Conventions in this Paper: I refer to the genus as Ranavirus, the disease as ranavirus or RV. Except in the Overview, I have used endnotes to identify the sources of important statements, to allow further exploration of any claim.

Overview

Global biodiversity is now severely threatened by Ranavirus, a genus of virus that infect fish, amphibians and reptiles. The virus has infected both cultured and wild fish populations worldwide, and caused amphibian mortality rates of 90% or more during outbreaks. Most ranaviruses have low host specificity. Research summarized here involves 126 different species and subspecies that have contracted ranavirus. Humans appear to play multiple roles in facilitating the spread of the virus.

Significant features of Ranavirus include:

  • Low host specificity: the unusual capacity to cross numerous poikilothermic species barriers. ranaviruses infect fish, amphibians, and reptiles. In areas of biodiversity, such as the Eastern US, mortality events tend to involve all species within the wetland (frogs, toads and salamanders) i

  • Infectiousness: Ranaviruses are highly infectious, as evidenced by the low doses needed to experimentally infect an animal. Ranaviruses can survive outside a host in the water, and can infect animals that make contact with that water. They weaken the animal, reducing its ability to escape predators, and animals that eat dead or dying infected animals become infected. Infections are not restricted to a life stage; both tadpoles and adult frogs can be infected. In wild amphibians, an aclinical carrier state is probably the most common state.ii That is, infection can come from an apparently healthy individual, who can often survive to the next spring, again resulting in mass mortality in the pond.

  • Robustness: Ranaviruses are robust viruses capable of surviving for extended periods of time even in dried material. ranaviruses are relatively stable in aquatic environments, persisting several week or longer outside a host organism.iii When released in water by immunocompromised infected adults, FV3 can infect adult and larval stages of Xenopus within three hours of exposure.iv Largemouth Bass Virus (LMBV) is stable in lab conditions at pH of 3-9. It remains viable in water for at least 3-4 hours, is 10% infective after 2 days, and is still detectable after 7 days.v Ranaviruses may be able to survive in the environment without a host.

  • Virulence: Painful death may occur within 5 days of infection. Can produce both “mass mortality events” and long-term population declines. Mortality rates of 90% or more have been reported. Throughout the UK, populations of the common frog have fallen by more than 80%.

  • Human Influence: Humans likely contribute significantly to the spread of ranavirus, through infected live baitvi, contaminated fishing equipment such as live wells, the pet trade, aquaculture, and confinement with infected individuals during captivity.

Taxonomy

Ranavirus is a genus of viruses within the family Iridoviridae. Some place it in the subfamily Chordiridovirinae, but the International Committee on Taxonomy of Viruses (ICTV) does not recognize this subfamily.

The family Iridoviridae:

  • Genus: Iridovirus
  • Genus: Chloriridovirus
  • Genus: Lymphocystivirus – wart‐like disease in freshwater and marine fish. Disfigurement, but low mortality.
  • Genus: Megalocytivirus – life threatening infections in >52 species of marine and freshwater fish in SE Asia.
  • Genus: Ranavirus – systemic disease in fish, reptiles, and amphibians accompanied by variable mortality.

Iridoviridae is one of seven families of “nucleocytoplasmic large DNA” (NCLDV) viruses. This clade of viruses have genetic similarities, but may or may not share a common origin.vii

Ranavirus is the only genus in its family that infects amphibians and reptiles, but one of three genera in this family which infect teleostviii fish. The genus Ranavirus is composed of 6-8 (or more) recognized species (FV3, ATV, BIV, EHNV, ECV, SCRV, SGIV, RCV‐Z), three of which are known to infect amphibians (Ambystoma tigrinum virus (ATV), Bohle iridovirus (BIV), and frog virus 3 (FV3)). There is speculation as to whether some of the “species” in this genus are actually isolates displaying various host preferences and degrees of pathology.ix One study suggests that “the ancestral Ranavirus was a fish virus and that several recent host shifts have taken place, with subsequent speciation of viruses in their new hosts. The data suggesting several recent host shifts among ranavirus species increase concern that these pathogens of cold-blooded vertebrates may have the capacity to cross numerous poikilothermic species barriers and the potential to cause devastating disease in their new hosts.”x

While some isolates of amphibian ranaviruses have been named, other strains or isolates of ranaviruses have informal names (e.g., Bohle virus in Australia, Redwood Creek virus in northern California, Southern High Plains virus, etc.), but the status of most isolates as species or strains of Ranavirus has yet to be clarified. xi

Epizoology

Amphibian mass mortality events due to ranavirus have been reported in Asia, Europe, North America, South Americaxii and Africaxiii (Most of the literature notes no outbreaks have been reported in Africa, but it has been found in tortoises from Ethiopia). Ranaviruses have been isolated from wild populations of amphibians in Australia, but have not yet been associated with mass mortality. xiv But Australia is not safe: The ranavirus Epizootic Haematopoietic Necrosis Virus (EHNV) from Australia was the first iridovirus to cause epizootic mortality in finfish.xv

History

It is likely that ranaviruses have recently and rapidly spread around the world, with that spread continuing and the rate of spread growing. The table below groups reports by five year periods. The “Number” column is the number of scientific studies reviewed in which some form of ranavirus was first reported in a species in some country. Numbers are drawn from the “Species Affected” table below. Note that the period 2005-2014 is actually 7.3 years, not 10, at this writing (May, 2012). All time periods are likely under-counted, because our literature search was exhausting, but not exhaustive.

Period Number
1965-1974 4
1975-1984 2
1985-1994 14
1995-2004 44
2005-2014 92

There is growing evidence that ranaviruses are now widely distributed in the wild, in aclinical carriers.

  • Xu et. al. report “ranaviruses have been associated with die-offs in cultured amphibians in China, but their presence in wild amphibians has not yet been assessed. We sampled free-ranging Rana dybowskii at seven sites throughout Heilongjiang Province to determine the presence and prevalence of ranaviruses in this region. Our results revealed an overall infection prevalence of 5.7% (18/315) for adults and 42.5% (51/120) for tadpoles by PCR… The results indicate that ranaviruses are broadly distributed throughout Heilongjiang Province”xvi
  • The USGS reports “Large die-offs of amphibians are often caused by ranaviruses. USGS scientists have isolated ranaviruses associated with die-offs in over 25 states involving more than 20 species of amphibians and two species of turtles in mortality events ranging from one to thousands of individuals. Some events may involve a single species, others may involve multiple species. Frogs and salamanders in the same pond, for example, may die from ranaviral infections at the same time… Ranavirus-caused die-offs in amphibians have occurred on private, state, and federal lands, including several National Parks and Wildlife Refuges. Many of the amphibian species involved in die-offs are fairly common and widespread in the United States, but some are either declining in number or are already threatened or endangered.” xvii

Transmission

There are many likely mechanisms for transmitting ranaviruses. In most of these transmissions, humans play a role.

  • Contact with an infected individual, including between parent and offspring. This contact is especially likely when the individuals are captive, and living under crowded conditions.
  • Ingestion of an infected individual, through predation, necrophagy, or cannibalism.
  • The bait trade. Use of infected frogs and salamanders as bait can transmit ranavirus either when the bait is taken or when a fisherman releases unused live bait into the water. Picco and Collins (2008) reported “ranaviruses were detected in the tiger salamander bait trade in Arizona, Colorado, and New Mexico. ranaviruses were spread geographically through the bait trade. All tiger salamanders in the bait trade were collected from the wild, and in general they moved east to west and north to south, bringing with them their multiple ranavirus strains. Finally, 26-73% of anglers used tiger salamanders as fishing bait, 26-67% of anglers released tiger salamanders bought as bait into fishing waters, and 4% of bait shops released tiger salamanders back into the wild after they were housed in shops with infected animals.”
  • Use of contaminated rubber boots, fishing gear. Transport of LMBV in North America probably occurs in live wells of fishing boats when infected fish or water are dumped into new habitat or put in contact with uninfected fish, which are then released.xviii
  • The pet trade in ornamental fish, reptiles, and amphibians, in which the animals are kept in unsanitary, crowded conditions prior to sale, and an infected individual is introduced to the caging.
  • Trade in live food fish. Any living food fish that is released is a potential problem.
  • Stocking of infected fish.xix
  • Emergence from unknown reservoir hosts associated with environmental change.

Host species

The table below provides a summary of the species affected by some form of ranavirus. Research summarized here involves 133 different species that have contracted ranavirus. Not all infections are accompanied by gross signs of disease. Most infections in this table were of wild populations, but increasingly, researchers are selecting species and, in the lab, performing “virus challenges” – determining if the tested individuals will contract some form of ranavirus.

The present author believes that there are likely no species of amphibian, reptile, or freshwater fish that are not susceptible, in some degree, to ranavirus.

Species Affected

Common Name Scientific Name Class Order Family Notes: Virus, Impact, Population Continent Nation Year of First Report Reference
White Sturgeon Acipenser transmontanus Actinopterygii Acipenseriformes
Acipenseridae
Unclassified North America USA 1990 Hedrick et al. 1990
Blanchard’s Cricket Frog Acris crepitans Amphibia Anura Hylidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2012 Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. 2012
Common Midwife Toad Alytes obstetricans Amphibia Anura Alytidae Mortality due to ranaviral disease. Wild population. Europe Spain 2009 Balseiro A., Dalton K.P., Cerro1 A., Marquez I., Cunningham A.A., Parra F., Prieto J.M., Casais R.  2009
Common Midwife Toad Alytes obstetricans Amphibia Anura Alytidae Mortality due to ranaviral disease. Wild population. Europe UK 2010 Duffus ALJ.  2010
Jefferson’s Salamander Ambystoma jeffersonianum Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011.
Central long-toed salamande Ambystoma macrodactylum Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011.
Spotted Salamander Ambystoma maculatum Amphibia Caudata Ambystomatidae  FV3-like North America USA 2003 Docherty et al. 2003
Spotted Salamander Ambystoma maculatum Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2001 Green D.E., Converse K.A., Schrader A.K. , 1996; Brunner J.L., Barnett K.E., Gosier C.J., McNulty S.A., Rubbo M.J., Kolozsvary M.B. 2011; Gahl M.K., Calhoun A.J.K. 2010; Petranka J.W., Murray S.M., Kennedy C.A. 2003; Todd-Thompson M. 2010
Blotched Tiger Salamander Ambystoma mavortium Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America Canada 1999 Bollinger T.K., Mao J., Schock D., Brigham R.M., Chinchar V.G.  1999; Schock D.M., Bollinger T.K., Collins J.P. 2010; Goater C.2011
Blotched Tiger Salamander Ambystoma mavortium Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2003 Docherty D.E., Meteyer C.U., Wang J., Mao J., Case S.T., Chinchar V.G. 2003; Jancovich J.K., Davidson E.W., Morado J.F., Jacobs B.L., Collins J.P. 1997; Jancovich J.K., Davidson E.W., Parameswaran N., Mao J., Chinchar V.G., Collins J.P., Jacobs B.L., Storfer A. 2005; Picco A.M., Collins J.P. 2008; Greer A.L., Brunner J.L., Collins J.P. 2009
Marbeled Salamander Ambystoma opacum Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2010 Todd-Thompson M. 2010.
Salamander Ambystoma spp. Amphibia Caudata Ambystomatidae Infection with no gross signs of ranaviral disease Wild population. North America Canada 2008 Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M.  2008
Sonoran Tiger Salamander Ambystoma tigrinum stebbinsi Amphibia Caudata Ambystomatidae Ambystoma tigrinum virus North America USA 1997 Jancovich et al. 1997
Tiger Salamander Ambystoma tigrinum diaboli Amphibia Caudata Ambystomatidae Regina Ranavirus-like North America USA 2003 Docherty et al. 2003
Tiger Salamander Ambystoma tigrinum diaboli Amphibia Caudata Ambystomatidae Regina Ranavirus North America Canada 1999 Bollinger et al. 1999
Tiger Salamander Ambystoma tigrinum melanostictum Amphibia Caudata Ambystomatidae Regina Ranavirus-like North America USA 2003 Docherty et al. 2003
Tiger Salamander Ambystoma tigrinum nebulosum Amphibia Caudata Ambystomatidae No morbidity or mortality found, but up to 57% infected with ATV. North America USA 2009 Greer, Brunner, Collins,2009
Tiger Salamander Ambystoma tigrinum Amphibia Caudata Ambystomatidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K., 2002; Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. 2012
Eastern American Toad Anaxyrus americanus Amphibia Bufonidae Bufonidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2012 Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. 2012
Boreal Toad Anaxyrus boreas boreas Amphibia Bufonidae Bufonidae Mortality due to ranaviral disease. Wild population. North America USA 2005 Converse K.A., Green D.E. Diseases of Tadpoles. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., 2005; Jones M.E.B., Pessier A.P. 2011.
Chinese Giant Salamander
Andrias davidianus Amphibia Caudata Cryptobranchidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Asia China 2011 Geng Y., Wang K.Y., Zhou Z.Y., Li C.W., Wang J., He M., Yin Z.Q., Lai W.M.  2011
Chinese Giant Salamander
Andrias davidianus
Amphibia Caudata Cryptobranchidae Chinese giant salamander virus (CGSV) Asia China 2010 Geng, Wang, Zhou, Li, Wang, He, Yin, Lai 2011
Patagonia Frog Atelognathus patagonicus Amphibia Anura Leptodactylidae Mortality due to ranaviral disease. Wild population. South America Argentina 2006  Fox S.F., Greer A.L., Tores-Cervantes R., Collins J.P.  2006
Fer de Lance Bothrops moojeni Reptilia Squamata Viperidae Snake Erythrocyte Virus. Captive.

2001 Johnsrude et al. 2001
Common Toad Bufo bufo Amphibia Anura Bufonidae Mortality due to ranaviral disease. Wild population. Europe UK 2010 Duffus ALJ.  2010; Hyatt A.D., Gould A.R., Zupanovic Z., Cunningham A.A., Hengstberger S., Whittington R.J., Kattenbelt J., Coupar B.E.H. 2010
Common Toad Bufo bufo Amphibia Anura Bufonidae
Europe UK 2000 Hyatt et al. 2000
Cane Toad Bufo marinus Amphibia Anura Bufonidae Iridovirus-like Australia Australia 1991 Spear et al. 1991
South American Cane Toad Bufo marinus Amphibia Anura Bufonidae Infection with no gross signs of ranaviral disease Captivity including zoological and ranaculture facilities, but excluding virus challenges. Central America Costa Rica 1991 Speare R., Freeland W.J., Bolton S.J 1991
South American Cane Toad Bufo marinus Amphibia Anura Bufonidae Infection with no gross signs of ranaviral disease Wild population. South America Venezuela 1998 Zupanovic Z., Lopz G., Hyatt A.D., Green B., Bartran G., Parkes H., Whittingtin R.J., Speare R. 1998
Cane Toad Bufo marinus Amphibia Anura Bufonidae BHV. Captive

1991 CSIRO 2008
Striped Jack Caranx delicatissimus Actinopterygii Perciformes Carangidae
FV3-Like. Aquaculture. Asia Japan 1997 Tamai et al. 1997
Gold Fish Carassius auratus Actinopterygii Cypriniformes
Cyprinidae
FV3-Like North America USA 1983 Berry et al. 1983
Chameleon Chamaeleo quadricornis Reptilia Squamata Chamaeleonidae Iridescent Virus-Like. Captive.

2001 Just et al. 2001
Frilled Lizard Chlamydosaurus kingii Reptilia Squamata Agamidae Iridescent Virus-Like. Captive.

2001 Just et al. 2001
Green python Chondropython viridis Reptilia Squamata Boidea Unclassified – New. Imported. Australia Australia 2002 Hyatt et al. 2002
Dwarf Gourami Colisa lalia Actinopterygii  Perciformes Osphronemidae Unclassified Australia Australia 1993 Anderson et al. 1993
Eastern Hellbender Cryptobranchus alleganiensis alleganiensis Amphibia Caudata Cryptobranchidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Gray M., Miller D., Sousa M. 2011. 
Green and Black Poison Arrow Frog Dendrobates auratus Amphibia Anura Dendrobatidae Infection with no gross signs of ranaviral disease Captivity including zoological and ranaculture facilities, but excluding virus challenges. North America USA 2008 Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A.  2008
Spotted Dusky Salamander Desmognathus conanti Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Northern Dusky Salamander Desmognathus fuscus Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Davidson S.R.A., Chambers D.L. 2011
Imitator Salamander Desmognathus imitator Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Seal Salamander Desmognathus monticola Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009; Davidson S.R.A., Chambers D.L. 2011
Ocoee Salamander Desmognathus ocoee Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Black-bellied salamander Desmognathus quadramaculatus Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009; DDavidson S.R.A., Chambers D.L. 2011
Santeetlah Dusky Salamander Desmognathus santeetlah Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Pigmy Salamander Desmognathus wrighti Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Pike Esox lucius Actinopterygii  Esociformes Esocidae haematopoietic necrosis virus (EHNV),  European sheatfish virus (ESV), pike-perch iridovirus (PPIV), New Zealand eel virus (NZeeIV). Captive.

2009 Jensen, Ersbøll, and Ariel (2009)
Chain Pickerel Esox niger Actinopterygii Esociformes
Esocidae
Largemouth Bass Virus (LMBV). Experimentally pathogenic


Kipp 2007
Southeastern Two-lined Salamander Eurycea cirrigera Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Davidson S.R.A., Chambers D.L. 2011
Long-tailed Salamander Eurycea longicauda Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Davidson S.R.A., Chambers D.L. 2011
Cave Salamander Eurycea lucifuga Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Davidson S.R.A., Chambers D.L. 2011
Blue Ridge Two-Lined Salamander Eurycea wilderae Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Burmese star tortoise Geochelone pardalis Reptilia Testudines Emydidae captive North America USA 2005 April J. Johnson, Allan P. Pessier, James F. X. Wellehan, April Childress, Terry M. Norton, Nancy L. Stedman, David C. Bloom, William Belzer, Valorie R. Titus,8, Robert Wagner, Jason W. Brooks, Jeffrey Spratt and Elliott R. Jacobson 2008
Leopard tortoise Geochelone pardalis Reptilia Testudines Testudinidae FV3-Like. Captive.

