We have observed a remarkable increase in large-scale, sudden onset of decline (unknown causes) and known disease (bacterial, fungal, viral) outbreaks in the last few decades, with more predicted globally (Ganley et al., 2009). Increases in temperature, changes in the timing and effectiveness of precipitation, the change in the frequency and intensity of other, catastrophic events (e.g. windthrows, tornadoes, bark beetle outbreaks) and invasions of both native and exotic pathogens have thrown unlikely combinations of host plants, plant pathogens and environmental variability together with unpredicted outcomes. A recent canker outbreak in Alnus tenuifolia in interior Alaska, associated with the hot, dry summer of 2004 (Ruess et al., 2009), has refocused attention on the role of temperature and drought in canker incidence (Schoeneweiss, 1975). In this issue of New Phytologist, Rohrs-Richey et al. (pp. 295–307) open a new line of research in host–pathogen relationships with clarity: an experimental test of the intersection of the phenology of host susceptibility (Alnus fruticosa), the life cycle of the pathogen (Valsa melanodiscus) and environmental variability (temperature, drought). ‘For the first time, Rohrs-Richey et al. quantified the reduction in transpiration directly attributable to a stem canker.’ Alnus is a circumpolar, dominant, deciduous broadleaf shrub in the boreal biome. It is the key genus responsible for nitrogen (N) fixation in floodplains of interior Alaska (Ruess et al., 2009). Alnus is an important food source for insect herbivores, microtines, rodents and ungulates. Warming at high latitudes, especially interior continental regions, has been twofold the global average (IPCC, 2007). Increased temperatures (both winter and summer) will favor an increase in deciduous woody species, but will probably increase plant drought stress (Chapin et al., 2010). Within this context, Rohrs-Richey et al. conducted two tests of the role of drought stress and host phenology in disease development. The first test was imposed at the peak of growth and the second test was imposed in late summer. At peak growth, significant plant drought stress developed additionally in the low-water treatment as a result of high temperatures and high evaporative demand. In late summer, temperatures and evaporative demand were much lower, and plant drought stress was more moderate than in the first test. Although canker development was greater for isolate 2 in the low-water treatment in the first test, disease severity was greater in the second test when conditions were probably more conducive to pathogen growth and spread within the stem (especially laterally). In the second test, there were significant differences in the severity of disease development between the two isolates, which in the first test were apparent only on a single date (day 60 after inoculation) in the low-water treatment for isolate 2. For the first time, Rohrs-Richey et al. quantified the reduction in transpiration to be directly attributable to a stem canker. This set of experiments demonstrates the importance of the intersection, and the interaction of host plant phenology (and the plant capacity for resistance, tolerance or defense) and the coincidence of optimal environmental conditions for pathogen growth. Their results challenge the role of drought stress in host susceptibility to cankers. Other studies have demonstrated the role of plant host phenology in susceptibility to disease. Active cambial tissue was correlated to successful infection (Quercus agrifolia to Phytophthora ramorum; Dodd et al., 2008). The timing of lignification after inoculation in peach canker disease was retrospectively analyzed (Prunus persica vs Cytospora; Biggs, 1997). The role of host phenology was also highlighted in Shaw (2009, pp. S8). The experimental design in Rohrs-Richey et al. was constructed to test the two hypotheses of host susceptibility: plant stress-induced predisposition or through multiple stressor effects on host physiology and thus susceptibility. In this glasshouse experiment, plants in the low-water treatment were not ‘predisposed’ to pathogens. Inoculation efficiency (successful inoculation/total inoculation) was slightly greater (92% vs 87%), as was ramet mortality attributable to V. melanodiscus (1% vs 8%) in test 2 where the overall degree of plant drought stress was moderate (chronic) vs acute in test 1. Disease severity increased with lower overall plant drought stress, but in late summer, the potential for lowered plant defense capacity was untested. There was a slight reduction in the proportion of inoculated ramets that produced callus (70% vs 63%) in late summer, suggesting at least down-regulated morphological defense (e.g. reduced cambial activity in late summer). The authors report some evidence for and against the multiple-stressors hypothesis. The evidence against the multiple-stressors hypothesis was a general depression in maximum photosynthesis: drought stress plus disease was not additive or synergistic. The evidence in support included a steeper quantum efficiency (greater carbon gain per mol of light received) and half the light-saturated photosynthetic rate accompanying plant drought stress plus disease. However, alder was less drought-stressed than perhaps phenologically challenged: the environmental conditions were more favorable to pathogen growth in late summer and were perhaps coupled with the plant host’s incapacity to respond (resist, tolerate and defend) to the pathogen in late summer. The pathogen is responsive over a short time-period: weeks to months. They are flexible organisms, particularly adapted to a changing