Emerging fungal threats to animal, plant and ecosystem health

Abstract

The past two decades have seen an increasing number of virulent infectious diseases in natural populations and managed landscapes. In both animals and plants, an unprecedented number of fungal and fungal-like diseases have recently caused some of the most severe die-offs and extinctions ever witnessed in wild species, and are jeopardizing food security. Human activity is intensifying fungal disease dispersal by modifying natural environments and thus creating new opportunities for evolution. We argue that nascent fungal infections will cause increasing attrition of biodiversity, with wider implications for human and ecosystem health, unless steps are taken to tighten biosecurity worldwide.

Figure 1. Worldwide reporting trends in fungal EIDs

a, b, Disease alerts in the ProMED database for pathogenic fungi of animals and plants (a), and the spatial location of the associated reports (b). c, d, Relative proportions of species extinction and/or extirpation events for major classes of infectious disease agents (c) and their temporal trends for fungal pathogens (d). Primary data sources are given in the Supplementary Information.

Figure 2. Fungal disease dynamics leading to host extinction

a, The presence of a threshold host population size for disease persistence does not prevent host extinction during a disease outbreak, especially in cases in which a lethal pathogen invades a large host population. In a large host population transmission is rapid and all hosts can become infected before the host population is suppressed below the threshold (pathogen transmission rate, β = 0.001 per individual per day; disease induced-death rate, α = 0.02 per day; simulations start with one infected individual and N₀ susceptible individuals). b, Long-lived infectious stages can increase the potential for host extinction. The fraction of hosts killed in a disease outbreak is shown as a function of the duration of the free-living infectious spore stage (pathogen transmission rate, β = 5 × 10⁻⁶; disease-induced death rate, α = 0.02; rate of release of spores from infected hosts, ϕ = 10; outbreaks initiated with one infected host in a population of N₀ susceptible individuals). c, Saprophytic growth: equilibrium densities of susceptible and infected hosts and free-living spores as a function of the rate of saprophytic growth, σ. With no (or low levels of) saprophytic growth, the basic reproductive rate of the pathogen (R₀) is less than 1, the pathogen cannot invade the system and the host persists at its disease-free equilibrium density. Intermediate levels of saprophytic growth allow the pathogen to invade and persist with the host. High levels of saprophytic growth lead to extinction of the host, and the pathogen persists in the absence of the host (host intrinsic rate of increase, r = b − d₀ = 0.01; density-independent host death rate, d₀ = 1 × 10⁻³; strength of density dependence in host death rate, d₁ = 1 × 10⁻⁴; pathogen transmission rate, β = 1 × 10⁻⁵; disease-induced death rate, α = 0.02; rate of release of spores from infected hosts, ϕ = 10, density-independent spore mortality rate, μ₀ = 1; strength of density-dependence in spore mortality rate, μ₁ = 1 × 10⁻⁴). d, The presence of a tolerant host species (host species A), which can become infected and shed infectious spores can lead to the extinction of a susceptible host species (host species B). Species A does not die because of the disease, but species B has a disease-induced per-capita mortality rate of α_B. Species B is driven extinct at high densities of species A. For all parameters, subscripts A or B indicate the host species. Host intrinsic rates of increase, r_A = r_B = 0.01; density-independent host death rates, d_A0 = d_B0 = 1 × 10⁻³; host birth rates, b_A = b_B = r_A + d_A0; density-independent death rate for species, B d_B1 = 1 × 10⁻⁴; rate of release of spores from infected hosts, ϕ_A = ϕ_B = 10; α_B = 0.05; spore mortality rate, μ = 1. The density of tolerant species N_A was varied by varying d_A1 (the strength of density-dependence in host species A), such that N_A = r_A/d_A1.