1887

Abstract

Despite recent advances in molecular techniques, infection studies remain an important tool for biosecurity, veterinary and conservation medicines. Experimental infection studies are performed for many reasons: to investigate causal links between pathogens and disease, to study host species susceptibility, to study immune response to inoculation, to investigate pathogen transmission and to investigate methods for infection control. Experimental infection studies using viruses in reptiles have been conducted sporadically since at least the 1930s and this continues to be a fertile area of research. This review catalogues previously published research in the field. The key parameters of each study are tabulated, providing a summary of more than 100 experiments linked to their original publications. Common themes and trends within the data are discussed.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-04-04
2024-12-14
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References

  1. Dodin A, Brygoo ER. Compléments enzymatiques et morphologiques a l’étude de Pirhemocyton chamaeleonis [Enzymatic and morphological contributions to the study of Pirhemocyton chamaeleonis]. Bull Soc Pathol Exot Filiales 1960; 53:613–616
    [Google Scholar]
  2. Telford SR Jr. Hemoparasites of the Reptilia: Color Atlas and Text, 1st ed. CRC Press; 2016
    [Google Scholar]
  3. Virus Taxonomy: 2021 Release [Internet]. International Committee on the Taxonomy of Viruses; 2021
  4. Mifune K, Shichijo A, Ueda Y, Suenaga O, Miyagi I. Low susceptibility of common snakes in Japan to Japanese encephalitis virus. Trop Med 1969; 11:27–32
    [Google Scholar]
  5. Hayes RO, Daniels JB, Maxfield HK, Wheeler RE. Field and laboratory studies on eastern encephalitis in warm- and cold-blooded vertebrates. Am J Trop Med Hyg 1964; 13:595–606 [View Article]
    [Google Scholar]
  6. Gebhardt LP, Stanton GJ, de St. Jeor S. Transmission of WEE virus to snakes by infected Culex tarsalis mosquitoes. Exp Biol Med 1966; 123:233–235 [View Article]
    [Google Scholar]
  7. Clark HF, Karzon DT. Iguana virus, a herpes-like virus isolated from cultured cells of a lizard, Iguana iguana. Infect Immun 1972; 5:559–569 [View Article]
    [Google Scholar]
  8. Dodin A, Brygoo ER. Pirhemocyton chamaeleonis n. sp., parasite des hématies de Chamaeleo lateralis observé a madagascar [Pirhemocyton chamaeleonis n. sp., parasite of red blood cells of Chamaeleo lateralis observed in Madagascar]. Bulletin de la Société de Pathologie Exotique 1956; 49:807–810
    [Google Scholar]
  9. Schumacher J, Jacobson ER, Homer BL, Gaskin JM. Inclusion body disease in boid snakes. J Zoo Wildl Med 1994; 25:
    [Google Scholar]
  10. Origgi FC, Romero CH, Bloom DC, Klein PA, Gaskin JM et al. Experimental transmission of a herpesvirus in Greek tortoises (Testudo graeca). Vet Pathol 2004; 41:50–61 [View Article]
    [Google Scholar]
  11. Darke S, Marschang RE, Hetzel U, Reinacher M. Experimental infection of Boa constrictor with an orthoreovirus isolated from a snake with inclusion body disease. J Zoo Wildl Med 2014; 45:433–436 [View Article] [PubMed]
    [Google Scholar]
  12. Ariel E, Wirth W, Burgess G, Scott J, Owens L. Pathogenicity in six Australian reptile species following experimental inoculation with Bohle iridovirus. Dis Aquat Organ 2015; 115:203–212 [View Article]
    [Google Scholar]
  13. Johnson AJ, Pessier AP, Jacobson ER. Experimental transmission and induction of ranaviral disease in Western Ornate box turtles (Terrapene ornata ornata) and red-eared sliders (Trachemys scripta elegans). Vet Pathol 2007; 44:285–297 [View Article]
    [Google Scholar]
