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Mass mortality of diadematoid sea urchins in the Red Sea and Western Indian Ocean

海洋学 印度洋 渔业 太平洋 地理 环境科学 生物 地质学
作者
Lachan Roth,Gal Eviatar,Lisa-Maria Schmidt,Marco Bonomo,Tamar Feldstein‐Farkash,Patrick Schubert,Maren Ziegler,Ali Al‐Sawalmih,Ibrahim Souleiman Abdallah,Jean‐Pascal Quod,Omri Bronstein
出处
期刊:Current Biology [Elsevier]
卷期号:34 (12): 2693-2701.e4 被引量:3
标识
DOI:10.1016/j.cub.2024.04.057
摘要

Sea urchins are primary herbivores on coral reefs, regulating algal biomass and facilitating coral settlement and growth. 1 McCook L. Jompa J. Diaz-Pulido G. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs. 2001; 19: 400-417https://doi.org/10.1007/s003380000129 Crossref Scopus (752) Google Scholar ,2 Klumpp D.W. Salita-Espinosa J.T. Fortes M.D. Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquat. Bot. 1993; 45: 205-229https://doi.org/10.1016/0304-3770(93)90022-O Crossref Scopus (103) Google Scholar ,3 Lawrence J.M. On the relationship between marine plants and sea urchins. Ocean. Mar. Biol. Ann. Rev. 1975; 13: 213-286 Google Scholar ,4 Benayahu Y. Seasonal occurrence of benthic-algae communities and grazing regulation by sea urchins at the coral reefs of Eilat, Red Sea. Int. Coral Reef Symp. 1977; 3: 383-389 Google Scholar ,5 Carpenter R.C. Edmunds P.J. Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol. Lett. 2006; 9: 271-280https://doi.org/10.1111/j.1461-0248.2005.00866.x Crossref PubMed Scopus (182) Google Scholar ,6 Birkeland C. Randall R.H. Facilitation of coral recruitment by echinoid excavations. in: Proc. 4th Int. Coral Reef Symp. 1981: 695-698 Google Scholar ,7 Sandin S.A. McNamara D.E. Spatial dynamics of benthic competition on coral reefs. Oecologia. 2012; 168: 1079-1090https://doi.org/10.1007/s00442-011-2156-0 Crossref PubMed Scopus (75) Google Scholar ,8 Lawrence J.M. Lawrence J.M. Sea urchins: biology and ecology. Academic press, 2013 Google Scholar ,9 Sammarco P.W. Echinoid grazing as a structuring force in coral communities: Whole reef manipulations. J. Exp. Mar. Biol. Ecol. 1982; 61: 31-55https://doi.org/10.1016/0022-0981(82)90020-X Crossref Scopus (196) Google Scholar ,10 Carpenter R.C. Sea urchin mass-mortality: effects on reef algal abundance, species composition, and metabolism and other coral reef herbivores. in: Proc. 5th Int. Coral Reef Symp.1985: 53-60 Google Scholar ,11 Van Steveninck E. de R. Breeman A.M. Deep water vegetations of Lobophora variegata (Phaeophyceae) in the coral reef of Curacao—population dynamics in relation to mass mortality of the sea urchin Diadema antillarum. Mar. Ecol. Prog. Ser. 1987; 36: 81-90 Crossref Google Scholar ,12 Hutchings P.A. Biological destruction of coral reefs. Coral Reefs. 1986; 4: 239-252https://doi.org/10.1007/BF00298083 Crossref Scopus (346) Google Scholar Recurring mass mortality events (MMEs) of Diadema species Gray, 1825 have been recorded globally, 13 Levitan D.R. Best R.M. Edmunds P.J. Sea urchin mass mortalities 40 y apart further threaten Caribbean coral reefs. Proc. Natl. Acad. Sci. 2023; 120e2218901120https://doi.org/10.1073/pnas.2218901120 Crossref Scopus (8) Google Scholar ,14 Lessios H.A. Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar. Biol. 1988; 99: 515-526https://doi.org/10.1007/BF00392559 Crossref Scopus (71) Google Scholar ,15 Hylkema A. Kitson-Walters K. Kramer P.R. Patterson J.T. Roth L. Sevier M.L.B. Vega-Rodriguez M. Warham M.M. Williams S.M. Lang J.C. The 2022 Diadema antillarum die-off event: Comparisons with the 1983-1984 mass mortality. Front. Mar. Sci. 2023; 91067449https://doi.org/10.3389/fmars.2022.1067449 Crossref Scopus (12) Google Scholar ,16 Girard D. Clemente S. Toledo-Guedes K. Brito A. Hernández J.C. A mass mortality of subtropical intertidal populations of the sea urchin Paracentrotus lividus: