ecology and epidemiology of ranaviruses
DESCRIPTION
2013 International Symposium on RanavirusesTRANSCRIPT
Ecology and Epidemiology of Ranaviruses:
Mechanisms Contributing to Outbreaks
University of TennesseeCenter for Wildlife Health
Department of Forestry, Wildlife and Fisheries
Matthew J. Gray
M. Niemiller
Presentation Contributors
M. Brand, University of TennesseeR. Brenes, University of TennesseeJ. Chaney, University of Tennessee
J. Earl, NSF NIMBioSN. Hilzinger, University of Tennessee
J. Hoverman, Purdue UniversityR. Huether, University of Tennessee
A. Kouba, Memphis ZooD. Miller, University of TennesseeP. Reilly, University of TennesseeS. Roon, Oregon State University
B. Sutton, Clemson UniversityJ. Tucker, Humboldt UniversityT. Waltzek, University of Florida
B. Wilkes, University of Tennessee
Unpublished Data
Ranavirus Ecology Gray et al. (2009)
Gray et al. (2009)
Global Distribution of Ranavirus Cases: Amphibians
All Latitudes, All Elevations14 Families: Alytidae, Ranidae, Hylidae, Bufonidae, Leptodactylidae, Dendrobatidae,
Discoglossidae, Myobatrachidae, Rhacophoridae, Scaphiopodidae, Ambystomatidae, Salamandridae, Hynobiidae, Cryptobranchidae
5 Continents: 1992
Miller et al. (2011)
>70 Species
Reported Ranavirus Cases in North America: Amphibians
>30 States & 5 Provinces;
46 Species
FamiliesBufonidae
HylidaeRanidae
ScaphiopodidaeAmbystomatidae
CryptobranchidaePlethodontidaeSalamandridae
Norman Wells, NWT
Uncommon
Lithobates sylvaticus
2011
Cases of FV3-like Ranaviral Disease in Reptiles
Over >95% homology with 1000-bp region of MCP
Gopherus polyphemus, Testudo hermanni, Terrapene carolina carolina, Trionyx sinensis, Uroplatus fimbriatus, and
Chondropython viridis
(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)
At least 14 reptile species Marschang (2011)
Cases of Ranaviral Disease in Fishes
Ictalurus melas, I. nebuosa, Silurus glanis, Psetta maxima, Sander lucioperca, Perca fluviatilis, P. flavescens, Oncorhynchus mykiss, Pomoxis nigromaculatus, Gambusia affinis, Epinephelus tauvina
Journal of Fish Diseases 33:95-122
At least 20 fish speciesEHNV, ECV LMBV, SGIV
Species ChallengesFV3-like Ranaviruses
Single-species FV3-like Challenges
Amphibians
Pe
rce
nt
mo
rta
lity
0
10
20
30
40
50
60
70
80
90
100
FV3
RI
Hoverman et al. (2011): 19 Species Tested
High Moderate
Low
Single-species FV3-like ChallengesAmphibians
Ambystomatidae Ranidae
Brenes (2013)
15 Additional Species
Life History and PhylogenyAmphibians
P = 0.354 • Fast development hatching time*• Low aquatic index • Breeding habitat (temporal)*• Breeding time (spring)
• Distance: Population & Isolate
Brenes (2013)
All Three Isolates
Smoky Mountains Isolate
No Phylogenetic Signal
35 spp
Co-evolution
High Correlation (r = 0.88) between
Infection Prevalence and Percent
Mortality
Single-species FV3-like ChallengesChelonians
Mississippi Map Turtle
Control Turtle Fish Amph
Soft-shelled Turtle
Brenes (2013)
Terrapene carolina, T. ornata, Elseya latisternum, Emydura krefftii , Trachemys scripta
Water bath exposure sufficient for transmission with some species.
Greatest infection and morbidity with IP infection or oral inoculation.