  14. Maclaine A, Mashkour N, Scott J, Ariel E. Susceptibility of eastern water dragons Intellagama lesueurii lesueurii to Bohle iridovirus. Dis Aquat Organ 2018; 127:97–105 [View Article]
    [Google Scholar]
  15. Miller D, Gray M, Storfer A. Ecopathology of ranaviruses infecting amphibians. Viruses 2011; 3:2351–2373 [View Article] [PubMed]
    [Google Scholar]
  16. Wirth W, Schwarzkopf L, Skerratt LF, Ariel E. Ranaviruses and reptiles. PeerJ 2018; 6:e6083 [View Article]
    [Google Scholar]
  17. Stenglein MD, Sanchez-Migallon Guzman D, Garcia VE, Layton ML, Hoon-Hanks LL et al. Differential disease susceptibilities in experimentally reptarenavirus-infected boa constrictors and ball pythons. J Virol 2017; 91:15 [View Article]
    [Google Scholar]
  18. Oya A, Doi R, Shirasaka A, Yabe S, Sasa M. Studies on Japanese encephalitis virus infection of reptiles. I. Experimental infection of snakes and lizards. Jpn J Exp Med 1983; 53:117–123
    [Google Scholar]
  19. Doi R, Oya A, Teleford SR. A preliminary report on infection of the lizard, Takydromus tachydromoides, with Japanese encephalitis virus. Jpn J Med Sci Biol 1968; 21:205–207 [View Article]
    [Google Scholar]
  20. Karstad LH. Reptiles as possible reservoir hosts for eastern encephalitis virus. Transactions of the 26th North American Wildlife and Natural Resources Conference 1961186–202
    [Google Scholar]
  21. Craighead JE, Shelokov A, Peralta PH. The lizard: a possible host for eastern equine encephalitis virus in Panama. Am J Hyg 1962; 76:82–87 [View Article] [PubMed]
    [Google Scholar]
  22. Spalatin J, Connell R, Burton AN, Gollop BJ. Western equine encephalitis in Saskatchewan reptiles and amphibians, 1961-1963. Can J Comp Med Vet Sci 1964; 28:131–142
    [Google Scholar]
  23. Uetz P, Freed P, Aguilar R, Hošek J. The Reptile Database; 2021 http://www.reptile-database.org accessed 11 June 2021
  24. Remlinger P. La tortue terrestre est réfractaire a la rage [The tortoise is refractory to rabies]. Comptes Rendus des Seances de la Societe de Biologie et de Ses Filiales 1904; 56:572–573
    [Google Scholar]
  25. Remlinger P, Bailly J. Sur la longue persistance (302 jours) du virus rabique dans l’encephale de la tortue [On the long persistence (302 days) of the rabies virus in the brain of the turtle]. C R Seances Soc Biol Fil 1931; 108:466–468
    [Google Scholar]
  26. Remlinger P, Manouélian Y, Bailly J. Recherches sur les centres nerveux de la tortue inoculée de virus rabique [Research on the nerve centres of tortoises inoculated with rabies virus]. Comptes Rendus de l’Académie des Sciences 1931; 193:1122–1124
    [Google Scholar]
  27. Remlinger P, Bailly J. Sur la longue persistance du virus rabique dans l’encéphale de la tortue d’eau douce (Clemmys leprosa) [On the long persistence of the rabies virus in the brain of the freshwater turtle (Clemmys leprosa). C R Seances Soc Biol Fil 1932; 110:421–423
    [Google Scholar]
  28. Remlinger P, Bailly J. Sur le comportement du virus rabique dans l’encéphale de la tortue [On the behaviour of the rabies virus in the brain of the turtle]. C R Seances Soc Biol Fil 1929; 101:860–863
    [Google Scholar]
  29. Marschang RE. Viruses infecting reptiles. Viruses 2011; 3:2087–2126 [View Article] [PubMed]
    [Google Scholar]
  30. Hepojoki J, Salmenperä P, Sironen T, Hetzel U, Korzyukov Y et al. Arenavirus coinfections are common in snakes with boid inclusion body disease. J Virol 2015; 89:8657–8660 [View Article]
    [Google Scholar]
  31. Stenglein MD, Jacobson ER, Chang L-W, Sanders C, Hawkins MG et al. Widespread recombination, reassortment, and transmission of unbalanced compound viral genotypes in natural arenavirus infections. PLoS Pathog 2015; 11:e1004900 [View Article]