environment. Plant phenological patterns are somewhat flexible within a growing season and somewhat plastic from generation to generation. However, photoperiodism will not be altered by climatic change. Plant programmed response to photoperiod is likely to require many, many generations, even with strong selection such as increased disease incidence. The authors have clarified a new approach to host–pathogen relationships: the nexus between the phenology of the host plant, the life history of the pathogen and the environmental conditions favorable for pathogen development. Warmer temperatures may lead to higher-water-content snow and to warmer snow that is heavier and remains in situ rather than being redistributed at high latitudes. Heavier snow may increase mechanical damage to underlying vegetation. Mechanical damage results in more wounding with subsequent pathogen entry (e.g. Cupressus macrocarpa vs Seiridium cardinal; Hood et al., 2009). The greater amplitude of temperature changes at high latitudes results in greater freeze–thaw cycles, which also result in greater likelihood of fungal, bacterial or viral entry points (Betula alba vs Botryosphaeria dothidea; Crist & Schoeneweiss, 1975). Because there is more, heavier snow, patterns of herbivory change: there may be more under-snow herbivory and wounding of stems. Increased temperatures at higher latitudes translate to greater survival rate of beetles, which are vector pathogens. Insect herbivory on stems also increases entry points for pathogens (Chamaecyparis obtuse vs Epinotia granitalis; Yamada et al., 2000; Pinus radiata vs Aphrophora canadensis; Storer et al., 1998). Conversely, canker presence increases attack by beetles, and in the case of P. radiata in urban ecosystems, an increase in invasive beetle attack (Dendroctonus valens; Storer et al., 2002). Higher temperatures increase the abundance of insects already in situ; they alter insect herbivores by permitting either new insect species, or new fungal, bacterial, or viral associates of already occurring insects, to move northward. It is these new associates that may have the greatest potential for future sources and magnitude of mortality (Lu et al., 2010). An increase in disease is almost always correlated to reduction in biomass and, in alder, to a reduction in N-fixing capabilities (Ruess et al., 2009). Alder occurs along rivers, and their N inputs through N fixation dominate freshwater N dynamics. Dissolved inorganic nitrogen (DIN) and dissolved organic nitrogen (DON) are the primary controllers of freshwater ecosystem productivity and food chains. The recent reduction in alder as a result of canker outbreak in 2004 was estimated to have reduced terrestrial N inputs by 30% (Ruess et al., 2009). The complexities of interactions in climate–host–disease–insect interactions are particularly difficult to predict, in part because relatively little is known about wildland vs agronomic cankers, the specificity of the attacks (host–pathogen), the diversity of the pathogens themselves (fungal, bacterial or viral) and the likelihood for climate-induced stress, stress-increased susceptibility to pathogen entry and pathogen-induced increases in susceptibility to insects or stress-enhancing effects (original or new stresses). Rohrs-Richey et al. open a new line of research in host–pathogen relationships: an intact-plant, experimental test of the intersection and inter-relationships of the phenology of host susceptibility, the life cycle of the pathogen and environmental variability (Fig. 1). Coupling host phenology and patterns of pathogen development will probably permit a more mechanistic approach to model the effects of climate change on disease and insect dynamics at the landscape level. Modification of the environment–host–pathogen triangle (Stevens, 1960), indicating the importance of interactions between the physiology of the host and the capability of successful inoculation and growth of the pathogen under changing environmental conditions. Important components of environmental change include elevated temperature and greater duration of favorable conditions for plant and pathogen growth; change in atmospheric chemistry; and changes in precipitation patterns, including higher frequency, duration and intensity of drought. Some of the attributes of the plant host that are relevant under changing environmental conditions include earlier onset of bud break and delayed onset of senescence; the potential for earlier and different magnitudes of peak growth; changes in tissue quantity and quality; and the potential for changes in the timing and type of responses to pathogens (plant capacity for resistance, tolerance, and mechanical and chemical defense). It is unclear for most species how environmental cues for phenology (e.g. degree days of warming, photoperiod) may limit the capacity of long-lived plants to synchronize plant growth with new environmental conditions in situ. Some of the attributes of the plant pathogen that are relevant under changing environmental conditions include the timing of optimal temperatures for growth relative to optimal moisture conditions, the nutritional status of the plant host (the ‘media’) and the changes in the cell structure that permit or slow pathogen growth. The author benefitted from, and wishes to acknowledge, the contributions of Charles G. (Terry) Shaw, Ron Neilson, Jeff Stone, Don Robinson, Jeff Hicke and Sarah Ashton in a group discussion on modeling pathosystems and climate change, 21 October 2010; Portland, OR, USA.
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N. E. Grulke (2010) studied this question.
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