An Aquatic Disease on a Terrestrial Salamander: Individual and Population Level Effects of the Amphibian Chytrid Fungus, Batrachochytrium dendrobatidis, on Batrachoseps attenuatus (Plethodontidae)
The pathogenic chytrid fungus Batrachochytrium dendrobatidis, typically associated with anuran amphibians, is present in natural populations of the terrestrial salamander, Batrachoseps attenuatus, from California, USA, and four congeners from California and Oregon, USA. I demonstrate that the chytrid has been present in wild populations of B. attenuatus since at least 1973, and while infected salamanders collected in the wild exhibited 100% mortality in the laboratory, wild populations appear to have remained stable with seasonally variable infection rates. Laboratory experiments showed that inoculated salamanders housed in dry microhabitats, mimicking summer aestivation conditions, are able to shed the chytrid infection. Combining these data with the decrease in prevalence from spring to fall suggests that environmental conditions in the natural range of B. attenuatus mediate the effects of this potentially highly lethal pathogen, stabilizing this host–pathogen relationship. While B. attenuatus continues to be an abundant salamander, other amphibians are experiencing marked declines. An understanding of the relationship between the amphibian chytrid fungus and species of Batrachoseps may be applicable to patterns of declines and persistence in other species of plethodontid salamanders, and amphibians in general.Abstract
Survival analysis of infected (n = 19) vs. uninfected (n = 11) Batrachoseps attenuatus collected in the field for survivorship study I. Kaplan Meier Curve, Log-rank test, P = 0.0001, censoring: 1 in each group at day 29. Day 0 represents the date of collection and the start of observations.
Regression analysis of zoospore quantity by time to death in Batrachoseps attenuatus collected with naturally acquired Batrachochytrium dendrobatidis infection in survivorship study I. Zoospore growth rate is positive and significantly greater than zero (one-tailed Student's t-test, mean = 0.014, SE = 0.043, t = 3.15, P = 0.0033).
Kaplan Meier Curve comparing survivorship between inoculated and control salamanders housed in wet and dry containers in survivorship study II. Uninfected controls are omitted from figure. (Log-rank test, P = 0.04).
Regression analysis of zoospore quantity by time since B. dendrobatidis inoculation in dry housed B. attenuatus in survivorship study II. Zoospore growth rate is negative and significantly less than zero (one-tailed Student's t-test, mean = −0.28, SE = 0.064, t = −4.41, P = 0.007).
A series of photographs of a single infected Batrachoseps attenuatus over a ten-minute observation period. Dark brown spots (example marked with arrow) are initially visible on the ventral surface of the salamander (A). The outer layer of skin is shed in fragments (B). Following shedding no dark marks are visible on the salamander (C). Photographs by Anand Varma.
Batrachochytrium dendrobatidis infecting Batrachoseps attenuatus. (A) Specimen collected in 1974 in Contra Costa County, with brown spots characteristic of Bd infection. Box demarcates area of skin removed for histological examination. (B) Histological section of skin showing zoosporangia (arrow) under melanized spot. Scale bar = 50 μm. (C) Sloughed skin showing concentration of chytrid thalli (arrow), at various stages of development, within melanized spot. Scale bar = 50 μm.
Contributor Notes
Associate Editor: M. J. Lannoo.