Tropical dead zones and mass mortalities on coral reefs
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Significance: Oxygen-starved coastal waters are rapidly increasing in prevalence worldwide. However, little is known about the impacts of these “dead zones” in tropical ecosystems or their potential threat to coral reefs. We document the deleterious effects of such an anoxic event on coral habitat and biodiversity, and show that the risk of dead-zone events to reefs worldwide likely has been seriously underestimated. Awareness of, and research on, reef hypoxia is needed to address the threat posed by dead zones to coral reefs.
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Land degradation is of great concern for oceans, manifested by the now more than 500 dead coastal marine zones where excessive nutrient runoff from agriculture has contributed to the collapse of coastal marine ecosystems.
“For instance, land degradation is of great concern for oceans, manifested by the now more than 500 dead coastal marine zones where excessive nutrient runoff from agriculture has contributed to the collapse of coastal marine ecosystems (5).”
From Restoring Degraded Lands (2021) · cites this paper as [5]
The passages labeled Abstract (page unavailable) link agricultural runoff and nutrient inputs to coastal hypoxia and report massive coral-reef mortality in a documented event. But the paper lists 494 coastal dead zones, not more than 500, and does not say that agricultural runoff caused the collapse of ecosystems in all of them. (LLM, conf=0.88)
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Spreading dead zones and consequences for marine ecosystems
Diaz, R. J., & Rosenberg, R. (2008) · Science · doi:10.1126/science.1156401 · Cited by 6,626 · see citing works
Coral Reefs Under Rapid Climate Change and Ocean Acidification
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., et al. (2007) · Science · doi:10.1126/science.1152509 · Cited by 5,885 · see citing works
Self-citationCoastal ocean acidification: The other eutrophication problem
Wallace, R. B., Baumann, H., Grear, J. S., Aller, R. C., & Gobler, C. J. (2014) · Estuarine, Coastal and Shelf Science · doi:10.1016/j.ecss.2014.05.027 · Cited by 607 · see citing works
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Research works printed but not linked: 68
- [2]Pandolfi JM, et al. Global trajectories of the long-term decline of coral reef ecosystems. Science. 2003;301(5635):955–958. doi: 10.1126/science.1085706. [DOI] [PubMed] [Google Scholar] · DOI
- [3]Bruno JF, et al. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 2007;5(6):e124. doi: 10.1371/journal.pbio.0050124. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [4]Mumby PJ, Steneck RS. Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol. 2008;23(10):555–563. doi: 10.1016/j.tree.2008.06.011. [DOI] [PubMed] [Google Scholar] · DOI
- [5]McCauley DJ, et al. Marine defaunation: Animal loss in the global ocean. Science. 2015;347(6219):1255641. doi: 10.1126/science.1255641. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
- [6]Jackson JBC, Donovan MK, Cramer KL, Lam W. Status and Trends of Caribbean Coral Reefs: 1970-2012. Global Coral Reef Monitoring Network. International Union for the Conservation of Nature; Gland, Switzerland: 2014. [Google Scholar]
- [8]Vaquer-Sunyer R, Duarte CM. Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci USA. 2008;105(40):15452–15457. doi: 10.1073/pnas.0803833105. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
- [9]Côté IM, Knowlton N. Coral reef ecosystems: A decade of discoveries. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ, editors. Marine Community Ecology and Conservation. Sinauer Associates; Sunderland, MA: 2013. pp. 299–314. [Google Scholar]
- [10]Jackson JBC, et al. Ecological effects of a major oil spill on Panamanian coastal marine communities. Science. 1989;243(4887):37–44. doi: 10.1126/science.243.4887.37. [DOI] [PubMed] [Google Scholar] · DOI
- [11]Cramer KL. History of human occupation and environmental change in western and central Caribbean Panama. Bull Mar Sci. 2013;89(4):955–982. [Google Scholar]
