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Batrachochytrium salamandrivorans: Determining the Risk to North America
1UTIA Center for Wildlife Health2TSU Department of Agricultural &
Environmental Sciences
Matthew J. Gray1, Debra L. Miller1, &William B. Sutton2
F. Pasmans, Ghent Univ.
Robertville, Belgium
Acknowledgements
Priya Nanjappa, AFWAJ. J. Apodaca, Warren Wilson College
Michelle Koo, UC-Berkeley Vance Vredenburg, San Francisco State University
Karen Lips, University of MarylandAllan Pessier, San Diego ZooAn Martel, Ghent University
Frank Pasmans, Ghent University
*2010: 96% wild mortality in Netherlands*2013 & 2014: wild mortality in Belgium *2015: UK (trade) and Germany (captivity) *Present in:*wild salamanders in Asia (Vietnam, Thailand, Japan)*museum records in Asia >150 yrs*possible Asia origin
Martel et al. 2013, PNAS;Martel et al. 2014. Science; Cunningham et al. 2015. Veterinary Record;Sabino-Pinto et al. 2015. Amphibia-Reptilia
The Pathogen
Frank Pasmans
Unknown to occur in North America
Salamandra salamandra
Bsal Pathology -- DEB
Multifocal erosions and deep ulcerations of the skin throughout the body
Death generally occurs in under 2 weeks after a short episode of anorexia, apathy, and ataxia
Dotearth.blogs.nytimes.com (Credit Frank Pasmans/Ghent University)
Blooi, M. et al. 2015
A lesion viewed under the microscope…
Dead cells (orange arrows)Bsal thalli (black arrows)
epidermis
Keratin
Photomicrograph courtesy Allan Pessier, UC Davis
How does Bsal chytridiomycosis differ from Bd chytridiomycosis?
Bd Bsal
Near full-thickness necrosis (loss) of epidermis with numerous chytrid thalli (mostly empty) that frequently show internal septa (colonial thalli; arrows). Orange circle shows an intact cell (keratinocyte) with 2 chytrid thalli in its cytoplasm.
Thickening of the skin (epidermis) and outer keratin layer with numerous thalli in superficial keratinocytes (note various stages; some with zoospores, green arrows; some empty, orange arrows). The cells (keratinocytes) within the epidermis are still distinct and somewhat in layers.
Photomicrographs courtesy Allan Pessier, UC Davis
epidermis
The Perils
Martel et al. 2014. Science
al
Salamander-specific pathogen?
10 Anurans24 Salamanders
Infected no deathInfected some deathInfected 100%
* 100,000+ annual salamander imports to US* primarily Asian newt species
* North American species are susceptible
The Perils
Jason Quinn
Gray et al. (in press). PLOS Pathogens
$1,000,000 per year
Pachytriton
95%
Jenkins et al. 2013. PNAS. http://www.biodiversitymapping.org/amphibians.htm
The Perils
Amphibian richness, 270 spp, 190 salamanders
The Perils
The Perils
Many SE States!
Thermal preference
Risk Model
Final Risk Assessment Model - Relative Risk = SpRich * Log ClimSuit Bsal
Appalachia and Southeast US
• Highest taxonomic diversity• 7/10 Families
– Plethodontidae– Salamandridae
• Up to 29 co-occurring species• Many endemic species• Includes Eastern Newt range
Photos by Henk Wallays and Todd Pierson
West Coast of the US• Highest Bsal habitat suitability• 5/10 Families
– Salamandridae and Plethodontidae• Up to 12 co-occurring species• Includes Rough-skinned newt range
Photos by Tiffany Yap, Harry Greene, Todd Pierson, and Sam Murray1
5
Central Highlands of Mexico
• Sierra Madre Occidental, Sierra Madre Oriental, and Trans-Mexican Volcanic Belt
• Hotspots of tropical salamander diversity
• High endemism; high beta diversity• Many are threatened or endangered
Photos by Abel Batista, Todd Pierson, Sean Rovito
6
Which NA Ports Pose Greatest Threats for Bsal Introduction?
Identification of At-Risk Ports:
•Shipments 2010 – 2014
•Native ranges in Asia
•Shipments through Asia
•99% shipments from Asia
•98% of shipments Asian species
•91% of shipments contained C. pyrrhogaster, C. cyanurus, & P. deloustali
North American Species Tested
Clinical Disease
Subclinical Disease
Not infected:
Martel et al. (2014)
Threat to southern Appalachian species
• Threat- moderate• 1 of 3 Hynobs “tolerant” to Bsal• Habitat of S. keyserlingii- terrestrial but breed in permanent
pools• Cryptobranchids unknown.
Salamandrids
• Threat- high• Nearly all species died from infection at a low dose• Large populations and widespread- might serve as amplification
host • Terrestrial and aquatic post-metamorphic forms & high dispersal
give this family the ability to rapidly spread Bsal
Salamandridae: North America – 7 Species
Dusky and climbing salamanders
• Threat- Possibly high• Bsal was lethal in Hydromantes, which is very similar
ecologically to Aneides• Desmogs: many regionally endemic; none tested.
Woodland Plethodontids
• Only one species tested: Plethodon glutinosus was not susceptible
• Very diverse; regionally endemic
Ambystomatids
• Threat- possibly low• 2 species tested; not susceptible
Sirenidae
• Threat - moderate• One species tested; “tolerant” of infection
Waterdogs and amphiumas
• None tested
Splerpines
• Gyrinophilus was not susceptible
• Eurycea & Pseudotriton not tested
• Hemidactylium not tested
Research Directions1) Host range: • Susceptibility Trials• SE Unique lineages• Cryptobranchids• Necturus• Desmognathus• Eurycea• Aneides• Amphiuma• Plethodon (limited)• Ambystoma (limited)
• NW Unique lineages• Dicamptodon • Rhyacotriton• Taricha (limited)
Dose Dependent (LD 50 Estimate)
5 x 103-6 Zoospores
Dec/Jan = P. shermani, A. opacum, L. chiricahuensis, H. chrysoscelis, L. sylvaticus
Spring/Summer = Chryptobranchus, Necturus,
A. laterale, L. clamitans, Pachytriton
Research Directions
2. Surveillance:• Wild populations (new vs. preserved)
• Captive populations
Locations?Species?
Organizational Structure
TAC Co-Chairs: Dede Olson (USFS), Jenn Ballard (USFWS) Southern Appalachian Task Force: Caleb Hickman (EBCN)