Divergent population responses following salamander mass mortalities and declines driven by the emerging pathogen Batrachochytrium salamandrivorans.

Understanding wildlife responses to novel threats is vital in counteracting biodiversity loss. The emerging pathogen Batrachochytrium salamandrivorans (Bsal) causes dramatic declines in European salamander populations, and is considered an imminent threat to global amphibian biodiversity. However, real-life disease outcomes remain largely uncharacterized. We performed a multidisciplinary assessment of the longer-term impacts of Bsal on highly susceptible fire salamander (Salamandra salamandra) populations, by comparing four of the earliest known outbreak sites to uninfected sites. Based on large-scale monitoring efforts, we found population persistence in strongly reduced abundances to over a decade after Bsal invasion, but also the extinction of an initially small-sized population. In turn, we found that host responses varied, and Bsal detection remained low, within surviving populations. Demographic analyses indicated an ongoing scarcity of large reproductive adults with potential for recruitment failure, while spatial comparisons indicated a population remnant persisting within aberrant habitat. Additionally, we detected no early signs of severe genetic deterioration, yet nor of increased host resistance. Beyond offering additional context to Bsal-driven salamander declines, results highlight how the impacts of emerging hypervirulent pathogens can be unpredictable and vary across different levels of biological complexity, and how limited pathogen detectability after population declines may complicate surveillance efforts.

Times from Infection to Disease-Induced Death and their Influence on Final Population Sizes After Epidemic Outbreaks.

For epidemic models, it is shown that fatal infectious diseases cannot drive the host population into extinction if the incidence function is upper density-dependent. This finding holds even if a latency period is included and the time from infection to disease-induced death has an arbitrary length distribution. However, if the incidence function is also lower density-dependent, very infectious diseases can lead to a drastic decline of the host population. Further, the final population size after an epidemic outbreak can possibly be substantially affected by the infection-age distribution of the initial infectives if the life expectations of infected individuals are an unbounded function of infection age (time since infection). This is the case for lognormal distributions, which fit data from infection experiments involving tiger salamander larvae and ranavirus better than gamma distributions and Weibull distributions.

Do fatal infectious diseases eradicate host species?

In simple SI epidemic and endemic models, three classes of incidence functions are identified for their potential to be associated with host extinction: weakly upper density-dependent incidences are never associated with host extinction. Power incidences that depend on the number of susceptibles and infectives by powers strictly between 0 and 1 are associated with initial-constellation-dependent host extinction for all parameter values. Homogeneous incidences, of which frequency-dependent incidence is a very particular case, and power incidences are associated with global host extinction for certain parameter constellations and with host survival for others. Laboratory infection experiments with salamander larvae are equally well fitted by power incidences and certain upper density-dependent incidences such as the negative binomial incidence and do not rule out homogeneous incidences such as an asymmetric frequency-dependent incidence either.

Can infectious diseases eradicate host species? The effect of infection-age structure.

It is a fundamental question in mathematical epidemiology whether deadly infectious diseases only lead to a mere decline of their host populations or whether they can cause their complete disappearance. Upper density-dependent incidences do not lead to host extinction in simple, deterministic SI or SIS (susceptible-infectious) epidemic models. Infection-age structure is introduced into SIS models because of the biological accuracy offered by considering arbitrarily distributed infectious periods. In an SIS model with infection-age structure, survival of the susceptible host population is established for incidences that depend on the infection-age density in a general way. This confirms previous host persistence results without infection-age for incidence functions that are not generalizations of frequency-dependent transmission. For certain power incidences, hosts persist if some infected individuals leave the infected class and become susceptible again and the return rate dominates the infection-age dependent infectivity in a sufficient way. The hosts may be driven into extinction by the infectious disease if there is no return into the susceptible class at all.

Resistance in persisting bat populations after white-nose syndrome invasion.

Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat (Myotis lucifugus) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans, which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting populations than in declining populations where the fungus has recently invaded. Fitted models indicate that this is most consistent with a reduction in the growth rate of the pathogen when fungal loads become high. The data are inconsistent with the evolution of tolerance or an overall reduced pathogen growth rate that might be caused by environmental factors. The existence of resistance in some persisting populations of little brown bats offers a glimmer of hope that a precipitously declining species will persist in the face of this deadly pathogen.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.

The Effect of Parasites on Host Population Density and Extinction: Experimental Epidemiology with Daphnia and Six Microparasites.

Parasites have been shown to reduce host density and to induce host population extinction in some cases but not in others. Epidemiological models suggest that variable effects of parasites on individual hosts can explain this variability on the population level. Here, we aim to support this hypothesis with a specific epidemiological model using a cross-parasite species approach. We compared the effect of six parasites on host fecundity and survival to their effects on density and risk of extinction of clonal host populations. We contrast our empirical results of population density with predictions from a deterministic model and contrast our empirical results of host and parasite extinction rates with those predicted by a stochastic model. Five horizontally transmitted microparasites (two bacteria: white bacterial disease, Pasteuria ramosa; two microsporidia: Glugoides intestinalis, Ordospora colligata; one fungus: Metschnikowiella biscuspidata); and six strains of a vertically transmitted microsporidium (Flabelliforma magnivora) of the planktonic crustacean Daphnia magna were used. In life table experiments, we quantified fecundity and survival in individual parasitized and healthy hosts and compared these with the effect of the parasites on host population density and on the likelihood of host population extinction in microcosm populations. Parasite species varied strongly in their effects on host fecundity, host survival, host density reduction, and the frequency with which they drove host populations to extinction. The fewer offspring an infected host produced, the lower the density of an infected host population. This effect on host density was relatively stronger for the vertically transmitted parasite strains than for the horizontally transmitted parasites. As predicted by the stochastic simulations, strong effects of a parasite on individual host survival and fecundity increased the risk of host population extinction. The same was true for parasite extinctions. Our results have implications for the use of microparasites in biological control programs and for the role parasites play in driving small populations to extinction.