Climate change and forest diseases: using today’s knowledge to address future challenges

The health of the earth’s forests and urban green spaces is increasingly challenged by the outcomes of human activities, including global climate change. As climate changes, the role and impact of diseases on trees in both forest ecosystems and in urban settings will also change. Knowledge of relationships between climate variables and diseases affecting forest and urban trees is reviewed, with specific emphasis on those affecting foliage, shoots, and stems. Evidence that forest diseases are already responding to the earth’s changing climate is examined (e.g., Dothistroma needle blight in northern British Columbia) as are predicted scenarios for future changes in impact on forests by other tree diseases. Outbreaks of tree diseases caused by native and alien pathogens are predicted to become more frequent and intense – this and other general predictions about the effects of climate change on forest and tree diseases are discussed. Despite the uncertainty that accompanies such predictions it is imperative that researchers, forest and urban tree managers, and policy makers work together to develop and implement management strategies that enhance the resilience of the worlds’ forests and urbanized trees. Strategies discussed include monitoring, forecasting, planning, and mitigation.


Introduction
The health and extent of the earth's forested land base is increasingly challenged by the outcomes of human activities, including global climate change.Boreal forests, occupying about 10% of the earth's land cover, are expected to experience some of the most extreme climate change-induced effects while the areas et al., 2006;Sturrock, 2007;La Porta et al., 2008;Moore and Allard, 2008;Dukes et al., 2009;Kliejunas et al., 2009;Tubby and Webber, 2010;Sturrock et al., 2011).These review papers make many common predictions about what to expect from hosts and pathogens and their interactions under future climate changes and the uncertainties associated with these predictions; all emphasize the importance of changes in interactions between biotic diseases and abiotic stressors (e.g., temperature and moisture), as these may represent the most substantial drivers of increased disease outbreaks.

Today's knowledge
At a basic level, healthy forests can perhaps be defined as those comprised of trees that are not limited by the availability of water or nutrients (e.g., nitrogen, phosphorus, sulphur, micronutrients), light or suitable temperatures, and which occur and interact with a complement of other biotic and abiotic factors in a dynamic, sustainable manner.Forest pathogens, which have similar basic requirements, regularly interact with trees and cause disease when their occurrence coincides with the presence of a susceptible host and a favourable environment -a relationship often visualized as the 'disease triangle' (Agrios, 2005).Since the 19 th century, forest management practices, the introduction of several invasive species, and other factors have disrupted the natural equilibrium of many tree host-pathogen interactions; climate change will redefine the shape of the disease triangle and the worlds' forests even further.

