Chytridiomycosis in CA slender salamanders

Threatened taxa

Data from 2013 IUCN Red List

The threat to amphibians
Amphibians have undergone massive population declines – nearly 1/3 of species are threatened (Skerratt et al. 2007). Threats to amphibians include habitat destruction, climate change, pollution, over-exploitation, UV radiation, competition from introduced species, and disease, such as chytridiomycosis.

What is chytridiomycosis?
Chytridiomycosis is an amphibian disease caused by a fungus, Batrachochytrium dendrobatidis (Bd). This disease has been found in 350+ species of frogs, salamanders, and caecilians worldwide (Fisher et al. 2009). To date, Bd has caused the extinction or decline of 200+ species (Skerratt et al. 2007). Fungal zoospores infect amphibian skin, disrupting water and ion levels. High fungal load (~10,000 zoospores) is often deadly.

Chytridiomycosis in California
The earliest reported case of Bd in California is from two American bullfrogs collected in 1961 near Stanford University (Padgett-Flohr and Hopkins 2009). Because chytridiomycosis was discovered after it had already become widespread, studies using museum collections to describe its historical presence are needed to fill in the timeline of disease emergence.

2 B. attenuatus

California slender salamanders

The California slender salamander
The most widespread terrestrial species known to host Bd infection is the California slender salamander, Batrachoseps attenuatus. Slender salamanders spend their entire lives on land and are super-abundant, presenting a carpet of potential Bd hosts. Large numbers of specimens are also resent in museum collections, providing an excellent opportunity to survey past disease prevalence. Bd is fatal to California slender salamanders, both in the wild and in captivity (Maiorana 1977a, Weinstein 2009).

2012-08-10 15.56.22

Jar of museum salamander specimens

Historical survey
I randomly sampled nearly 1500 museum specimens collected between 1940-2009, housed at the California Academy of Sciences and the Museum of Vertebrate Zoology at Berkeley. I detected disease presence by testing skin swabs for Bd DNA using qPCR methods (Boyle et al. 2004, Hyatt et al. 2007,   Cheng et al. 2011).

Field work
I visited 14 of the same locations where Bd-positive museum specimens were collected and swabbed live salamanders from the same populations. Salamanders were not harmed during field swabbing, and every effort was made to avoid spreading Bd.

Historical results
My research showed that Bd spread in California much more quickly than previously thought (Padgett-Flohr and Hopkins 2009). A decade after the first positive in 1961 near Stanford, CA, Bd was present in Sonoma County to the north, Butte County to the northeast, and Santa Cruz County to the south. The rapid spread over such large distances means that Bd was likely either introduced in multiple locations, or it was moved around the landscape by humans (Daszak et al. 2003; McKenzie and Peterson 2012). Disease prevalence also increased from the 1960’s through the 1990’s (see figure below).

Prop Inf and ZSwab

Historical results. Bars show the proportion of Bd-positive specimens per decade. Lines show the average infection intensity (number of zoospores calculated from amount of Bd DNA per swab).

Additionally, proximity to permanent lakes was an important factor in predicting when Bd arrived at sites. The distance to the nearest lake OR river was not significant, however. This suggests that amphibian species that are found near still water, but not running water are assisting the spread of Bd. American bullfrogs are one such species, are known carriers of Bd, and are not native to California (Pope and Museum 1947; Mazzoni et al. 2003; Schloegel et al. 2009).

Field results
Field specimens had significantly lower prevalence of Bd than historical specimens in the 1990’s, but not 2000’s (see orange bar in above figure). Except in two specimens, disease intensity (zoospore counts) was extremely low.

Split Zswab Prop Inf graph

Field sampling results are arranged in order of year of first historical positive at site, oldest to the left. (Lower panel) Bars show the proportion of Bd-positive specimens per site. (Upper panel) Lines show the average infection intensity.

Current Bd prevalence at a site is negatively correlated with the age of historical infection – sites with earlier infection had lower prevalence than more recent sites. This suggests that the Bd shifts from being a highly fatal, invasive disease when it it first introduced (epizootic) to being in a more stable, less dangerous dynamic with its salamander hosts in these populations (enzootic).

3 B. attenuatus

California slender salamanders from under the same log waiting to be swabbed

California slender salamanders are also highly social, often found under logs together in close proximity. At the sites with earlier introduction of Bd, salamanders were found in smaller groups than at sites with more recent introduction. This may indicate that at older sites, salamanders choose to spend less time close together in order to avoid exposure to Bd. However, with only 14 field sites, this is not enough data to support this conclusively.

Implications
This study revises the timeline of Bd spread in California, showing that Bd spread much farther and faster than seen in previous historical studies. Additionally, introduced amphibians may be important in spreading Bd. Controlling invasive species may likewise help in restricting further spread of this harmful disease.

Host aggregation may be an important mechanism of disease transfer in terrestrial species. Terrestrial species may be able to evolve reduced sociality in response to the introduction of new diseases. So far, most Bd studies have focused on aquatic amphibians. Understanding how this disease spreads among terrestrial hosts might alter disease management practices.

Tiny slender salamanderTo read more about Bd:
Chytridiomycosis on AmphibiaWeb

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