Amphibian Decline: Disease Samantha Iversen Nov. 24th, 2009 © Vlad Gerasimov

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Status and Trends of Amphibian Declines and Extinctions Worldwide Stuart et al. 2004. Science 306:1783 Amphibians are more threatened and declining faster than mammals or birds. As of 2004: Mammals = 23% endangered Birds = 12% endangered Amphibians = 32.5% 435 species that are “rapidly declining” - became endangered since 1980. 50 - “overexploited” - heavy extraction 183 - “reduced habitat” 207 - “enigmatic decline” - disease or climate change? 1294 species too poorly known to assess

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Can Disease Cause Extinction? McCallum and Dobson. 1995 Trends Ecol. Evol. 10:8 Parasites usually cannot drive a host species to extinction: As disease : abundance of hosts & abundance of immune individuals . Disease transmission reduced to zero. =Pathogen becomes extinct before host

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Mechanisms of disease-induced extinction Castro and Bolker. 2005. Ecology Letters 8:117-126 Disease can make extinction more likely - drive species to low numbers = genetic bottleneck, random events have a greater effect Biotic Reservoirs: Multiple hosts Abiotic Reservoir: disease survives in environment Already Endangered: Species is endangered before epidemic hits Disease reduces fecundity Disease has intermediate virulence: kills host, but not before disease can spread reservoirs: disease can remain at high incidence independent of population crashes

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation The Effect of Trematode Infection on Amphibian Limb Development and Survivorship Johnson et al. 1999 Science 284:802 1996-1998: Surveyed 35 ponds in Santa Clara County, CA. 4/13 ponds had severely abnormal Pacific treefrogs (15-45%) n=8818 Water tests did not find pesticides, PCBs or heavy metals Collected 200 eggs: hatched normally in lab The 4 ponds with abnormal frogs were only ponds to also support Planorbella tenuis, a snail host to a trematode parasite Ribeiroia sp. Proposed that this parasite could be responsible for the abnormal treefrogs.

Abnormalities Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Abnormalities Different types of abnormalities produced in tadpoles exposed to Ribeiroia: Normal extension in right hindlimb C)Completely missing limbs D) Partially missing limbs E) 4 Extra hindlimbs F) cutaneous fusion in right limb: skin webbing connecting femur to tibiofibula G) bony triangle in left limb H) magnified view of a frog with a femoral projection dorsal side of right femur.

Trematode Experiment Johnson et al. 1999 Science 284:802 Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Trematode Experiment Johnson et al. 1999 Science 284:802 Exposed tadpoles to 6 treatments: 4 equal doses over 10 days Alaria mustelae: another trematode parasite also found in frogs from Santa Clara County. Infection levels chosen to encompass range of parasite densities found in naturally infected abnormal frogs collected from the field sites. Alaria: http://www.fws.gov/longlake/Photo%20Albums/Research%20Album/index.htm Tadpole: 2007 Steven Holt/Stockpix.com Ribeiroia: Dr. Boris Kuperman and Dr. Victoria Matey 1) 0 Ribeiroia (Control) 5) 80 Alaria mustelae cercariae 2) 16 Ribeiroia cercariae 3) 32 Ribeiroia cercariae 4) 48 Ribeiroia cercariae 6) 80 Alaria cercariae +32 Ribeiroia cercariae

Survivorship and Abnormality Frequency Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Survivorship and Abnormality Frequency Dashed line: Abnormality Frequency (# of abnormal metamorphosing frogs/total # of metamorphosing frogs within a given treatment) Solid line: Survivorship (# of tadpoles surviving to metamorphosis stage/N) Black: Survivorship White: Abnormality Frequency B) Alaria does not cause abnormalities and does not cause mortality. Since the second two treatments are the same, only Ribeiroia is responsible for the death and abnormalities.

Chytridiomycosis Berger et al. 1998. Population Biology 95:9031-9036 Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Chytridiomycosis Berger et al. 1998. Population Biology 95:9031-9036 Caused by Cochytrium dendrobatidis, a fungus. Grows in the skin of adult amphibians, and causes erosions and sloughing and roughening of the skin. Causes death in adult amphibians by impairing cutaneous respiration and osmoregulation Also affects tadpoles, but only in the mouth region so it is not fatal. Found infecting amphibians in both South America and Africa. Quickly transmitted © Vance Vredenburg