- [12]Guzmán HM, Barnes PAG, Lovelock CE, Feller IC. A site description of the CARICOMP mangrove, seagrass and coral reef sites in Bocas del Toro, Panama. Caribb J Sci. 2005;41(3):430–440. [Google Scholar]
- [13]Guzmán HM. Caribbean coral reefs of Panama: Present status and future perspectives. In: Cortés J, editor. Latin American Coral Reefs. Elsevier Science; Amsterdam: 2003. pp. 241–274. [Google Scholar]
- [14]Altieri AH. Dead zones enhance key fisheries species by providing predation refuge. Ecology. 2008;89(10):2808–2818. doi: 10.1890/07-0994.1. [DOI] [PubMed] [Google Scholar] · DOI
- [15]Diaz RJ, Rosenberg R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Annu Rev. 1995;33:245–303. [Google Scholar]
- [16]Collin R, D’Croz L, Gondola P, Del Rosario JB. Climate and hydrological factors affecting variation in chlorophyll concentration and water clarity in the Bahia Almirante, Panama. Smithson Contrib Mar Sci. 2009;38:323–334. [Google Scholar]
- [17]Neal BP, et al. When depth is no refuge: Cumulative thermal stress increases with depth in Bocas del Toro, Panama. Coral Reefs. 2014;33(1):193–205. [Google Scholar]
- [18]Levitan DR, Boudreau W, Jara J, Knowlton N. Long-term reduced spawning in Orbicella coral species due to temperature stress. Mar Ecol Prog Ser. 2014;515:1–10. [Google Scholar]
- [19]Vaquer-Sunyer R, Duarte CM. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob Change Biol. 2011;17(5):1788–1797. [Google Scholar]
- [21]Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA. 2008;105(45):17442–17446. doi: 10.1073/pnas.0804478105. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
- [22]Stubler AD, Furman BT, Peterson BJ. Sponge erosion under acidification and warming scenarios: Differential impacts on living and dead coral. Glob Change Biol. 2015;21(11):4006–4020. doi: 10.1111/gcb.13002. [DOI] [PubMed] [Google Scholar] · DOI
- [23]Duarte CM, et al. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries Coasts. 2013;36(2):221–236. [Google Scholar]
- [24]Altieri AH, Gedan KB. Climate change and dead zones. Glob Change Biol. 2015;21(4):1395–1406. doi: 10.1111/gcb.12754. [DOI] [PubMed] [Google Scholar] · DOI
- [25]Fabricius KE. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar Pollut Bull. 2005;50(2):125–146. doi: 10.1016/j.marpolbul.2004.11.028. [DOI] [PubMed] [Google Scholar] · DOI
- [26]Pandolfi JM, et al. Ecology. Are U.S. coral reefs on the slippery slope to slime? Science. 2005;307(5716):1725–1726. doi: 10.1126/science.1104258. [DOI] [PubMed] [Google Scholar] · DOI
- [27]Burke L, Reytar K, Spalding M, Perry A. Reefs at Risk Revisited. World Resources Institute; Washington, DC: 2011. p. 130. [Google Scholar]
- [28]Sandin SA, et al. Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One. 2008;3(2):e1548. doi: 10.1371/journal.pone.0001548. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [29]Knowlton N, Jackson JBC. Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol. 2008;6(2):e54. doi: 10.1371/journal.pbio.0060054. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [30]Aronson RB, MacIntyre IG, Wapnick CM, O’Neill MW. Phase shifts, alternative states, and the unprecedented convergence of two reef systems. Ecology. 2004;85(7):1876–1891. [Google Scholar]
- [31]Cramer KL, Jackson JBC, Angioletti CV, Leonard-Pingel J, Guilderson TP. Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching. Ecol Lett. 2012;15(6):561–567. doi: 10.1111/j.1461-0248.2012.01768.x. [DOI] [PubMed] [Google Scholar] · DOI
- [32]Aronson RB, Hilbun NL, Bianchi TS, Filley TR, McKee BA. Land use, water quality, and the history of coral assemblages at Bocas del Toro, Panama. Mar Ecol Prog Ser. 2014;504:159–170. [Google Scholar]
- [33]Nelson HR, Kuempel CD, Altieri AH. The resilience of reef invertebrate biodiversity to coral mortality. Ecosphere. 2016;7(7):e1399. [Google Scholar]
- [34]Kuempel CD, Altieri AH. The emergent role of small-bodied herbivores in pre-empting phase shifts on degraded coral reefs. Sci Rep. 2017;7:39670. doi: 10.1038/srep39670. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [35]Diaz RJ, Selman M, Chique C. Global Eutrophic and Hypoxic Coastal Systems. World Resources Institute; Washington, DC: 2011. [Google Scholar]
