Ecology and Epidemiology of Ranaviruses

transcript

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Unpublished Data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

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

Hoverman et al. (2011): 19 Species Tested

High Moderate

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

Mosquito fish

No Transmission: tilapia, bluegill and fathead minnow

Brenes (2013)

Reservoirs or Amplification Hosts?FV3-like Ranaviruses

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%)

Gray Bull Wood

Transmission to Turtles

Brenes Presentation

Gray et al. (unpubl. data)

Superspreaders and Amplifying Species

Paull et al. (2012)

Frontiers in Ecology and the

Environment 10:75-82

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%

Chorus Frogs

Spotted Salam

Wood Frogs

Spotted Salam

Chorus Frogs

Wood Frogs

Chorus Frogs 44%

Spotted Salam 6%

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%

Chorus Frogs

Southern Toad

Gopher Frog

Southern Toad

Chorus Frogs

Gopher Frog

Chorus Frogs 78%

Southern Toad 76%

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 =

(T-90 Values)

Impacts of Stressors

Gray et al. (2009)

= 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

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)

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?

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

Teacher et al. 2010

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

Questions??

mgray11@utk.edu865-974-2740

Photo: N. Wheelwright

Ecology and Epidemiology of Ranaviruses

Education