Chytridiomycosis: Origin Weldon et al. 2004. Emerg Infect dis 10:12 Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Chytridiomycosis: Origin Weldon et al. 2004. Emerg Infect dis 10:12 Originated in Southern Africa: Frogs there don’t die from it Stable endemic infection for 23 years before found outside Africa 2.7% prevalence International trade in Xenopus laevis started in 1930’s Introduced to South America: Hosts there have no immunity X. laevis: African Clawed Frog A common aquarium frog

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Emerging Infectious disease and the loss of biodiversity in a Neotropical amphibian community Lips et al. 2006 PNAS 103:9 Surveyed amphibian populations from 1998 to 2005: 4 streams and 3 terrestrial transects in El Cope, Panama. 698 transect surveys (187 km) and 29,645 captures of amphibians. Checked for presence of B. dendrobatidis in environment: on rocks and in water column as spores Performed tests on the dead frogs for presence of Chytridiomycosis via PCR and histology

Map of Central America: Sites of reported decline Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Map of Central America: Sites of reported decline Population collapses reported in a series of habitats from north to south. El Cope was chosen because it was ahead of the postulated epidemic wave. Map of Central America, with sites of published population declines; lines represent date and location of reported declines (36). Allows prediction of entry into other communities Other communities can act as disease reservoirs: Santa Fe: high pop abundance, high prevalence of the disease, and potential for long-distance dispersal ©2006 by National Academy of Sciences Lips K R et al. PNAS 2006;103:3165-3170

Mortality rates for riparian and terrestrial transects, Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Mortality rates for riparian and terrestrial transects, No dead frogs found in the transects until October, 2004. By January 2005 abundance was severely reduced. Of 318 dead amphibians examined during this time, all but 3 were moderately to heavily infected with Chytridiomycosis Mortality rates for riparian and terrestrial transects, calculated as the proportion of dead frogs in all captures for both night and day transects (1998–2005). No dead animals were found on transects until October 4, 2004, at which time mortality increased until January, 2005, by which time abundance was significantly reduced. Those three were too decomposed to be sure what killed it. Doesn’t mean it wasn’t chytridiomycosis. 1,566 individuals from 59 species tested before October, 2004. None were infected. Infecting 40 species by December 2004. 6/7 samples from substrates associated with dead frogs were positive for B. dendrobatidis Lips K R et al. PNAS 2006;103:3165-3170

Amphibian Density and Species Richness: 1998-2005 Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Amphibian Density and Species Richness: 1998-2005 Amphibian densities and statistical models for riparian and terrestrial transects (1998–2005). By using a segmented linear model for the riparian transects, we found a highly significant difference (θ2) in slope (t = −24.44, df = 486, P < 0.0001), with the estimated time of change (α) being September 4, 2004 (95% confidence interval, September 1–6). We could fit a linear model to only the terrestrial transects (see text for details). Diurnal transects were significantly lower in density than nocturnal ones (t = −13.05, df = 486, P < 0.0001 for riparian transects; t = −9.11, df = 212, P < 0.0001 for terrestrial transects). Species richness and statistical models for riparian and terrestrial transects (1998–2005). By using the segmented linear model for the riparian transects, we found a highly significant difference (θ2) in slope (t = −6.97, df = 486, P < 0.0001), with the estimated time of change (α) being October 22, 2004 (95% confidence interval, October 11–November 3, 2004). We could fit a linear model to only the terrestrial transects (see text for details). Diurnal transects were significantly lower in density than nocturnal transects (t = −21.33, df = 486, P < 0.0001 for riparian transects; t = −6.14, df = 212, P < 0.0001 for terrestrial transects). 6 years of high and increasing population abundances, followed by an abrupt decline in September 2004 for diurnal and nocturnal riparian amphibian communities Little evidence of a decline in terrestrial transects. . ©2006 by National Academy of Sciences Lips K R et al. PNAS 2006;103:3165-3170

Conclusion: Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Conclusion: Strong evidence that Chytridiomycosis is at least partly the cause of amphibian decline. Climate change may have increased the susceptibility to chytridiomycosis or influenced mode of spread. Disease can cause extinction: Presence of abiotic and biotic reservoirs Multiple hosts Long virulence period (24-220 days before frog dies)

Evidence of Decline Causes: Chytrids Causes: Trematodes Conservation Amphibian Conservation plan IUCN/SSC Amphibian Conservation Summit 2005 No available vaccines for Chytridiomycosis. Anti-fungal agents wouldn’t work in wild Breeding in captivity and release into a disease-free zone Breeding to select for resistance. Collection of animals ahead of epidemic spread Disinfection of footwear with bleach to prevent spread of diseases by tourists Try to understand why some species are tolerant, resistant, or able to recover