Advertisement

EcoHealth

, Volume 16, Issue 2, pp 248–259 | Cite as

Chelonid Alphaherpesvirus 5 DNA in Fibropapillomatosis-Affected Chelonia mydas

  • Isabela G. Domiciano
  • Matt K. Broadhurst
  • Camila Domit
  • Karina K. M. C. Flaiban
  • Daphne W. Goldberg
  • Juliana T. T. Fritzen
  • Ana Paula F. R. L. BracarenseEmail author
Original Contribution
  • 93 Downloads

Abstract

Fibropapillomatosis is a panzootic and chronic disease among Chelonia mydas—usually associated with anthropogenic impacts. This study contributes towards understanding fibropapillomatosis implications for C. mydas populations as a reflector of environmental quality, via prevalence and histological, molecular and blood analyses at a World Heritage site in southern Brazil. Sixty-three juvenile C. mydas (31.3–54.5 cm curved carapace length–CCL) were sampled during two years. Eighteen specimens (~ 29%) had tumours (which were biopsied), while 45 had none. Degenerative changes in the epidermis and Chelonid alphaherpesvirus 5 DNA detection with three variants support a herpesvirus infection. Phylogenetic analysis indicated that variants A and B were similar to a herpesvirus lineage from the Atlantic group, but variant C was similar to a herpesvirus from the eastern Pacific lineage and represents the first published case for marine turtles off Brazil. Significantly lower levels of seven blood parameters, but greater numbers of eosinophils, were observed in tumour-afflicted animals. These observations were attributed to metabolism efficiencies and/or differences in diet associated with temporal-recruitment bias and disease development, and greater non-specific immune stimulation. While most animals had adequate body condition independent of disease, longer-term studies are required to elucidate any protracted population effects.

Keywords

Green turtles Blood parameters Molecular analysis Histology Diseases Environmental sentinel 

Notes

Acknowledgements

We thank the research team from LEC/UFPR, Associação MarBrasil, Fundação Pró-Tamar, Karumbe, especially Daniel Gonzalez, Gabriela Velez-Rubio, Gustavo Martinez Souza and Ignacio Bruno, for their assistance with C. mydas sampling, and Alcides Branco, Daniela Nóbrega and Giovana Balarin for laboratory assistance. Dr. Thierry Work is thanked for reviewing an earlier draft of the paper and for his helpful discussions.

Funding

This study was funded by Petrobras (REBIMAR), Fundação Araucária/ Fundação Grupo Boticário (Projeto ProTartas), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior grant (99999.005563/2014-03) and Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico grant (302816/2014-3).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and Animal Rights

All applicable institutional and/or national guidelines for the care and use of animals were followed.

