Controls on pathogen species richness in plants' introduced and native ranges: roles of residence time, range size and host traits

Abstract

Introduced species escape many pathogens and other enemies, raising three questions. How quickly do introduced hosts accumulate pathogen species? What factors control pathogen species richness? Are these factors the same in the hosts' native and introduced ranges? We analysed fungal and viral pathogen species richness on 124 plant species in both their native European range and introduced North American range. Hosts introduced 400 years ago supported six times more pathogens than those introduced 40 years ago. In hosts' native range, pathogen richness was greater on hosts occurring in more habitat types, with a history of agricultural use and adapted to greater resource supplies. In hosts' introduced range, pathogen richness was correlated with host geographic range size, agricultural use and time since introduction, but not any measured biological traits. Introduced species have accumulated pathogens at rates that are slow relative to most ecological processes, and contingent on geographic and historic circumstance.

Figure 1

The relative importance of biological (black bars) and historic/geographic (grey bars) variables in explaining (a) pathogen species richness in hosts’ native range, (b) pathogen richness in hosts’ introduced range, (c) proportional pathogen release in hosts’ introduced range (i.e. native range richness minus introduced range richness, then divided by native range richness). Each bar indicates the sum of the Akaike weights of the 11 models that included each explanatory variable. The possible range is from 0 (minimal importance) to 1 (maximal importance). In plants’ native ranges, biological, historic and geographic factors were all important in explaining pathogen richness. In plants’ introduced ranges, pathogen richness and pathogen release were both explained chiefly by historic and geographic, not biological, factors.

Figure 2

In hosts’ native range, pathogen species richness was greater on hosts that occupied a greater number of habitat types (quasi-likelihood Wald test scaled by the model’s residual deviance divided by its degrees of freedom: χ²₁ = 53.3, P< 0.0001). When points had identical x and y coordinates, the x-coordinate was jittered to render all points visible. For simplicity, results from a one-way model are shown. Results were similar in all models analysed, regardless of additional explanatory variables included (e.g. Figure S2).

Figure 3

Historic/geographic factors explaining pathogen species richness and proportional release from pathogens in hosts’ introduced range. Black circles indicate hosts with no history of agricultural use, and grey diamonds indicate hosts with a history of agricultural use. Symbols that are only half-visible are located on the x–y plane (i.e. pathogen richness equals zero or release from pathogens equals one). Chi-square values are from quasi-likelihood Wald tests scaled by the model’s residual deviance divided by its degrees of freedom. Statistics are from the AIC best model for each response variable, which included only sampling effort (log-transformed citation count) and the three explanatory variables shown. Results were similar in all models analysed. (a) Pathogen richness was greater on hosts that had a larger introduced geographic range size (χ²₁ = 34.1, P< 0.0001), a longer residence time in the introduced range (χ²₁ = 19.8, P< 0.0001) and a history of agricultural use (χ²₁ = 26.6, P< 0.0001). (b) Release from pathogens was lesser on hosts that had a larger introduced geographic range size (χ²₁ = 23.8, P< 0.0001), a longer residence time in the introduced range (χ²₁ = 15.3, P< 0.0001) and a history of agricultural use (χ²₁ = 14.7, P= 0.0001). To render all data points visible, the z-axis for pathogen release is reversed, so that 0% release is at the top, and 100% is at the bottom.