analysis of potential links with environmental conditions. Mar. Ecol. 2012; 33: 377-385https://doi.org/10.1111/j.1439-0485.2011.00491.x Crossref Scopus (46) Google Scholar ,17 Lessios H. Mass mortality of Diadema antillarum in the Caribbean: what have we learned?. Annu. Rev. Ecol. Syst. 1988; 19: 371-393 Crossref Google Scholar ,18 Hewson I. Ritchie I.T. Evans J.S. Altera A. Behringer D. Bowman E. Brandt M. Budd K.A. Camacho R.A. Cornwell T.O. et al. A scuticociliate causes mass mortality of Diadema antillarum in the Caribbean Sea. Sci. Adv. 2023; 9eadg3200https://doi.org/10.1126/sciadv.adg3200 Crossref PubMed Scopus (10) Google Scholar ,19 Lessios H.A. Cubit J.D. Robertson D.R. Shulman M.J. Parker M.R. Garrity S.D. Levings S.C. Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs. 1984; 3: 173-182https://doi.org/10.1007/BF00288252 Crossref Scopus (123) Google Scholar ,20 Lessios H.A. Robertson D.R. Cubit J.D. Spread of Diadema mass mortality through the Caribbean. Science. 1984; 226: 335-337https://doi.org/10.1126/science.226.4672.335 Crossref PubMed Scopus (441) Google Scholar ,21 Hernández J.C. Clemente S. Sea urchins, natural events and benthic ecosystems functioning in the Canary Islands. in: Fernández-Palacios J.M. de Nascimento L. Hernández J.C. Clemente S. González A. Díaz-González J.P. Climate change perspectives from the Atlantic: past, present and future. Servicio de Publicaciones de la Universidad de La Laguna, Tenerife. 2013: 487-512 Google Scholar ,22 Clemente S. Lorenzo-Morales J. Mendoza J. López C. Sangil C. Alves F. Kaufmann M. Hernández J.C. Sea urchin Diadema africanum mass mortality in the subtropical eastern Atlantic: role of waterborne bacteria in a warming ocean. Mar. Ecol. Prog. Ser. 2014; 506: 1-14https://doi.org/10.3354/meps10829 Crossref Scopus (49) Google Scholar ,23 Zirler R. Schmidt L.M. Roth L. Corsini-Foka M. Kalaentzis K. Kondylatos G. Mavrouleas D. Bardanis E. Bronstein O. Mass mortality of the invasive alien echinoid Diadema setosum (Echinoidea: Diadematidae) in the Mediterranean Sea. R. Soc. Open Sci. 2023; 10230251https://doi.org/10.1098/rsos.230251 Crossref PubMed Scopus (2) Google Scholar the most notorious and ecologically significant of which occurred in the Caribbean in 1983, 14 Lessios H.A. Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar. Biol. 1988; 99: 515-526https://doi.org/10.1007/BF00392559 Crossref Scopus (71) Google Scholar ,17 Lessios H. Mass mortality of Diadema antillarum in the Caribbean: what have we learned?. Annu. Rev. Ecol. Syst. 1988; 19: 371-393 Crossref Google Scholar ,19 Lessios H.A. Cubit J.D. Robertson D.R. Shulman M.J. Parker M.R. Garrity S.D. Levings S.C. Mass mortality of Diadema antillarum on the Caribbean coast of Panama. Coral Reefs. 1984; 3: 173-182https://doi.org/10.1007/BF00288252 Crossref Scopus (123) Google Scholar ,20 Lessios H.A. Robertson D.R. Cubit J.D. Spread of Diadema mass mortality through the Caribbean. Science. 1984; 226: 335-337https://doi.org/10.1126/science.226.4672.335 Crossref PubMed Scopus (441) Google Scholar contributing to the shift from coral to algal-dominated ecosystems. 17 Lessios H. Mass mortality of Diadema antillarum in the Caribbean: what have we learned?. Annu. Rev. Ecol. Syst. 1988; 19: 371-393 Crossref Google Scholar ,24 Lawrence J.M. Mass mortality of echinoderms from abiotic factors. in: Jangoux M. Lawrence J.M. Echinoderm studies. CRC Press, 1996: 103-137 Google Scholar ,25 Hughes T.P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science. 