    [Google Scholar]
  32. Ng TFF, Wellehan JFX, Coleman JK, Kondov NO, Deng X et al. A tortoise-infecting picornavirus expands the host range of the family Picornaviridae. Arch Virol 2015; 160:1319–1323 [View Article]
    [Google Scholar]
  33. Johnson PD, Besselsen DG. Practical aspects of experimental design in animal research. Inst Lab Anim Res J 2002; 43:202–206 [View Article]
    [Google Scholar]
  34. Remlinger P, Bailly J. Sur le comportement du virus herpétique dans l’encéphale de la tortue [On the behaviour of the herpes virus in the brain of the tortoise]. C R Seances Soc Biol Fil 1929; 101:
    [Google Scholar]
  35. Gebhardt LP, Hill DW. Overwintering of Western equine encephalitis virus. Proc Soc Exp Biol Med 1960; 104:695–698 [View Article]
    [Google Scholar]
  36. Skalka AM, Flint J, Rall GF, Racaniello VR. Principles of Virology, Volume I: Molecular Biology, 4th ed. Washington, DC: ASM Press; 2015 [View Article]
    [Google Scholar]
  37. Mahy BWJ, Kangro HO. eds Virology Methods Manual London: Academic Press; 1996
    [Google Scholar]
  38. Haines H, Kleese WC. Effect of water temperature on a herpesvirus infection of sea turtles. Infect Immun 1977; 15:756–759 [View Article]
    [Google Scholar]
  39. McGavern DB, Kang SS. Illuminating viral infections in the nervous system. Nat Rev Immunol 2011; 11:318–329 [View Article] [PubMed]
    [Google Scholar]
  40. Reisen WK, Brault AC, Martinez VM, Fang Y, Simmons K et al. Ability of transstadially infected Ixodes pacificus (Acari: Ixodidae) to transmit West Nile virus to song sparrows or western fence lizards. J Med Entomol 2007; 44:320–327 [View Article]
    [Google Scholar]
  41. Rebell G, Rywlin A, Haines H. A herpesvirus-type agent associated with skin lesions of green sea turtles in aquaculture. Am J Vet Res 1975; 36:1221–1224
    [Google Scholar]
  42. Herbst LH, Jacobson ER, Moretti R, Brown T, Sundberg JP et al. Experimental transmission of green turtle fibropapillomatosis using cell-free tumor extracts. Dis Aquat Org 1995; 22:1–12 [View Article]
    [Google Scholar]
  43. MacLachlan NJ, Dubovi EJ. eds Fenner’s Veterinary Virology, 4th ed. London: Elsevier; 2011
    [Google Scholar]
  44. Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL. Transmission of ranavirus between ectothermic vertebrate hosts. PLoS One 2014; 9:e92476 [View Article] [PubMed]
    [Google Scholar]
  45. Brenes R, Miller DL, Waltzek TB, Wilkes RP, Tucker JL et al. Susceptibility of fish and turtles to three ranaviruses isolated from different ectothermic vertebrate classes. J Aquat Anim Health 2014; 26:118–126 [View Article]
    [Google Scholar]
  46. Origgi FC, Klein PA, Mathes K, Blahak S, Marschang RE et al. Enzyme-linked immunosorbent assay for detecting herpesvirus exposure in mediterranean tortoises (spur-thighed tortoise [Testudo graeca] and hermann’s tortoise [Testudo hermanni]). J Clin Microbiol 2001; 39:3156–3163
    [Google Scholar]
  47. Allender MC, Barthel AC, Rayl JM, Terio KA. Experimental transmission of frog virus 3–like ranavirus in juvenile chelonians at two temperatures. J Wildl Dis 2018; 54:716–725 [View Article]
    [Google Scholar]
  48. Coe JE, Thomas LA, Cory JC, Patzer ER. Antibody development in garter snakes (Thamnophis spp.) experimentally infected with western equine encephalitis virus. Am J Trop Med Hyg 1980; 29:112–117 [View Article]
    [Google Scholar]
  49. Wozniak E, McBride J, DeNardo D, Tarara R, Wong V et al. Isolation and characterization of an antigenically distinct 68-kd protein from nonviral intracytoplasmic inclusions in boa constrictors chronically infected with the inclusion body disease virus (IBDV: Retroviridae). Vet Pathol 2000; 37:449–459 [View Article]