- [36]Hodgson G, Maun L, Shuman C. Reef Check Survey Manual. Reef Check. Institute of the Environment, University of California; Los Angeles, CA: 2004. [Google Scholar]
- [37]Diaz RJ. Overview of hypoxia around the world. J Environ Qual. 2001;30(2):275–281. doi: 10.2134/jeq2001.302275x. [DOI] [PubMed] [Google Scholar] · DOI
- [38]Levin LA, et al. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences. 2009;6(10):2063–2098. [Google Scholar]
- [39]Rabalais NN, et al. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences. 2010;7(2):585–619. [Google Scholar]
- [40]Laboy-Nieves EN, et al. Mass mortality of tropical marine communities in Morrocoy, Venezuela. Bull Mar Sci. 2001;68(2):163–179. [Google Scholar]
- [41]Simpson CJ, Cary JL, Masini RJ. Destruction of corals and other reef animals by coral spawn slicks on Ningaloo Reef, Western Australia. Coral Reefs. 1993;12(3-4):185–191. [Google Scholar]
- [42]Hobbs J-PA, McDonald CA. Increased seawater temperature and decreased dissolved oxygen triggers fish kill at the Cocos (Keeling) Islands, Indian Ocean. J Fish Biol. 2010;77(6):1219–1229. doi: 10.1111/j.1095-8649.2010.02726.x. [DOI] [PubMed] [Google Scholar] · DOI
- [43]Hobbs J-PA, Macrae H. Unusual weather and trapped coral spawn lead to fish kill at a remote coral atoll. Coral Reefs. 2012;31(4):961. [Google Scholar]
- [44]Andréfouët S, Dutheil C, Menkes CE, Bador M, Lengaigne M. Mass mortality events in atoll lagoons: Environmental control and increased future vulnerability. Glob Change Biol. 2015;21(1):195–205. doi: 10.1111/gcb.12699. [DOI] [PubMed] [Google Scholar] · DOI
- [45]Guzman HM, Cortes J, Glynn PW, Richmond RH. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama) Mar Ecol Prog Ser. 1990;60(3):299–303. [Google Scholar]
- [46]Jokiel PL, Hunter CL, Taguchi S, Watarai L. Ecological impact of a fresh-water reef kill in Kaneohe Bay, Oahu, Hawaii. Coral Reefs. 1993;12(3-4):177–184. [Google Scholar]
- [47]Lapointe BE, Matzie WR. Effects of stormwater nutrient discharges on eutrophication processes in nearshore waters of the Florida Keys. Estuaries. 1996;19(2B):422–435. [Google Scholar]
- [48]Roberts KL, Eate VM, Eyre BD, Holland DP, Cook PLM. Hypoxic events stimulate nitrogen recycling in a shallow salt-wedge estuary: The Yarra River estuary, Australia. Limnol Oceanogr. 2012;57(5):1427–1442. [Google Scholar]
- [49]Conley DJ, et al. Hypoxia is increasing in the coastal zone of the Baltic Sea. Environ Sci Technol. 2011;45(16):6777–6783. doi: 10.1021/es201212r. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
- [50]Chantraine J-M. La Lagune Abe (Cote D'Ivoire) morphologie, hydrologie, parametres physico-chimiques. Documents Scientifique de Centre de recherches oceanographiques Abidjan. 1980;11:39–77. [Google Scholar]
- [51]Seisdedo Losa M. Variaciones espaciales y temporales en indicadores de la calidad ambiental de las aguas de la Bahia de Cienfuegos, Cuba. Rev Investig Mar. 2006;27(2):159–164. [Google Scholar]
- [52]Lanoux A, et al. Factors contributing to hypoxia in a highly turbid, macrotidal estuary (the Gironde, France) Environ Sci Process Impacts. 2013;15(3):585–595. doi: 10.1039/c2em30874f. [DOI] [PubMed] [Google Scholar] · DOI
- [53]Gianni A, Kehayias G, Zacharias I. Geomorphology modification and its impact to anoxic lagoons. Ecol Eng. 2011;37(11):1869–1877. [Google Scholar]
- [54]Ferentinos G, et al. Fjord water circulation patterns and dysoxic/anoxic conditions in a Mediterranean semi-enclosed embayment in the Amvrakikos Gulf, Greece. Estuar Coast Shelf Sci. 2010;88(4):473–481. [Google Scholar]
- [55]Shanmugam P, Neelamani S, Ahn YH, Philip L, Hong GH. Assessment of the levels of coastal marine pollution of Chennai city, Southern India. Water Resour Manage. 2007;21(7):1187–1206. [Google Scholar]
- [56]Vijay R, Sardar VK, Dhage SS, Kelkar PS, Gupta A. Hydrodynamic assessment of sewage impact on water quality of Malad Creek, Mumbai, India. Environ Monit Assess. 2010;165(1-4):559–571. doi: 10.1007/s10661-009-0967-9. [DOI] [PubMed] [Google Scholar] · DOI