2007 Benetka et al. 2007
Burmese star tortoise Geochelone platynota Reptilia Testudines Testudinidae Burmese Star
Tortoise Virus. Captive.



Johnson et al. 2007
Gopher tortoise Gopherus polyphemus Reptilia Testudines Testudinidae Unclassified North America USA 1996 Westhouse et al. 1996
Gopher tortoise Gopherus polyphemus Reptilia Testudines Emydidae Free-ranging North America USA 2005 April J. Johnson, Allan P. Pessier, James F. X. Wellehan, April Childress, Terry M. Norton, Nancy L. Stedman, David C. Bloom, William Belzer, Valorie R. Titus,8, Robert Wagner, Jason W. Brooks, Jeffrey Spratt and Elliott R. Jacobson 2008
West Virginia Spring Salamander Gyrinophilus porphyriticus Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Southern Gray Treefrog Hyla chrysoscelis Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2009 Green D.E., Ip H.S. 2011; Driskell E.A., Miller D.L., Swist S.L., Gyimesi Z.S. 2009
Green Treefrog Hyla cinerea Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2005 Green D.E., Converse K.A. 2005
Chameleon Treefrog Hyla versicolor Amphibia Anura Hylidae Infection with no gross signs of ranaviral disease Wild population. North America Canada 2008 Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M.  2008
Grey Treefrog Hyla versicolor Amphibia Anura Hylidae FV3-like North America Canada 2008 Duffus et al. 2008
Mitsjama salamander Hynobius nebulosus Amphibia Caudata Hynobiidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Asia Japan 2009 Une Y., Nakajinma K., Taharaguchi S., Ogihara K., Murakami M. R 2009
Alpine Newt Ichthyosaura alpestris Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Wild population. Europe Spain 2010  Balseiro A., Dalton K.P., Del Cerro A., Marquez I., Parra F., Prieto J.M., Casias R.  2010
Doctorfish Labroides dimidiatus Actinopterygii Perciformes Labridae Unclassified Australia Australia 1995 Hedrick and McDowell 1995
Mountain lizard Lacerta monticola Reptilia Squamata Lacertidae FV3-Like Europe Portugal 2011 de Matos AP, Caeiro MF, Papp T, Matos BA, Correia AC, Marschang RE. 2011
Bluegill Lepomis macrochirus Actinopterygii Perciformes Centrarchidae Largemouth Bass Virus (LMBV). Experimentally pathogenic


Kipp 2007
Frog Leptodactylus sp. Amphibia Anura Leptodactylidae Infection with no gross signs of ranaviral disease Wild population. South America Venezuela 1998 Zupanovic Z., Lopz G., Hyatt A.D., Green B., Bartran G., Parkes H., Whittingtin R.J., Speare R. 1998
Ornate Burrowing Frog Limnodynastes ornatus Amphibia Anura Myobatrachidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Australia Australia 1992 Speare R., Smith J.R.  1992
Ornate Burrowing Frog Limnodynastes ornatus
Amphibia Anura Limnodynastidae Bohle Iridovirus Australia Australia 1993 Spear and Smith 1992; Hengstberger et al. 1993
Bosca’s newt Lissotriton boscai Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Wild population. Europe Portugal 2008 Alves de Matos A.P., Caeiro M.F., Marschang R.E., Papp T., Soares C., Marçal M.R., Carretero M.A.  2008
Smooth Newt Lissotriton vulgaris Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Wild population. Europe Netherlands 2010 Kik M., Martel A., Spitzen-van der Sluijs A., Pasmans F., Wohlsein P., Gröne A., Rijks J.M.  2010
Smooth Newt Lissotriton vulgaris Amphibia Caudata Salamandridae Infection with no gross signs of ranaviral disease Wild population. Europe UK 2010 Duffus ALJ. 2010
Common Newt Lissotriton vulgaris Amphibia Caudata Salamandridae Unclassified Europe Netherlands
Kik et. al., 2010
Plains Leopard Frog Lithobates blairi Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011. 
American Bullfrog Lithobates catesbeianus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. Asia Japan 2009 Une Y., Sakuma A., Matsueda H., Nakai K., Murakami M.  2009
American Bullfrog Lithobates catesbeianus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 1969 Green D.E., Converse K.A., Schrader A.K. , 2002; Gahl M.K., Calhoun A.J.K. 2010; Davidson S.R.A., Chambers D.L. 2011; Gray M.J., Miller D.L., Schmutzer A.C., Baldwin C.A. 2007; Majji S., LaPatra S., Long S.M., Sample R., Bryan L., Sinning A., Chinchar V.G. 2006; Miller D.L., Rajeev S., Gray M.J., Baldwin C. 2007; Miller D.L., Gray M.J., Rajeev S., Schmutzer A.C., Burton E.C., Merrill A., Baldwin C. 2009; Wolf K., Bullock G.L., Dunbar C.E., Quimby M.C. 1969
American Bullfrog Lithobates catesbeianus Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. South America Brazil 2009 Mazzoni R., José de Mesquita A., Fleury L.F.F., Diederichsen de Brito W.M.E., Nunes I.A., Robert J., Morales H., Coelho A.S.G., Barthasson D.L., Galli L., et al. 2009
American Bullfrog Lithobates catesbeianus Amphibia Anura Ranidae Infection with no gross signs of ranaviral disease Captivity including zoological and ranaculture facilities, but excluding virus challenges. South America Uruguay 2006 Galli L., Pereira A., Márquez A., Mazzoni R. 2006
Green frog Lithobates clamitans Amphibia Anura Ranidae Unclassified Europe The Netherlands 2010 Spitz, Kingdom, Veldman, and Zandt (2011)
Green frog Lithobates clamitans Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America Canada 2008 Gahl M. 2011.; St-Amour V., Wong W.M., Garner T.W.M., Lesbarreres D. 2008; Forzán M. 2011. 
Green frog Lithobates clamitans Amphibia Anura Ranidae Unclassified North America Canada 2009 Forzán, Gahl and Pauli, 2009
Green frog Lithobates clamitans Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K. 2002; Gahl M.K., Calhoun A.J.K. 2010; Gray M.J., Miller D.L., Schmutzer A.C., Baldwin C.A. 2007; Miller D.L., Rajeev S., Gray M.J., Baldwin C. 2007; Johnson A.J., Pessier A.P., Jacobson E.R. 2007
Pickeral Frog Lithobates palustris Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K. , 2002; Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. 2012; Davidson S.R.A., Chambers D.L. 2011
Northern Leopard Frog Lithobates pipiens Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America Canada 2005 Schock D.M., Bollinger T.K. 2005; Forzán M. 2011; Greer A.L., Berrill M., Wilson P.J. 2005; Echaubard P., Little K., Pauli B., Lesbarrères D. 2010; Paetow L.J., Pauli B.D., McLoughlin J.D., Bidulka J., Marcogliese D.J. 2011;
Northern Leopard Frog Lithobates pipiens Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 1965 Green D.E., Converse K.A., Schrader A.K. 2002; Clark H.F., Brennan J.C., Zeigel R.F., Karzon D.T. 1968; Granoff A., Came P.E., Rafferty K.A. 1965; Uyehara I.K, Gamble T., Cotner S. 2010
Mink frog Lithobates septentrionalis Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K.  2002
Southern Leopard Frog Lithobates sphenocephalus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2007 Green D.E., Ip H.S. 2011; Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. 2012; Johnson A.J., Pessier A.P., Jacobson E.R. 2007
Wood frog Lithobates sylvaticus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America Canada 2008 Schock D.M., Bollinger T.K., Chinchar V.G., Jancovich J.K., Collins J.P. 2008; Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M. 2008; Gahl M. 2011; Forzán M. 2011; Greer A.L., Berrill M., Wilson P.J. 2005; Schock D.M., Ruthig G.R., Collins J.P., Kutz S.J., Carrière S., Gau R.J., Veitch A.M., Larter N.C., Tate D.P., Guthrie G., et al. 2010
Wood frog Lithobates sylvaticus Amphibia Anura Ranidae Unclassified North America Canada 2009 Forzán, Gahl and Pauli, 2009
Wood frog Lithobates sylvaticus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K. 2002; Brunner J.L., Barnett K.E., Gosier C.J., McNulty S.A., Rubbo M.J., Kolozsvary M.B. 2011; Gahl M.K., Calhoun A.J.K. 2010; Petranka J.W., Murray S.M., Kennedy C.A. 2003; Todd-Thompson M. 2010; Uyehara I.K, Gamble T., Cotner S. 2010; Harp E.M., Petranka J.W. 2006
Alpine Newt Mesotrition alpestirs cyreni Amphibia Caudata Salamandridae
Europe Spain
Balseiro et al. in press
Smallmouth Bass Micropterus dolomieui Actinopterygii Perciformes Centrarchidae Largemouth Bass Virus (LMBV). Experimentally pathogenic


Kipp 2007
Largemouth Bass Micropterus salmoides Actinopterygii Perciformes Centrarchidae Largemouth Bass Virus (LMBV) North America USA 2000 Kipp 2007
Striped Bass Morone saxatilis Actinopterygii Perciformes Moronidae LMBV. Experimentally pathogenic. North America Captive 2007 Rebekah M. Kipp. 2007
Eastern Spotted Newt Notophthalmus viridescens Amphibia Caudata Salamandridae FV3-like. Infection with no gross signs of ranaviral disease Wild population. North America Canada 2008 Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M. 2008
Eastern Spotted Newt Notophthalmus viridescens Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Wild population. North America USA 1965 Green D.E., Converse K.A., Schrader A.K. 2002; Granoff A., Came P.E., Rafferty K.A. 1965; Glenney J.W., Julian J.T., Quartz W.M. 2010
Rainbow trout Oncorhynchus mykiss Osteichthyes
Salmoniformes Salmonidae EHNV Australia Australia 1996 Reddacliff and Whittington 1996
Red Seabream Pagrus major Actinopterygii Perciformes Sparidae FV3-Like. Aquaculture. Asia Japan 1997 Tamai et al. 1997
Flounder Paralichthys olivaceus
Osteichthyes Pleuronectiformes Paralichthyidae
Lymphocystis Asia China 2004 Zhang et al. 2004
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. Europe Croatia 1991 Fijan N., Matasin Z., Petrinec Z., Valpotic I., Zillenberg L.O.  1991
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae
Europe Croatia 1968 Kunst and Valpotić 1968; Fijan et al. 1991
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. Europe Denmark 2009 Ariel E., Kielgast J., Svart H.E., Larsen K., Tapiovaara H., Bang Jensen B., Holopainen R.  2009
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae
Europe Denmark 2009 Ariel et al. 2009
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae
Europe Eastern Europe 1981 Mişcalencsu et al. 1981
Edible Frog Pelophylax esculentus Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Europe Switzerland 2011 Marschang R.  2011
Eurasian Marsh Frog Pelophylax ridibundus Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Europe Switzerland 2011 Marschang R.  2011
Frog Pelophylax spp. Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. Europe Netherlands 2010 Kik M., Martel A., Spitzen-van der Sluijs A., Pasmans F., Wohlsein P., Gröne A., Rijks J.M.  2010
Water frog Pelophylax spp. Amphibia Anura Ranidae Unclassified Europe The Netherlands 2010 Dutch Wildlife Health Centre 2010
Red-Finned Perch Perca fluviatilis
Actinopterygii Perciformes Percidae Epizootic haematopoetic virus (EHNV) Australia Australia 1986 Langdon et al. 1986; Reddacliff and Whittington 1996
Golden Poison Frog Phyllobates terribilis Amphibia Anura Dendrobatidae Infection with no gross signs of ranaviral disease Captivity including zoological and ranaculture facilities, but excluding virus challenges. North America USA 2008 Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A.  2008
Northern Slimy Salamander Plethodon glutinosus complex Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2011 Davidson S.R.A., Chambers D.L. 2011
Appalachian Woodland Salamander Plethodon jordani Amphibia Caudata Plethodontidae Infection with no gross signs of ranaviral disease Wild population. North America USA 2009 Gray M.J., Miller D.L., Hoverman J.T. 2009.
Guppy Poecilia reticulata
Osteichthyes Cyprinodontiformes
Poeciliidae Unclassified Australia Australia 1995 Hedrick and McDowell 1995
Bearded Dragon Pogona vitticeps Reptilia  Squamata Agamidae Iridescent Virus-Like
Captive 2001 Just et al. 2001
Crappie Pomoxis spp. Actinopterygii Perciformes Centrarchidae Largemouth Bass Virus (LMBV). Experimentally pathogenic


Kipp 2007
Spotted Chorus Frog Pseudacris clarkii Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2010 Torrence S.M., Green D.E., Benson C.J., Ip H.S., Smith L.M., McMurray S.T. 2010
Spring Peeper Pseudacris crucifer Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America Canada 2011 Gahl M. 2011. 
Spring peeper Pseudacris crucifer Amphibia Anura Hylidae Unclassified North America Canada 2009 Forzán, Gahl and Pauli, 2009
Spring Peeper Pseudacris crucifer Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2002 Green D.E., Converse K.A., Schrader A.K. , 2002; Gahl M.K., Calhoun A.J.K. 2010; Todd-Thompson M. 2010
Spring Peeper Pseudacris crucifer Amphibia Anura Hylidae Not Classified North America USA 2002 Green et al. 2002
Southeastern Chorus Frog Pseudacris feriarum Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2010 Todd-Thompson M., 2010; Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L., 2012
Pacific Chorus Frog Pseudacris regilla Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011.
Sierran Treefrog Pseudacris sierra Amphibia Anura Hylidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Russell D.M., Goldberg C.S., Sprague L., Waits L.P., Green D.E., Schuler K.L., Rosenblum E.B. , 2011
Chorus Frog Pseudacris spp. Amphibia Anura Hylidae Infection with no gross signs of ranaviral disease Wild population. North America Canada 2008 Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M.  2008
Green Toad Pseudepidalea viridis Amphibia Anura Bufonidae Infection with no gross signs of ranaviral disease Wild population. Europe Israel 2011 Milstein D., King R., Leader N.  2011
Angel Fish Pterophyllum scalare Actinopterygii Perciformes Cichlidae Unclassified North America Canada 1990 Shuch and Sherly 1990; Paperna et al. 2001
African Bullfrog Pyxicephalus adspersus Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. North America USA 2008 Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A. 2008
Red-legged Frog Rana aurora Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 1999 Mao J. D., Green E., Fellers G., Chinchar V.G.  1999
California Red-legged Frog Rana draytonii Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011.
Dybowski’s frog Rana dybowskii Amphibia Anura Ranidae Infection with no gross signs of ranaviral disease Wild population. Asia China 2010 Xu K., Zhu D., Wei Y., Schloegel L.M., Chen X., Wang X, 2010
Pig frog Rana grylio Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Asia China 1996 Zhang Q., Li Z., Jiang Y., Liang S., Gui J. 1996; Zhang Q.Y., Xiao F., Li Z.Q., Gui J.F., Mao J., Chinchar V.G. 2001
Pig frog Rana grylio Amphibia Anura Ranidae FV3-like Asia
2001 Zhang et al. 2001
River frog Rana heckscheri Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Green D.E., Ip H.S. 2011.
Columbia Spotted Frog Rana luteiventris Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2006 Converse K.A., Green D.E. 2005; Green D.E., Converse K.A. 2005; Russell D.M., Goldberg C.S., Sprague L., Waits L.P., Green D.E., Schuler K.L., Rosenblum E.B. 2011
Southern Mountain Yellow-Legged Frog Rana muscosa Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. North America USA 2005 Converse K.A., Green D.E. 2005
Common Frog Rana temporaria Amphibia Anura Ranidae Mortality due to ranaviral disease. Wild population. Europe UK 1993 Cunningham A.A., Langton T.E.S., Bennett P.M., Lewin J.F., Drury S.E.N., Gough R.E., MacGregor S.K. 1996; Teacher A.G.F., Cunningham A.A., Garner W.J. 2010; Duffus ALJ. 2010; Cunningham A.A., Langton T.E.S., Bennett P.M., Drury S.E.N., Gough R.E., Kirkwood K.E. 1993; Drury S.E.N., Gough R.E., Cunningham A.A. 1995
Common Frog Rana temporaria Amphibia Anura Ranidae
Europe UK 1996 Cunningham et al. 1996
European common frog Rana temporaria Amphibia Anura Ranidae Unclassified Europe UK Late 1980’s ZSL Frog Health Checks
Indian Treefrog Rana tigrina Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Asia China 2002 Weng S.P., He J.G., Wang X.H., Lü L., Deng M., Chan S.-M. 2002
Indian Treefrog Rana tigrina Amphibia Anura Ranidae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Asia Thailand 1998 Kanchanakhan S. 1998
Blanford’s Tree Frog Rhacophorus dennysi Amphibia Anura Rhacophoridae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. North America USA 2008 Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A. 2008
Pike-Perch Sander lucioperca Actinopterygii Perciformes Percidae epizootic haematopoietic necrosis virus (EHNV). Experimentally induced,