References

  1. Aguirre AA, Lutz PL (2004) Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator?. EcoHealth 1: 275–283Google Scholar
  2. Aguirre AA, Balazs GH (2000) Blood biochemistry values of green turtles, Chelonia mydas, with and without fibropapillomatosis. Comparative Haematology International 10: 132–137CrossRefGoogle Scholar
  3. Aguirre AA, Balazs GH, Spraker TR, Gross TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomatosis. Physiological Zoology 68: 831–854CrossRefGoogle Scholar
  4. Bolten AB, Bjorndal KA (1992) Blood profiles for a wild population of green turtles (Chelonia mydas) in the southern Bahamas: size-specific and sex-specific relationships. Journal of Wildlife Disease 28: 407–413CrossRefGoogle Scholar
  5. Bourjea J, Lapègue S, Gagnevin L, Broderick D, Mortimer JA, Ciccione S, Roos D, Taquet C, Grizel H (2007) Phylogeography of the green turtle, Chelonia mydas, in the Southwest Indian Ocean. Molecular Ecology 16: 175–186CrossRefGoogle Scholar
  6. Campbell TW (2014) Clinical pathology. In: Current therapy in reptile medicine and surgery, Mader DR, Divers SJ (editors), Missouri: Elsevier, 70–92CrossRefGoogle Scholar
  7. Carretero R, Sektioglu IM, Garbi, N, Salgado OC, Beckhove P (2015) Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nature Immunology 16: 609–617CrossRefGoogle Scholar
  8. Coelho VF, Domit C, Broadhurst MK, Nishizawa H, Prosdocimi L, Almeida FS (2018) Intra-specific variation in skull morphology of juvenile Chelonia mydas in the southwestern Atlantic Ocean. Marine Biology 165:174CrossRefGoogle Scholar
  9. Chaloupka M, Work TM, Balazs GH, Murakawa SKK, Morris M (2008) Cause-specific temporal and spatial trends in green sea turtle strandings in the Hawaiian archipelago (1982–2004). Marine Biology 154: 887–898CrossRefGoogle Scholar
  10. Diniz GS, Barbarino E, Lourenço SO (2012) On the chemical profile of marine organisms from the coastal subtropical environments: gross composition and nitrogen-to-protein conversion factors. In: Marcelli, M (ed) Oceanography. Intech, Rijeka, pp 297–320Google Scholar
  11. Domiciano IG, Domit C, Bracarense APFRL (2017) The Green turtle Chelonia mydas as a marine and coastal environmental sentinels: anthropogenic activities and diseases. Semina 38: 3417–3434Google Scholar
  12. Domiciano IG, Domit C, Broadhurst MK, Koch MS, Bracarense APFRL (2016) Assessing disease and mortality among small cetaceans stranded at a World Heritage Site in southern Brazil. PloS ONE 11: e0149295.1– e0149295.17CrossRefGoogle Scholar
  13. Doweiko JP, Nompleggi DJ (1991) The role of albumin in human physiology and pathophysiology, Part III: albumin and disease state. Journal of Parenteral and Enteral Nutrition 15: 476–483CrossRefGoogle Scholar
  14. Felsenstein, J. (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39: 783-791CrossRefGoogle Scholar
  15. Flint M, Morton JM, Limpus CJ, Patterson-Kane JC, Murray PJ, Mills PC (2009) Development and application of biochemical and haematological reference intervals to identify unhealthy green sea turtles (Chelonia mydas). The Veterinary Journal 185: 299–304CrossRefGoogle Scholar
  16. Foley AM, Schroeder BA, Redlow AE, Fick-Child K, Teas WG (2005) Fibropapillomatosis in stranded green turtles (Chelonia mydas) from the eastern United States (1980–98): trends and association with environmental factors. Journal of Wildlife Disease 41: 29–41CrossRefGoogle Scholar
  17. Gama LR, Domit C, Broadhurst MK, Fuentes MPB, Millar RB (2016) Green turtle Chelonia mydas foraging ecology at 25°S in the western Atlantic: evidence to support a feeding model driving by intrinsic and extrinsic variability. Marine Ecology Progress Series 542: 209–219CrossRefGoogle Scholar
  18. Goldwasser P, Feldman J (1997) Association of serum albumin and mortality risk. Journal of Clinical Epidemiology 50: 693–703CrossRefGoogle Scholar
  19. Greenblatt RJ, Work TM, Dutton P, Sutton C, Spraker TR, Casey RN, Diez CE, Parker, D, St. Leger J, Balazs GH, Casey JW (2005) Geographic variation in marine turtle fibropapillomatosis. Journal of Zoo and Wildlife Medicine 36: 527–530CrossRefGoogle Scholar
  20. Hamann M, Schäuble CS, Simon T, Evans S (2006) Demographic and health parameters of green sea turtle Chelonia mydas foraging in the Gulf of Carpentaria, Australia. Endangered Species Research 2: 81–88.CrossRefGoogle Scholar
  21. Hasbún CR, Lawrence AJ, Naldo J, Samour JH, Al-Ghais SM (1998) Normal blood chemistry of free-living green sea turtles, Chelonia mydas, from the United Arab Emirates. Comparative Haematology International 8: 174–177CrossRefGoogle Scholar