Using today's knowledge to predict what might happen under climate change
It is probably safe to say that there is a high level of uncertainty about how to profile fungal tree pathogens into a 'climate-changed future' because 1) generally less is known about their occurrence, incidence, and impact compared with other disturbance agents such as fire and insects and 2) many have complicated life cycles (e.g., rusts with four types of spores), exhibit pleomorphy (Tubby and Webber, 2010), or little is known about their life history and epidemiology.Despite this uncertainty it is necessary to assess the likelihood of possible outcomes for tree diseases under climate change (Dukes et al., 2009).In general, it appears that canker/dieback pathogens of trees are likely to be fa-of temperate and tropical forests may actually expand (Krankina et al., 1997).Although the beneficial effects of increased atmospheric CO 2 concentrations on tree productivity through enhanced photosynthesis will be realized in some locations, elsewhere they are likely to be offset by the negative effects of temperature-induced water stress on trees and increased incidence and interactions between biotic disturbances such as pathogens and insects and abiotic agents such as fire (McCullough et al., 1998;Lewis and Lindgren, 2000;Parker et al., 2006;Tubby and Webber, 2010).
The benefits that urban forests and treed greenspaces provide to community well-being are also at risk under climate change (Tubby and Webber, 2010).These 'urban ecosystems' (Bolund and Hunhammar, 1999), which often include non-native 'plants for planting', may act as 'sentinel plantings' and be some of the first settings where both climate change effects and new, native and/or introduced pathogens are seen (Tubby and Webber, 2010).
Although this is often not recognized, the ecological importance and economic impact of native tree diseases in forests and urban settings is significant (Castello et al., 1995;McCarthy, 2001;Brandt et al., 2003;Cruickshank et al., 2011).These diseases play fundamental roles in shaping forest structure and composition and can have a profound effect on the ability of forests to provide ecosystem services such as carbon sequestration.However, where their natural patterns of disturbance are altered by human activities such as monoculture timber production or fire exclusion, native tree pathogens may grow and spread unrestricted by coevolved limits to their population growth, conflicting with human-desired outcomes with enormous negative economic consequences (Singh, 1993).Non-native tree pathogens have even greater negative impacts, which are often very difficult to stop or even mitigate.
The purpose of this brief review paper is to improve understanding and management of diseases impacting forest and urban trees under a changing climate.Information on climate factors affecting several forest and tree foliage, shoot, and stem diseases is summarized along with predictions about how these relationships might change or are already changing.Several strategies for the imperative of managing forest and urban trees and their health under a changing climate are discussed.
There are several recent reviews from a few different perspectives on the topic of 'climate change and forest and tree diseases and/or pests' (e.g., Ayres and Lombardero, 2000;Boland et al., 2004; Desprez-Loustau Climate change and forest diseases voured in areas where host stress is increased, especially by drought; the incidence and impact of foliar pathogens will be enhanced in areas that become both warmer and wetter (Sturrock et al., 2011).Researchers and modellers are working together to prepare such assessments, starting with identification of the environmental variables most influential on pathogen and host interactions.Such information is summarized here (Table 1) for several foliage, shoot, stem and root diseases on their 'present-day status and predicted future status under climate change', including: Dothistroma needle blight (Dothistroma septosporum (Dorog.)Morelet and D. pini (Hulbary)), Cytospora canker of alder (Valsa melanodiscus G.H. Otth), Pine wilt disease (Bursaphelenchus xylophilus (Steiner & Buhrer) Nickle), Chestnut blight (Cryphonectria parasitica (Murr.)Barr.), Armillaria root rot (Armillaria ostoyae (Romagnesi) Herink), Phytophthora root rot (Phytophthora cinnamomi Rands), and sudden aspen death.

Managing forest diseases under climate change
Tree mortality, whether it is caused by climate alone, a single pathogen, or a whole suite of disturbance agents, must be expected and planned for now and in the future.This seems a straightforward task but in reality is a significant challenge because of the complexities around first understanding and then predicting changes to biological systems and how and why society should respond to these changes (Stenlid et al., 2011).Also, many of the world's forests will have to adapt to climate change without the aid of humans (Spittlehouse 2009) and the care of urban trees may take second place to other priorities in cities, towns and villages.Despite these realities, trees can be managed to mitigate the undesirable effects of projected increases in their mortality that will be driven by biotic and abiotic phenomena (Sturrock et al., 2011).
Forest managers, urban planners and local to regional authorities must think proactively and embrace a modified suite of forest management approaches because current management strategies will not protect forest values under a changing climate (Moore and Allard, 2011;Sturrock et al., 2011).The best management approaches for tree diseases under a changing climate will be those that enhance the diversity of tree species in both urban plantings and in forested settings.This could include planting and/or regenerating with mixes of both deciduous and coniferous tree species: the phenotypic plasticity of conifers means that they are generally better adapted to drought than broadleaved species (Rohde and Junttila, 2008) while deciduous trees (Brisson and Levrault, 2010) are thought to generally return more water to the environment than do conifers (Hasselquist et al., 2010).Clearly, decisions about the kinds and numbers of trees to be deployed on any landscape should be tailored to the location and its predicted future condition.

Monitoring
The forest sector and agencies responsible for the health of urban greenspaces need effective monitoring and detection protocols and tools to allow even the possibility for quick action in the face of changing or increasing pathogen impact (Moore and Allard, 2008).Systematic surveys of overall tree health should be conducted regularly by experienced people.Urban trees and areas of 'plants for planting' should be given special attention because of their 'ability' to act as early warnings or sentinels to changing pathogen conditions and their high potential to 'receive' invasive species.Monitoring activities should be coordinated across all levels of jurisdictional boundaries and results communicated to experts, policy makers, and the public in language they each understand.Such coordination is essential for the detection of new diseases or epidemics, which are expected to increase as the earth warms and global trade intensifies.In many instances 'news' about the importance of existing or new tree diseases may receive more supportive responses from society if they are described in quantifiable economic terms (Stenlid et al., 2011).