2011 Jensen, Halopainen, Tapiovaara, and Ariel (2011)
Eastern Spadefoot  toad Scaphiopus holbrookii Amphibia Anura Scaphiopodidae Mortality due to ranaviral disease. Wild population. North America USA 2011 Pessier A.P. 2011.
Turbot Scophthalmus maximus Osteichthyes
Pleuronectiformes Scophthalmidae Unclassified. Aquaculture. Europe Denmark 1990 Bloch and Larsen 1990
Sheatfish Silurus glanis Osteichthyes Siluriformes Siluridae Icosahedral Cytoplasmic Deoxyribovirus. Aquaculture. Europe Germany 1990 Ahne et al. 1990
Florida box turtle Terrapene carolina bauri Reptilia Testudines Emydidae Free-ranging North America USA 2005 April J. Johnson, Allan P. Pessier, James F. X. Wellehan, April Childress, Terry M. Norton, Nancy L. Stedman, David C. Bloom, William Belzer, Valorie R. Titus,8, Robert Wagner, Jason W. Brooks, Jeffrey Spratt and Elliott R. Jacobson 2008
Eastern box turtle Terrapene carolina carolina Reptilia Testudines Emydidae FV3, FV3-Like North America USA
Allender et al. 2006
Eastern box turtle Terrapene carolina carolina Reptilia Testudines Emydidae Free-ranging North America USA 2005 April J. Johnson, Allan P. Pessier, James F. X. Wellehan, April Childress, Terry M. Norton, Nancy L. Stedman, David C. Bloom, William Belzer, Valorie R. Titus,8, Robert Wagner, Jason W. Brooks, Jeffrey Spratt and Elliott R. Jacobson 2008
Western ornate box turtle Terrapene ornata ornata Reptilia Testudines Emydidae Experimentally pathogenic. North America USA 2007 Johnson AJ, Pessier AP, Jacobson ER. 2007
Spur-thighed tortoise Testudo graeca Reptilia Testudines Testudinidae
Europe Germany 1999 Blahak S., Uhlenbrok C. 2010; Marschang, R. E., P. Becher, H. Posthaus, P. Wild, H. J. Thiel, U. Muller-Doblies, E. F. Kaleta, and L. N. Bacciarini. 1999.
Hermann’s tortoise Testudo hermanni Reptilia Testudines Testudinidae FV3-Like
Captive 1999 Marschang et al. 1999
Russian tortoise Testudo horsfieldii Reptilia Testudines Testudinidae Wild population. Africa Ethiopia 2007 V. Benetka, E. Grabensteiner, M. Gumpenberger, C. NeuBauer, B. Hirschmuller, and K. Mostl
Egyptian tortoise Testudo kleinmanni Reptilia Testudines Testudinidae
Europe Germany 1996 Uhlenbrok, 2011
Marginated tortoise Testudo marginata Reptilia Testudines Testudinidae captive Europe Germany 2010 Blahak and Uhlenbrok, 2010; Uhlenbrok, 2011
Red-eared slider Trachemys scripta elegans Reptilia Testudines Emydidae Experimentally pathogenic. North America USA 2007 Johnson AJ, Pessier AP, Jacobson ER. 2007
Gourami Trichogaster trichopterus Actinopterygii Perciformes Osphronemidae Similar to Haemapoetic Necrosis Virus (HNV) North America USA 1993 Fraser et al. 1993; Paperna et al. 2001
Chinese Soft-shelled turtle Trionyx sinnesis Reptilia Testudines Trionychidae Soft-Shelled Turtle Virus Asia China 1999 Chen et al. 1999; Huang et al. 2009
Marbled newt Triturus marmoratus Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Wild population. Europe Portugal 2008 Alves de Matos A.P., Caeiro M.F., Marschang R.E., Papp T., Soares C., Marçal M.R., Carretero M.A.  2008
Red Tailed Knobby
Newt
Tylototriton kweichowensis Amphibia Caudata Salamandridae Mortality due to ranaviral disease. Captivity including zoological and ranaculture facilities, but excluding virus challenges. Europe Belgium 2008  Pasmans F., Blahak S., Martel A., Pantchev N., Zwart P.  2008
Red Tailed Knobby
Newt
Tylototriton kweichowensis Amphibia Caudata Salamandridae Unclassified. Imported. Europe Belgium 2004 Pasmans et al. 2008
Red Tailed Knobby
Newt
Tylototriton kweichowensis Amphibia Caudata Salamandridae Unclassified. Imported. Europe The
Netherlands
2004 Pasmans et al. 2008
Leaf-Tailed Gecko Uroplatus fimbriatus Reptilia Squamata Gekkonidae FV3-Like

2005 Marschang RE, Braun S, Becher P. 2005
African Clawed Frog Xenopus laevis Amphibia Anura Pipidae FV3. Cultured, and possibly wild, populations. North America USA 2007 Robert J, Abramowitz L, Gantress J, Morales HD. 2007
Swordtail Xiphophorus hellerii Osteichthyes Cyprinodontiformes Poeciliidae Lymphocystis – Like

2001 Paperna et al. 2001

Notes on the above table

  • Ambystoma tigrium from Miller, Gray, and Storfer 2011 is coded as Ambystoma tigrinum here.
  • Ambystoma spp, Pelophylax spp., and Pseudacris spp. Cannot be determined to be different species than those already listed. Including them as different species in this table likely inflates the total species count by up to 3.
  • This table contains 77 amphibian species listed in Miller et al, 6 amphibian species or subspecies not listed there, and a total of 126 species and subspecies including fish and reptiles. The amphibians not listed in Miller are: Ambystoma tigrinum stebbinsi, Ambystoma tigrinum diaboli, Ambystoma tigrinum melanostictum, Ambystoma tigrinum nebulosum, Mesotrition alpestirs cyreni, and Xenopus laevis.
  • The current table eliminates rows for synonyms, primarily over confusion relating to Lithobates v. Rana. Although it appears that Rana will survive renaming efforts by some biologists, this paper is adopting the convention of Miller et. al. Rana sylvatica has become Lithobates sylvaticus.

Factors in Mortality

A number of conditions are now understood to contribute to morbidity and mortality from ranaviruses.

 

  • Life stage. In many amphibians, mortality is highest in larval stages including during metamorphosis, lowest while an egg.xx In one study, tadpoles exposed to ranavirus had an increased developmental rate. According to the USGS, “Mortality events due to ranaviruses occur most commonly in larval amphibians such as mole salamanders (Ambystoma spp.), true frogs (Lithobates spp. and Rana spp.) and chorus frogs (Pseudacris spp.). Infrequent isolates have been obtained from adult newts (Notophthalmus viridescens), adult tree frogs (Hyla spp.) and post-metamorphic Columbia spotted frogs (Lithobates luteiventris).” xxi
  • Role of biodiversity. According to the USGS, “In states east of the Mississippi River, especially Atlantic coastal states, mortality events tend to involve all species within the wetland (frogs, toads and salamanders) while those in western states, with less amphibian species diversity, tend to involve only one species.” xxii
  • Elevation. Some studies suggest that North American amphibians living at higher elevations have an increased risk of ranavirus infection.xxiii
  • Seasonality. Because mortality events due to ranaviruses mostly affect larval amphibians, there is a strong correlation between the presence of amphibian larvae in the spring and summer and ranaviral die-offs. Mortality events often are first detected in April when large populations of wood frogs (Lithobates sylvaticus, formerly Rana sylvatica) are present in eastern and northern wetlands. Early and mid-summer die-offs due to ranaviruses tend to involve a variety of amphibian species nationwide. Late summer and autumn mortality events involve mostly larval bullfrogs (Lithobates catesbeianus) and tiger salamanders (Ambystoma tigrinum). xxiv
  • Genetic diversity. Studies find that inbred individuals have less resistance to ranavirus than those with more genetic diversity.xxv This has implications for aquaculture and the pet trade.
  • Life history. Amphibian species in North America that develop faster as larvae, have restricted distributions, or inhabit semi-permanent breeding sites tend to be more susceptible than slow developing, widespread species that live in temporary wetlandsxxvi
  • Role of captivity. Again according to the USGS, “ranavirus infections in turtles have occurred mostly in captive colonies of eastern box turtles (Terrapene carolina carolina) and true tortoises, but die-offs of free-ranging box turtles also have been observed (Johnson and others, 2008). Because box turtles in the wild usually are solitary animals, it has been difficult to document die-offs of multiple box turtles from an area. Ranavirus also was associated with a die-off of snapping turtles in central Pennsylvania (NWHC unpublished data).”xxvii Studies in Europe find that mortality is “common” in captivesxxviii, perhaps dues to increased transmission associated with high host density, from stress, or other factors. In the case of box turtles, all confirmed cases of ranaviral infection in wild eastern box turtles on file at the USGS NWHC are from Maryland. Additional ranaviral disease outbreaks in box turtles have been reported by others in New York, Pennsylvania, Georgia, and Florida. Unexplained die-offs of wild box turtles with signs resembling ranaviral infection have been reported in other eastern states.xxix Because the Maryland box turtles who died were wearing transmitters and had all been in captivity at the same time and location, it is this author’s opinion that the infection was captivity-induced. It seems unlikely that undisturbed box turtles in the wild would contract ranavirus, and if they did, unlikely to spread it to other box turtles – they are likely to die before they meet a colleague in the woods. The fact that the box turtles in Maryland all died at about the same time is another reason to look at captivity as the source of the problem.
  • Acquired immunity. Once exposed to LMBV, a population of largemouth bass produces antibodies such that subsequent exposures result in less extreme manifestations of the disease. Fish kills can be slow and last for several weeks (Goldberg 2002; Woodland et al. 2002; Grizzle and Brunner 2003; Grizzle et al. 2003; Whelan 2004). xxx Studies of Xenopus also suggest that adult frogs can generate long lasting immunological memory involving protective antibodies (Gantress et al., 2003; Maniero et al., 2006).

Pathology

Pathogenesis

Mechanisms of development (pathogenesis) for ranaviruses:

  • ranaviruses infect several kinds of cells.
  • Synthesis of viral proteins begins within hours of viral entryxxxi
  • Necrosis or apoptosis may occur within a few hours of infection.xxxii
  • Mass mortality events may take days or monthsxxxiii, but deaths toward the end of the period may be due to secondary bacterial or fungal infections, rather than the ranavirus itself.xxxiv

Gross Pathology

Behavioral manifestations of ranaviruses:

  • erratic swimming, buoyancy problems, lethargy, and anorexia frequently occur.xxxv

Clinical manifestations of ranaviruses:

  • Miller, Gray, and Storfer (2011) summarize the clinical manifestations “In fatal cases, gross findings may include swelling of the legs and body; erythema (redness) of the legs and ventrum; ecchymosis (red blotches) near the vent and/or urostyle; petechiation (pinpoint hemorrhages) or ecchymosis of the skin and internal organs (especially the mesonephros (kidneys and liver); and irregular patches of discoloration on the skin. In metamorphs and adults, the gastrointestinal tract may be empty or contain minimal ingesta and the gall bladder may be enlarged, both of which are consistent with fasting. Although hemorrhages and swellings are the most common gross lesions noted in the larvae, cutaneous erosions and ulcerations are more frequently seen in adult anurans in Europe and adult caudates in North America”xxxvi
  • Infections often culminate in organ necrosis and massive hemorrhaging.
  • Gross lesions associated with ranavirus infection include erythema, generalized swelling, hemorrhage, limb swelling, and swollen and friable livers.[7] xxxvii
  • In largemouth bass (Micropterus salmoides), signs of the disease may include increased blood flow and darkened skin, distended abdomen, bloated swim bladder, lesions in the membrane lining the body cavity, necrosis (burst cells resulting in inflammation) of gastrointestinal mucosa, pale liver, red spleen, red intestinal caeca, infected gills, lethargic swimming, decreased responsiveness, swimming at the surface and/or in circles, and difficulty remaining upright. Sores or lesions on the outside of the body are secondary and not caused by the actual viral infection (Zilberg et al. 2000; Goldberg 2002; Brunner 2003; Grizzle and Whelan 2004; Beck et al. 2006)xxxviii.
  • In Chinese giant salamanders, clinical signs included anorexia, lethargy, ecchymoses and swollen areas on the head and limbs, and skin ulceration. Necropsy examination reveals subcutaneous and intramuscular oedema, swollen and pale livers with multifocal haemorrhage, swollen kidneys with multifocal haemorrhage and distended fluid-filled intestines with areas of haemorrhage.xxxix
  • While clinical signs of ranavirus may be obvious, some infected individuals show no such symptoms.

Images

The images below present some of the clinical manifestsations of ranavirus, and suggest what a painful death ranavirus can cause.

These Internet images had no copyright notice. The URL of the image is provided.

Fish

A largemouth bass infected with Largemouth Bass Virus – USFWS. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657

Salamanders

Ambystoma larvae showing signs of ranavirus infection. http://www.esf.edu/efb/brunner/research.htm

Tadpoles

Ranavirus-infected tadpole. Creative Commons licensing. http://www.flickr.com/photos/ajc1/6481331873/in/photostream/

http://www.dnr.state.md.us/wildlife/Plants_Wildlife/herps/catalogue_frogs.asp

Image: grodyngel-m-ranavirus-webb.jpg

Tadpoles with acute ranavirus infektion. Bleeding is seen in the skin of the hind legs. Photo: Matt Gray http://www.sva.se/sv/Mer-om-SVA1/Pressrum/Nyheter-fran-SVA/Hall-Sverige-Rent/

Adult Frogs

http://webspace.qmul.ac.uk/ranichols/ranavirus2.jpg

image: conservation-02.jpg

Adult northern green frog (Lithobates clamitans melanota) found dying in urban Virginia from wide-spread bacterial infection, see red areas on legs, later determined to be Aeromonas hydraphilla, and Ranavirus infection confirmed by PCR analysis. This frog also suffered from a rectal prolapse. http://www.vcu.edu/rice/research/research-conservation.html

adult_ranavirus_dickwillems_dsc01359.jpg

Adult green frog infected with the Ranavirus. Visible blood in the mouth and a few small spots on the flank (Photo: Dick Willems) http://www.natuurbericht.nl/?id=5702

image: 100625_BMT_Chest_ulcer_with_credit.jpg

The effects of ranavirus can be pretty brutal. Amazingly, this frog was still alive. Stephen Price http://intercrossing.wikispaces.com/Stephen+Price

 

 

Box Turtles

http://www.dnr.state.md.us/wildlife/Plants_Wildlife/herps/catalogue_frogs.asp

 

 

image: ph-turtles%20006_1328718000.jpg

The Ranavirus is impacting reptiles and amphibians in Montgomery County.

MONTGOMERY COUNTY, MD – Scott Farnsworth examining the mouth of a sick turtle. A healthy turtle mouth is bright pink. The yellowish plaques present in the mouth of this individual are one of the signs of a potential Ranavirus infection. This individual later died and tested positive for Ranavirus. Researchers from Towson University found cases of Ranavirus during the study. The disease is wiping out tadpoles and baby salamanders in Rock Creek in Montgomery County and killing off box turtles in Montgomery County. (Photo by Scott Farnsworth , Towson University)

Scott Farnsworth / Towson University http://www.washingtonpost.com/local/education/the-ranavirus-is-impacting-reptiles-and-amphibians-in-montgomery-county/2012/02/08/gIQAs6zZ9Q_photo.html

image: f1.large.jpg

Gross lesions associated with iridovirus infections in turtles and tortoises. (A) Photograph of the Burmese star tortoise with nasal discharge and palpebral and cervical edema. (B) Photograph of the wild Gopher tortoise with nasal discharge and palpebral edema. (C) Photograph of the wild Florida box turtle with palpebral edema and ocular discharge. (D) Photograph of caseous plaques in the oral cavity of a box turtle.

Journal of Wildlife Diseases http://www.jwildlifedis.org/content/44/4/851.full

Ecology and Population

Topics to be developed:

  • RVs and species declines Gray, Storfer, et al.
  • Viral transmission and persistence: Brunner, Jensen, Picco
  • Host susceptibility and pathology: Hoverman, Green, Miller
  • Pesticides and RV infections: Kirby
  • Host shifts among Rvs: Jancovich
  • Host‐Pathogen co‐evolution: Lesbarreres, Storfer
  • Host anti‐viral immunity and viral anti‐host immunity: Robert, ChinChar

Diagnosis and Detection

Field signs of a ranaviral epizootic include sudden or explosive onset of illness in amphibians in a wetland, often with hundreds or thousands of sick and dead amphibians found in a 1–5 day period. Overall mortality rates in juvenile frogs and salamanders in a wetland can exceed 90%. Affected individuals usually present with subtle to severe hemorrhages in the ventral skin, especially at the base of the hind limbs and around the vent opening. Hemorrhages may be present from tip of chin to tip of tail ventrally and may be pinpoint or irregular patches. xl

Other clinical signs include lethargy, swimming erratically, weakly, or on their sides, and mild to severe fluid accumulation under the skin (in lymphatic sacs) of the abdomen and proximal hind limbs. Internally, there may be fluid accumulation (clear or red-tinged) in the body cavity (called hydrocoelom), and hemorrhages on the serosal surfaces of viscera, especially heart, stomach and liver. Occasionally, white minute foci of necrosis are evident in the liver or spleen. Ulcers of the skin and palate tend to be randomly scattered, but are detected in a low percentage of casualties. xli

Box turtles with ranavirus infection show weakness, swollen eyelids, discharge from the nose and mouth, and the tongue and palate may show dull, white or thick, yellow plaques. At dissection, these plaques also may be found in the pharynx and esophagus. Occasionally, turtles may show ulcers on the bottom of their feet. Like ranaviral infections in tadpoles and salamanders, infection in box turtles spreads throughout the body affecting many organs including blood vessels. Additional research is needed to determine whether ranaviruses from box turtles and amphibians are identical and may be transmitted between the different genera and species. xlii

A single dead frog can be the result of many natural forces, but several dead frogs appearing at the same time is not natural, and may indicate disease. Ranavirus is most apparent during summer, especially on hot summer days, as it is most virulent at temperatures above 77°F. Infected frogs may appear slower and/or thinner than usual, and there may be bleeding or ulceration, however in some cases the dead frogs have no obvious symptoms.

