A scuticociliate causes mass mortality of Diadema antillarum in the Caribbean Sea

Author:

Hewson Ian1ORCID,Ritchie Isabella T.2ORCID,Evans James S.3ORCID,Altera Ashley1ORCID,Behringer Donald45ORCID,Bowman Erin67ORCID,Brandt Marilyn8ORCID,Budd Kayla A.8ORCID,Camacho Ruleo A.9ORCID,Cornwell Tomas O.10ORCID,Countway Peter D.11ORCID,Croquer Aldo12,Delgado Gabriel A.13ORCID,DeRito Christopher1ORCID,Duermit-Moreau Elizabeth4ORCID,Francis-Floyd Ruth414,Gittens Samuel8ORCID,Henderson Leslie15ORCID,Hylkema Alwin1617ORCID,Kellogg Christina A.3ORCID,Kiryu Yasunari18,Kitson-Walters Kimani A.1920ORCID,Kramer Patricia21ORCID,Lang Judith C.21,Lessios Harilaos22ORCID,Liddy Lauren23,Marancik David24,Nimrod Stephen25ORCID,Patterson Joshua T.4ORCID,Pistor Marit10,Romero Isabel C.2ORCID,Sellares-Blasco Rita26ORCID,Sevier Moriah L. B.8ORCID,Sharp William C.13ORCID,Souza Matthew8ORCID,Valdez-Trinidad Andreina26ORCID,van der Laan Marijn27ORCID,Vilanova-Cuevas Brayan1ORCID,Villalpando Maria26ORCID,Von Hoene Sarah D.8ORCID,Warham Matthew6ORCID,Wijers Tom1617ORCID,Williams Stacey M.28ORCID,Work Thierry M.29,Yanong Roy P.4ORCID,Zambrano Someira30ORCID,Zimmermann Alizee31ORCID,Breitbart Mya2ORCID

Affiliation:

1. Department of Microbiology, Cornell University, Ithaca, NY, USA.

2. College of Marine Science, University of South Florida, St. Petersburg, FL, USA.

3. U.S. Geological Survey, St. Petersburg Coastal and Marine Science Center, St. Petersburg, FL, USA.

4. School of Forest, Fisheries, and Geomatics Sciences, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, USA.

5. Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA.

6. Department of Planning and Natural Resources, Virgin Islands Government, Christiansted, VI, USA.

7. National Coral Reef Management Fellowship, Nova Southeastern University, Fort Lauderdale, FL, USA.

8. Center for Marine and Environmental Studies, University of the Virgin Islands, Saint Thomas, VI, USA.

9. Antigua and Barbuda National Parks Authority, Nelson’s Dockyard, Antigua and Barbuda.

10. St Eustatius National Parks Foundation, Oranjestad, Caribbean, Netherlands.

11. Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA.

12. Central Caribbean Program, The Nature Conservancy, Santo Domingo, Dominican Republic.

13. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Marathon, FL, USA.

14. College of Veterinary Medicine, University of Florida, Gainesville, FL, USA.

15. National Oceanic and Atmospheric Administration Office for Coastal Management, Silver Spring, MD, USA.

16. Van Hall Larenstein University of Applied Sciences, Leeuwarden, Netherlands.

17. Marine Animal Ecology Group, Wageningen University, Wageningen, Netherlands.

18. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, St. Petersburg, FL, USA.

19. Caribbean Netherlands Science Institute, St. Eustatius, Caribbean, Netherlands.

20. NIOZ Royal Netherlands Institute for Sea Research, Oranjestad, Caribbean, Netherlands.

21. Ocean Research and Education Foundation, Atlantic and Gulf Rapid Reef Assessment, Big Pine Key, FL, USA.

22. Smithsonian Tropical Research Institute, Panama City, Republic of Panama.

23. Montclair State University, Montclair, NJ, USA.

24. School of Veterinary Sciences, St. George’s University, St. George’s, Grenada.

25. Department of Biology, Ecology and Conservation, St. George’s University, St. George’s, Grenada.

26. Fundación Dominicana de Estudios Marinos, Bayahibe, Dominican Republic.

27. Saba Conservation Foundation, Saba, Caribbean, Netherlands.

28. Institute for Socio-Ecological Research, Lajas, Puerto Rico.

29. U.S. Geological Survey, National Wildlife Health Center, Honolulu Field Station, Honolulu, HI, USA.

30. Red Arrecifal Dominicana, Santo Domingo, Dominican Republic.

31. Turks and Caicos Reef Fund, Providenciales, Turks and Caicos Islands.

Abstract

Echinoderm mass mortality events shape marine ecosystems by altering the dynamics among major benthic groups. The sea urchin Diadema antillarum , virtually extirpated in the Caribbean in the early 1980s by an unknown cause, recently experienced another mass mortality beginning in January 2022. We investigated the cause of this mass mortality event through combined molecular biological and veterinary pathologic approaches comparing grossly normal and abnormal animals collected from 23 sites, representing locations that were either affected or unaffected at the time of sampling. Here, we report that a scuticociliate most similar to Philaster apodigitiformis was consistently associated with abnormal urchins at affected sites but was absent from unaffected sites. Experimentally challenging naïve urchins with a Philaster culture isolated from an abnormal, field-collected specimen resulted in gross signs consistent with those of the mortality event. The same ciliate was recovered from treated specimens postmortem, thus fulfilling Koch’s postulates for this microorganism. We term this condition D. antillarum scuticociliatosis.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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