Forecasting
Models can be good predictive tools and development of those that integrate the best available information about disturbance, vegetation, and climate dynamics will help to reduce the often significant uncertainty around their forecasts.There are an increasing number of models available to project future distribution of forest pathogens using both climate variables and retrospective data.For example, CLIMEX, which was developed to predict the potential geographical distribution of weed species, at least initially, has been used to look at the potential distribution of tree pathogens such as Phytophthora ramorum Werres, De Cock & Man in`t Veld (Venette and Cohen, 2006).Rutherford and Webster, 1987;Enda, 1989;Mota et al., 1999;Kiritani and Moromoto, 2004;Pérez et al., 2008;Abelleira et al., 2011 Chestnut blight ~ Cryphonectria parasitica Introduced to North America from Asia in late 1800s; likely spread from USA to Europe in 1920s; devastated Castanea spp.trees in both regions; Hypovirulent strains that arose and infected virulent strains in Europe have reduced epidemic but this has not occurred in North America; Both strains have optimum growth range of 27-32 °C.
Warmer temperatures in Europe may enhance 1) exchange of dsRNA (cause of hypovirulence in this fungus) and 2) activity of chestnut endophytes antagonistic to C. parasitica and therefore may contribute to decrease in disease.
Epidemic of chestnut blight expected to continue in North America to extent that suitable host is available and temperatures not lethal to C. parasitica.
See La Porta et al., 2008 Climate change and forest diseases Other models designed to predict future distributions for tree pathogens include one for pine wilt disease (Evans, 2007), one for Dothistroma needle blight (Desprez-Loustau et al., 2007), and one for Diplodia shoot blight (Fabre et al., 2011), all in Europe, and one for Swiss needle cast in the Pacific Northwest of the USA (Manter et al., 2005).Efforts are underway to improve modelling of climate change and forest diseases and this should include their ongoing evaluation and adjustment.

Planning
As climate changes so too will the effects of tree diseases and other disturbance agents on forest and urban tree ecosystems and society must plan for these changes.Forest health programs already in place must be maintained and funded.Policies and legislation per-tinent to all aspects of tree health should be reviewed to ensure that problems can be quickly responded to (Sturrock et al., 2011).Despite the existence of global plant health legislation and standards for the movement of a wide range of plants and forest products around the world, many professionals feel that gaps and weaknesses in enforcing the legislation may result in major biosecurity problems (Brasier, 2008).Clearly, this issue must be addressed.Risk assessments and related rating systems are also valuable planning tools and coordination and sharing of these systems would likely be very beneficial to managing disease problems as they emerge.

Mitigation
The establishment and maintenance of a diversity of tree species in forests and urban plantings can help Disease associated with several factors, including drought and secondary pathogens and insects.
Incidence and impact of this kind of 'multi-factor' tree death is predicted to increase in all world forests.Worrall et al., 2008Worrall et al., , 2010b;;Hogg et al., 2004Hogg et al., , 2008 them maintain resilience to mortality and the other adverse effects that may be brought on by diseases and climate change.Other effective mitigation strategies include tree breeding programs that promote genetic diversity, disease resistance and tolerance to environmental stresses (Sturrock et al., 2011).Also proposed is the practice of assisted migration (AM), where humans deliberately move tree species and seed sources (populations).Assisted migration is envisioned to be practiced at three increasingly aggressive and 'riskier' scales: the first, assisted population migration, involves the translocation of genotypes within their existing range, the second, assisted range expansion, is translocation just beyond species' range limits, and the third, assisted long-distance migration, involves translocation over long distances (Winder et al., 2011).Forest managers should use AM "within a framework that allows for flexibility, uses best available science and predictive tools, considers risk and uncertainty, and evaluates and monitors results to ensure that unintended consequences are minimal" (Leech et al., 2011).

Conclusions
Outbreaks of diseases caused by native and alien tree pathogens are predicted to become more frequent and intense as international trade increases and as abiotic stressors and drought are amplified under climate change.These outbreaks will drive change in forests and urban greenspaces as will the convergence of human needs for key goods from forests such as food, fuel, and fibre and for essential ecosystem services (Sampson et al., 2005).Activities under the key strategies of monitoring, forecasting, planning, and mitigation must be implemented to deal with these emerging problems.

Table 1 .
Selected tree diseases: a summary of present-day status and predicted changes in future impact on trees due to climate change

Table 1 (
cont.).Selected tree diseases: a summary of present-day status and predicted changes in future impact on trees due to climate change