1994; 265: 1547-1551https://doi.org/10.1126/science.265.5178.1547 Crossref PubMed Scopus (2316) Google Scholar Recently, first evidence of Diadema setosum mass mortality was reported from the eastern Mediterranean Sea. 23 Zirler R. Schmidt L.M. Roth L. Corsini-Foka M. Kalaentzis K. Kondylatos G. Mavrouleas D. Bardanis E. Bronstein O. Mass mortality of the invasive alien echinoid Diadema setosum (Echinoidea: Diadematidae) in the Mediterranean Sea. R. Soc. Open Sci. 2023; 10230251https://doi.org/10.1098/rsos.230251 Crossref PubMed Scopus (2) Google Scholar Here, we report extensive mass mortalities of several diadematoid species inhabiting the Red Sea and Western Indian Ocean (WIO) 26 Fishelson L. Ecology and distribution of the benthic fauna in the shallow waters of the Red Sea. Mar. Biol. 1971; 10: 113-133https://doi.org/10.1007/BF00354828 Crossref Scopus (137) Google Scholar ,27 Bronstein O. Loya Y. Echinoid community structure and rates of herbivory and bioerosion on exposed and sheltered reefs. J. Exp. Mar. Biol. Ecol. 2014; 456: 8-17https://doi.org/10.1016/j.jembe.2014.03.003 Crossref Scopus (36) Google Scholar ,28 Muthiga N.A. McClanahan T.R. Diadema. in: Lawrence J.M. Sea urchins: biology and ecology. Academic Press, 2020: 397-418 Crossref Scopus (10) Google Scholar including first evidence of mortalities in the genus Echinothrix Peters, 1853. Mortalities initiated in the Gulf of Aqaba on December 2022 and span the Red Sea, the Gulf of Oman, and the Western Indian Ocean (Réunion Island), with population declines reaching 100% at some sites. Infected individuals are characterized by spine loss and tissue necrosis, resulting in exposed skeletons (i.e., tests) and mortality. Molecular diagnostics of the 18S rRNA gene confirm the presence of a waterborne scuticociliate protozoan most closely related to Philaster apodigitiformis in infected specimens—identical to the pathogen found in the 2022 Caribbean mass mortality of Diadema antillarum. 13 Levitan D.R. Best R.M. Edmunds P.J. Sea urchin mass mortalities 40 y apart further threaten Caribbean coral reefs. Proc. Natl. Acad. Sci. 2023; 120e2218901120https://doi.org/10.1073/pnas.2218901120 Crossref Scopus (8) Google Scholar ,15 Hylkema A. Kitson-Walters K. Kramer P.R. Patterson J.T. Roth L. Sevier M.L.B. Vega-Rodriguez M. Warham M.M. Williams S.M. Lang J.C. The 2022 Diadema antillarum die-off event: Comparisons with the 1983-1984 mass mortality. Front. Mar. Sci. 2023; 91067449https://doi.org/10.3389/fmars.2022.1067449 Crossref Scopus (12) Google Scholar ,18 Hewson I. Ritchie I.T. Evans J.S. Altera A. Behringer D. Bowman E. Brandt M. Budd K.A. Camacho R.A. Cornwell T.O. et al. A scuticociliate causes mass mortality of Diadema antillarum in the Caribbean Sea. Sci. Adv. 2023; 9eadg3200https://doi.org/10.1126/sciadv.adg3200 Crossref PubMed Scopus (10) Google Scholar Collapse of these key benthic grazers in the Red Sea and Western Indian Ocean may lead to algal dominance over corals, threatening the stability of coral reefs on a regional scale. 29 Hughes T.P. Baird A.H. Bellwood D.R. Card M. Connolly S.R. Folke C. Grosberg R. Hoegh-Guldberg O. Jackson J.B.C. Kleypas J. et al. Climate change, human impacts, and the resilience of coral reefs. Science. 2003; 301: 929-933https://doi.org/10.1126/science.1085046 Crossref PubMed Scopus (2916) Google Scholar ,30 Spalding M.D. Brown B.E. Warm-water coral reefs and climate change. Science. 2015; 350: 769-771https://doi.org/10.1126/science.aad0349 Crossref PubMed Scopus (184) Google Scholar ,31 Knowlton N. The future of coral reefs. Proc. Natl. Acad. Sci. 2001; 98: 5419-5425https://doi.org/10.1073/pnas.091092998 Crossref PubMed Scopus (443) Google Scholar ,32 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. Coral reefs under rapid climate change and ocean acidification. Science. 2007; 318: 1737-1742https://doi.org/10.1126/science.1152509 Crossref PubMed Scopus (4222) Google Scholar We issue a warning regarding the further expansion of mortalities and call for immediate monitoring and conservation efforts for these key ecological species.
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