  22. Herbst L, Ene A, Su M, Desalle R, Lenz J (2004) Tumor outbreaks in marine turtles are not due to recent herpesvirus mutation. Current Biology 14: 697–699CrossRefGoogle Scholar
  23. Herbst LH, Jacobson ER (2003) Practical approaches for studying sea turtle health and disease. In: The Biology of Sea Turtles, Volume II, Lutz PL, Musick JA, Wyneken J (editors), Florida: CRC press, 385–410Google Scholar
  24. Herbst LH, Jacobson ER, Klein PA, Balazs GH, Moretti R, Brown T, Sundberg JP (1999) Comparative pathology and pathogenesis of spontaneous and experimentally induced fibropapillomas of green turtles (Chelonia mydas). Veterinary Pathology 36: 551–564CrossRefGoogle Scholar
  25. IUCN (2018) The International Union for Conservation of Nature Red List of Threatened Species. Version 2017-1 (cited in 07 March 2018). Available from: http://www.iucnredlist.org/
  26. Jones K, Ariel E, Burgess G, Read M (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). Veterinary Journal 212: 48–57CrossRefGoogle Scholar
  27. Kage-Karjian A, Norton TM, Krimer P, Groner M, Nelson SE, Gottdenker NL (2014) Factors influencing survivorship of rehabilitating green sea turtles (Chelonia mydas) with fibropapillomatosis. Journal of Zoo and Wildlife Medicine 45: 507–519CrossRefGoogle Scholar
  28. Keller JM, Balazs GH, Nielsen F, Rice M, Work TM, Jensen BA (2014) Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis. Environmental Science & Technology 48: 7807–7816CrossRefGoogle Scholar
  29. Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874CrossRefGoogle Scholar
  30. Labrada-Martagón V, Mendéz-Rodríguez LC, Gardner SC, Cruz-Escalona VH, Zenteno-Savín T (2010) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. II. Body condition index. Chelonian Conservation Biology 9: 173–183CrossRefGoogle Scholar
  31. Lewbart GA, Hirschfeld M, Denkinger J, Vasco K, Guevara N, García J, Muñoz J, Lohmann KJ (2014) Blood gases, biochemistry, and hematology of Galapagos green turtle (Chlonia mydas). PloS ONE 9: e96487CrossRefGoogle Scholar
  32. March DT, Vinette-Herrin K, Peters A, Ariel E, Blyde D, Hayward D, Christidis L, Kelaher BP (2018) Hematological and biochemical characteristics of stranded green sea turtles. Journal of Veterinary Diagnostic Investigation 30: 423–429CrossRefGoogle Scholar
  33. Masat RJ, Dessauer HC (1968). Plasma albumin in reptiles. Comparative Biochemistry and Physiology 25: 119–122CrossRefGoogle Scholar
  34. Monezi TA, Mehnert DU, Moura EMM, Muller NMG, Garrafa P, Matushima ER, Werneck MR, Borella MI (2016). Chelonid herpesvirus 5 in secretions and tumor tissues from Green turtles (Chelonia mydas) from Southeastern Brazil: a ten-year study. Veterinary Microbiology 186: 150–156CrossRefGoogle Scholar
  35. Morrison CL, Iwanowicz L, Work TM, Fahsbender E, Breitbart M, Adams C, Iwanowicz D, Sanders L, Ackermann M, Cornman RS (2018) Genomic evolution, recombination, and inter-strain diversity of chelonid alphaherpesvirus 5 from Florida and Hawaii green sea turtles with fibropapillomatosis. PeerJ 6: e4386. Doi: 10.7717/peerj.4386CrossRefGoogle Scholar
  36. Naro-Maciel E, Le M, FitzSimmons N, Amato G (2008) Evolutionary relationships of marine turtles: A molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution 49: 659–662CrossRefGoogle Scholar
  37. Page-Karjian A, Rivera S, Torres F, Diez C, Moore D, van Dam R, Brown C (2015) Baseline blood values for healthy free-ranging green sea turtles (Chelonia mydas) in Puerto Rico. Comparative Clinical Pathology 24: 567–573CrossRefGoogle Scholar
  38. Patrício AR, Herbst LH, Duarte A, Vélez-Zuazo X, Loureiro NS, Pereira N, Tavares L, Toranzos GA (2012) Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of General Virology 93: 1035–1045CrossRefGoogle Scholar
  39. Proietti MC, Reisser JW, Kinas PG (2007) Avaliação preliminar da ocorrência de fibropapilomatose em tartarugas-verde (Chelonia mydas) incidentes na Reserva Biológica Marinha do Arvoredo. In Proceedings of the 12nd Congresso Latino-Americano de Ciências do Mar (COLACMAR)’, (AOCEANO: Florianópolis), pp 1–3Google Scholar
  40. Quackenbush SL, Casey RN, Murcek RJ, Paul TA, Work TM, Limpus CJ, Chaves A, duToit L, Perez JV, Aguirre AA, Spraker TR, Horrocks JA, Vermeer LA, Balasz GH, Casey JW (2001) Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real-time PCR. Virology 287: 105–111CrossRefGoogle Scholar
  41. Ramirez AC (2017) Investigation into Chelonid Alphaherpesvirus 5 infection and fibropapillomatosis in the Pacific green turtle (Chelonia mydas agassizii) and the olive Ridley turtle (Lepidochelys olivacea) in the Pacific of Costa Rica and Nicaragua. Dissertation at Faculties of Veterinary Medicine and Medicine of the Justus Liebig University Giessen.Google Scholar