Advice to Wildlife Rehabilitators

Rehabbers have the potential to be a big part of the problem, or a big part of the solution. It all depends on how you care for reptiles, amphibians(, and fish), and what you do with those in your care. Those working with animals potentially infected with ranavirus must realize that they are dealing with pathogens that are highly virulent to fish, amphibians, and reptiles, and must adopt suitable standards of biocontainment to prevent transmission to other captives or release in the wild.

At present, ranaviral infections appear to be limited to fish, amphibians and reptiles. The virus generally cannot be cultured at temperatures above 30 degrees C (86 degrees F), so it probably is not infectious to birds and mammals. At present, it is unclear how many strains or species of ranavirus are infecting and killing amphibians and turtles. Ranaviral outbreaks involving more than one class of vertebrates (i.e., fish and amphibians, or amphibians and reptiles) at a site are rarely reported in the wild, but such mortality events are of great interest ecologically.xliii

A study of 101 Eastern box turtles at three rehab centers and 39 free-ranging nonrehabilitation specimens found that box turtles from two of the three centers had ranavirus, whereas non of the free-ranging specimens were infected. The authors write “Wildlife (rehab) centers may be useful in detection of Ranavirus infection and may serve as a useful early monitoring point for regional diseaxlivse outbreaks.”

  • Any ectotherm – fish, amphibian, or reptile – is potentially a reservoir or carrier for ranavirus, even if it does not show any symptoms. To avoid infecting another ectotherm, always house each ectotherm in their own private tank, in which they may not make contact with each other. No turtle ponds or communal amphibian tanks – even briefly.
  • Your hands can spread contamination from one cage to the next. After handling any ectotherm or touching the inside of its tank or any water that it has made contact with, remove your gloves, wash your hands with soap, dry them thoroughly, and put on new gloves. Humans cannot get ranavirus, but it is near-certain that humans are effective transmitters.
  • After an ectotherm has completed their stay with you, for any reason, clean their cage thoroughly, and allow to dry for several days before re-use. Do not allow the wash water to enter any body of water, such as a stream or pond. Flush waste water down the toilet only if you are connected to a septic field – otherwise pour it on dry soil. (ranavirus will likely persist in sewer water. It might be killed at the water treatment plant if enough chlorinexlv is used – otherwise, ranavirus could enter the water supply.) Glutaraldehyde, bleach and artificially generated ultraviolet light are effective disinfectants. Ethyl alcohol is not an effective disinfectant for ranaviruses.xlvi
  • For any ectotherm admitted, be certain to capture exact details of where it was found. If it dies, contact the authorities (see Reporting, below) for further instructions. If you cannot deliver it same day to a lab for necropsy, place it in a plastic bag and freeze it. In your report, be sure to include the information on where it was found.
  • For laboratory diagnosis of ranaviral disease in dead animals, submit fresh or frozen carcases, fresh or frozen tissues (spleen or kidney is best), or tissues fixed in 10% formalin or 70% ethyl alcohol.xlvii

Reporting

Ongoing research by USGS scientists and others will help to determine whether die-offs due to ranavirus are contributing to population declines in turtles and amphibians. The USGS is very interested in receiving reports of amphibian and turtle die-offs, and potentially receiving specimens for diagnostic evaluation so they can get a more complete picture of ranavirus infection in these species.xlviii To report or request assistance for wildlife mortality events or health issues, visit http://www.nwhc.usgs.gov/mortality_events/reporting.jsp or contact Dr. Anne Ballmann, 608-270-2445, aballmann@usgs.gov; Dr. LeAnn White, 608-270-2491, clwhite@usgs.gov; Barb Bodenstein, 608-270-2447, bbodenstein@usgs.gov; Dr. Thierry Work, 808-792-9520, thierry_work@usgs.gov (Hawaii and Pacific Islands); or Jennifer Bradsby, 608-270-2443, jbradsby@usgs.gov (single mortality events nationwide).

Global Ranavirus Consortium

See http://fwf.ag.utk.edu/mgray/ranavirus/ranavirus.htm for a summary and list of scientists participating.

Second International Symposium on Ranaviruses

27 – 29 July 2013 concurrently with the International Conference of the Wildlife Disease Association in Knoxville, Tennessee, USA.

ListServ

Join the GRC (Global Ranavirus Consortium) List at http://listserv.utk.edu/cgi-bin/wa

Acknowledgments

I wish to thank the following for useful comments on earlier drafts of this paper: Amanda Duffus, Jacques Robert, Matt Gray, James Jancovich.

