K.K. Austin B. Brondizio E.S. et al.A spatial overview of the global importance of Indigenous lands for conservation.Nat. Sustain. 2018; 1: 369-374Crossref Scopus (350) Google Scholar,31von der Porten S. Ota Y. Cisneros-Montemayor A. Pictou S. The Role of Indigenous Resurgence in Marine Conservation.Coast. Manage. 2019; 47: 527-547Crossref Scopus (10) Google Scholar and a wider recognition of the foundational efforts of SIDSs to redefine sustainable development approaches under a blue economy.20Cisneros-Montemayor A.M. Moreno-Báez M. Reygondeau G. Cheung W.W.L. Crosman K.M. González-Espinosa P.C. Lam V.W.Y. Oyinlola M.A. Singh G.G. Swartz W. et al.Enabling conditions for an equitable and sustainable blue economy.Nature. 2021; 591: 396-401Crossref PubMed Scopus (31) Google Scholar,32Keen M.R. Schwarz A.-M. Wini-Simeon L. Towards defining the Blue Economy: Practical lessons from pacific ocean governance.Mar. Policy. 2018; 88: 333-341Crossref Scopus (69) Google Scholar The global community has identified the importance of ecosystem services provided by coral reefs through its commitment to achieve targets associated with SDG2 (end hunger, achieve food security and improved nutrition, and promote sustainable agriculture) and SDG14 (conserve and sustainably use the oceans, seas, and marine resources for sustainable development). Coral cover on tropical reefs has declined substantially over the last 40 years.6Bruno J.F. Selig E.R. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons.PLoS ONE. 2007; 2: e711Crossref PubMed Scopus (831) Google Scholar,8Eddy T.D. Cheung W.W.L. Bruno J.F. Historical baselines of coral cover on tropical reefs as estimated by expert opinion.PeerJ. 2018; 6: e4308Crossref PubMed Scopus (13) Google Scholar,33Gardner T.A. Côté I.M. Gill J.A. Grant A. Watkinson A.R. Long-term region-wide declines in Caribbean corals.Science. 2003; 301: 958-960Crossref PubMed Scopus (1458) Google Scholar, 34Aronson R.B. Precht W.F. Conservation, precaution, and Caribbean reefs.Coral Reefs. 2006; 25: 441-450Crossref Scopus (187) Google Scholar, 35Hughes T.P. Anderson K.D. Connolly S.R. Heron S.F. Kerry J.T. Lough J.M. Baird A.H. Baum J.K. Berumen M.L. Bridge T.C. et al.Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.Science. 2018; 359: 80-83Crossref PubMed Scopus (920) Google Scholar Anthropogenic ocean warming has triggered mass bleaching and disease outbreaks, greatly reducing the extent of coral cover of nearly all the world’s tropical coral reefs.6Bruno J.F. Selig E.R. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons.PLoS ONE. 2007; 2: e711Crossref PubMed Scopus (831) Google Scholar,35Hughes T.P. Anderson K.D. Connolly S.R. Heron S.F. Kerry J.T. Lough J.M. Baird A.H. Baum J.K. Berumen M.L. Bridge T.C. et al.Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.Science. 2018; 359: 80-83Crossref PubMed Scopus (920) Google Scholar, 36Baker A.C. Glynn P.W. Riegl B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook.Estuar. Coast. Shelf Sci. 2008; 80: 435-471Crossref Scopus (806) Google Scholar, 37Selig E.R. Casey K.S. Bruno J.F. Temperature-driven coral decline: the role of marine protected areas.Glob. Change Biol. 2012; 18: 1561-1570Crossref Scopus (88) Google Scholar, 38Randall C.J. van Woesik R. Contemporary white-band disease in Caribbean corals driven by climate change.Nat. Clim. Chang. 2015; 5: 375-379Crossref Scopus (82) Google Scholar Local drivers like pollution and overfishing are thought to contribute to coral loss in some locations;39MacNeil M.A. Mellin C. Matthews S. Wolff N.H. McClanahan T.R. Devlin M. Drovandi C. Mengersen K. Graham N.A.J. Water quality mediates resilience on the Great Barrier Reef.Nat. Ecol. Evol. 2019; 3: 620-627Crossref PubMed Scopus (74) Google Scholar,40Donovan M.K. Burkepile D.E. Kratochwill C. Shlesinger T. Sully S. Oliver T.A. Hodgson G. Freiwald J. van Woesik R. Local conditions magnify coral loss after marine heatwaves.Science. 