- [57]Deshkar S, Lakhmapurkar J, Gavali D. State of three estuaries of Gulf of Khambhat. Indian J Mar Sci. 2012;41(1):70–75. [Google Scholar]
- [58]Rixen T, et al. The Siak, a tropical black water river in central Sumatra on the verge of anoxia. Biogeochemistry. 2008;90(2):129–140. [Google Scholar]
- [59]Henry LM, Kennedy R, Keegan BF. An investigation of periodic hypoxia at Ardbear Salt Lake. J Mar Biol Assoc U K. 2008;88(7):1297–1307. [Google Scholar]
- [60]Haraguchi K, Yamamoto T, Chiba S, Shimizu Y, Nagao M. Effects of phytoplankton vertical migration on the formation of oxygen depleted water in a shallow coastal sea. Estuar Coast Shelf Sci. 2010;86(3):441–449. [Google Scholar]
- [61]Ichikawa T, Aizaki M, Takeshita M. Numerical study on amelioration of water quality in Lakes Shinji and Nakaumi: A coastal brackish lagoon system. Limnology. 2007;8(3):281–294. [Google Scholar]
- [62]Okada T, Nakayama K. Density intrusion and variation in dissolved oxygen concentrations in a bay with a sill at its mouth. J Environ Eng. 2007;133(4):447–453. [Google Scholar]
- [63]Jang PG, Shin K, Chang M, Kim D. Spatial and temporal trends in water quality in response to sewage discharge in Masan and Hangam Bays, Korea. J Coast Res. 2011;27(6A):144–155. [Google Scholar]
- [64]Bouchet VMP, Alve E, Rygg B, Telford RJ. Benthic foraminifera provide a promising tool for ecological quality assessment of marine waters. Ecol Indic. 2012;23:66–75. [Google Scholar]
- [65]San Diego-McGlone ML, Azanza RV, Villanoy CL, Jacinto GS. Eutrophic waters, algal bloom and fish kill in fish farming areas in Bolinao, Pangasinan, Philippines. Mar Pollut Bull. 2008;57(6-12):295–301. doi: 10.1016/j.marpolbul.2008.03.028. [DOI] [PubMed] [Google Scholar] · DOI
- [66]Mikhailik TA, Tishchenko PY, Koltunov AM, Tishchenko PP, Shvetsova MG. The effect of Razdol’naya River on the environmental state of Amur Bay (The Sea of Japan) Water Resour. 2011;38(4):512–521. [Google Scholar]
- [67]Kaselowski T, Adams JB. Not so pristine - characterising the physico-chemical conditions of an undescribed temporarily open/closed estuary. Water SA. 2013;39(5):627–635. [Google Scholar]
- [68]Canedo-Arguelles M, Rieradevall M, Farres-Corell R, Newton A. Annual characterisation of four Mediterranean coastal lagoons subjected to intense human activity. Estuar Coast Shelf Sci. 2012;114:59–69. [Google Scholar]
- [69]Hsieh WC, et al. Community metabolism in a tropical lagoon: Carbon cycling and autotrophic ecosystem induced by a natural nutrient pulse. Environ Eng Sci. 2012;29(8):776–782. [Google Scholar]
- [70]Weston K, et al. Sedimentary and water column processes in the Oyster Grounds: A potentially hypoxic region of the North Sea. Mar Environ Res. 2008;65(3):235–249. doi: 10.1016/j.marenvres.2007.11.002. [DOI] [PubMed] [Google Scholar] · DOI
- [71]Tyler RM, Brady DC, Targett TE. Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries Coasts. 2009;32(1):123–145. [Google Scholar]
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- Authors
- Altieri, A. H., Harrison, S. B., Seemann, J., Collin, R., Diaz, R. J., & Knowlton, N.
- Affiliations
- Smithsonian Tropical Research Institute (PA)
- Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062;
- Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2017-03-20
- Volume
- 114
- Issue
- 14
- Pages
- 3660-3665
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5389270
- OpenAlex
- W2597848358
- Cited by
- 338
- References
- 3
- Citations by year
- 2026: 21 · 2025: 37 · 2024: 41 · 2023: 66 · 2022: 38 · 2021: 43 · 2020: 37 · 2019: 23 · 2018: 26 · 2017: 5
- FWCI
- 18.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- W&M Publish (College of William & Mary) (submittedVersion, cc-by)
- Topics
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Ocean Acidification Effects and Responses
- Keywords
- hypoxia, coral reefs, coral bleaching, mass mortality, eutrophication, risk assessment, coral reef resilience, coastal water quality
- MeSH terms
- Animals, Conservation of Natural Resources, Oxygen, Panama, Population Dynamics, Tropical Climate, Anthozoa, Biodiversity, Coral Reefs, Water Quality
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