Reconstructing historical and contemporary disease dynamics: A case study using the California slender salamander
Introduction
The current global outlook for amphibians is grim (Wake and Vredenburg, 2008). Due to factors such as habitat destruction, climate change, pollution, direct exploitation, the spread of invasive species, and emergent amphibian diseases such as chytridiomycosis (Hof et al., 2011), nearly one third (32.5%) of amphibian species are threatened with extinction, and 43% of amphibian species are experiencing population declines (Stuart et al., 2004). Retrospective studies have found that chytridiomycosis was likely the cause of many of the “enigmatic” amphibian declines (Cheng et al., 2011, Olson et al., 2013) that occurred before the disease was identified in the late 1990’s (Berger et al., 1998, Blaustein, 1994, Pechmann and Wilbur, 1994). Chytridiomycosis, caused by the virulent fungal pathogen Batrachochytrium dendrobatidis (Bd), has now been implicated in mass amphibian die-offs in western North and Central America, often in protected or remote habitats (Lips et al., 2006, Skerratt et al., 2007, Vredenburg et al., 2010), and is associated with declines and possible extinctions in Europe and Australia (Fisher and Walker, 2009, Skerratt et al., 2007).
Because chytridiomycosis was already widespread before it was described, retrospective studies utilizing museum collections are needed to fill in the timeline of disease emergence. Recently developed techniques for reconstructing the history of Bd in museum collections (Cheng et al., 2011) can, in theory, be combined with contemporary sampling of exact localities in order to address hypotheses about disease emergence and persistence. Common species with large numbers of museum specimens are ideal for this approach, because they allow for unbiased sampling across space and time in order to accurately reconstruct disease history.
The California slender salamander, Batrachoseps attenuatus, provides a unique opportunity to perform a retrospective survey of Bd emergence in Northern California. Batrachoseps attenuatus is the most abundant and widespread terrestrial species known to host Bd. This species has a large geographic range throughout coastal Northern California into Oregon and in the northern Sierra Nevada Mountains and is estimated to attain densities of 4470 animals/acre (Anderson, 1960). Additionally, more than 23,000 specimens were collected in the last century and are deposited in permanent museum collections (HerpNet.org), allowing for random subsampling from these extensive samples.
Previous historical studies in California have found early Bd positives dating before the pathogen was first identified, however historical sampling has been both geographically and temporally haphazard. Padgett-Flohr and Hopkins (2009) performed a histological study of ranid frogs and Pacific chorus frogs (Pseudacris regilla), concluding that Bd experienced a slow, radial expansion from a late 1950s introduction site in the San Francisco Bay Area. However, their sampling effort was also highly concentrated in that region. Huss et al. (2014) found earlier positives in an introduced species, the American bullfrog, Rana (Lithobates) catesbeiana, in 1928 in Sacramento County, 1929 at Stanford University in Santa Clara County, 1931 in Butte County, and 1957 in Sonoma County (Fig. 1, Fig. S1), suggesting that Bd has been present in California for almost a century. Field observations from 1973-4 in nearby Alameda County reported B. attenuatus dying in the wild with clinical symptoms characteristic of chytridiomycosis (Maiorana, 1977a). This later prompted a histological study of 34 historical B. attenuatus specimens, which found Bd-positive specimens from as early as 1973 in Contra Costa County, CA (Weinstein, 2009). The same study showed that Bd is almost always fatal to B. attenuatus salamanders in captivity.
The arrival or emergence of Bd in naïve amphibian populations is characterized by a rapid increase in Bd prevalence in host populations, while infection intensities on individuals grow to over 4-5 orders of magnitude (Vredenburg et al., 2010). These epizootic events are characterized by high Bd prevalence and transmission rates, and high host mortality (Brem and Lips, 2008, Briggs et al., 2010). Epizootic events generally result in one of two alternatives: the extirpation of host populations or the establishment of more stable pathogen/host dynamics (a sustained enzootic state). Once a disease has become enzootic in a population and the number of susceptible individuals is low, lower transmission rates, disease prevalence, and infection intensities can be expected (Briggs et al., 2010). However most enzootic populations are encountered by collectors after the epizootic phase has passed; therefore a clear reconstruction of the history of disease in a population following the transition from and enzootic to epizootic state is rare.
Utilizing the large museum collections of B. attenuatus specimens, we conducted a randomly sampled retrospective survey to describe the spread of Bd across N. California. We evaluated the effect of disease history (based on museum specimens) on the disease presence in contemporary populations. We also evaluated historical and contemporary Bd levels with respect to several biotic and abiotic factors that may affect the ecology of Bd (e.g. temperature, precipitation, proximity to standing water). Finally, we also recorded salamander group size to examine the relationship between social behavior and disease dynamics. Given B. attenuatus’ large range and the time elapsed since Bd’s introduction to California, we predicted that a retrospective survey would reveal variation among populations in their Bd infection histories. By evaluating both historical and contemporary populations of B. attenuatus, at the same locations, we were able to reveal important insights into the temporal dynamics of Bd, as well as the ecological drivers of Bd infections.
Section snippets
Historical survey with museum specimens
We generated a list of 15,007 available B. attenuatus museum specimens housed at the Museum of Vertebrate Zoology in Berkeley and the California Academy of Sciences (using http://www.herpnet2.org). The 12 California counties with the highest museum representation spanning seven decades, 1940-2009, were chosen to be included in this study (Alameda, Butte, Contra Costa, Del Norte, Humboldt, Marin, Mendocino, San Francisco, San Mateo, Santa Clara, Santa Cruz, Sonoma; Fig. S1). Up to twenty
Linking historical and contemporary spread of Bd
Of the 1266 specimens included in the retrospective survey, 40 specimens from 27 distinct localities tested positive for Bd. The earliest positive detected was a 1967 specimen collected in Sonoma County. By the early 1970s, Bd was present in Sonoma, Santa Cruz, and Butte Counties (Fig. 1). Bd was not detected in the northernmost coastal counties Mendocino, Humboldt, and Del Norte in any decade. The second round of historical sampling at Bd-positive sites added 311 specimens at historically
Discussion
The emergence of Bd in the 1960’s in our samples and subsequent proliferation corresponds with known amphibian die-offs in California beginning in the 1970’s and continuing through the present day (Maiorana, 1977a, Bradford, 1991, Weinstein, 2009, Vredenburg et al., 2010). On the other hand, we found no positive Bd individuals from the 1940’s and 50’s. Our retrospective survey of over 1500 samples suggests that Bd likely experienced saltatory spread through California, given the distances
Acknowledgements
We are grateful to the numerous graduate students at San Francisco State University who assisted with salamander swabbing in the field: Angel Conde, Celeste Dodge, Silas Ellison, Raul Figureoa, Andrea Manzano, Audrey Salinas, Jon Young. Also thanks to the undergrads who assisted in swabbing museum collections and field specimens: Jason Anders, Cheyenne Anderson, Allen Atallah, Eleonora Bondareva, Michelle Davila, Alex Harencar, Pearl Tam, Susi Ngoi. Thanks to Dr. Ed Connor and Celeste Dodge for
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