2021; 372: 977-980Crossref PubMed Scopus (36) Google Scholar however, these effects have been difficult to assess, measure, and quantify.41Darling E.S. McClanahan T.R. Maina J. Gurney G.G. Graham N.A.J. Januchowski-Hartley F. Cinner J.E. Mora C. Hicks C.C. Maire E. et al.Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.Nat. Ecol. Evol. 2019; 3: 1341-1350Crossref PubMed Scopus (82) Google Scholar,42Precht W.F. Aronson R.B. Gardner T.A. Gill J.A. Hawkins J.P. Hernández-Delgado E.A. Jaap W.C. McClanahan T.R. McField M.D. Murdoch T.J.T. et al.Chapter Twelve - The timing and causality of ecological shifts on Caribbean reefs.in: Riegl B.M. Advances in Marine Biology Population Dynamics of the Reef Crisis. Academic Press, 2020: 331-360Crossref Scopus (7) Google Scholar What remains unknown are the aggregated implications of these regional trends for the global capacity of coral reefs to provide ecosystem services for the millions of people who rely on them.16Woodhead A.J. Graham N.A.J. Robinson J.P.W. Norström A.V. Bodin N. Marie S. Balett M.-C. Hicks C.C. Fishers perceptions of ecosystem service change associated with climate-disturbed coral reefs.People Nat. 2021; 3: 639-657Crossref Scopus (2) Google Scholar,2Cisneros-Montemayor A.M. Pauly D. Weatherdon L.V. Ota Y. A Global Estimate of Seafood Consumption by Coastal Indigenous Peoples.PLoS ONE. 2016; 11: e0166681Crossref PubMed Scopus (98) Google Scholar,26Wabnitz C.C.C. Cisneros-Montemayor A.M. Hanich Q. Ota Y. Ecotourism, climate change and reef fish consumption in Palau: Benefits, trade-offs and adaptation strategies.Mar. Policy. 2018; 88: 323-332Crossref Scopus (38) Google Scholar Here, we provide a global analysis of trends in living coral cover, associated fishery catches and effort, balance of fishing across the food web, coral-reef-associated biodiversity, and seafood consumption by coastal Indigenous peoples. We combined datasets from coral reef surveys, estimated coral-reef-associated biodiversity, fishery catches and effort, fishery impacts on food-web structure, and Indigenous consumption of coral-reef-associated fish. Our analysis indicates that the capacity of coral reefs to provide ecosystem services has declined by about half globally. This study speaks to the importance of how we manage coral reefs not only at regional scales but also at the global scale and the livelihoods of communities that rely on them. Overall, historical coral coverage was estimated to range from 58% to 70% in coral reef systems worldwide.8Eddy T.D. Cheung W.W.L. Bruno J.F. Historical baselines of coral cover on tropical reefs as estimated by expert opinion.PeerJ. 2018; 6: e4308Crossref PubMed Scopus (13) Google Scholar There has been approximately a 50% decline in coral reef cover globally from 1957–2007 (Figure 1A). There were only a few observations in the early part of the time series, which originated from the western Indian Ocean, indicating high uncertainty around what the average coral cover was during the mid-20th century. The effects of climate change worldwide started prior to this period, suggesting that the historical baseline could have been higher (Figures S1 and S2). The average decadal rate of loss in coral coverage during the study period ranged from 4.7% to 6.8% (Figure 1A). Most regions had relatively low sampling effort, except for countries in the western central Atlantic and the western central Pacific (Figure S1). Most countries showed declines in coral cover, although some countries in the Caribbean (Barbados, Cuba, Panama) and the western Pacific (Japan, Malaysia, Philippines, Thailand) showed increases based on available survey data (Figure 1B). Countries with the greatest coral-reef-associated biodiversity were typically found in the Pacific, although there was no clear separation among ocean basins (Figure 2A). We examined