Ranavirus: An Emerging Pathogen in Amphibian, Fish and Reptile Populations in Tennessee and Beyond University of Tennessee Center for Wildlife Health Department of Forestry, Wildlife and Fisheries Matthew J. Gray M. Niemiller 6 March 2014, 10:30 AM, TN-TWS Fall Creek Falls State Park
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Ranavirus: an emerging pathogen in amphibian, fish and reptile populations in Tennessee and beyond
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Ranavirus: An Emerging Pathogen in Amphibian, Fish and Reptile
Populations in Tennessee and Beyond
University of TennesseeCenter for Wildlife Health
Department of Forestry, Wildlife and Fisheries
Matthew J. Gray
M. Niemiller
6 March 2014, 10:30 AM, TN-TWS Fall Creek Falls State Park
Outline
I. Ranavirus-Host Characteristics
II.II. Learning about Ranavirus EcologyLearning about Ranavirus Ecology
III. Can Ranaviruses Contribute to Declines?
IV. Mechanisms of Emergence
Ranavirus Characteristics•dsDNA, 150-280K bp
•120-300 nm in diameter (3x smaller than bacteria)
•Icosahedral Shape (20)
Family: Iridoviridae
Virion
Chinchar et al. (2011)
Iridovirus, Chloriridovirus, Ranavirus, Megalocytivirus, and Lymphocystivirus Genera:
(Westhouse et al. 1996; Marschang et al. 1999, 2005; Hyatt et al. 2002; DeVoe et al. 2004; Huang et al. 2009; Allender et al. 2006, 2011; Johnson et al. 2007, 2008, 2011)
• No mortality of turtles or fish exposed to infected tadpoles
• Suggests that turtles and fish may be reservoirs of ranavirus
• Amphibians may be amplifying species
Brenes et al. (PLoS ONE, accepted)
Are Ranaviruses Capable of Causing
Local Extirpations and Species Declines?
0
50
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1960
1963
1966
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1975
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1981
1984
1987
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1993
1996
Nu
mb
er
of
Po
pu
lati
on
s
Collins & Crump (2009)
Muths et al. (2006)
Evidence of Local ExtinctionDr. Amber TeacherSoutheastern England
Animal Conservation
13:514-522
1996/97 and 2008
Ranavirus (+) populations
81% Median Reduction
Larger PopulationsGreatest
Proportional Declines
A. Teacher
A. Teacher
Teacher et al. 2010
81%
Evidence of Local ExtinctionDr. Jim Petranka
Tulula Wetland Complex, NC
Rescue Effect
Biological Conservation 138:371-380
Wetlands 23:278-2901998-2006
Recruitment at most wetlands failed due
to ranavirus
Persistence Possible from Source Populations
Any Concern for Common Species?Wood Frog Example
Most Widely Distributed Species in North America
p<0.001
Stage Susceptibility of Wood Frogs
Egg = 60% Survival
Hatchling = 20% Survival
Larvae = 0% Survival
Metamorph = 0% Survival
Haislip et al. (2011)
103 PFU/mL
Wood Frog Population DataDrs. Keith Berven and Elizabeth Harper
Berven (1990), Harper et al. (2008)
Pre-meta 1 yr. old 2 yr. old 3+ yr. old
• Stage-structured discrete-time matrix model (K = 1500 females)• Simulated Exposure for each Stage (egg, hatchling, larva, meta)• Exposure Interval: 50, 25, 10, 5, and 2 years (every year)• Demographic and ranavirus survival probabilities multiplied • 1000 Simulations (one-year steps) • Built in stochasticity in the model• Closed Population
7-year: Beltsville, Maryland
J. Earl
Extinction Probability in 1000 yearsEarl and Gray (in review; EcoHealth)
Closed Population
Time to ExtinctionEarl and Gray (in review; EcoHealth)Closed Population
25 years
Every Year = 5 years
Female Population SizeEarl and Gray (in review; EcoHealth)
Death of Pre-metamorphic Stages
Matters!
Closed Population
Evidence of Rare Species EffectsSutton et al. (in review)
Endangered Dusky Gopher FrogDiseases of Aquatic
Organisms
n = 18 /trt
ADULTS
Evidence of Rare Species EffectsChaney, Gray, Miller & Kouba
Threatened Boreal Toad
Tadpoles Metamorphs
2 – 5 d5 – 7 d
Factors Contributing to Emergence
Other Possible Stressors: Pesticide Mixtures, Nitrogenous Waste, Endocrine Disruptors, Acidification, Climate Change, Heavy Metals
Pathogen Pollution:
Anthropogenic introduction of novel strains to naïve populations
(Cunningham et al. 2003)
•Fishing Bait •Ranaculture Facilities
•Biological Supply Companies•International Food & Pet Trade
•Contaminated FomitesPicco et al. (2007) Schloegel et al. (2009)
Anthropogenic Stressors:
1) Herbicide (Atrazine)
Forson & Storfer (2006); Gray et al. (2007); Greer et al. (2008); Kerby et al. (2011)
ATV SusceptibilityA. tigrinum
2) Cattle Land Use: Prevalence Green Frogs and Tiger Salamanders
Insecticide (Carbaryl)
Global Trade of Ranavirus Hosts
From 2000-2006, the U.S. imported >1.5 billion individual animals (fish & wildlife; Smith et al. 2009)
90% fish, 2% amphibians, 1% reptiles25 million live amphibians imported to U.S./year
Ranavirus Positive
•Hong Kong = 89%•Dominican Republic = 70%•Madagascar = 57%
Kristine Smith, DVM
Smith et al. (unpubl. data)
Pe
rce
nt
mo
rta
lity
0
10
20
30
40
50
60
70
80
90
100
FV3
RI
Ranaculture isolate 2X more lethal than FV3
Risk of Pathogen PollutionMajji et al. (2006), Storfer et al. (2007), Mazzoni et al. (2009), Hoverman et al. (2011a), Brenes (2013)
Should we be concerned?
•Ranavirus are Multi-species Pathogens •Amphibians with fast-developing larvae most susceptible
•Transmission is efficient – Multiple Routes •Environmental Persistence is long (1 – 3 mo)
•Anthropogenic Stressors and Pathogen Pollution contribute to Ranavirus Emergence
Ranaviruses represent a significant threat to the global biodiveristy of ectothermic vertebrates
What can we do?
•Establish surveillance programs (broad then focus on hotspots, >40% infection)
•Identify mechanisms of emergence(natural, stressors, novel strains)
•Identify and implement intervention strategies(break host-pathogen cycle, reduce stressors,
biosecurity precautions)
Gray and Miller (2013)
Global Ranavirus Consortiumhttp://fwf.ag.utk.edu/mgray/ranavirus/ranavirus.htm
The goal of the GRC is to facilitate communication and collaboration among scientists and veterinarians conducting research on ranaviruses and diagnosing