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Vermetid gastropods as key intermediate hosts for a lineage of marine turtle blood flukes (Digenea: Spirorchiidae), with evidence of transmission at a turtle rookery
Affiliation:1. School of Science, STEM College, RMIT University, Bundoora, VIC 3083, Australia;2. Institute for Glycomics, Griffith University, Southport, QLD 4215, Australia;3. Institute for Marine and Antarctic Studies, University of Tasmania, Locked Bag 1370, Launceston, TAS 7250, Australia;4. ARC Centre of Excellence for Nanoscale BioPhotonics, Griffith University, Southport, QLD 4215, Australia;5. Department of Immunology, Monash University, Melbourne, VIC 3004, Australia;6. Department of Surgery, Austin Health, University of Melbourne, Heidelberg, VIC 3084, Australia;1. Public Health Agency of Canada, Agence de la Santé Publique du Canada, 200 René-Lévesque Blvd., Montréal, Québec H2Z 1X4, Canada;2. School of Public Health, University of Alberta, 357F South Academic Building, 116 St. and 85th Ave., Alberta T6G 2R3, Canada;3. Office of Campus Ministries, 110 E. 12th St. Hope College, Holland, MI 49423, United States;5. Saint Joseph High School, 2521 Stadium Dr., Saint Joseph, MI 49085, United States;1. National Animal Protozoa Laboratory & College of Veterinary Medicine, China Agricultural University, Beijing 100193, China;2. Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China;3. Department of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA;4. Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA;1. Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben-Gurion, Israel;2. French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben-Gurion, Israel;1. General Zoology, Institute for Biology, Martin-Luther University Halle-Wittenberg, Hoher Weg 8, 06120 Halle (Saale), Germany;2. Laboratorio de Entomología Aplicada y Parasitología–LENAP, Escuela de Biología, Facultad de Farmacia, Universidad de San Carlos de Guatemala, Guatemala;3. Instituto de Investigaciones, Centro Universitario de Zacapa, Universidad de San Carlos de Guatemala, Guatemala;1. Department of Biochemistry, School of Medicine, Tzu Chi University, Hualien, Taiwan;2. Institute of Medical Sciences, Tzu Chi University, Hualien, Taiwan;3. Department of Molecular Parasitology and Tropical Diseases, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan;4. Center for International Tropical Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
Abstract:Blood flukes of the family Spirorchiidae Stunkard, 1921 are significant pathogens of marine turtles, both in the wild and in captivity. Despite causing considerable disease and mortality, little is known about the life cycles of marine species, with just four reports globally. No complete life cycle has been elucidated for any named species of marine spirorchiid, but the group is reported to use vermetid and fissurellid gastropods, and terebelliform polychaetes as intermediate hosts. Here we report molecular evidence that nine related spirorchiid species infect vermetid gastropods as first intermediate hosts from four localities along the coast of Queensland, Australia. ITS2 rDNA and cox1 mtDNA sequence data generated from vermetid infections provides the first definitive identifications for the intermediate hosts for the four species of Hapalotrema Looss, 1899 and Learedius learedi Price, 1934. Additionally, we provide a new locality report for larval stages of Amphiorchis sp., and evidence of three additional unidentified spirorchiid species in Australian waters. Based on the wealth of infections from vermetids during this study, we conclude that the previous preliminary report of a fissurellid limpet as the intermediate host for L. learedi was likely mistaken. The nine species found infecting vermetids during this study form a strongly supported clade exclusive of species of the other two marine spirorchiid genera for which sequence data are available; Carettacola Manter & Larson, 1950 which falls sister to the vermetid-infecting clade + a small clade of freshwater spirorchiids, and Neospirorchis Price, 1934 which is distantly related to the vermetid-infecting clade. We provide further evidence that spirorchiid transmission can occur in closed system aquaria and show that spirorchiid transmission occurs at both an important turtle rookery (Heron Island, southern Great Barrier Reef, Australia) and foraging ground (Moreton Bay, Australia). We discuss the implications of our findings for the epidemiology of the disease, control in captivity, and the evolution of vermetid exploitation by the Spirorchiidae.
Keywords:Trematoda  Cercaria  Life cycle  Vermetidae  Sea turtle  Conservation
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