Bibliography

  • Acevedo–Whitehouse, K., and A.L.J. Duffus. 2009. Effects of Environmental Change on Wildlife Health. Philosophical Transactions of the Royal Society B: Biological Sciences. 364:3429-3438; DOI:10.1098/rstb.2009.0128.
  • Ahne, W., Bremont, M., Hedrick, R.P., Hyatt, A.D., and R.J. Whittington. 1997. Special topic review: Iridoviruses associated with epizootic haematopoietic necrosis (EHN) in aquaculture. World Journal of Microbiology and Biotechnology, 13:367-373.
  • Ahne, W., Ogawa, M., and H.J. Schlotfeldt. 1990. Fish viruses: Transmission and pathogenicity of an iscohedral cytoplasmic deoxyribovirus isolated from sheatfish (Silurus glanis). Journal of Veterinary Medicine, 37:187-190.
  • Alford, R.A., and S.J. Richards. 1999. Global amphibian declines: A problem in applied ecology. Annual Review of Ecology and Systematics, 30:133-165.
  • Allen L.J.S. An Introduction to Mathematical Biology. Prentice Hall; Upper Saddle River, NJ, USA: 2007. p. 368.
  • Allender, M.C., Fry, M.M., Irizarry, A.R., Craig, L., Johnson, A.J., and M. Jones. 2006. Intracytoplasmic inclusions in circulating leukocytes from an eastern box turtle (Terrapene carolina carolina) with iridoviral infection. Journal of Wildlife Diseases, 42:677-684.
  • Alves de Matos A.P., Caeiro M.F., Marschang R.E., Papp T., Soares C., Marçal M.R., Carretero M.A. Adaptation of ranaviruses from Peneda-Gerês National Park (Portugal) to Cell Cultures and Their Characterization. Microsc. Microanal. 2008;14:139–140.
  • Anderson R.M., May R.M. Population Biology of Infectious Disease. Nature. 1979;280:361–461.
  • Anderson, I.G., Prior, H.C., Rodwell, B.J., and G.O. Harris. 1993. Iridovirus-like virions in imported dwarf gouramis (Colisa lalia) with systemic amoebiasis. Australian Veterinary Journal, 70:66-67.
  • Anderson, R.M. and R.M. May. 1979. Population biology of infectious diseases: Part 1. Nature, 280:361-367.
  • April J. Johnson, Allan P. Pessier, James F. X. Wellehan, April Childress, Terry M. Norton, Nancy L. Stedman, David C. Bloom, William Belzer, Valorie R. Titus,8, Robert Wagner, Jason W. Brooks, Jeffrey Spratt and Elliott R. Jacobson ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. jwildlifedis October 1, 2008 vol. 44 no. 4 851-863
  • Aquatic Animal Health Code (2011) Available online: http://www.oie.int/international-standard-setting/aquatic-code/access-online/ (accessed on 31 October 2011).
  • Araújo, M.B., Thuiller, W., and R.G. Pearson. 2006. Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography, 33:1712-1728.
  • Ariel E. James Cook University; Queensland, Australia: 1997. Pathology and Serological Aspects of Bohle Iridovirus Infections in Six Selected Water-Associated Reptiles in North Queensland. Ph.D. Thesis,
  • Ariel E., Kielgast J., Svart H.E., Larsen K., Tapiovaara H., Bang Jensen B., Holopainen R. ranavirus in Wild Edible Frogs, Pelophylax kl. esculentus in Denmark. Dis. Aquat. Organ. 2009;85:7–14.
  • Ariel E., Kielgast J., Svart H.E., Larsen K., Tapiovaara H., Bang Jensen B., Holopainen R. ranavirus in Wild Edible Frogs, Pelophylax kl. Esculentus, in Denmark. Dis. Aquat. Organ.2009;85:7–14.
  • Ariel, E., Kielgast, J., Svart, H.E., Larsen, K., Tapiovaara, H., Jensen, B.B., and R. Holopainene. 2009. ranavirus in wild edible frogs Pelophylax kl. esculentus in Denmark. Diseases of Aquatic Organisms, 85:7-14.
  • Balseiro A., Dalton K.P., Cerro1 A., Marquez I., Cunningham A.A., Parra F., Prieto J.M., Casais R. Pathology, Isolation and Molecular Characterisation of a ranavirus from the Common Midwife ToadAlytes obstetricans on the Iberian Peninsula. Dis. Aquat. Organ. 2009;84:95–104.
  • Balseiro A., Dalton K.P., Del Cerro A., Marquez I., Parra F., Prieto J.M., Casias R. Outbreak of Common Midwife Toad Virus in Alpine Newts (Mesotriton alpestris cyreni) and Common Midwife Toads (Alytes obstetricans) in Northern Spain: Comparative Pathological Study of an Emerging ranavirus. Vet. J. 2010;186:256–258.
  • Balseiro, A., Dalton, K.P., del Cerr, A., Marquez, I., Parra, F., Prieto, J. M., and R. Casais. In Press. Outbreak of common midwife toad virus in alpine newts (Mesotriton alpestris cyreni) and common midwife toad (Alytes obstetricans) in Northern Spain: A comparative pathological study of an emerging ranavirus. The Veterinary Journal. DOI:10.1016/j.tvjl.2009.07.038
  • Balseiro, A., Dalton, K.P., Marquez, I., Cunningham, A.A., Parra, F., Prieto, J. M., and R. Casais. 2009. Pathology, isolation and molecular characterization of a ranavirus from the common midwife toad Alytes obstetricans on the Iberian peninsula. Diseases of Aquatic Organisms, 84:95-104.
  • Bang Jensen B.B., Ersboll A.K., Ariel E. Susceptibility of Pike, Esox lucius, to a Panel of ranavirus Isolates. Dis. Aquat. Organ. 2009;83:169–179.
  • Beck, B. H., R. S. Bakal, C. J. Brunner, and J. M. Grizzle. 2006. Virus distribution and signs of disease after immersion exposure to largemouth bass virus. Journal of Aquatic Animal Health 18(3):176-183.
  • Benetka, V., E. Grabensteiner, M. Gumpenberger, C. NeuBauer, B. Hirschmuller, and K. Mostl First report of an iridovirus (Genus ranavirus) infection in a Leopard tortoise (Geochelone pardalis pardalis) Vet. Med. Austria / Wien. Tierärztl. Mschr. 94 (2007), 243 – 248 http://www.schildkroeten-sfb.ch/fileadmin/docs/news/729-pantherschildkroete.pdf
  • Benetka, V., Grabensteiner, E., Gumpenberger, M., Neubauer, C., Hirschmüller, H., and K. Möstl. 2007. First report of an iridovirus (Genus ranavirus) in a leopard tortoise (Geochelone pardalis pardalis). Wiener Tierärztliche Monatsschrift, 94:243-248.
  • Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt, A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Marantelli, G., and H. Parkes. Chytridiomycosis causes amphibian mortality associated with populations declines in the rain forests of Australia and central America. Proceedings of the National Academy of Sciences, USA, 95:9013-9036.
  • Berry, E.S., Shea, T.B., and J. Gabliks. 1983. Two iridovirus isolates from Carassius auratus (L.). Journal of Fish Diseases, 6:501-510.
  • Blahak S., Uhlenbrok C. ranavirus infections in European terrestrial tortoises in Germany. Proceedings of the 1st International Conference on Reptile and Amphibian Medicine; Munich, Germany. 4–7 March 2010; pp 17–23
  • Blaustein A.R., Romansic J.M., Kiesecker J.M., Hatch A.C. Ultraviolet Radiation, Toxic Chemicals, and Amphibian Population Declines. Diversity and Distribution. 2003;9:123–140.
  • Bloch, B., and J.L. Larsen. 1993. An iridoviruse-like agent associated with systemic infection in cultured turbot Scophthalmus maximus fry in Denmark. Diseases of Aquatic Organisms, 15:235-240.
  • Bolker B.M., Castro F., Storfer A., Mech S., Harvey E., Collins J.P. Disease as a Selective Force Precluding Widespread Cannibalism: A Case Study of an Iridovirus of Tiger SalamandersAmbystoma tigrinum. Evol. Ecol. 2008;14:213–224.
  • Bollinger T.K., Mao J., Schock D., Brigham R.M., Chinchar V.G. Pathology, Isolation, and Preliminary Molecular Characterization of a Novel Iridovirus from Tiger Salamanders in Saskatchewan. J. Wildl. Dis. 1999;35:413–429.
  • Bollinger, T.K., Mao, J., Schock, D., Brigham, R.M., and V.G. Chinchar. 1999. Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. Journal of Wildlife Diseases, 35:413-429.
  • Bosch, J., Martínez-Solano, I, and M. García-París. 2001. Evidence of a chytrid fungus involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation, 97:331-337.
  • Bossart, G.D. Emerging diseases in marine mammals: From dolphins to manatees. Microbe, 2:544-548.
  • Brunner J.L., Barnett K.E., Gosier C.J., McNulty S.A., Rubbo M.J., Kolozsvary M.B. ranavirus Infection in Die-Offs of Vernal Pool Amphibians in New York, USA. Herpetol. Rev. 2011;42:76–79.
  • Brunner J.L., Richards K., Collins J.P. Dose and Host Characteristics Influence Virulence of ranavirus Infections. Oecologia. 2005;144:399–406.
  • Brunner J.L., Schock D.M., Collins J.P. Transmission Dynamics of the Amphibian ranavirusAmbystoma tigrinum Virus. Dis. Aquat. Organ. 2007;77:87–95.
  • Brunner J.L., Schock D.M., Davidson E.W., Collins J.P. Intraspecific Reservoirs: Complex Life History and the Persistence of a Lethal ranavirus. Ecology. 2004;85:560–566.
  • Brunner, J.L., Richards, K., and J.P. Collins. 2005. Dose and host characteristics influence virulence of ranavirus infections. Oecologica, 144:399-406.
  • Brunner, J.L., Schock, D.M., Davidson, E.W., and J.P. Collins. 2004. Intraspecific reservoirs: Complex life history and the persistence of a lethal ranavirus. Ecology, 85:560-566.
  • Bryan L.K., Baldwin C.A., Gray M.J., Miller D.L. Efficacy of Select Disinfectants at Inactivating ranavirus. Dis. Aquat. Organ. 2009;84:89–94.
  • Burton E.C., Gray M.J., Schmutzer A.C., Miller D.L. Differential Responses of Postmetamorphic Amphibians to Cattle Grazing in Wetlands. J. Wildl. Manage. 2009;73:269–277.
  • Burton E.C., Miller D.L., Styer E.L., Gray M.J. Amphibian Ocular Malformation Associated with Frog Virus 3. Vet. J. 2008;177:442–444.
  • Caipang C.M, Takano T., Hirono I., Aoki T. Genetic Vaccines Protect Red Seabream, Pagrus major, Upon Challenge with Red Sea Bream Iridovirus (RSIV) Fish Shellfish Immunol. 2006;21:130–138.
  • Carey C.D., Cohen N., Rollins-Smith L. Amphibian Declines: An Immunological Perspective.Dev. Comp. Immunol. 1999;23:459–472.
  • Charbonneau, M. 2006. Amphibian declines: Pesticide immunotoxicity and chytridiomycosis in larval Rana catesbeiana and ranaviral disease in Rana sylvatica tadpoles of central Ontario. MSc. Thesis, Watershed Ecosystems Graduate Program, Trent University, Peterborough, Ontario.
  • Che, J., Pang, J., Zhao, H., Wu., G., Zhao, E., and Y. Zhang. 2007. Phylogeny of Raninae (Anura:Randiae) inferred from mitochondrial and nuclear sequences. Molecular Phylogenetics and Evolution, 43:1-13.
  • Chen G., Ward B.M., Yu K.H., Chinchar V.G., Robert J. Improved Knockout Methodology Reveals That Frog Virus 3 Mutants Lacking either the 18K Immediate-Early Gene or the Truncated vIF-2{alpha} Gene Are Defective for Replication and Growth In Vivo. J. Virol. 2011;85:11131–11138.
  • Chen, Z., Zheng, J., and Y. Jiang. 1999. A new iridovirus isolated from soft-shell turtle. Virus Research, 63:147-151.
  • Chinchar V.G. ranaviruses (Family Iridoviridae): Emerging Cold-Blooded Killers. Arch. Virol.2002;147:447–470.
  • Chinchar, V.G. 2002. ranaviruses (family Iridoviridae): Emerging cold-blooded killers. Archives of Virology, 147:447-470.
  • Chinchar, V.G., Hyatt, A., Miyazaki, T., and T. Williams. 2009. Family Iridoviridae: Poor viral relations no longer. Current Topics in Microbiology and Immunology, 328: 123-170.
  • Clark H.F., Brennan J.C., Zeigel R.F., Karzon D.T. Isolation and Characterizatoin of Viruses from the Kidneys of Rana pipiens with Renal Adenocarcinoma before and after Passage in the Red Eft (Triturus viridescens) J. Virol. 1968;2:629–640.
  • Clark, H.F., Brennan, J.C., Zeigel, R.F., and D.T. Karzon. 1968. Isolation and characterization of viruses from the kidneys of Rana pipiens with renal adenocarcinoma before and after passage in the red eft (Triturus viridescens). Journal of Virology, 2:629-640.
  • Collins J.P., Zerba K.E., Sredl M.J. Shaping Intraspecific Variation: Development, Ecology and the Evolution of Morphology and Life History Variation in Tiger Salamanders. Genetica. 1993;89:167–183.
  • Converse K.A., Green D. Diseases of Salamanders. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 117–130. Chapter 9,
  • Converse K.A., Green D.E. Diseases of Tadpoles. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 72–88. Chapter 7,
  • CSIRO Cane toad research. December 8, 2008 | Updated October 14 2011 http://www.csiro.au/Outcomes/Safeguarding-Australia/Cane-Toad-Research.aspx
  • Cullen B.R., Owens L. Experimental Challenge and Clinical Cases of Bohle Iridovirus (BIV) in Native Australian Anurans. Dis. Aquat. Organ. 2002;49:83–92.
  • Cullen, B.R., and L. Owens. 2002. Experimental challenge and clinical cases of Bohle iridovirus (BIV) in native Australian anurans. Diseases of Aquatic Organisms, 49:83-92.
  • Cullen, B.R., Owens, L., and R.J. Whittington. 1995. Experimental infection of Australian anurans (Limnodynastes terraereginae and Litoria latopalmata) with Bohle iridovirus. Diseases of Aquatic Organisms, 23:83-92.
  • Cunningham A.A., Langton T.E.S., Bennett P.M., Drury S.E.N., Gough R.E., Kirkwood K.E. Unusual Mortality Associated with Poxvirus-Like Particles in Frogs (Rana temporaria) Vet. Rec. 1993;133:141–142.
  • Cunningham A.A., Langton T.E.S., Bennett P.M., Lewin J.F., Drury S.E.N., Gough R.E., MacGregor S.K. Pathological and Microbiological Findings from Incidents of Unusual Mortality of the Common Frog (Rana temporaria) Philos. Trans. R. Soc. Lon. B. Biol. Sci. 1996;351:1539–1557.
  • Cunningham A.A., Tems C.A., Russell P.H. Immunohistochemical Demonstration of ranavirus Antigen in the Tissues of Infected Frogs (Rana temporaria) with Systemic Haemorrhagic or Cutaneous Ulcerative Disease. J. Comp. Pathol. 2008;138:3–11.
  • Cunningham, A.A. 2001. Investigations into mass mortality events of the common frog (Rana temporaria) in Britain: Epidemiology and Aetiology. PhD Thesis, Royal Veterinary College, University of London.
  • Cunningham, A.A., Hyatt, A.D., Russell, P., and P.M. Bennett. 2007a. Emerging epidemic diseases of frogs in Britain are dependant on the source of ranavirus agent and the route of exposure. Epidemiology and Infection, 135:1200-1212.
  • Cunningham, A.A., Hyatt, A.D., Russell, P., and P.M. Bennett. 2007b. Experimental transmission of a ranavirus disease of common toads (Bufo bufo) to common frogs (Rana temporaria). Epidemiology and Infection, 135:1213-1216.
  • Cunningham, A.A., Langton, T.E.S., Bennett, P.M., Drury, S.E.N., Gough, R.E., and J.K. Kirkwood. 1993. Unusual mortality associated with poxvirus-like particles in frogs (Rana temporaria). Veterinary Record, 133:141-142.
  • Cunningham, A.A., Langton, T.E.S., Bennett, P.M., Lewin, J.F., Drury, S.E.N., Gough, R.E., and S.K. MacGregor. 1995. Investigations into unusual mortalities of the common frog (Rana temporaria) in Britain. In F. Zwart, and G. Matz (Ed.), Fifth international colloquium on the pathology of reptiles and amphibians (pp. 19-27). The Netherlands: Alphen ann den Rijn.
  • Cunningham, A.A., Langton, T.E.S., Bennett, P.M., Lewin, J.F., Drury, S.E.N., Gough, R.E., and S.K. MacGregor. 1996. Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philosophical Transactions of the Royal Society, London B, 351:1539-1557.
  • Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D., Green, D.E., and R. Speare. 1999. Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases, 5:735-748.
  • Daszak, P., Cunningham, A.A., and A.D. Hyatt. 2003. Infectious disease and amphibian population declines. Diversity and Distribution, 9:141-150.
  • Daszak, P., Scott, D.E., Kilpatrick, A.M., Faggioni, C., Gibbons, J.W., and D. Porter. 2005. Amphibian population declines at Savannah River site are linked to climate, not chytridiomycosis. Ecology, 86:3232-3237.
  • Davidson S.R.A., Chambers D.L. ranavirus Prevalence in Amphibian Populations of Wise County, Virginia, USA. Herpetol. Rev. 2011;42:214–215.
  • Day, T. 2002. The evolution of virulence in vector-borne and directly transmitted parasites. Theoretical Population Biology, 62:199-213.
  • Day, T. 2003. Virulence evolution and the timing of disease life-history events. Trends in Ecology and Evolution, 18:113-118.
  • de Castro, F., and B. Bolker. 2005. Mechanisms of disease-induced extinction. Ecology Letters, 8:117-126.
  • de Matos AP, Caeiro MF, Papp T, Matos BA, Correia AC, Marschang RE. New viruses from Lacerta monticola (Serra da Estrela, Portugal): further evidence for a new group of nucleo-cytoplasmic large deoxyriboviruses. Microsc Microanal. 2011 Feb;17(1):101-8. Epub 2010 Dec 8.
  • Dell, R.B., Holleran, S., and R. Ramakrishnan. 2002. Sample size determination. ILAR Journal, 43:207-213.
  • Docherty D.E., Meteyer C.U., Wang J., Mao J., Case S.T., Chinchar V.G. Diagnostic and Molecular Evaluation of Three Iridovirus-Associated Salamander Mortality Events. J. Wildl. Dis. 2003;39:556–566.
  • Docherty, D.E., Meteyer, C.U., Wang, J., Mao, J., Case, S.T., and V.G. Chinchar. 2003. Diagnostic and molecular evaluation of three iridovirus-associated salamander mortality events. Journal of Wildlife Diseases, 39:556-566.
  • Drennan J.D., LaPatra S.E., Siple J.T., Ireland S., Cain K.D. Transmission of White Sturgeon Iridovirus in Kootenai River White Sturgeon Acipenser transmontanus. Dis. Aquat. Organ.2006;70:37–45.
  • Driskell E.A., Miller D.L., Swist S.L., Gyimesi Z.S. PCR Detection of ranavirus in Adult Anurans from the Louisville Zoological Garden. J. Zoo Wildl. Med. 2009;40:559–563.
  • Drury S.E.N., Gough R.E., Cunningham A.A. Isolation of an Iridovirus-Like Agent from Common Frogs (Rana temporaria) Vet. Rec. 1995;137:72–73.
  • Drury, S.E.N., Gough, R.E. and A.A. Cunningham. 1995. Isolation of an iridoviruslike agent from common frogs (Rana temporaria). Veterinary Record, 137:72- 73.
  • Duffus A.L.J., Cunningham A.A. Major disease threats to European amphibians. Herpetol. J.2010;20:117–127.
  • Duffus A.L.J., Pauli B.D., Wozney K., Brunetti C.R., Berrill M. Frog Virus 3-Like Infections in Aquatic Amphibian Communities. J. Wildl. Dis. 2008;44:109–120.
  • Duffus ALJ. Queen Mary: University of London, UK; 2010. ranavirus Ecology in Common Frogs (Rana temporaria) from the United Kingdom: Transmission Dynamics, Alternate Hosts and Host-Strain Interactions. Ph.D. Thesis,
  • Duffus, A.L.J. 2006. Field monitoring, transmission and influences of immunosuppression on ranaviral infections in native North American amphibian species. MSc. Thesis, Watershed Ecosystems Graduate Program, Trent University, Peterborough, Ontario.
  • Duffus, A.L.J., Pauli, B.D., Wozney, K., Brunetti, C.R., and M. Berrill. 2008. Frog virus 3-like infections in aquatic amphibian communities. Journal of Wildlife Diseases, 44:109-120.
  • Dutch Wildlife Health Centre 2010 ranavirus associated mass mortality of water frogs, Dwingeldeveld, september 2010. http://www.dwhc.nl/HomeUK/Species/Amphibians/Waterfrogs/A_ranainf.html
  • Echaubard P., Little K., Pauli B., Lesbarrères D. Context-Dependent Effects of Ranaviral Infection on Northern Leopard Frog Life History Traits. PLoS One. 2010;5:e13723.
  • Evans, A.S. 1976. Causation and Disease: The Henle-Koch Postulates Revisited. The Yale Journal of Biology and Medicine, 49:175-195.
  • Ewald P.W., Mims C.A., Lachmann P.J., Hughes A.L., Gillett J.D., Parker C.E. Evolution of Mutation Rate and Virulence among Human Retroviruses. Philos. Trans. R. Soc. London (Biol.)1994;346:333–343.
  • Fellers, G.M., Green, D.E., and J.E. Longcore. 2001. Oral chytridiomycosis in the mountain yellow-legged frog (Rana mucosa). Copeia, 2001:945-953.
  • Fijan N., Matasin Z., Petrinec Z., Valpotic I., Zillenberg L.O. Isolation of an Iridovirus-Like Agent from the Green Frog (Rana esculenta L.) Vet. Arch. 1991;61:151–158.
  • Fijan, N., Matašin, Z., Petrinec, Z., Valpotić, I., and L.O. Zwillenberg. 1991. Isolation of an iridovirus-like agent from the green frog (Rana esculenta L.). Veterinarski Archives, 61:151-158.
  • Forson D., Storfer A. Effects of Atrazine and Iridovirus Infection on Survival and Life History Characteristics in Long-Toed Salamanders Ambystoma macrodactylum. Environ. Toxicol. Chem.2006;25:168–173.
  • Forson D.D., Storfer A. Atrazine Increases ranavirus Susceptibility in the Tiger SalamanderAmbystoma tigrinum. Ecol. Appl. 2010;16:2325–2332.
  • Forzán M. Canadian Cooperative Wildlife Health Centre, Charlottetown, Prince Edward Island, Canada. 2011. Unpublished work,
  • Forzán, Gahl and Pauli, Tadpole die-offs in New Brunswick due to ranavirus, summer 2009 December 15, 2009 http://atlantic.ccwhc.ca/?p=327
  • Fox S.F., Greer A.L., Tores-Cervantes R., Collins J.P. First Case of ranavirus-Associated Morbidity and Mortality in Natural Populations of the South American Frog Atelognathus patagonicus.Dis. Aquat. Organ. 2006;72:87–92.
  • Frank, S.A. 1996. Models of parasite virulence. The Quarterly Review of Biology, 71:37-78.
  • Fraser, W.A., Keefe, T.J., and B. Bolon. 1993. Isolation of an iridovirus from farmraised gouramis (Trichogaster trichopterus) with fatal disease. Journal Veterinary Diagnostic Investigation, 5:250-253.
  • Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B., de Sá, R.O., Channing, A., Wilkinson, M., Donnellan, S.C., Raxworthy, C.J., Campbell, J.A., Blotto, B,L., Moler, P., Drewes, R.C., Nussbaum, R.A., Lynch, J.D., Green, D.M., and W.C. Wheeler. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History, 297:1-370.
  • Gahl M. 2011. Bates College, Lewiston, ME, USA. Unpublished work,
  • Gahl M.J., Calhoun A.J.K. Landscape setting and Risk of ranavirus Mortality Events. Biol. Cons.2008;141:2679–2689.