    [Google Scholar]
  50. Alves de Matos AP, Paperna I, Crespo E. Experimental infection of lacertids with lizard erythrocytic viruses. Intervirology 2002; 45:150–159 [View Article] [PubMed]
    [Google Scholar]
  51. Bosco-Lauth AM, Hartwig AE, Bowen RA. Reptiles and amphibians as potential reservoir hosts of chikungunya virus. Am J Trop Med Hyg 2018; 98:841–844 [View Article]
    [Google Scholar]
  52. Doi R, Oya A, Shirasaka A, Yabe S, Sasa M. Studies on Japanese encephalitis virus infection of reptiles. II. Role of lizards on hibernation of Japanese encephalitis virus. Jpn J Exp Med 1983; 53:125–134
    [Google Scholar]
  53. Klenk K, Komar N. Poor replication of West Nile virus (New York 1999 strain) in three reptilian and one amphibian species. Am J Trop Med Hyg 2003; 69:260–262 [View Article] [PubMed]
    [Google Scholar]
  54. Smith AW, Anderson MP, Skilling DE, Barlough JE, Ensley PK. First isolation of calicivirus from reptiles and amphibians. Am J Vet Res 1986; 47:1718–1721 [PubMed]
    [Google Scholar]
  55. Remlinger P, Bailly J. Sur la comportement du virus de la maladie d’Aujeszky dans le cerveau de la tortue [On the behaviour of the aujeszky’s disease virus in the brain of the turtle]. C R Seances Soc Biol Fil 1933; 114:889–890
    [Google Scholar]
  56. Gandar F, Wilkie GS, Gatherer D, Kerr K, Marlier D et al. The genome of a tortoise herpesvirus (Testudinid Herpesvirus 3) has a novel structure and contains a large region that is not required for replication in vitro or virulence in vivo. J Virol 2015; 89:11438–11456 [View Article]
    [Google Scholar]
  57. Pees M, Neul A, Müller K, Schmidt V, Truyen U et al. Virus distribution and detection in corn snakes (Pantherophis guttatus) after experimental infection with three different ferlavirus strains. Vet Microbiol 2016; 182:213–222 [View Article]
    [Google Scholar]
  58. Gaskin JM, Haskell M, Keller N, Jacobson E. Serodiagnostics of ophidian paramyxovirus infections. In [Abstracts] Third International Colloquium on the Pathology of Reptiles and Amphibians vol 1989 Orlando, FLFL January 13-15: 1989 pp 21–23
    [Google Scholar]
  59. Lloyd ML, Flanagan J. Recent developments in ophidian paramyxovirus research and recommendations on control. In Proceedings: American Association of Zoo Veterinarians - Annual Meeting 1991 1991 pp 151–156
    [Google Scholar]
  60. Neul A, Schrödl W, Marschang RE, Bjick T, Truyen U et al. Immunologic responses in corn snakes (Pantherophis guttatus) after experimentally induced infection with ferlaviruses. Am J Vet Res 2017; 78:482–494 [View Article]
    [Google Scholar]
  61. Starck JM, Neul A, Schmidt V, Kolb T, Franz-Guess S et al. Morphology and morphometry of the lung in corn snakes (Pantherophis guttatus) infected with three different strains of ferlavirus. J Comp Pathol 2017; 156:419–435 [View Article]
    [Google Scholar]
  62. Hausmann JC, Wack AN, Allender MC, Cranfield MR, Murphy KJ et al. Experimental challenge study of FV3-like ranavirus infection in previously FV3-like ranavirus infected eastern box turtles (Terrapene carolina carolina) to assess infection and survival. J Zoo Wildl Med 2015; 46:732–746 [View Article]
    [Google Scholar]
  63. Allender MC, Mitchell MA, Torres T, Sekowska J, Driskell EA. Pathogenicity of frog virus 3-like virus in red-eared slider turtles (Trachemys scripta elegans) at two environmental temperatures. J Comp Pathol 2013; 149:356–367 [View Article]
    [Google Scholar]
  64. Rayl JM, Allender MC. Temperature affects the host hematological and cytokine response following experimental ranavirus infection in red-eared sliders (Trachemys scripta elegans). PLoS One 2020; 15:e0241414 [View Article]
