Climate change accelerates local disease extinction rates in a long‐term wild host–pathogen association

Abstract

Pathogens are a significant component of all plant communities. In recent years, the potential for existing and emerging pathogens of agricultural crops to cause increased yield losses as a consequence of changing climatic patterns has raised considerable concern. In contrast, the response of naturally occurring, endemic pathogens to a warming climate has received little attention. Here, we report on the impact of a signature variable of global climate change - increasing temperature - on the long-term epidemiology of a natural host-pathogen association involving the rust pathogen Triphragmium ulmariae and its host plant Filipendula ulmaria. In a host-pathogen metapopulation involving approximately 230 host populations growing on an archipelago of islands in the Gulf of Bothnia we assessed changes in host population size and pathogen epidemiological measures over a 25-year period. We show how the incidence of disease and its severity declines over that period and most importantly demonstrate a positive association between a long-term trend of increasing extinction rates in individual pathogen populations of the metapopulation and increasing temperature. Our results are highly suggestive that changing climatic patterns, particularly mean monthly growing season (April-November) temperature, are markedly influencing the epidemiology of plant disease in this host-pathogen association. Given the important role plant pathogens have in shaping the structure of communities, changes in the epidemiology of pathogens have potentially far-reaching impacts on ecological and evolutionary processes. For these reasons, it is essential to increase understanding of pathogen epidemiology, its response to warming, and to invoke these responses in forecasts for the future.

Pathogen exposure disrupts an organism's ability to cope with thermal stress

“…Ockendon et al, ; Sinclair et al, ), our understanding of how co‐occurring stressors will interact to shape the responses of species and populations remains poor (see Schäfer & Piggott, ). With both thermal environments and the geographical distributions of pathogens predicted to undergo considerable shifts in the coming years (Gehman et al, ; Tesla et al, ; Zhan, Ericson, & Burdon, ), the interplay between temperature and pathogen exposure will likely determine both the capacity of a population to cope with global change and the spread of infectious disease (Gehman et al, ; Greenspan et al, ; Shapiro, Whitehead, & Thomas, ; Shocket, Vergara, et al, ; Sternberg & Thomas, ). Few studies, however, have examined the impact of infection on a host's capacity to cope with thermal stress (but see Greenspan et al, , and references therein).…”

Strategies of Phytophthora infestans adaptation to local UV radiation conditions

“…Climate change, a multiple-component phenomenon involving long-term shifts in the average and distribution of many weather parameters such as air temperature, UV radiation, and precipitation (Häder et al, 2015;Milchunas et al, 2004;Siepielski et al, 2017;Zhan, Ericson, & Burdon, 2018), is posing an imminent threat to the earth. Intergovernmental Panel on Climate Change (IPCC) and…”

“…Climate change, a multiple‐component phenomenon involving long‐term shifts in the average and distribution of many weather parameters such as air temperature, UV radiation, and precipitation (Häder et al, ; Milchunas et al, ; Siepielski et al, ; Zhan, Ericson, & Burdon, ), is posing an imminent threat to the earth. Intergovernmental Panel on Climate Change (IPCC) and other scientific assessments predict that the current cycle of climate change may continue for decades (Altizer et al, ; Gleick et al, ; IPCC, ) and warn that immediate actions should be taken to mitigate potentially and irreversibly catastrophic impacts of climate change on ecological functions and sustainability.…”

Rapid adaptation of the Irish potato famine pathogen Phytophthora infestans to changing temperature

“…The epidemiological development of infectious diseases results from the interaction of three main factors: a conducible environment, a susceptible host, and a virulent pathogen (Madden, Hughes, & Bosch, 2007). Climate change is expected to exert a strong impact on the epidemics and ecology of plant and animal diseases (Garrett, Dendy, Frank, Rouse, & Travers, 2006;Sparks, Forbes, Hijmans, & Garrett, 2014;Zhan, Ericson, & Burdon, 2018), greatly threatening food security, natural landscapes, and human health (Boland, Melzer, Hopkin, Higgins, & Nassuth, 2004;Kalinda, Chimbari, & Mukaratirwa, 2017;Myers et al, 2017). These epidemic effects on infectious diseases can result from the influences of climate changes on the survival, reproduction, and transmission of both pathogens and hosts and can occur at various spatial and temporal scales (Koelle, Pascual, & Yunus, 2005).…”