  • Gahl M.K., Calhoun A.J.K. The Role of Multiple Stressors in ranavirus-Caused Amphibian Mortalities in Acadia National Park Wetlands. Can. J. Zool. 2010;88:108–118.
  • Galli L., Pereira A., Márquez A., Mazzoni R. ranavirus Detection by PCR in Cultured Tadpoles (Rana catesbeiana Shaw, 1802) from South America. Aquaculture. 2006;257:78–82.
  • Gantress J., Maniero G.D., Cohen N., Robert J. Development and Characterization of a Model System to Study Amphibian Immune Responses to Iridoviruses. Virology. 2003;311:254–262.
  • Geng Y., Wang K.Y., Zhou Z.Y., Li C.W., Wang J., He M., Yin Z.Q., Lai W.M. First Report of a ranavirus Associated with Morbidity and Mortality in Farmed Chinese Gian Salamanders (Andrias davidianus) J. Comp. Pathol. 2011;145:95–102.
  • Geng, Y., K.Y. Wang, Z.Y. Zhou, C.W. Li, J. Wang, M. He, Z.Q. Yin, W.M. Lai First Report of a ranavirus Associated with Morbidity and Mortality in Farmed Chinese Giant Salamanders (Andrias davidianus). Journal of Comparative Pathology Volume 145, Issue 1, July 2011, Pages 95-102. http://www.sciencedirect.com/science/article/pii/S0021997510003427
  • Gibbons, M.M., and T.K. McCarthy. 1984. Maturation and survival of frogs Rana temporaria L. Holartic Ecology, 4:419-427.
  • Gibson-Kueh, S., Netto, P., Ngoh-Lim, G.H., Chang, S.F., Ho, L.L., Qin, Q.W., Chua, F.H.C., Ng, M.L., and H.W. Ferguson. 2003. The pathology of systemic irdidoviral disease in fish. Journal of Comparative Pathology, 129:111-119.
  • Glenney J.W., Julian J.T., Quartz W.M. Preliminary Amphibian Health Survey in the Delaware Water Gap National Recreation Area. J. Aquat. Anim. Health. 2010;22:102–114.
  • Global ranavirus Consortium. Available online:http://fwf.ag.utk.edu/mgray/ranavirus/ranavirus.htm (accessed on 31 October 2011).
  • Go, J., Lancaster, M., Deece, K., Dhunyel, O., and R. Whittington. 2006. The molecular epidemiology of iridovirus in Murray cod (Maccullochella peelii peelii) and dwarf gourami (Colisa lalia) from distant biogeographical regions suggests a link between trade in ornamental fish and emerging iridoviral disease. Molecular and Cellular Probes, 20:212-222.
  • Goater C. University of Lethbridge, Lethbridge, Alberta, Canada. 2011. Unpublished work,
  • Gobbo F., Cappellozza E., Pastore M.R., Bovo G. Susceptibility of Black Bullhead, Ameiurus melas, to a Panel of ranavirus Isolates. Dis. Aquat. Organ. 2010;90:167–174.
  • Goldberg, T. L. 2002. Largemouth bass virus: an emerging problem for warmwater fisheries? Pp. 411 – 416 in D. P. Philipp, ed. Black bass: ecology, conservation, and management. Proceedings of the American Fisheries Society Symposium 31, St. Louis, Missouri, USA, August 21 – 24, 2000. 724 pp.
  • Goldberg, T. L., D. A. Coleman, E. C. Grant, K. R. Inendino, and D. P. Philipp. 2003. Strain variation in an emerging iridovirus of warm-water fishes. Journal of Virology 77:812-8818.
  • Gosner, K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16:183-190.
  • Granoff A., Came P.E., Rafferty K.A. The Isolation and Properties of Viruses from Rana pipiens: Their Possible Relationship to the Renal Adenocarcinoma of the Leopard Frog. Ann. NY Acad. Sci.1965;126:237–255.
  • Grant, E. C., D. P. Philipp, K. R. Indendino, and T. L. Goldberg. 2003. Effects of temperature on the susceptibility of largemouth bass to largemouth bass virus. Journal of Aquatic Animal Health 15(3):215-220.
  • Grant, E. C., K. R. Inendino, W. J. Love, D. P. Philipp, and T. L. Goldberg. 2005. Effects of practices related to catch-and-release angling on mortality and viral transmission in juvenile largemouth bass infected with largemouth bass virus. Journal of Aquatic Animal Health 17(4):315-322.
  • Gray M., Miller D., Sousa M. 2011. University of Tennessee, Knoxville, TN, USA. Unpublished work,
  • Gray M.J., Miller D.L., Hoverman J.T. Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Organ. 2009;87:243–266.
  • Gray M.J., Miller D.L., Hoverman J.T. First Report of ranavirus Infecting Lungless Salamanders.Herpetol. Rev. 2009;40:316–319.
  • Gray M.J., Miller D.L., Schmutzer A.C., Baldwin C.A. Frog Virus 3 Prevalence in Tadpole Populations at Cattle-Access and Non-Access Wetlands in Tennessee, U.S.A. Dis. Aquat. Organ.2007;77:97–103.
  • Gray, MJ; Miller, DL; Hoverman, JT (2009). “Ecology and pathology of amphibian ranaviruses”. Diseases of Aquatic Organisms 87 (3): 243–266.
  • Green D.E., Converse K.A. Diseases of Frogs and Toads. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 89–117. Chapter 8,
  • Green D.E., Converse K.A., Schrader A.K. Epizootiology of Sixty-Four Amphibian Morbidity and Mortality Events in the USA, 1996–2001. Ann. NY Acad. Sci. 2002;969:323–339.
  • Green D.E., Gray M.J., Miller D.L. Disease Monitoring and Biosecurity. In: Dodd C.K., editor.Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press; New York, NY, USA: 2010. pp. 481–505. Chapter 26,
  • Green D.E., Ip H.S. 2011. US Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA. Unpublished work,
  • Green, D.E., Converse, K.A., and A.K. Schrader. 2002. Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Annals of the New York Academy of Science, 969:323-339.
  • Greer A.L., Berrill M., Wilson P.J. Five Amphibian Mortality Events Associated with ranavirus Infection in South Central Ontario, Canada. Dis. Aquat. Organ. 2005;67:9–14.
  • Greer A.L., Briggs C.I., Collins J.P. Testing a Key Assumption of Host-Pathogen Theory: Density and Disease Transmission. Oikos. 2008;117:1667–1673.
  • Greer A.L., Brunner J.L., Collins J.P. Spatial and Temporal Patterns of Ambystoma tigrinum Virus (ATV) Prevalence in Tiger Salamanders Ambystoma tigrinum nebulosum. Dis. Aquat. Organ.2009;85:1–6.
  • Greer A.L., Collins J.P. Habitat Fragmentation as a Result of Biotic and Abiotic Factors Controls Pathogen Transmission Throughout a Host Population. J. Anim. Ecol. 2008;77:364–369.
  • Greer, A.L., Berrill, M., and P.J. Wilson. 2005. Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Diseases of Aquatic Organisms, 67:9-14.
  • Grizzle, J. M. and C. J. Brunner. 2003. Review of largemouth bass virus. Fisheries (Bethesda) 28(11):10-14. Grizzle, J. M., I. Altinok, and A. D. Noyes. 2003. PCR method for detection for largemouth bass virus. Diseases of Aquatic Organisms 54(1):29-33.
  • Grizzle, J. M., I. Altinok, W. A. Fraser, and R. Francis-Floyd. 2002. Diseases of Aquatic Organisms 50(3):233-235. Hanson, L. A., L. Petrie-Hanson, K. O. Meals, V. G. Chinchar, and M. Rudis. 2001. Persistence of largemouth bass virus infection in a northern Mississippi reservoir after a die-off. Journal of Aquatic Animal Health 13:27-34.
  • Gruia-Gray J., Desser S.S. Cytopathological Observations and Epizootiology of Frog Erythrocytic Virus in Bullfrogs (Rana catesbeiana) J. Wildl. Dis. 1992;28:34–41.
  • Haislip N.A., Gray M.J., Hoverman J.T., Miller D.L. Development and Disease: How Susceptibility to an Emerging Pathogen Changes through Anuran Development. PLoS One. 2011;6:e22307.
  • Harp E.M., Petranka J.W. ranavirus in Wood Frogs (Rana sylvatica): Potential Sources of Transmission within and between Ponds. J. Wildl. Dis. 2006;42:307–318.
  • Harp, E.M., and J.W. Petranka. 2006. ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases, 42:307-318.
  • Hedrick, R.P., and T.S. McDowell. 1995. Properties of iridoviruses from ornamental fish. Veterinary Research, 26:523-427.
  • Hedrick, R.P., Groff, J.M., McDowell, T., and W.H. Wingfield. 1990. An iridovirus infection of the integument of the white sturgeon Acipenser transmontanus. Diseases of Aquatic Organisms, 8:39-44.
  • Hengstberger, S.G., Hyatt, A.D., Speare, R., and B.E.H. Coupar. 1993. Comparison of epizootic haematopoietic necrosis and Bolhe iridoviruses, recently isolated Australian iridoviruses. Diseases of Aquatic Organisms, 15:93-107.
  • Holopainen R., Honkanenb J., Bang-Jensen B., Ariel E., Tapiovaaraa H. Quantitation of ranaviruses in Cell Culture and Tissue Samples. J. Virol. Methods. 2011;171:225–233.
  • Houlahan, J.E., Findlay, C.S., Schmidt, B.R., Meyer, A.H., and S.L. Kuzmin. 2000. Quantitative evidence for global amphibian declines. Nature, 440:752-755.
  • Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth. 2011 doi: 10.1007/s10393-011-0717-7. [Cross Ref]
  • Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. Widespread occurrence of ranavirus in pond-breeding amphibian populations. EcoHealth. 2012 in press,
  • Hoverman J.T., Gray M.J., Miller D.L. Anuran Susceptibilities to ranavirus: The Role of Species Identity, Exposure Route, and Novel Virus Isolates. Dis. Aquat. Organ. 2010;89:97–107.
  • Hsieh C.Y. National Pingtung University of Science and Technology, Pingtung, Taiwan. 2011. Unpublished work,
  • Huang, Y., Huang, X., Liu, H., Gong, J., Ouyang, Z., Cui, H., Cao, J., Zhao, Y., Wang, X., Jiang, Y., and Q. Qin. 2009. Complete sequence determination of a novel reptile iridovirus isolated from soft-shelled turtle and evolutionary analysis of Iridoviridae. BMC Genomics, 10:224. DOI: 10.1186/1471-2164- 10-224.
  • Huelsenbeck J.P., Rannala B., Yang Z. Statistical Tests of Host-Parasite Conspeciation.Evolution. 1997;51:410–419.
  • Hunter W., Sinisterra X.H., McKenxie C.L., Shatters R.G. Iridovirus Infection and Vertical Transmission in Citrus Aphids. Proc. Florida State Hort. Soc. 2001;114:70–72.
  • Hyatt A.D., Gould A.R., Zupanovic Z., Cunningham A.A., Hengstberger S., Whittington R.J., Kattenbelt J., Coupar B.E.H. Comparative Studies of Piscine and Amphibian Iridoviruses. Arch. Virol.2010;145:301–331.
  • Hyatt, A.D., Gould, A.R., Zupanovic, Z., Cunningham, A.A., Hengstberger, S., Whittington, R.J., Kattenbelt, J., and B.E.H. Coupar. 2000. Comparative studies of piscine and amphibian iridoviruses. Archives of Virology, 145:301- 331.
  • Hyatt, A.D., Williamson, M., Coupar, B.E.H., Middleton, D., Hengstberger, S., Gould, A.R., Selleck, P., Wise, T.G., Kattenbelt, J., Cunningham, A.A., and J. Lee. 2002. First identification of a ranavirus from green pythons (Chondropython viridis). Journal of Wildlife Diseases, 38:239-252.
  • Inendino, K. R., -E. C .Grant, D. P. Philipp, and T. L. Goldberg. 2005. Effects of factors related to water quality and population density on the sensitivity of juvenile largemouth bass to mortality induced by viral infection. Journal of Aquatic Animal Health 17(4):304-314.
  • Jacques Robert, Erica George, Francisco De Jesús Andino, Guangchun Chen. Waterborne infectivity of the ranavirus frog virus 3 in Xenopus laevis. Virology. 2011 Sep 1;417(2): 410-7
  • Jancovich J.K., Bremont M., Touchman J.W., Jacobs B.L. Evidence for Multiple Recent Host Species Shifts among the ranaviruses (Family Iridoviridae) J. Virol. 2010;84:2634–2647.
  • Jancovich J.K., Davidson E.W., Morado J.F., Jacobs B.L., Collins J.P. Isolation of a Lethal Virus from the Endangered Tiger Salamander Ambystoma tigrinum stebbinsi. Dis. Aquat. Organ.1997;31:161–167.
  • Jancovich J.K., Davidson E.W., Parameswaran N., Mao J., Chinchar V.G., Collins J.P., Jacobs B.L., Storfer A. Evidence for Emergence of an Amphibian Iridoviral Disease because of Human-Enhanced Spread. Mol. Ecol. 2005;14:213–224.
  • Jancovich J.K., Davidson E.W., Seiler A., Jacobs B.L., Collins J.P. Transmission of the Ambystoma tigrinum Virus to Alternative Hosts. Dis. Aquat. Organ. 2001;46:159–163.
  • Jancovich J.K., Jacobs B.L. Innate Immune Evasion Mediated by the Ambystoma tigrinum Virus Eukaryotic Translation Initiation Factor 2{alpha} Homologue. J. Virol. 2011;85:5061–5069.
  • Jancovich J.K., Mao J., Chinchar V.G., Wyatt C., Case S.T., Kumar S., Valente G., Subramanian S., Davidson E.W., Collins J.P., Jacobs B.L. Genomic Sequence of a ranavirus (Family Iridoviridae) Associated with Salamander Mortalities in North America. Virology. 2003;316:90–103.
  • Jancovich, J.K., Davidson, E.W., Morado, J.F., Jacobs, B.L., and J.P. Collins. 1997. Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi. Diseases of Aquatic Organisms, 31:161-167.
  • Jancovich, J.K., Davidson, E.W., Seiler, A., Jacobs, B.L., and J.P. Collins. 2001. Transmission of the Ambystoma tigrinum virus to alternative hosts. Diseases of Aquatic Organisms, 46:159-163.
  • Jancovich, James K., Michael Bremont, Jeffrey W. Touchman, and Bertram L. Jacobs Evidence for Multiple Recent Host Species Shifts among the ranaviruses (Family Iridoviridae) First published December 2009, doi: 10.1128/JVI.01991-09J. Virol. March 2010 vol. 84 no. 62636-2647
  • Jensen, Ersbøll, and Ariel Susceptibility of pike Esox lucius to a panel of ranavirus isolates. Diseases Of Aquatic Organisms 83 2009 (3) page 169-179
  • Jensen, Halopainen, Tapiovaara, and Ariel Susceptibility of pike-perch Sander lucioperca to a panel of ranavirus isolates Aquaculture 313, 2011 (1-4) page 24-30
  • Johnson A.J., Pessier A.P., Jacobson E.R. Experimental Transmission and Induction of Ranaviral Disease in Western Ornate Box Turtles (Terrapene ornate ornate) and Red-eared Sliders (Trachemys scripta elegans) Vet. Path. 2007;44:285–297.
  • 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 May;44(3):285-97.
  • Johnson, A.J., Pessier, A.P., and E.R. Jacobson. 2007. Experimental transmission and induction of ranaviral disease in western ornate box turtles (Terrapene ornate ornate) and red-eared sliders (Trachemys scripta elegans). Veterinary Pathology, 44:285-297.
  • Johnson, A.J., Pessier, A.P., Wellehan, J.F., Childress, A., Norton, T.M., Stedman, N.L. Bloom, D.C., Belzer, W., Titus, V.R., Wagner, R., Brooks, J.W., Spratt, J., and Jacobson, E., 2008, ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. Journal of Wildlife Diseases, v. 44 no. 4, p. 851-863.
  • Johnson, P.T.J., Lunde, K.B., Thurman, E.M., Ritchie, E.G., Wray, S.N., Sutherland, D.R., Kapfer, J.M., Frest, T.J., Bowerman, J., and A.R. Blaustein. 2002. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs, 72:151-168.
  • Johnsrude, J.D., Raskin, R.E., Hoge, A.Y.A., and G.W. Erdos. 1997. Intraerythrocytic inclusions associated with iridoviral infection in a Fer de Lance (Bothrops moojeni) snake. Veterinary Pathology, 34:235-238.
  • Jones M.E.B., Pessier A.P. 2011. San Diego Zoo Global, San Diego, CA, USA. Unpublished work,
  • Just, F., Essbauer, W., Ahne, W., and B. Blahak. 2001. Occurrence of an invertebrate iridescent-like virus in reptiles. Journal of Veterinary Medicine B, 48:685-694.
  • Kanchanakhan S. An Ulcerative Disease of the Cultured Tiger Frog, Rana tigrina, in Thailand: Virological Examination. AAHRI News. 1998;7:1–2.
  • Kerby J. 1st International Symposium on ranaviruses. Froglog. 2011;98:35–37.
  • Kerby J.L., Hart J.A., Storfer A. Combined Effects of Virus, Pesticides, and Predator Cue on Larval Tiger Salamander (Ambystoma trigrinum) EcoHealth. 2011 doi: 10.1007/s10393-011-0682-1.[Cross Ref]
  • Kerby J.L., Richards-Hrdlicka K.L., Storfer A., Skelly D.K. An Examination of Amphibian Sensitivity to Environmental Contaminants: Are Amphibians Poor Canaries. Ecol. Lett. 2010;13:60–67.
  • Kik M., Martel A., Spitzen-van der Sluijs A., Pasmans F., Wohlsein P., Gröne A., Rijks J.M. ranavirus-Associated Mass Mortality in Wild Amphibians, the Netherlands, 2010: A First Report. Vet. J. 2011 doi: 10.1016/j.tvjl.2011.08.031. [Cross Ref]
  • Kik, Martel, Spitzen-van der Sluijs, Pasmans, Wohlsein, Gröne, Rijks ranavirus-associated mass mortality in wild amphibians, The Netherlands, 2010: A first report. The Veterinary Journal Volume 190, Issue 2, November 2011, Pages 284–286 http://www.sciencedirect.com/science/article/pii/S1090023311003297
  • Kipp, Rebekah M. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007
  • Kleinbaum, D.G., and M. Klein. 2005. Survival analysis: A self-learn text. Second Edition. Springer Science + Business Media, LLC, New York, USA.
  • Kunst, L., and I. Valpotić. 1968. Nova zarazna bolest zaba uzrokovana virusom. (A new infectious disease of frogs caused by virus). Veterinarski Archives, 38:103-113.
  • Langdon J.S. Experimental Transmission and Pathogenicity of Epizootic Haematopoietic Necrosis Virus (EHNV) in Redfin Perch, Perca fluviatilis L., and 11 Other Teleosts. J. Fish. Dis.1989;12:295–310.
  • Langdon, J.S., and J.D. Humphrey. 1987. Epizootic haematopoietic necrosis, a new viral disease in redfin perch, Perca fluviatilis L., in Australia. Journal of Fish Diseases, 10:289-297.
  • Langdon, J.S., Humphrey, J.D., Williams, L.M., Hyatt, A.D., and H.A. Westbury. 1986. First virus isolation from an Australian fish: an iridovirus-like pathogen from redfin perch, Perca fluviatilis L. Journal of Fish Diseases, 9:263-268.
  • Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., and D.G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23:2947-2948.
  • Lesbarreres D., Balseiro A., Brunner J., Chinchar V., Duffus A., Kerby J., Miller D.L., Robert J., Schock D., Waltzek T., Gray M. ranavirus; past, present and future. Biol. Lett. 2011 doi: 10.1098/rsbl.2011.0951. [Cross Ref]
  • Lipsitch, M., Siller, S., and M.A. Nowak. 1996. The evolution of virulence in pathogens with horizontal and vertical transmission. Evolution, 50:1729-1741.
  • Machin D., Cheung, Y.B., and M.K.B. Parmar. 2006. Survival analysis, a practical approach. Second Edition. John Wiley and Sons, Ltd. West Sussex, England.
  • Majji S., LaPatra S., Long S.M., Sample R., Bryan L., Sinning A., Chinchar V.G. Rana catesbeianaVirus Z (RCV-Z): A Novel Pathogenic ranavirus. Dis. Aquat. Organ. 2006;73:1–11.
  • Majji, S., LaPatra, S., Long, S.M., Sample, R., Bryan, L., Sinning, A., and V.G. Chinchar. 2006. Rana catesbeiana virus Z (RCV-Z): A novel pathogenic ranavirus. Diseases of Aquatic Organisms, 73:1-11.
  • Manual of Diagnostic Tests for Aquatic Animals 2011. Available online:http://www.oie.int/international-standard-setting/aquatic-manual/access-online/ (accessed on 31 October 2011).
  • Mao J. D., Green E., Fellers G., Chinchar V.G. Molecular Characterization of Iridoviruses Isolated from Sympatric Amphibians and Fish. Virus Res. 1999;63:45–52.
  • Mao J., Tham T.N., Gentry G.A., Aubertin A., Chinchar V.G. Cloning, Sequence Analysis, and Expression of the Major Capsid Protein of the Iridovirus Frog Virus 3. Virology. 1996;216:431–436.
  • Mao, J., Green, D.E., Fellers, G., and V.G. Chinchar. 1999. Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. Virus Research, 63:45- 52.
  • Mao, J., Hedrick, R.P., and V.G. Chinchar. 1997. Molecular characterization, sequence analysis and taxonomic position of newly isolated fish iridoviruses. Virology, 229:212-220.
  • Mao, J., J. Wang, G. D. Chinchar, and V. G. Chinchar. 1999. Molecular characterization of a ranavirus isolated from largemouth bass Micropterus salmoides. Diseases of Aquatic Organisms 37(2):107-114.
  • Mao, J., Tham, T.N., Gentry, G.A., Aubertin, A., and V.G. Chinchar. 1996. Cloning, sequence analysis, and expression of the major capsid protein of the Iridovirus frog virus 3. Virology, 216:431-436.
  • Marco, A., and M. Lizana. 2002. The absence of species and sex recognition during mate search by male common toads, Bufo bufo. Ethology, Ecology and Evolution, 14:1-8.
  • Marschang R. Universität Hohenheim, Stuttgart, Germany. 2011. Unpublished work,
  • Marschang RE, Braun S, Becher P. Isolation of a ranavirus from a gecko (Uroplatus fimbriatus). J Zoo Wildl Med. 2005 Jun;36(2):295-300. http://www.ncbi.nlm.nih.gov/pubmed/17323572
  • Marschang, R. E., P. Becher, H. Posthaus, P. Wild, H. J. Thiel, U. Muller-Doblies, E. F. Kaleta, and L. N. Bacciarini. 1999. Isolation and characterization of an iridovirus from Hermann’s tortoises (Testudo hermanni). Arch. Virol. 144: 1909–1922.
  • Marschang, R.E., Becher, P., Posthaus, H., Wild, P., Theil, H.-J., Müller – Doblies, U., Kaleta, E.F., and L.N. Bacciarini. 1999. Isolation and characterization of an iridovirus from Hermann’s tortoises (Testudo hermanni). Archives of Virology, 144:1909-1922.
  • Matos A.P.A., Silva Trabucho Caeiro M.F.A., Papp T., Cunha Almeida Matos B.A., Correia A.C.L, Marschang R.E. New Viruses from Lacerta Monticola (Serra da Estrela, Portugal): Further Evidence for a New Group of Nucleo-Cytoplasmic Large Deoxyriboviruses. Microsc. Microanal. 2011;17:101–108.
  • May, R.M., and R.M. Anderson. 1979. Population biology of infectious diseases: Part II. Nature, 280:455-461.
  • Mazzoni R., José de Mesquita A., Fleury L.F.F., Diederichsen de Brito W.M.E., Nunes I.A., Robert J., Morales H., Coelho A.S.G., Barthasson D.L., Galli L., et al. Mass Mortality Associated with a Frog Virus 3-Like ranavirus Infection in Farmed Tadpoles, Rana catesbeiana, from Brazil. Dis. Aquat. Organ. 2009;86:181–191.
  • McCallum H., Barlow N., Hone J. How Should Pathogen Transmission Be Modeled. Trends Ecol. Evol. 2001;16:295–300.
  • McClenahen, S. D., B. H. Beck, and J. M. Grizzle. 2005. Evaluation of cell culture methods for detection of largemouth bass virus. Journal of Aquatic Animal Health 17(4):365-372.
  • Miaud, C., Guyétant, R., and J. Elmberg. 1999. Variations in life-history traits in the common frog Rana temporaria (Amphibia: Anura): A literature review and new data from the French Alps. Journal of Zoology, London, 249:61-73.
