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Batrachochytrium salamandrivorans: Determining the Risk to North America
- 1. Batrachochytrium salamandrivorans: Determining the Risk to North America 1 UTIA Center for Wildlife Health 2 TSU Department of Agricultural & Environmental Sciences Matthew J. Gray1 , Debra L. Miller1 , & William B. Sutton2 F. Pasmans, Ghent Univ. Robertville, Belgium
- 2. Acknowledgements Priya Nanjappa, AFWA J. J. Apodaca, Warren Wilson College Michelle Koo, UC-Berkeley Vance Vredenburg, San Francisco State University Karen Lips, University of Maryland Allan Pessier, San Diego Zoo An Martel, Ghent University Frank Pasmans, Ghent University
- 3. *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
- 4. 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
- 5. A lesion viewed under the microscope… Dead cells (orange arrows) Bsal thalli (black arrows) epidermis Keratin Photomicrograph courtesy Allan Pessier, UC Davis
- 6. 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
- 7. The Perils Martel et al. 2014. Science al Salamander-specific pathogen? 10 Anurans 24 Salamanders Infected no death Infected some death Infected 100%
- 8. * 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%
- 9. Jenkins et al. 2013. PNAS. http://www.biodiversitymapping.org/amphibians.htm The Perils
- 10. Amphibian richness, 270 spp, 190 salamanders The Perils
- 11. The Perils Many SE States!
- 14. Risk Model Final Risk Assessment Model - Relative Risk = SpRich * Log ClimSuit Bsal
- 15. 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
- 16. 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 Murray 1 5
- 17. 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
- 18. 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
- 19. North American Species Tested Clinical Disease Subclinical Disease Not infected: Martel et al. (2014)
- 20. 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.
- 21. 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
- 22. Salamandridae: North America – 7 Species
- 23. 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.
- 24. Woodland Plethodontids • Only one species tested: Plethodon glutinosus was not susceptible • Very diverse; regionally endemic
- 25. Ambystomatids • Threat- possibly low • 2 species tested; not susceptible
- 26. Sirenidae • Threat - moderate • One species tested; “tolerant” of infection
- 27. Waterdogs and amphiumas • None tested
- 28. Splerpines • Gyrinophilus was not susceptible • Eurycea & Pseudotriton not tested • Hemidactylium not tested
- 29. Research Directions 1) 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
- 30. Research Directions 2. Surveillance: • Wild populations (new vs. preserved) • Captive populations Locations? Species?
- 31. Organizational Structure TAC Co-Chairs: Dede Olson (USFS), Jenn Ballard (USFWS) Southern Appalachian Task Force: Caleb Hickman (EBCN)
Editor's Notes
- - fire salamanders considered extirpated in Netherlands, add’l wild mortality in Belgium Martel’s 2014 study sampled wild, museum, pet store/capitve collection animals, several thousands in total – found Bsal in low prevalence, but where detected, present in primarily Asian spp Deep, ulcerative lesions – invades all epidermal layers and keratinocytes, causes apathy, ataxia, and anorexia - see background pic - pockmarks, as well as foreground lesions, histological/electron microscopy
- Three families found in US showed susceptibility to Bsal infection; Two species found in US had lethal impacts; One species found in US was tolerant – infection in absence of clinical disease Sample sizes low, but high susceptibility among salamandrids US has 7 species of salamandrids in both eastern and western US, and some of these are quite abundant
- Over 10 yrs, 2.3 million imported into US, majority of these are Asian newt spp. - Imports have declined in the past 5-6 yrs, reasons unclear.
- Clinton Jenkins et al patterns terrestrial biodiversity 655 species of salamanders worldwide 25% of all species occur in North Americ
- 190 spp of sallies (out of 270 amphibs) 100 species of salamanders in Appalachians alone State perspective – states charged with managing all species in the public trust = ensuring healthy, sustainable populations Bd was here by the time we started looking, but at least 3 frog spp affected /listed in past decade Currently 17 spp of salamanders listed, few more petitioned WNS provides an example of an emerging disease that has already impacted 7 species; 2 of these were already endangered, one petitioned for listing
- To put this in perspecitve, 47-48 bats total in continental US – can see that in NC alone, more spp of sallies Sallies most abundant in smokies/appalachians, but also CA and PNW - bats, 15% (7 of 47) of known N Amer bat species impacted - If 15 % of sallies affected, that would be 28 species… given disproportionate distributions of sallies, some states in SE may bear a much larger brunt of impact – a majority of the hypothetical 15% impacted could plausibly be found within a handful of states
- the moderate Bs habitat suitability (Fig. 1A) combined with high species richness (Fig. 1B) make this area the most expansive, high-vulnerability zone in North America Discuss alpha and beta diversity 61 salamander species in NC, 48 are Plethodontids Notophthalmus viridescens – eastern newt/red-spotted newt – super expansive range that overlaps with entire vulnerability zone, may act as superspreaders of disease by greatly increasing Bs transmission 3=New York 4=Atlanta, GA 2=Tampa, FL
- large, vagile populations (e.g. efts) that are important in both terrestrial and freshwater ecosystems. Along the west coast of the US and in the Sierra Nevada mountains, they are sympatric with at least 12 other salamander species and Taricha granulosa has the largest range – Bsal lethal to it Alpha vs beta diversity 44 species of salamanders in CA, though at most 12 overlap with each other 1= Los Angeles 5= SF
- Although species richness is not as high as the Appalachian region, this area has some of the highest beta diversity of salamanders in the world Sierra Madre Occidental – western mountain range In addition, previous studies, document the spread of Bd from northern California into Mexico and continuing southward to South America, the same regions highlighted by our salamander Bs vulnerability model. (Lips et al. 2008, Cheng et al 2010) NEW SP. RATE???