Ariel (1997), Johnson et al. (2007), Allender (2012), Gray et al. (unpubl. data)
Single-species FV3-like & ATV Challenges
Fishes
Amelurus melas, Esox luscious, Sander lucioperca, Micropterus salmoides
Cyprinus carpio, Carassius auratus, Lepomis cyanellus
Scaphirhynchus albus
No Transmission:
Low Transmission:
High Mortality:
Jancovich et al. (2001), Bang Jensen et al. (2011a)
Gobbo et al. (2010), Bang Jensen et al. (2009, 2011b), Picco et al. (2010)
Waltzek et al. (unpubl. data)
Single-species FV3-like ChallengesFishes
Channel catfish
Control Turtle Fish Amph
Mosquito fish
Control Turtle Fish Amph
No Transmission: tilapia, bluegill and fathead minnow
Brenes (2013)
Reservoirs or Amplification Hosts?FV3-like Ranaviruses
Low Mortality(Subclinical)
Low Mortality(Subclinical)
Low – High Mortality(Subclinical & Clinical)
Reservoir Reservoir or Amplification
Reservoir
Can Interclass Transmission Occur?
Bandin & Dopazo (2011)
Evidence from the Wild
13 February 2012
26 of 31 Box Turtles Die
from Ranaviral
Disease
Larval anurans and salamanders
dead too
Farnsworth and Seigel, Towson U.
2008 – 2011
North Branch Stream Valley
State Park
Evidence of Interclass TransmissionBayley et al. (2013)
Pike-perch Iridovirus Common Frog Tadpoles
Frog Virus 3Pike
Pike-perchBlack Bullhead
Bang Jensen 2009, 2011; Gobbo et al. 2010
Pallid
Transmission to AnuransGray et al. (unpubl. data)
85% 80% 95%
(35 – 70%) (5%) (95%)
5%
Gray Bull Wood
Transmission to Turtles
35%
45%
5%
Brenes Presentation
Gray et al. (unpubl. data)
Superspreaders and Amplifying Species
Paull et al. (2012)
Frontiers in Ecology and the
Environment 10:75-82
2012
Superspreading Individuals Amplification Species
Disease Hotspots
Susceptibility Contact RateShedding Rate Contact
Host Community Contact RatePersistence Dispersal
•Green et al. (2002)•Petranka et al.
(2003)•Harp and
Petranka (2006)
•Gahl and Calhoun (2010)•Uyeharaet al.
(2010) •Brunner et al.
(2011)
Ranavirus Superspreaders Reilly, Gray, & Miller (unpubl. data)
6 hrs cohabitation
3-day 103PFU/mL
n = 10 tadpoles/tub
20/80 Rule: Superspreading
Exposure Order MattersBrenes (2013)
Only Wood FrogsOnly Chorus Frogs
Only Spotted SalamandersControl
n = 5 pools/trt10 larvae/spp
Inoculated in Lab103 PFU/mL FV3
60 days
Exposure Treatments
Design
Wood Frogs 100%43%
12%
Chorus Frogs
Spotted Salam
72%
3%
Wood Frogs
Spotted Salam
24%
18%
Chorus Frogs
Wood Frogs
Chorus Frogs 44%
Spotted Salam 6%
52%
16%
40%
Appalachian Community
Ecosystem Effects?Disease-induced Trophic Cascades
Community Composition MattersBrenes (2013)
Only Gopher FrogsOnly Chorus Frogs
Only Southern ToadControl
n = 5 pools/trt10 larvae/spp
Inoculated in Lab103 PFU/mL FV3
60 days
Exposure Treatments
Design
Gopher Frogs 100%52%
34%
Chorus Frogs
Southern Toad
70%
58%
Gopher Frog
Southern Toad
32%
80%
Chorus Frogs
Gopher Frog
Chorus Frogs 78%
Southern Toad 76%
62%
62%
68%
Gulf Coastal Plain, USA
Evidence of Environmental Persistence
(Nazir et al. 2012)
•Soil: 13-22 d
•Soil: 30-48 d
(1) FV3, FV3-like
•PW (unsterile): 22-34 d •PW (unsterile): 58-72 d
20 C =
4 C =
(T-90 Values)
Impacts of Stressors
Gray et al. (2009)
*
****
**
23
= 40.1 ; p<0.001
Hatchling – 3X > EmbryoLarval – 4X > EmbryoMetamorph – 5X > Embryo
Impacts of DevelopmentAcross Seven Species
ML Estimate:
Egg membrane may act as a
protective barrier
Haislip et al. (2011)
Tree frog Chorus frog Wood frog Green frog
b
cb
c
a
bb
bb
Kerby et al. (2011)
Anax increased susceptibility to ATV
(A. tigrinum)
Competing Temperature Hypotheses• Virus Replication Hypothesis– Ranavirus replication increases with temperature
up to 32 C– Caveat: Immune function in ectotherms also
increases with temperature• Temperature Induced Stress Hypothesis– Early Spring Breeding Species: • Stressed by Warm Temp
– Summer Breeding Species:• Stressed by Cold Temp
High Pathogenicity at Higher Temperatures
Pathogenicity is Species-specific and Related to Typical Water Temperature Experienced During Tadpole Development
Bayley et al. (2013)
Impacts of Genetic Isolation
Pearman and Garner (2005)
Factors Contributing to Emergence
Other Possible Stressors: Pesticide Mixtures, Nitrogenous Waste, Endocrine Disruptors, Acidification, Global Warming, 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)
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. (2011)
Are Ranaviruses Capable of Causing
Local Extirpations and Species Declines?