    [Google Scholar]
  65. Ariel E, Elliott E, Meddings JI, Miller J, Santos MB et al. Serological survey of Australian native reptiles for exposure to ranavirus. Dis Aquat Organ 2017; 126:173–183 [View Article]
    [Google Scholar]
  66. Wirth W, Schwarzkopf L, Skerratt LF, Tzamouzaki A, Ariel E. Dose-dependent morbidity of freshwater turtle hatchlings, Emydura macquarii krefftii, inoculated with Ranavirus isolate (Bohle iridovirus, Iridoviridae). J Gen Virol 2019; 100:1431–1441 [View Article]
    [Google Scholar]
  67. Wirth W, Ariel E, Lesbarrères D. Temperature-dependent infection of freshwater turtle hatchlings, Emydura macquarii krefftii, inoculated with a ranavirus isolate (Bohle iridovirus, Iridoviridae). Facets 2020; 5:821–830 [View Article]
    [Google Scholar]
  68. Tyler KL, Nathanson N et al. Pathogenesis of viral infections. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al. eds Fundamental Virology, 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2001 pp 199–243
    [Google Scholar]
  69. Jacobson ER, Gaskin JM, Gardiner CH. Adenovirus-like infection in a boa constrictor. J Am Vet Med Assoc 1985; 187:1226–1227
    [Google Scholar]
  70. Papp T, Marschang RE. Detection and characterization of invertebrate iridoviruses found in reptiles and prey insects in Europe over the past two decades. Viruses 2019; 11:600 [View Article]
    [Google Scholar]
  71. Dodin A, Brygoo ER. Compléments morphologiques et enzymatiques a l’étude de l’inclusion leucocythémique de Chamaeleo lateralis [Morphological and enzymatic contributions to the study of the leucocythemic inclusion in Chamaeleo lateralis]. Bull Soc Pathol Exot Filiales 1960; 53:620–622
    [Google Scholar]
  72. Brumpt E, Lavier G. Sur un hématozoaire nouveau du lézard vert, Pirhemocyton lacertæ n sp [On a new haematozoon of the green lizard, Pirhemocyton lacertæ n. sp.]. Annales de Parasitologie Humaine et Comparée 1935; 13:537–543
    [Google Scholar]
  73. Shi Y, Hu S, Duan W, Ding T, Zhao Z. The distinct evolutionary properties of the tripartite motif-containing protein 39 in the Chinese softshell turtle based on its structural and functional characterization. Dev Comp Immunol 2019; 99:103407 [View Article] [PubMed]
    [Google Scholar]
  74. Goodman RM, Carter ED, Miller DL. Influence of herbicide exposure and ranavirus infection on growth and survival of juvenile red-eared slider turtles (Trachemys scripta elegans). Viruses 2021; 13:1440 [View Article]
    [Google Scholar]
  75. Allender MC, Mitchell MA. Hematologic response to experimental infections of frog virus 3-like virus in red-eared sliders (Trachemys scripta elegans). J Herpetol Med Surg 2013; 23:25 [View Article]
    [Google Scholar]
  76. Wirth W, Forzán MJ, Schwarzkopf L, Ariel E. Pathogenesis of Bohle iridovirus infection in Krefft’s freshwater turtle hatchlings (Emydura macquarii krefftii). Vet Pathol 2023; 60:139–150 [View Article]
    [Google Scholar]
  77. Maclaine A, Forzán MJ, Mashkour N, Scott J, Ariel E. Pathogenesis of Bohle Iridovirus (genus Ranavirus) in experimentally infected juvenile eastern water dragons (Intellagama lesueurii lesueurii). Vet Pathol 2019; 56:465–475 [View Article]
    [Google Scholar]
  78. Dodin A, Brygoo ER. Formation intraleucocytaire chez Chamaeleo lateralis, processus leucémique à inclusions. [intraleucocyte formation in Chamaeleo lateralis, leukemic process with inclusions]. Arch Inst Pasteur Madagascar 1959; 27:79–84
    [Google Scholar]
  79. Svet-Moldavsky GJ, Trubcheninova L, Ravkina LI. Pathogenicity of the chicken sarcoma virus (Schmidt-Ruppin) for amphibians and reptiles. Nature 1967; 214:300–302 [View Article]
    [Google Scholar]
