Dynamics of an emerging disease drive large-scale amphibian population extinctions

Abstract

Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host-pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host-pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at approximately 700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the near-simultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.

Fig. 1.

Maps of the three study metapopulations showing the spread of Bd and frog population status (adults only) during a 4-year period following the initial detection of Bd. Depicted are Milestone Basin (A–E), Sixty Lake Basin (F–J), and Barrett Lakes Basin (K–O). Lake color (green, yellow, and black) shows the Bd infection and frog population status, and the light gray shaded region surrounds the area in which frog populations were Bd-positive in each year. Lakes shown with a thick black outline are fishless, and a thin gray outline indicates that nonnative fish were present (details on the historic fish distribution are presented in SI Text). The infection status of frog populations depicted in A and K is based on mouthpart surveys of 459 tadpoles. The infection status of frog populations in B–J and L–O is based on 4,591 skin swabs analyzed using a real-time PCR assay.

Fig. 2.

Total number of adult and subadult frogs in the three study metapopulations during 1996–2008 before and after the detection of Bd: Milestone Basin (A), Sixty Lake Basin (B), and Barrett Lakes Basin (C).

Fig. 3.

Box plots showing the effect of Bd arrival on the yearly population growth rate (r_t) of three categories of frog populations: (i) populations before detection of Bd (r_t for each lake averaged over all years before Bd arrival), (ii) populations during the year in which Bd was detected, and (iii) populations 1 year after Bd was detected. In each case, r_t = ln(N_t) − ln(N_t−1), where N_t is the number of adult frogs in the lake in year t. Box plots display the median yearly frog population growth rate (horizontal line), 25th and 75th percentiles (gray boxes), 10th and 90th percentiles (whiskers), and all points that lie outside of the 10th and 90th percentiles (•). Data are from 88 frog populations located in all three study basins (1996–2008).

Fig. 4.

Frog–Bd dynamics in eight intensively sampled populations in Milestone and Sixty Lake Basins before and after detection of Bd: frog counts (adults + subadults) from visual encounter surveys (A); infection prevalence, defined as the fraction of skin swabs collected from each population on each date positive for Bd (B); and infection intensity, defined as the average zoospore equivalents on swabs collected from each population on each date (C). Data are from frog populations that were sampled more than once per year, experienced >80% declines by the end of 2006, and for which the decline in the number of frogs was >10. This last criterion excluded populations that were very small before Bd arrival. Populations were aligned along the x axis such that “0” represents the date on which each frog population began to decline. This was calculated for each population by determining the date at which the number of postmetamorphic frogs dropped below 20% of the average population count before that point.