the species-area relationship43Drakare S. Lennon J.J. Hillebrand H. The imprint of the geographical, evolutionary and ecological context on species-area relationships.Ecol. Lett. 2006; 9: 215-227Crossref PubMed Scopus (404) Google Scholar for coral-reef-associated organisms by the main taxonomic groups (macroalgae, macroinvertebrates, and fish). Regression (log-log linear) between the estimated area of coral and total species richness among exclusive economic zones (EEZs) (n = 94) showed a positive relationship with a slope of 0.30 (p = 4.98e-07) and an intercept of 1.58 (p = 1.04e-08), with a Spearman coefficient of 0.63 (Figure 2B). Macroinvertebrates had a slope of 0.40, an intercept of 0.03 (p = 7.79e-06; p = 0.93, respectively), and a Spearman coefficient of 0.52. Fish had a slope of 0.30, an intercept of 0.70 (p = 2.88e-06; p = 0.01, respectively), and a Spearman coefficient of 0.52. Mammals had a slope of 0.09, an intercept of 0.95 (p = 0.01; p = 5.51e-09), and a Spearman coefficient of 0.28. We also subset EEZs that had a latitudinal centroid of coral reef area within the tropics and found that the species-area relationship increased for all groups, with a Spearman coefficient of 0.74. Global catches of coral-reef-associated fish steadily increased from 1950 until they peaked at approximately 2.3 million tons in 2002, representing 2.0% of global catches, after which they steadily declined and represented 2.5% of global catches in 2010 (Figures 3A, S3, and S4). Global fishing effort for coral-reef-associated species in EEZs with coral reefs increased from 1950–2010 (Figure S5), and the resulting catch-per-unit effort (CPUE) trend peaked in 1971, after which it decreased—an indication of declining coral reef fish abundance in many countries (Figure 3B). The fishing in balance (FIB) index increased through time and then leveled off, indicating increasingly unbalanced removal of higher trophic-level species (Figure 4). The countries with the highest per-capita Indigenous consumption of coral reef fish—Palau, Micronesia, and Kiribati (Figure 5)—are SIDSs. Other areas with high per-capita consumption include eastern Africa, southeast Asia, and the Bay of Bengal (Figure 5). In these and other areas, the protection and state of social-ecological systems that provide local seafood from coral reefs is particularly pertinent given broader national food-security issues. For example, Palau has established new national policies related to seafood production and tourist consumption specifically to prioritize consumption of reef fishes for local Palauans and their traditional fisheries.26Wabnitz C.C.C. Cisneros-Montemayor A.M. Hanich Q. Ota Y. Ecotourism, climate change and reef fish consumption in Palau: Benefits, trade-offs and adaptation strategies.Mar. Policy. 2018; 88: 323-332Crossref Scopus (38) Google ScholarFigure 4Global coral reef fisheries food-web impactShow full captionFIB index of coral-reef-associated fish in grid cells where coral reefs occur, weighted by EEZ area of coral reef habitat.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 5Consumption of coral-reef-associated fish by Indigenous communities by exclusive economic zoneShow full captionIndigenous consumption data from Cisneros-Montemayor;2Cisneros-Montemayor A.M. Pauly D. Weatherdon L.V. Ota Y. A Global Estimate of Seafood Consumption by Coastal Indigenous Peoples.PLoS ONE. 2016; 11: e0166681Crossref PubMed Scopus (98) Google Scholar coral reef fish catch data from Sea Around Us.44Pauly D. Zeller D. Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining.Nat. Commun. 2016; 7: 10244Crossref PubMed Scopus (639) Google ScholarView Large Image Figure ViewerDownload Hi-res image Download (PPT) FIB index of coral-reef-associated fish in grid cells where coral reefs occur, weighted by EEZ area of coral reef habitat. Indigenous consumption data from Cisneros-Montemayor;2Cisneros-Montemayor A.M. Pauly D. Weatherdon L.V. Ota Y. A Global Estimate of Seafood Consumption by Coastal Indigenous Peoples.PLoS ONE. 2016; 11: e0166681Crossref PubMed Scopus (98) Google Scholar coral reef fish catch data from Sea Around Us.44Pauly D. Zeller D. Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining.Nat. Commun. 2016; 7: 10244Crossref PubMed Scopus (639) Google Scholar Our study has aggregated regional trends of coral reefs to provide ecosystem services and demonstrated that the continuing decline of healthy coral reefs and the quality of habitat that they provide is contributing to a global decrease in provision of ecosystem services for the millions of people who rely on them. Particularly, our results highlight the erosion of biodiversity and food provision. The species-area relationship suggests a high sensitivity of species richness as a function of coral habitat. The estimated historical loss in coral habitat directly translates into loss in capacity of the remaining coral reefs to support biodiversity.11Worm B. Barbier E.B. Beaumont N. Duffy J.E. Folke C. Halpern B.S. Jackson J.B.C. Lotze H.K. Micheli F. Palumbi S.R. et al.Impacts of biodiversity loss on ocean ecosystem services.Science. 2006; 314: 787-790Crossref PubMed Scopus (2967) Google Scholar,43Drakare S. Lennon J.J. Hillebrand H. The imprint of the geographical, evolutionary and ecological context on species-area relationships.Ecol. Lett. 2006; 9: 215-227Crossref PubMed Scopus (404) Google Scholar The decline in global CPUE, an index of relative abundance of coral-reef-associated fisheries resources, suggests a loss in the production potential of many fish stocks that are important sources of food, culture, and livelihoods for coastal dependent communities. Other studies have suggested that for some coral reefs, the mean trophic level of the community (an indication of top predators in an ecosystem) can increase with fishing pressure, because exploited lower trophic-level herbivores get replaced by middle trophic-level species.45Graham N.A.J. McClanahan T.R. MacNeil M.A. Wilson S.K. Cinner J.E. Huchery C. Holmes T.H. Human Disruption of Coral Reef Trophic Structure.Curr. Biol. 2017; 27: 231-236Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar We did not report this result, which could be due to only using fishery catches and not surveying unexploited species that make up the wider coral reef community as reported in Graham et al.45Graham N.A.J. McClanahan T.R. MacNeil M.A. Wilson S.K. Cinner J.E. Huchery C. Holmes T.H. Human Disruption of Coral Reef Trophic Structure.Curr. Biol. 2017; 27: 231-236Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar Our results highlight the sensitivity of coral reef ecosystems, because of their biology, as well as the high dependence on them by human communities.23IPCC (2019). Special Report on the Ocean and Cryosphere in a Changing Climate, H.-O. Pörtner, D.C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, and N.M. Weyer, eds. (IPCC).Google Scholar,46IPBES (2019). Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, E.S. Brondizio, J. Settele, S. Díaz, and H.T. Ngo, eds. (IPBES).Google Scholar Our study has also highlighted important data gaps that exist for many nations—improved monitoring and reporting for healthy coral reef coverage, associated biodiversity abundance, fisheries’ catches and effort, and seafood consumption could reduce uncertainty in future coral reef ecosystem service analyses. Essential measures that are defined and agreed targets of the SDGs, such as reducing overexploitation through effective fisheries management47Mora C. Myers R.A. Coll M. Libralato S. Pitcher T.J. Sumaila R.U. Zeller D. Watson R. Gaston K.J. Worm B. Management effectiveness of the world’s marine fisheries.PLoS Biol. 2009; 7: e1000131Crossref PubMed Scopus (292) Google Scholar (SDG 14.4, 14.7), encouraging ecosyste