  80. Vermeil C, Maurin J. Toxoplasmose et virus chorio-méningitique chez le caméléon (Chamoeleo vulgaris D.) [Toxoplasmosis and chorio-meningitis viruses in chameleon (Chamoeleo vulgaris D.)]. Ann Parasitol Hum Comp 1953; 28:333–338 [View Article]
    [Google Scholar]
  81. Hetzel U, Korzyukov Y, Keller S, Szirovicza L, Pesch T et al. Experimental reptarenavirus infection of boa constrictor and python regius. J Virol 2021; 95:e01968–20 [View Article]
    [Google Scholar]
  82. Lee HW. Multiplication and antibody formation of japanese encephalitis virus in snakes. Seoul J Med 1968; 9:157–161
    [Google Scholar]
  83. Yuill TM. Mosquitoes for drawing blood from small reptiles. Trans R Soc Trop Med Hyg 1969; 63:407–408 [View Article] [PubMed]
    [Google Scholar]
  84. Grešíková-Kohútová M, Albrecht P. Experimental pathogenicity of the tick-borne encephalitis virus for the green lizard, Lacerta viridis (Laurenti 1768). J Hyg Epidemiol Microbiol Immunol 1959; 3:258–263
    [Google Scholar]
  85. Řeháček J, Nosek J, Grešíková M. Study of the relation of the green lizard (Lacerta viridis Laur.) to natural foci of tick-borne encephalitis. J Hyg Epidemiol Microbiol Immunol 1961; 5:366–372
    [Google Scholar]
  86. Sekeyová M, Gresíková M, Lesko J. Formation of antibody to tick-borne encephalitis virus in Lacerta viridis and L. agilis lizards. Acta Virol 1970; 14:87
    [Google Scholar]
  87. Klenk K, Snow J, Morgan K, Bowen R, Stephens M et al. Alligators as West Nile virus amplifiers. Emerg Infect Dis 2004; 10:2150–2155 [View Article] [PubMed]
    [Google Scholar]
  88. Byas AD, Gallichotte EN, Hartwig AE, Porter SM, Gordy PW et al. American alligators are capable of West Nile virus amplification, mosquito infection and transmission. Virology 2022; 568:49–55 [View Article] [PubMed]
    [Google Scholar]
  89. Habarugira G, Moran J, Colmant AMG, Davis SS, O’Brien CA et al. Mosquito-independent transmission of West Nile virus in farmed saltwater crocodiles (Crocodylus porosus). Viruses 2020; 12:198 [View Article]
    [Google Scholar]
  90. Steinman A, Banet-Noach C, Simanov L, Grinfeld N, Aizenberg Z et al. Experimental infection of common garter snakes (Thamnophis sirtalis) with West Nile virus. Vector Borne Zoonotic Dis 2006; 6:361–368 [View Article]
    [Google Scholar]
  91. Ragan IK, Blizzard EL, Gordy P, Bowen RA. Investigating the potential role of North American animals as hosts for Zika virus. Vector Borne Zoonotic Dis 2017; 17:161–164 [View Article]
    [Google Scholar]
  92. Placidi L. Essai de transmission du virus de newcastle à des vertébrés inférieurs [Attempted transmission of newcastle virus to lower vertebrates]. Ann Inst Pasteur 1956
    [Google Scholar]
  93. Jacobson ER, Adams HP, Geisbert TW, Tucker SJ, Hall BJ et al. Pulmonary lesions in experimental ophidian paramyxovirus pneumonia of Aruba Island rattlesnakes, Crotalus unicolor. Vet Pathol 1997; 34:450–459 [View Article]
    [Google Scholar]
  94. Sudia WD, Chamberlain RW, Coleman PH. Experimental vector-host studies with Tensaw virus, a newly recognized member of the Bunyamwera arbovirus group. Am J Trop Med Hyg 1969; 18:98–102 [View Article]
    [Google Scholar]
  95. Aspöck H, Kunz C. Untersuchungen über die überwinterung von tahyna- und calovo-virus in amphibien und reptilien [Research on the hibernation of tahyna and calovo virus in amphibians and reptiles]. Zentralblatt für Bakteriologie, I Abteilung Originale 1971; 216:1–8
    [Google Scholar]
  96. Findlay GM. Rift valley fever or enzootic hepatitis. Transac Royal Soc Trop Med Hyg 1932; 25:229–IN11 [View Article]
    [Google Scholar]
  97. Rissmann M, Kley N, Ulrich R, Stoek F, Balkema-Buschmann A et al. Competency of amphibians and reptiles and their potential role as reservoir hosts for Rift Valley Fever Virus. Viruses 2020; 12:1206 [View Article]
