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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Vet. Sci. | doi: 10.3389/fvets.2019.00372

Caryospora-like coccidia infecting green turtles (Chelonia mydas): an emerging disease with evidence of interoceanic dissemination

 Brian A. Stacy1*,  Phoebe A. Chapman2,  Heather Stockdale-Walden3,  Thierry M. Work4, Julie Dagenais4, Allen M. Foley5, Morgan Wideroff5,  James F. Wellehan6, April L. Childress6, Charles A. Manire7, Maya Rodriguez8, Trevor T. Zachariah9, Lydia Staggs10, Bette Zirkelbach11, Nina Nahvi12, Whitney Crowder13, Shane M. Boylan14, Shelly Marquardt15,  Craig Pelton16 and  Terry M. Norton11, 17
  • 1National Marine Fisheries Service (NOAA), United States
  • 2Veterinary Marine Animal Research Teaching and Investigation Unit, School of Veterinary Science, University of Queensland, Australia
  • 3Department of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, United States
  • 4National Wildlife Health Center, United States Geological Survey, United States
  • 5Florida Fish and Wildlife Conservation Commission, United States
  • 6Department of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, United States
  • 7Loggerhead Marinelife Center, United States
  • 8Independent researcher, United States
  • 9Sea Turtle Healing Center, United States
  • 10Independent researcher, United States
  • 11The Turtle Hospital, United States
  • 12Independent researcher, United States
  • 13Independent researcher, United States
  • 14Independent researcher, United States
  • 15Independent researcher, United States
  • 16Marine Science Center, United States
  • 17Independent researcher, United States

Protozoa morphologically consistent with Caryospora sp. are one of the few pathogens associated with episodic mass mortality events involving free-ranging sea turtles. Parasitism of green turtles (Chelonia mydas) by these coccidia and associated mortality was first reported in maricultured turtles in the Caribbean during the 1970s. Years later, epizootics affecting wild green turtles in Australia occurred in 1991 and 2014. The first clinical cases of Caryospora-like infections reported elsewhere in free-ranging turtles were from the southeastern US in 2012. Following these initial individual cases in this region, we documented an epizootic and mass mortality of green turtles along the Atlantic coast of southern Florida from November 2014 through April 2015 and continued to detect additional, sporadic cases in the southeastern US in subsequent years. No cases of coccidial disease were recorded in the southeastern US prior to 2012 despite clinical evaluation and necropsy of stranded sea turtles in this region since the 1980s, suggesting that the frequency of clinical coccidiosis has increased here. Moreover, we also recorded the first stranding associated with infection by a Caryospora-like organism in Hawai’i in 2018. To further characterize the coccidia, we sequenced part of the 18S ribosomal and mitochondrial cytochrome oxidase I genes of coccidia collected from 62 green turtles found in the southeastern US and from 1 green turtle found in Hawai’i. We also sequenced the ribosomal internal transcribed spacer regions from selected cases and compared all results with those obtained from Caryospora-like coccidia collected from green turtles found in Australia. Eight distinct genotypes were represented in green turtles from the southeastern US. One genotype predominated and was identical to that of coccidia collected from the green turtle found in Hawai’i. We also found a coccidian genotype in green turtles from Florida and Australia with identical 18S and mitochondrial sequences, and only slight inter-regional differences in the internal transcribed spacer 2. We found no evidence of geographical structuring based on phylogenetic analysis. Low genetic variability among the coccidia found in green turtle populations with minimal natural connectivity suggests recent interoceanic dissemination of these parasites, which could pose a risk to sea turtle populations.

Keywords: Caryospora, Eimeriidae, Mortality, Stranding, pathogen pollution, Sea Turtle

Received: 08 Aug 2019; Accepted: 08 Oct 2019.

Copyright: © 2019 Stacy, Chapman, Stockdale-Walden, Work, Dagenais, Foley, Wideroff, Wellehan, Childress, Manire, Rodriguez, Zachariah, Staggs, Zirkelbach, Nahvi, Crowder, Boylan, Marquardt, Pelton and Norton. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Brian A. Stacy, National Marine Fisheries Service (NOAA), Silver Spring, United States, Brian.Stacy@noaa.gov