Evaluating environmental DNA-based quantification of ranavirus infection in wood frog populations

Molecular Ecology Resources

Volumn 16, Issue 2, 2016, Pages 423-433

  Hall, Emily M ^a   Crespi, Erica J ^a   Goldberg, Caren S ^a   Brunner, Jesse L ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Amphibian; Disease surveillance; Environmental DNA; Ranavirus

Indexed keywords

ANIMAL; DNA VIRUS INFECTIONS; ISOLATION AND PURIFICATION; MICROBIOLOGY; RANAVIRUS; RANIDAE; VETERINARY; VIROLOGY; VIRUS LOAD;

ANIMALS; DNA VIRUS INFECTIONS; RANAVIRUS; RANIDAE; VIRAL LOAD; WATER MICROBIOLOGY;

EID: 84956587737     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/1755-0998.12461     Document Type: Article

References (57)

1. Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics, 30, 133-165.
2. Blaustein AR, Han BA, Relyea RA et al. (2011) The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Annals of the New York Academy of Sciences, 1223, 108-119.
3. Bohmann K, Evans A, Gilbert MTP et al. (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends in Ecology & Evolution, 29, 358-367.
4. Brunner JL, Collins JP (2009) Testing assumptions of the trade-off theory of the evolution of parasite virulence. Evolutionary Ecology Research, 11, 1169-1188.
5. Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms, 77, 87-95.
6. Brunner JL, Barnett KE, Gosier CJ et al. (2011) Ranavirus infection in die-offs of vernal pool amphibians in New York, USA. Herpetological Review, 42, 76-79.
7. Cameron AR, Baldock FC (1998) A new probability formula for surveys to substantiate freedom from disease. Preventive Veterinary Medicine, 34, 1-17.
8. Cheng K, Jones ME, Jancovich JK et al. (2014) Isolation of a Bohle-like iridovirus from boreal toads housed within a cosmopolitan aquarium collection. Diseases of Aquatic Organisms, 111, 139-152.
9. Chestnut T, Anderson C, Popa R et al. (2014) Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS One, 9, e106790.
10. Chinchar VG, Waltzek TB (2014) Ranaviruses: not just for frogs. PLoS Pathogens, 10, e1003850.
11. Cooch EG, Conn PB, Ellner SP, Dobson AP, Pollock KH (2012) Disease dynamics in wild populations: modeling and estimation: a review. Journal of Ornithology, 152, 485-509.
12. Crofton H (1971) A model of host-parasite relationships. Parasitology, 63, 343-364.
13. Darling JA, Mahon AR (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environmental Research, 111, 978-988.
14. Dejean T, Valentini A, Duparc A et al. (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS One, 6, e23398.
15. Duffus AL, Waltzek TB, Stöhr AC et al. (2015) Distribution and host range of ranaviruses. In: Ranaviruses (eds Gray MJ, Chinchar VG), pp. 9-57. Springer International Publishing.
16. Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using rocky mountain tailed frogs and idaho giant salamanders. PLoS One, 6, e22746.
17. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183-190.
18. Gray MJ, Miller DL, Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms, 87, 243-266.
19. Gray MJ, Miller DL, Hoverman JT (2012) Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms, 99, 1-6.
20. Greer AL, Collins JP (2007) Sensitivity of a diagnostic test for amphibian ranavirus varies with sampling protocol. Journal of Wildlife Diseases, 43, 525-532.
21. Haislip NA, Gray MJ, Hoverman JT, Miller DL (2011) Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS One, 6, e22307.
22. Harp EM, Petranka JW (2006) Ranavirus in wood frogs (Rana sylvatica): potential sources of transmission within and between ponds. Journal of Wildlife Diseases, 42, 307-318.
23. Hayes TB, Falso P, Gallipeau S, Stice M (2010) The cause of global amphibian declines: a developmental endocrinologist's perspective. Journal of Experimental Biology, 213, 921-933.
24. Hyman OJ, Collins JP (2012) Evaluation of a filtration-based method for detecting batrachochytrium dendrobatidis in natural bodies of water. Diseases of Aquatic Organisms, 97, 185-195.
25. IUCN (2013) IUCN Red List. Available from http://www.iucnredlist.org/initiatives/amphibians.
26. Johnson A, Brunner J (2014) Persistence of an amphibian ranavirus in aquatic communities. Diseases of Aquatic Organisms, 111, 129-138.
27. Kiesecker JM, Skelly DK (2000) Choice of oviposition site by gray treefrogs: the role of potential parasitic infection. Ecology, 81, 2939-2943.
28. Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007) Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms, 77, 11-15.
29. Martel A, Spitzen-van der Sluijs A, Blooi M et al. (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences, 110, 15325-15329.
30. Mattison K, Bidawid S (2009) Analytical methods for food and environmental viruses. Food and Environmental Virology, 1, 107-122.
31. McCallum ML (2007) Amphibian decline or extinction? Current declines dwarf background extinction rate. Journal of Herpetology, 41, 483-491.
32. Mendelson JR, Lips KR, Gagliardo RW et al. (2006) Biodiversity-confronting amphibian declines and extinctions. Science, 313, 48.
33. Miller D, Gray M, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses (Basel), 3, 2351-2373.
34. Minamoto T, Honjo MN, Uchii K et al. (2009) Detection of cyprinid herpesvirus 3 DNA in river water during and after an outbreak. Veterinary Microbiology, 135, 261-266.
35. Minamoto T, Honjo MN, Yamanaka H et al. (2011) Detection of cyprinid herpesvirus-3 DNA in lake plankton. Research in Veterinary Science, 90, 530-532.
36. Nazir J, Spengler M, Marschang RE (2012) Environmental persistence of amphibian and reptilian ranaviruses. Diseases of Aquatic Organisms, 98, 177-184.
37. Ogram A, Sayler GS, Barkay T (1987) The extraction and purification of microbial DNA from sediments. Journal of Microbiological Methods, 7, 57-66.
38. Picco AM, Brunner JL, Collins JP (2007) Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection. Journal of Wildlife Diseases, 43, 286-290.
39. Pilliod DS, Goldberg CS, Arkle RS, Waits LP (2013) Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Canadian Journal of Fisheries and Aquatic Sciences, 70, 1123-1130.
40. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/.
41. Rachowicz LJ, Knapp RA, Morgan JAT et al. (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology, 87, 1671-1683.
42. Rees HC, Maddison BC, Middleditch DJ, Patmore JR, Gough KC (2014) REVIEW: the detection of aquatic animal species using environmental DNA-a review of eDNA as a survey tool in ecology. Journal of Applied Ecology, 51, 1450-1459.
43. Robert J, George E, De Jesus Andino F, Chen G (2011) Waterborne infectivity of the Ranavirus frog virus 3 in Xenopus laevis. Virology, 417, 410-417.
44. Schmidt BR, Kéry M, Ursenbacher S et al. (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods in Ecology and Evolution, 4, 646-653.
45. Skelly DK (2004) Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution, 58, 160-165.
46. Skelly DK, Bolden SR, Holland MP et al. (2006) Urbanization and disease in amphibians. In: Disease Ecology: Community Structure and Pathogen Dynamics (eds Collinge SK, Ray C), pp. 153-167. Oxford University Press, Cary, NC, USA.
47. Staley C, Gordon KV, Schoen ME, Harwood VJ (2012) Performance of two quantitative PCR methods for microbial source tracking of human sewage and implications for microbial risk assessment in recreational waters. Applied and Environment Microbiology, 78, 7317-7326.
48. St-Amour V, Lesbarrères D (2007) Genetic evidence of Ranavirus in toe clips: an alternative to lethal sampling methods. Conservation Genetics, 8, 1247-1250.
49. Stuart SN, Chanson JS, Cox NA et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783-1786.
50. Thomsen PF, Kielgast J, Iversen LL et al. (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565-2573.
51. Venables BH, Hornik K, Maechler M (2015) polynom: A Collection of Functions to Implement a Class for Univariate Polynomial Manipulations. R package version 1.3-8. Available from http://CRAN.R-project.org/package=polynom.
52. Walker SF, Baldi Salas M, Jenkins D et al. (2007) Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Diseases of Aquatic Organisms, 77, 105-112.
53. Warne RW, Crespi EJ, Brunner JL (2011) Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology, 25, 139-146.
54. Wheelwright NT, Gray MJ, Hill RD, Miller DL (2014) Sudden mass die-off of a large population of wood frog (Lithobates sylvaticus) tadpoles in Maine, USA, likely due to ranavirus. Herpetological Review, 45, 240-242.
55. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews, 64, 69-114.
56. Yates MV, Gerba CP, Kelley LM (1985) Virus persistence in groundwater. Applied and Environment Microbiology, 49, 778-781.
57. Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News, 2, 7-10.