    [Google Scholar]
  98. Paries S, Funcke S, Kershaw O, Failing K, Lierz M. The role of Virus “X” (Tortoise Picornavirus) in kidney disease and shell weakness syndrome in European tortoise species determined by experimental infection. PLoS One 2019; 14:e0210790 [View Article]
    [Google Scholar]
  99. Trubcheninova LP, Khutoryansky AA, Svet-Moldavsky GJ, Kuznetsova LE, Sokolov PP et al. Body temperature and tumor virus infection. I. Tumorogenicity of Rous sarcoma virus for reptiles. Neoplasma 1977; 24:3–19 [PubMed]
    [Google Scholar]
  100. Veskova TK, Trubcheninova LP, Dook IL. Tumours in reptiles inoculated with chicken Rous sarcoma material. Folia Biol 1970; 16:353–355
    [Google Scholar]
  101. Remlinger P, Bailly J. L’évolution du parasite de la rage comport-t-elle un cycle? [Does the evolution of the rabies parasite have a cycle?. Ann Inst Pasteur 1929; 43:1396–1407
    [Google Scholar]
  102. Lamirande EW, Nichols DK, Owens JW, Gaskin JM, Jacobson ER. Isolation and experimental transmission of a reovirus pathogenic in ratsnakes (Elaphe species). Virus Res 1999; 63:135–141 [View Article]
    [Google Scholar]
  103. Hoon-Hanks LL, Layton ML, Ossiboff RJ, Parker JSL, Dubovi EJ et al. Respiratory disease in ball pythons (Python regius) experimentally infected with ball python nidovirus. Virology 2018; 517:77–87 [View Article] [PubMed]
    [Google Scholar]
  104. Hayes RO. Studies on eastern encephalitis in Massachusetts during 1960. Proceedings of the Annual Meeting of the New Jersey Mosquito Extermination Association 1961; 4859–62
    [Google Scholar]
  105. Smith AL, Anderson CR. Susceptibility of two turtle species to eastern equine encephalitis virus. J Wildl Dis 1980; 16:615–617 [View Article] [PubMed]
    [Google Scholar]
  106. White G, Ottendorfer C, Graham S, Unnasch TR. Competency of reptiles and amphibians for eastern equine encephalitis virus. Am J Trop Med Hyg 2011; 85:421–425 [View Article] [PubMed]
    [Google Scholar]
  107. Bowen GS. Prolonged western equine encephalitis viremia in the Texas tortoise (Gopherus berlandieri). Am J Trop Med Hyg 1977; 26:171–175 [View Article]
    [Google Scholar]
  108. Thomas LA, Eklund CM, Rush WA. Susceptibility of garter snakes (Thamnophis spp.) to western equine encephalomyelitis virus. Proc Soc Exp Biol Med 1958; 99:698–700 [View Article]
    [Google Scholar]
  109. Thomas LA, Eklund CM, Larson CL. Overwintering of western equine encephalomyelitis virus in experimentally infected garter snakes and transmission to mosquitoes. Exp Biol Med 1960; 105:52–55 [View Article]
    [Google Scholar]
  110. Thomas LA, Eklund CM. Overwintering of western equine encephalomyelitis virus in garter snakes experimentally infected by Culex tarsalis. In Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine New York, NY: 1962 pp 421–424 [View Article]
    [Google Scholar]
  111. Gebhardt LP, Stanton GJ, Hill DW, Collett GC. Natural overwintering hosts of the virus of western equine encephalitis. N Engl J Med 1964; 271:172–177 [View Article]
    [Google Scholar]
  112. St Jeor SC. Experimental and Natural Western Equine Encephalitis Virus Infections in Reptiles University of Utah; 1969
    [Google Scholar]
  113. Gebhardt LP, Jeor SC, Stanton GJ, Stringfellow DA. Ecology of Western encephalitis virus. Proc Soc Exp Biol Med 1973; 142:731–733 [View Article]
    [Google Scholar]
  114. Rosenbusch F. Equine encephalomyelitis in the Argentine in its experimental aspects. In Proceedings of the Sixth Pacific Science Congress 1939 pp 209–214
    [Google Scholar]
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