  42. Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo MTD, Ataíde MW, Reis KDHL, Testa P, Alieve MM, Canal CW (2014) Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Diseases of Aquatic Organisms 11: 207–217CrossRefGoogle Scholar
  43. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425Google Scholar
  44. Santos MRD, Martins AS, Baptistotte C, Work TM (2015) Health condition of juvenile green turtles in southeastern Brazil. Diseases of Aquatic Organisms 115: 193–201CrossRefGoogle Scholar
  45. Santos RG, Martins AS, Torezani E, Baptistotte C, Farias JN, Horta PA, Work TM, Balazs GH (2010) Relationship between fibropapillomatosis and environmental quality: a case study with Chelonia mydas off Brazil. Diseases of Aquatic Organisms 89: 87–95CrossRefGoogle Scholar
  46. Spotila JR (2004) Sea turtles: a complete guide to their biology, behavior, and conservation. 1st ed. Baltimore: The Johns Hopkins University Press and Oakwood ArtsGoogle Scholar
  47. Stacy NI, Allemann AR, Sayler KA (2011) Diagnostic hematology of reptiles. Clinics in Laboratory Medicine 31: 87–108CrossRefGoogle Scholar
  48. Stacy NI, Boylan S (2014) Clinical pathology of sea turtles. http://www.seaturtleguardian.org/clinical-pathology-of-sea-turtles. Accessed July 4, 2018
  49. Swimmer JY (2000) Biochemical responses to fibropapillomatosis and captivity in the green turtle. Journal of Wildlife Disease 36: 102–110CrossRefGoogle Scholar
  50. Tagliolatto AB, Guimarães SM, Lobo-Hajdu G, Monteiro-Neto C (2016) Characterization of fibropapillomatosis in green turtles Chelonia mydas (Cheloniidae) captured in a foraging area in southeastern Brazil. Diseases of Aquatic Organisms 121: 233–240CrossRefGoogle Scholar
  51. Tonyushkina K, Nichols JA (2009) Glucose meters: a review of technical challenges to obtaining accurate results. Journal of Diabetes Science and Technology 3: 971–980CrossRefGoogle Scholar
  52. Torezani E, Baptistotte C, Mendes SL, Barata PCR (2010) Juvenile green turtles (Chelonia mydas) in the effluent discharge channel of a steel plant, Espírito Santo, Brasil, 2000-2006. Journal of the Marine Biological Association of United Kingdom 90: 233–246CrossRefGoogle Scholar
  53. Whiting SD, Guinea ML, Limpus CL, Fomiatti K (2007) Blood chemistry reference values for two ecologically distinct populations of foraging green turtles, eastern Indian Ocean. Comparative Clinical Pathology 16: 109–118CrossRefGoogle Scholar
  54. Whyte MP, Walkenhorst DA, Fedde KN, Henthorn PS, Hill C (1996) Hypophosphatasia: levels of bone alkaline phosphatase immunoreactivity in serum reflect disease severity. The Journal of Clinical Endocrinology & Metabolism 81: 2142–2148Google Scholar
  55. Work TM, Balazs GH (1999) Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. Journal of Wildlife Diseases 35:804–807CrossRefGoogle Scholar
  56. Work TM, Balazs GH, Rameyer RA, Morris RA (2004) Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian islands, 1993-2003. Diseases of Aquatic Organisms 62: 163–176CrossRefGoogle Scholar
  57. Work TM, Dagenais J, Balazs GH, Schettle N, Ackermann M (2015) Dynamics of virus shedding and in situ confirmation of Chelonid herpesvirus 5 in Hawaiian green turtles with fibropapillomatosis. Veterinary Pathology 52: 1195–1201CrossRefGoogle Scholar
  58. Zwarg T, Rossi S, Sanches TC, Cesar MO, Werneck MR, Matushima ER (2014) Hematological and histopathological evaluation of wildlife green turtles (Chelonia mydas) with and without fibropapilloma from the north coast of São Paulo state, Brazil. Pesquisa Veterinária Brasileira 34: 682–688CrossRefGoogle Scholar

Copyright information

© EcoHealth Alliance 2019

Authors and Affiliations

  1. 1.Laboratório de Patologia Animal, Departamento de Medicina Veterinária PreventivaUniversidade Estadual de LondrinaLondrinaBrazil
  2. 2.Laboratório de Ecologia e Conservação, Centro de Estudos do MarUniversidade Federal do ParanáPontal do ParanáBrazil
  3. 3.NSW Department of Primary Industries, Fisheries Conservation Technology UnitNational Marine Science CentreCoffs HarbourAustralia
  4. 4.Marine and Estuarine Ecology Unit, School of Biological SciencesUniversity of QueenslandBrisbaneAustralia
  5. 5.Associação MarBrasil – ONGPontal do ParanáBrazil
  6. 6.Laboratório de Patologia Clínica, Departamento de Medicina Veterinária PreventivaUniversidade Estadual de LondrinaLondrinaBrazil
  7. 7.Fundação Pró-TamarFlorianópolisBrazil
  8. 8.Laboratório de Virologia Animal, Departamento de Medicina Veterinária PreventivaUniversidade Estadual de LondrinaLondrinaBrazil

Personalised recommendations