  • Miller D. 2011. University of Tennessee, Knoxville, TN, USA. Unpublished work
  • Miller D.L., Gray M.J., Rajeev S., Schmutzer A.C., Burton E.C., Merrill A., Baldwin C. Pathological Findings in Larval and Juvenile Anurans Inhabiting Farm Ponds in Tennessee, U.S.A. J. Wildl. Dis.2009;45:314–324.
  • Miller D.L., Gray M.J., Storfer, A. “Ecopathology of ranaviruses Infecting Amphibians”. Viruses. 2011 November; 3(11): 2351–2373. Published online 2011 November 22.http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3230856/#b64-viruses-03-02351
  • Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A. Concurrent Infection withranavirus, Batrachochytrium dendrobatidis, and Aeromonas in a Captive Anuran Colony. J. Zoo Wildl. Med. 2008;39:445–449.
  • Miller D.L., Rajeev S., Gray M.J., Baldwin C. Frog Virus 3 Infection, Cultured American Bullfrogs.Emerg. Infect. Dis. 2007;13:342–343.
  • Milstein D., King R., Leader N. Israel Parks and Nature Authority, Jerusalem, Israel. 2011. Unpublished work,
  • Mişcanlenu, D., Alfy, M.E., Mailat, F., and G. Mihăescu. 1981. Viral particles in the hepatocytes of Rana esculenta (L.). Revue Roumaine de Medicine et Virologie, 32:123-125.
  • Moody N.J.G., Owens L. Experimental Demonstration of the Pathogenicity of a Frog Virus, Bohle iridovirus, for a Fish Species, Barramundi Lates calcarifer. Dis. Aquat. Organ. 1994;18:95–102.
  • Morales H.D., Abramowitz L., Gertz J., Sowa J., Vogel A., Robert J. Innate Immune Responses and Permissiveness to ranavirus Infection of Peritoneal Leukocytes in the Frog Xenopus leavis. J. Virol. 2010;84:4912–4922.
  • Naing, L., Winn, T., and B.N. Rusli. 2006. Practical issues in calculating sample size for prevalence studies. Archives of Orofacial Sciences, 1:9-14.
  • Nakajima D., Maeno Y., Honda A., Yokoyama K., Tooriyama T., Manabe S. Effectiveness of a Vaccine Against Red Sea Bream Iridoviral Disease in a Field Trial Test. Dis. Aquat. Organ.1999;1999;36:73–75.
  • Nazir J., Spengler M., Marschang R.E. Environmental Persistence of Amphibian and Reptilian ranaviruses. Dis. Aquat. Organ. 2012 in press,
  • Nei, M., and S. Kumar. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, New York.
  • Oliver, J.A. 1955. The natural history of North American amphibians and reptiles. D. Van Nostrand Company, Inc., Princeton, New Jersey.
  • Otto, S.P. and T. Day. 2007. A biologist’s guide to mathematical modelling in ecology and evolution. Princeton University Press, Woodstock, Oxfordshire, England.
  • Paetow L.J., Pauli B.D., McLoughlin J.D., Bidulka J., Marcogliese D.J. First Detection of ranavirus in Lithobates pipiens in Quebec. Herpetol. Rev. 2011;42:211–214.
  • Paperna, I., Vilenkin, M., and A.P. Alves de Matos. 2001. Iridovirus infections in farm reared tropical fish. Diseases of Aquatic Organisms, 48:17-25.
  • Parris M.J., Storfer A., Collins J.P., Davidson E.W. Life History Responses to Pathogens in Tiger Salamander (Ambystoma tigrinum) Larvae. J. Herpetol. 2005;39:366–372.
  • Pasmans F., Blahak S., Martel A., Pantchev N., Zwart P. ranavirus-Associated Mass Mortality in Imported Red Tailed Knobby Newts (Tylototriton kweichowensis): A Case Report. Vet. J.2008;176:257–259.
  • Pasmans F., Blahak S., Martel A., Pantchev N., Zwart P. ranavirus-Associated Mass Mortality in Imported Red Tailed Knobby Newts (Tylototriton kweichowensis): A Case Report. Vet. J.2008;176:257–259.
  • Pasmans, F., Blahak, S., Martel, A., Pantchev, N., and P. Zwart. 2008. ranavirus-associated mass mortality in imported red tailed knobby newts (Tylototriton kweichowensis): A case report. The Veterinary Journal, 176:257-259. http://www.sciencedirect.com/science/article/pii/S1090023307000925
  • Pasmans, F., Mutschmann, F., Halliday, T., and P. Zwart. 2006. Amphibian decline: The urgent need for amphibian research in Europe. The Veterinary Journal, 171:18-19.
  • Pearman P.B., Garner T.W.J. Susceptibility of Italian Agile Frog Populations to an Emerging Strain of ranavirus Parallels Population Genetic Diversity. Ecol. Lett. 2005;8:401–408.
  • Pearman P.B., Garner T.W.J., Straub M., Greber U.F. Response of the Italian Agile Frog (Rana latastei) to a ranavirus, Frog Virus 3: A Model for Viral Emergence in Naïve Populations. J. Wildl. Dis.2004;40:660–669.
  • Pearman, P.B., and T.W.J. Garner. 2005. Susceptibility of Italian agile frog populations to an emerging strain of ranavirus parallels population genetic diversity. Ecology Letters, 8:401-408.
  • Pearman, P.B., Garner, T.W.J., Straub, M., and U.F. Greber. 2004. Response of the Italian agile frog (Rana latastei) to a ranavirus, frog virus 3: A model for viral emergence in naïve populations. Journal of Wildlife Diseases, 40:660-669.
  • Pessier A.P. 2011. San Diego Zoo Global, San Diego, CA, USA. Unpublished work,
  • Petranka J.W., Harp E.M., Holbrook C.T., Hamel J.A. Long-Term Persistence of Amphibian Populations in a Restored Wetland Complex. Biol. Cons. 2007;138:371–380.
  • Petranka J.W., Murray S.M., Kennedy C.A. Response of Amphibians to Restoration of a Southern Appalachian Wetland: Perturbations Confound Post-Restoration Assessment. Wetlands.2003;23:278–290.
  • Pfennig D.W., Loeb M.L.G., Collins J.P. Pathogens as a Factor Limiting the Spread of Cannibalism in Tiger Salamanders. Oecologia. 1991;99:161–166.
  • Piaskoski, T. O., J. A. Plumb, and S. R. Roberts. 1999. Characterization of the largemouth bass virus in cell culture. Journal of Aquatic Animal Health 11(1):45-51.
  • Picco A.M., Brunner J.L., Collins J.P. Susceptibility of the Endangered California Tiger Salamander, Ambystoma californiense, to ranavirus Infection. J. Wildl. Dis. 2007;43:286–290.
  • Picco A.M., Collins J.P. Amphibian Commerce as a likely Source of Pathogen Pollution. Conserv. Biol. 2008;22:1582–1589.
  • Picco A.M., Karam A.P., Collins J.P. Pathogen Host Switching in Commercial Trade with Management Recommendations. EcoHealth. 2010;7:252–256.
  • Picco AM, Collins JP. Amphibian commerce as a likely source of pathogen pollution.Conserv Biol. 2008 Dec;22(6):1582-9. Epub 2008 Aug 19. http://www.ncbi.nlm.nih.gov/pubmed/18717688
  • Plumb, J. A., A. D. Noyes, S. Graziano, J. Wang, J. Mao, and V. G. Chinchar. 1999. Isolation and identification of viruses from adult largemouth bass during a 1997 – 1998 survey in the southeastern United States. Journal of Aquatic Animal Health 11(4):391-399.
  • Plumb, J. A., J. M. Grizzle, H. E. Young, A. Noyes, and S. Lamprecht. 1996. An iridovirus isolated from wild largemouth bass. Journal of Aquatic Animal Health 8(4):265-270.
  • Qin, Q.W., Lam, T.J., Sin, Y.M., Shen, Y.M., Chang, S.F., Ngoh, G.H., and C.L. Chen. 2001. Electron microscopic observations on a marine fish iridovirus isolated from brown-spotted grouper, Epinephelus tauvina. Journal of Virological Methods, 98:17-24.
  • Rebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 RevisionDate: 6/12/2007
  • Reddacliff, L.A., and R.J. Whittington. 1996. Pathology of epizootic haematopoietic necrosis virus (EHNV) in rainbow trout (Oncorhynhus mykiss Walbaum) and Redfin perch (Perca fluviatilis L.). Journal of Comparative Pathology, 115:103- 115.
  • Ridenhour B.J., Storfer A. Geographically Variable Selection in Ambystoma tigrinum Virus (Iridoviridae) throughout the Western United States. J. Evol. Biol. 2008;21:1151–1159.
  • Ridenhour, B.J., and A.T. Storfer. 2008. Geographically variable selection in Ambystoma tigrinum virus (Iridoviridae) through out the western USA. Journal of Evolutionary Biology, 21:1151-1159.
  • Robert J, Abramowitz L, Gantress J, Morales HD. Xenopus laevis: a possible vector of ranavirus infection? J Wildl Dis. 2007 Oct;43(4):645-52. http://www.ncbi.nlm.nih.gov/pubmed/17984259
  • Robert J. Emerging Ranaviral Infectious Diseases and Amphibian Decline. Diversity. 2010;2:330.
  • Robert J., Abramowitz L., Gantress J., Morales H.D. Xenopus laevis: A Possible Vector of ranavirus Infection? J. Wildl. Dis. 2007;43:645–652.
  • Robert J., Chinchar V.G. ranaviruses: An emerging threat to ectothermic vertebrates. Report of the First International Symposium on ranaviruses, Minneapolis MN, USA, 8 July 2011. Dev. Comp. Immunol. 2011;36:259–261.
  • Robert J., George E., De Jesús Andino F., Chen G. Waterborne Infectivity of the ranavirus Frog Virus 3 in Xenopus laevis. Virology. 2011;2:410–417.
  • Robert J., Morales H., Buck W., Cohen N., Marr S., Gantress J. Adaptive Immunity and Histopathology in Frog Virus 3-Infected Xenopus. Virology. 2005;332:667–675.
  • Rojas S., Richards K., Jancovich J.K., Davidson E.W. Influence of Temperature on ranavirus Infection in Larval Salamanders Ambystoma tigrinum. Dis. Aquat. Organ. 2005;63:95–100.
  • Rollins-Smith L.A. Metamorphosis and the Amphibian Immune System. Immunol. Rev.1998;166:221–230.
  • Rollins-Smith L.A. Neuroendocrine-Immune System Interactions in Amphibians Implications for Understanding Global Amphibian Declines. Immunol. Res. 2001;23:273–280.
  • Russell D.M., Goldberg C.S., Sprague L., Waits L.P., Green D.E., Schuler K.L., Rosenblum E.B. ranavirus Outbreaks in Amphibian Populations of Northern Idaho. Herpetol. Rev. 2011;42:223–225.
  • Ryder J.J., Miller M.R., White A., Knell R.J., Boots M. Host-Parasite Population Dynamics Under Combined Frequency- and Density-Dependent Transmission. Oikos. 2007;116:2017–2026.
  • Ryder, J.J., Miller, M.R., White, A., Knell, R.J., and M. Boots. 2007. Host parasite population dynamics under combined frequency- and density-dependent transmission. Oikos, 116:2017-2026.
  • Sample R, Bryan L., Long S., Majii S., Hoskins G., Olivier J., Chinchar V.G. Inhibition of Iridovirus Protein Synthesis and Virus Replication by Antisense Morpholino Oligonucleotides Targeted to the Major Capsid Protein, the 18 kDa Immediate-Early Protein, and a Viral Homolog of RNA Polymerase II. Virology. 2007;358:311–320.
  • Schetter, C., Grünemann, B., Hölker, I., and W. Doerfler. 1993. Patterns of frog virus 3 DNA methylation and DNA methyltransferase activity in nuclei of infected cells. Journal of Virology, 67:6973-6978.
  • Schloegel L.M., Daszak P., Cunningham A.A., Speare R., Hill B. Two Amphibian Diseases, Chytridiomycosis and Ranaviral Disease, are now Globally Notifiable to the World Organization for Animal Health (OIE): An Assessment. Dis. Aquat. Organ. 2010;92:101–108.
  • Schloegel L.M., Picco A.M., Kilpatrick A.M., Davies A.J., Hyatt A.D., Daszak P. Magnitude of the US Trade in Amphibians and Presence of Batrachochytrium dendrobatidis and ranavirus Infection in Imported North American Bullfrogs (Rana catesbeiana) Biol. Cons. 2009;142:1420–1426.
  • Schmutzer A.C. University of Tennessee; Knoxville, TN, USA: 2007. Influences of Cattle on Larval Amphibians and the Aquatic Environment in Cumberland Plateau Wetlands; p. 216. Master Thesis,
  • Schock D.M., Bollinger T.K. An Apparent Decline of Northern Leopard Frogs (Rana pipiens) on the Rafferty Dam Mitigation Lands near Esteven, Saskatchewan. Blue Jay. 2005;63:144–154.
  • Schock D.M., Bollinger T.K., Chinchar V.G., Jancovich J.K., Collins J.P. Experimental Evidence that Amphibian ranaviruses Are Multi-Host Pathogens. Copeia. 2008;1:133–143.
  • Schock D.M., Bollinger T.K., Collins J.P. Mortality Rates Differ among Amphibian Populations Exposed to Three Strains of a Lethal ranavirus. EcoHealth. 2010;6:438–448.
  • Schock D.M., Ruthig G.R., Collins J.P., Kutz S.J., Carrière S., Gau R.J., Veitch A.M., Larter N.C., Tate D.P., Guthrie G., et al. Amphibian Chytrid Fungus and ranaviruses in the Northwest Territories, Canada. Dis. Aquat. Organ. 2010;92:231–240.
  • Schock, D.M., and T.K. Bollinger. 2005. Apparent decline of Northern Leopard frogs (Rana pipiens) on the Rafferty Dam mitigation lands near Estevan, SK. Blue Jay, 63:144-154.
  • Schock, D.M., Bollinger, T.K., Chinchar, V.G., Jancovich, J.K., and J.P. Collins. 2008. Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia, 1:133-143.
  • Schuh, J.C.L., and I.G. Shirley. 1990. Viral hematopoietic necrosis in an angel fish (Pterophyllum scalare). Journal of Zoo and Wildlife Medicine, 21:95-98.
  • Scott, B. A. and G. M. Aron. 2002. Effect of chemical and physical agents on the infectivity of largemouth bass virus. Abstracts of the General Meeting of the American Society for Microbiology 102:421.
  • Scott, M.E. 1988. The impact of infection and disease on animal populations: Implications for Conservation Biology. Conservation Biology, 2:40-56.
  • Sleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012.
  • Smail, D.A. 1982. Viral erythrocytic necrosis in fish: a review. Proceedings of the Royal Society of Edinburgh, 81B:169-176.
  • Speare R., Freeland W.J., Bolton S.J. A Possible Iridovirus in Erythrocytes of Bufo marinus in Costa Rica. J. Wildl. Dis. 1991;27:457–462.
  • Speare R., Smith J.R. An Iridovirus-Like Agent Isolated from the Ornate Burrowing FrogLimnodynastes ornatus in Northern Australia. Dis. Aquat. Organ. 1992;14:51–57.
  • Speare, R., and J.R. Smith. 1992. An iridovirus-like agent isolated from the ornate burrowing frog Limnodynastes ornatus in northern Australia. Diseases of Aquatic Organisms, 14:51-57.
  • Speare, R., Freeland, W.J., and S.J. Bolton. 1991. A possible iridovirus in erythrocytes on Bufo marinus in Costa Rica. Journal of Wildlife Diseases 27:457-462.
  • Speare, Rick. Summary of Formidable Infectious Diseases of Amphibians.Updated 16 February 2003 http://www.jcu.edu.au/school/phtm/PHTM/frogs/formidable.htm
  • Spitz, Kingdom, Veldman, and Zandt Virus threatens Dutch frogs (2011) http://www.natuurbericht.nl/?id=5702
  • St-Amour V., Wong W.M., Garner T.W.M., Lesbarreres D. Anthropogenic Influence on Prevalence of 2 Amphibian Pathogens. Emerg. Infect. Dis. 2008;14:1175–1176.
  • Storfer A., Alfaro M.E., Ridenhour B.J., Jancovich J.K., Mech S.G., Parris M.J., Collins J.P. Phylogenetic Concordance Analysis Shows an Emerging Pathogen is Novel and Endemic. Ecol. Lett.2007;10:1075–1083.
  • Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L., and R.W. Walker. 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306:1783-1786.
  • Tamai, T., Tsujimura, K., Shirahata, S., Oda, H., Noguchi, T., Kusuda, R., Sato, N., Kimura, S., Katakura, Y., and H. Murakami. 1997. Development of DNA diagnostic methods for the detection of new fish iridoviral diseases. Cytotechnology, 23:211-220.
  • Tamaru Y., Ohtsuka M., Kato K., Manabe S., Kuroda K., Sanada M., Ueda M. Application of the Arming System for the Expression of the 380R Antigen from Red Sea Bream Iridovirus (RSIV) on the Surface of Yeast Cells: A First Step for the Development of an Oral Vaccine. Biotechnol. Prog.2006;22:949–953.
  • Tamura, K., Dudley, J., Nei, M. and S. Kumar. 2007. MEGA 4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24:1596-1599.
  • Teacher A.G.F, Garner T.W.J., Nichols R.A. Evidence for Directional Selection at a Novel Major Histocompatibility Class I Marker in Wild Common Frogs (Rana temporaria) Exposed to a Viral Pathogen (ranavirus) PLoS One. 2009;4:e4616.
  • Teacher A.G.F., Cunningham A.A., Garner W.J. Assessing the Long-Term Impact of ranavirus Infection in Wild Common Frog Populations. Anim. Con. 2010;13:514–522.
  • Teacher, A.F.G. 2009. Population and immunocompetent genetic variation: A field based study. PhD Thesis. Queen Mary, University of London.
  • Teacher, A.F.G., Garner, T.W.J., and R.A. Nichols. 2009a. Evidence for directional selection at a novel major histocompatibility class 1 marker in wild common frogs (Rana temporaria) exposed to a viral pathogen (ranavirus). PLoS One 4: e4616. DOI: 10.1371/journal.pone.0004616
  • Teacher, A.F.G., Garner, T.W.J., and R.A. Nichols. 2009b. Population genetic patterns suggest a behavioural change in wild common frogs (Rana temporaria) following disease outbreaks (ranavirus). Molecular Ecology, 18:3163-3172.
  • Tidona, C.A., Schnitzler, P., Khem, R., and G. Darai. 1998. Is the major capsid protein of Iridoviruses as suitable target for the study of viral evolution? Virus Genes, 16:59-66.
  • Todd-Thompson M. University of Tennessee; Knoxville, TN, USA: 2010. Seasonality, Variation in Species Prevalence, and Localized Disease for ranavirus in Cades Cove (Great Smoky Mountains National Park) amphibians. Master Thesis, Available online:http://trace.tennessee.edu/utk_gradthes/665 (accessed on 17 November 2011).
  • Torrence S.M., Green D.E., Benson C.J., Ip H.S., Smith L.M., McMurray S.T. A New ranavirus Isolated from Pseudacris clarkii Tadpoles in Playa Wetlands in the Southern High Plains, Texas. J. Aquat. Anim. Health. 2010;22:65–72.
  • Tsai, C.-T., Ting, J.-W., Wu, M.-H., Wu, M.-F., Guo, I.-C., and C.-Y. Chang. 2005. Complete genome sequence of the grouper iridovirus and comparison of genomic organisation with those of other iridoviruses. Journal of Virology, 79:2010-2023.
  • Tweedell K., Granoff A. Viruses and Renal Carcinoma of Rana pipiens. V. Effect of Frog Virus 3 on Developing Frog Embryos and Larvae. J. Nat. Cancer Inst. 1968;40:407–410.
  • Une Y., Nakajinma K., Taharaguchi S., Ogihara K., Murakami M. ranavirus Infection Outbreak in the Salamander (Hynobius nebulosus) in Japan. J. Comp. Pathol. 2009;141:310.
  • Une Y., Sakuma A., Matsueda H., Nakai K., Murakami M. ranavirus Outbreak in North American Bullfrogs (Rana catesbeiana), Japan. Emerg. Infect. Dis. 2009;15:1146–1147.
  • Uyehara I.K, Gamble T., Cotner S. The Presence of ranavirus in Anuran Populations at Itasca State Park, Minnesota, USA. Herpetol. Rev. 2010;41:177–179.
  • Warne R.W., Crespi E.J., Brunner J.L. Escape from the Pond: Stress and Developmental Responses to ranavirus Infection in Wood Frog Tadpoles. Funct. Ecol. 2011;25:139–146.
  • Wells K.D. The Ecology and Behavior of Amphibians. University of Chicago Press; Chicago, IL, USA: 2007. p. 1148.
  • Weng S.P., He J.G., Wang X.H., Lü L., Deng M., Chan S.-M. Outbreaks of an Iridovirus Disease in Cultured Tiger Frog, Rana tigrina rugulosa, in Southern China. J. Fish. Dis. 2002;25:423–427.
  • Westhouse, R.A., Jacobson, E.R., Harris, R.K., Winter, K.R., and B.L. Homer. 1996. Respiratory and pharyngo-esophageal iridovirus infection in a gopher tortoise (Gopherus polyphemus). Journal of Wildlife Diseases, 32:682-686.
  • Whelan, G. 2004. Largemouth bass virus continues to spread in Michigan waters. Michigan Department of Natural Resources Press Release. Woodland, J. E., A. D. Noyes, and J. M. Grizzle. 2002. A survey to detect largemouth bass virus among fish from hatcheries in the southeastern USA. Transactions of the American Fisheries Society 131(2):308-311.
  • Whitley D.S., Sample R.C., Sinning A.R., Henegar J., Chinchar V.G. Antisense approaches for elucidating ranavirus gene function in an infected fish cell line. Dev. Comp. Immunol. 2010;35:937–948.
  • Whittington R.J., Becker J.A., Dennis M.M. Iridovirus Infections in Finfish—Critical Review with Emphasis on ranaviruses. J. Fish. Dis. 2010;33:95–122.
  • Williams T., Barbosa-Solomieu V., Chinchar G.D. A Decade of Advances in Iridovirus Research.Adv. Virus Res. 2005;65:173–248.
  • Wolf K., Bullock G.L., Dunbar C.E., Quimby M.C. Tadpole Edema Virus: A Viscerotropic Pathogen for Anuran Amphibians. J. Infect. Dis. 1969;118:253–262.
  • Woodland, J. E., C. J. Brunner, A. D. Noyes, and J. M. Grizzle. 2002. Experimental oral transmission of largemouth bass virus. Journal of Fish Diseases 25(11):669-672.
  • Woolhouse, M.E.J., Taylor, L.H., and D.T. Haydon. 2001. Population biology of multihost pathogens. Science, 292:1109-1112.
  • Xu K, Zhu DZ, Wei Y, Schloegel LM, Chen XF, Wang XL. Broad distribution of ranavirus in free-ranging Rana dybowskii in Heilongjiang, China. Ecohealth. 2010 Aug;7(1):18-23. Epub 2010 Mar 9. http://www.ncbi.nlm.nih.gov/pubmed/20217181
  • Xu K., Zhu D., Wei Y., Schloegel L.M., Chen X., Wang X. Broad Distribution of ranavirus in Free-Ranging Rana dybowskii in Heilongjiang, China. EcoHealth. 2010;7:18–23.
  • Zhang Q., Li Z., Jiang Y., Liang S., Gui J. Preliminary Studies on Virus Isolation and Cell Infection from Diseased Frog Rana grylio. Acta Hydrobiologica Sinica. 1996;4:390–392.
  • Zhang Q.Y., Xiao F., Li Z.Q., Gui J.F., Mao J., Chinchar V.G. Characterization of an Iridovirus from the Cultured Pig Frog, Rana grylio, with Lethal Syndrome. Dis. Aquat. Organ. 2001;48:27–36.
  • Zhang, Q.-A., Xiao, F., Li, Z.-Q., Gui, J.-F., Mao, J., and V.G. Chinchar. 2001.
  • Zilberg, D., J. M. Grizzle, and J. A. Plumb. 2000. Preliminary description of lesions in juvenile largemouth bass injected with largemouth bass virus. Diseases of Aquatic Organisms 39(2):143-146.
  • ZSL Frog Health Checks http://www.zsl.org/conservation/species/amphibians/frog-health-checks,1825,AR.html
  • Zupanovic Z., Lopz G., Hyatt A.D., Green B., Bartran G., Parkes H., Whittingtin R.J., Speare R. Giant Toads, Bufo marinus, in Australia and Venezuela Have Antibodies against ranaviruses. Dis. Aquat. Organ. 1998;32:1–8.