0
50
100
150
200
250
1960
1963
1966
1969
1972
1975
1978
1981
1984
1987
1990
1993
1996
Nu
mb
er
of
Po
pu
lati
on
s
Collins & Crump (2009)
Muths et al. (2006)
Traditional Theory(Anderson and May 1979)
Extirpation is possible if:Frequency Dependent
All Conditions Met with
Ranavirus-Host System
Evidence of DeclinesDr. Amber TeacherSoutheastern England
Animal Conservation
13:514-522
1996/97 and 2008
Ranavirus (+) populations
81% Median Reduction
A. Teacher
A. Teacher
Teacher et al. 2010
81%
Evidence of Re-occuring Die-offsDr. 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
Extinction Probability in 1000 yearsEarl and Gray (unpubl. data)
Haislip et al. (2011)Keith Berven
Female Population SizeEarl and Gray (unpubl. data)
Death of Pre-metamorphic Stages
Matters!
Evidence of Rare Species EffectsSutton, Gray, Miller & Kouba
Endangered Dusky Gopher Frog
Evidence of Rare Species EffectsChaney, Gray, Miller & Kouba
Threatened Boreal Toad
Tadpoles Metamorphs
2 – 5 d5 – 7 d
Commonality of Being UncommonSoutheastern United States
Federally Listed:
Species of Concern:
Rana capito sevosa, Ambystoma cingulatum, Phaeognathus hubrichti, Ambystoma bishopi
113 Species and 25 Genera Total
1) Alabama = 14 species (11 genera)2) Arkansas = 25 species (12 genera)3) Florida = 19 species (12 genera)4) Georgia = 22 species (15 genera)5) Kentucky = 22 species (11 genera)6) Louisiana = 15 species (10 genera)7) Mississippi = 18 species (12 genera)8) North Carolina = 41 species (15 genera)9) South Carolina = 19 species (13 genera)10) Tennessee = 26 species (14 genera)
50% U.S.
If uncommon species are highly susceptible, ranaviruses could have a significant impact
on amphibian communities.
Take Home MessagesShould we be Concerned?
•Ranavirus Die-offs have Global Distribution•Ranavirus Prevalence can be High
•Ranaviruses Infect Multiple Amphibian Species with Different Susceptibilities
•Community Composition Matters •Interclass Transmission is Possible – Abundant Reservoirs
•Ranavirus Persistence is Long•High Transmission: Breeding and for Schooling Spp.•Anthropogenic Stressors and Pathogen Pollution
contribute to Ranavirus Emergence
Epidemiological Theory AND Initial Simulations Supports the Premise that Ranaviruses Could Cause Local
Population Extirpations and Contribute to Species Declines
Host-Pathogen Community
Aeromonas hydrophila
RanavirusesBatrachochytrium
dendrobatidis
Alveolates
Complex EpidemiologySpatially Structured Breeding Sites
I(t)ijkl S(t)ijkl
IM(t)ijkl
EM(t)ijkl
i = species
j = age class
k = pathogen
l = wetland
P(Nt)il < 0
S(t|k)ijklI(t|k)ijkl
Metacommunity of Hosts & Pathogens