End Notes

iSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

iiSpeare, Rick. Summary of Formidable Infectious Diseases of Amphibians.Updated 16 February 2003 http://www.jcu.edu.au/school/phtm/PHTM/frogs/formidable.htm

iii Gray, MJ; Miller, DL; Hoverman, JT (2009). “Ecology and pathology of amphibian ranaviruses”. Diseases of Aquatic Organisms 87 (3): 243–266.

ivJacques Robert, Erica George, Francisco De Jesús Andino, Guangchun Chen. Waterborne infectivity of the ranavirus frog virus 3 in Xenopus laevis. Virology. 2011 Sep 1;417(2): 410-7 abstract

vRebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007

viJancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, Collins JP, Jacobs BL, Storfer A. Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Mol Ecol. 2005 Jan;14(1):213-24. http://www.ncbi.nlm.nih.gov/pubmed/15643965

viiAnon. Wikipedia. Nucleocytoplasmic large DNA viruses. link.

viiiTeleosts are bony, ray-finned fish, as opposed to cartilaginous fish, such as sharks, rays, and skates. Nearly all fish – about 20,000 species — are teleosts – members of the infraclass Teleostei of the class Actinopterygii.

ixChinchar. ranaviruses: Past, Present, and Future. First International Symposium on ranaviruses, Minneapolis MD July 7, 2011. link.

xJancovich, James K., Michael Bremont, Jeffrey W. Touchman, and Bertram L. Jacobs Evidence for Multiple Recent Host Species Shifts among the ranaviruses (Family Iridoviridae) First published December 2009, doi: 10.1128/JVI.01991-09J. Virol. March 2010 vol. 84 no. 62636-2647 abstract

xiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xiiGray, MJ; Miller, DL; Hoverman, JT (2009). “Ecology and pathology of amphibian ranaviruses”. Diseases of Aquatic Organisms 87 (3): 243–266. doi:10.3354/dao02138PMID 20099417

xiii Grabensteiner, M. Gumpenberger, C. NeuBauer, B. Hirschmuller, and K. Mostl First report of an iridovirus (Genus ranavirus) infection in a Leopard tortoise (Geochelone pardalis pardalis) Vet. Med. Austria / Wien. Tierärztl. Mschr. 94 (2007), 243 – 248 http://www.schildkroeten-sfb.ch/fileadmin/docs/news/729-pantherschildkroete.pdf

xivAnon. Wikipedia. ranavirus.April 4, 2012. link.

  1. xv R J Whittington,  J A Becker,  M M Dennis Iridovirus infections in finfish – critical review with emphasis on ranaviruses. Journal of Fish Diseases December 28, 2009. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2761.2009.01110.x/abstract

xviXu K, Zhu DZ, Wei Y, Schloegel LM, Chen XF, Wang XL. Broad distribution of ranavirus in free-ranging Rana dybowskii in Heilongjiang, China.Ecohealth. 2010 Aug;7(1):18-23. Epub 2010 Mar 9. http://www.ncbi.nlm.nih.gov/pubmed/20217181

xvii Sleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xviiiRebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007

xixRebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007

xxiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xxiiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xxiiiGray M.J., Miller D.L., Hoverman J.T. First Report of ranavirus Infecting Lungless Salamanders.Herpetol. Rev. 2009;40:316–319.; Gahl M.J., Calhoun A.J.K. Landscape setting and Risk of ranavirus Mortality Events. Biol. Cons.2008;141:2679–2689.

xxivSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xxvGantress J., Maniero G.D., Cohen N., Robert J. Development and Characterization of a Model System to Study Amphibian Immune Responses to Iridoviruses. Virology. 2003;311:254–262.

xxvi Hoverman J.T., Gray M.J., Haislip J.T., Miller D.L. Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth. 2011 doi: 10.1007/s10393-011-0717-7.

 

xxvii Sleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xxviii Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A. Concurrent Infection withranavirus, Batrachochytrium dendrobatidis, and Aeromonas in a Captive Anuran Colony. J. Zoo Wildl. Med. 2008;39:445–449.; Driskell E.A., Miller D.L., Swist S.L., Gyimesi Z.S. PCR Detection of ranavirus in Adult Anurans from the Louisville Zoological Garden. J. Zoo Wildl. Med. 2009;40:559–563.; Miller D.L., Rajeev S., Gray M.J., Baldwin C. Frog Virus 3 Infection, Cultured American Bullfrogs.Emerg. Infect. Dis. 2007;13:342–343.; Pasmans F., Blahak S., Martel A., Pantchev N., Zwart P. ranavirus-Associated Mass Mortality in Imported Red Tailed Knobby Newts (Tylototriton kweichowensis): A Case Report. Vet. J.2008;176:257–259. ; Jancovich J.K., Davidson E.W., Morado J.F., Jacobs B.L., Collins J.P. Isolation of a Lethal Virus from the Endangered Tiger Salamander Ambystoma tigrinum stebbinsiDis. Aquat. Organ.1997;31:161–167.; Converse K.A., Green D.E. Diseases of Tadpoles. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 72–88. Chapter 7,

xxixSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xxx Rebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007

xxxiChinchar, VG (2002). “ranaviruses (family Iridoviridae) emerging cold-blooded killers”. Archives of Virology 147 (3): 447–470.

xxxiiWilliams T, Barbosa-Solomieu V, Chinchar GD (2005). “A decade of advances in iridovirus research” 173-148. In Maramorosch K, Shatkin A (eds). Advances in virus research, Vol. 65 Academic Press, New York, USA. Also: Chinchar, VG; Bryan, L; Wang, J; Long, S; Chinchar, GD (2003). “Induction of apoptosis in frog virus 3-infected cells”. Virology 306: 303–312

xxxiii Converse K.A., Green D.E. Diseases of Tadpoles. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 72–88. Chapter 7,; Converse K.A., Green D. Diseases of Salamanders. In: Majumdar S.K., Huffman J.E., Brenner F.J., Panah A.I., editors. Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. The Pennsylvania Academy of Science; Easton, PA, USA: 2005. pp. 117–130. Chapter 9,

xxxivJancovich J.K., Davidson E.W., Morado J.F., Jacobs B.L., Collins J.P. Isolation of a Lethal Virus from the Endangered Tiger Salamander Ambystoma tigrinum stebbinsiDis. Aquat. Organ.1997;31:161–167.; Miller D.L., Rajeev S., Brookins M., Cook J., Whittington L., Baldwin C.A. Concurrent Infection withranavirus, Batrachochytrium dendrobatidis, and Aeromonas in a Captive Anuran Colony. J. Zoo Wildl. Med. 2008;39:445–449.; Warne R.W., Crespi E.J., Brunner J.L. Escape from the Pond: Stress and Developmental Responses to ranavirus Infection in Wood Frog Tadpoles. Funct. Ecol. 2011;25:139–146.

xxxv Bollinger T.K., Mao J., Schock D., Brigham R.M., Chinchar V.G. Pathology, Isolation, and Preliminary Molecular Characterization of a Novel Iridovirus from Tiger Salamanders in Saskatchewan. J. Wildl. Dis. 1999;35:413–429

;  Docherty D.E., Meteyer C.U., Wang J., Mao J., Case S.T., Chinchar V.G. Diagnostic and Molecular Evaluation of Three Iridovirus-Associated Salamander Mortality Events. J. Wildl. Dis. 2003;39:556–566.;

xxxviMiller, Debra, Matthew Gray, and Andrew Storfer “Ecopathology of ranaviruses Infecting Amphibians”. Viruses. 2011 November; 3(11): 2351–2373. Published online 2011 November 22.http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3230856/#b64-viruses-03-02351

xxxviiAnon. Wikipedia. ranavirus.April 4, 2012. link.

xxxviiiRebekah M. Kipp. 2012. ranavirus. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=2657 Revision Date: 6/12/2007

xxxix Geng, Y., K.Y. Wang, Z.Y. Zhou, C.W. Li, J. Wang, M. He, Z.Q. Yin, W.M. Lai First Report of a ranavirus Associated with Morbidity and Mortality in Farmed Chinese Giant Salamanders (Andrias davidianus). Journal of Comparative Pathology Volume 145, Issue 1, July 2011, Pages 95-102. http://www.sciencedirect.com/science/article/pii/S0021997510003427

xlSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xliSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xliiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xliiiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.

xlivAllender, M.C., M. Abd-Eldaim,J.Schumacher, D. McRuer, L.S. Christian,and M. Kennedy. PCR Prevalence of Ranavirus in Free-Ranging Eastern Box Turtles (Terrapene carolina carolina) at Rehabilitation Centers in Three Southeastern US States. Journal of Wildlife Diseases, 47(3), 2011, pp. 759–764. http://fwf.ag.utk.edu/mgray/ranavirus/2011Publications/Allenderetal2011.pdf

xlvN Z. Elaraky, Leon N.D. Potgieter, and Melissa A. Kennedy. “Virucidal efficacy of four new disinfectants” Journal of the American Animal Hospital Association 38.3 (2002): 231-234.

xlvi Speare, Rick. Summary of Formidable Infectious Diseases of Amphibians.Updated 16 February 2003 http://www.jcu.edu.au/school/phtm/PHTM/frogs/formidable.htm

xlvii Speare, Rick. Summary of Formidable Infectious Diseases of Amphibians.Updated 16 February 2003 http://www.jcu.edu.au/school/phtm/PHTM/frogs/formidable.htm

xlviiiSleeman, Jonathan. USGS National Wildlife Health Center. Update on ranavirus in Amphibians and Reptiles. March 23, 2012. link.