Future Scenarios for Plant Virus Pathogens as

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CHAPTER THREE

Future Scenarios for Plant Virus Pathogens as Climate Change Progresses R.A.C. Jones1 Institute of Agriculture, University of Western Australia, Crawley, WA, Australia Department of Agriculture and Food Western Australia, South Perth, WA, Australia 1 Corresponding author: e-mail address: [email protected]

Contents 1. Introduction 2. General Considerations 3. Direct Climate Effects 3.1 Greenhouse Gases 3.2 Temperature 3.3 Rainfall 3.4 Relative Humidity and Leaf Microclimates 3.5 Wind Speed and Direction 4. Indirect Climate Effects 4.1 Alterations in Cultivated Plants Grown and Regional Areas Cultivated 4.2 Alterations in Weed or Cultivated Plant Reservoir Hosts 4.3 Changes in Cultivation Systems 5. Implications for Control 6. Information Gaps and Deficiencies 7. Conclusions Acknowledgments References

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Abstract Knowledge of how climate change is likely to influence future virus disease epidemics in cultivated plants and natural vegetation is of great importance to both global food security and natural ecosystems. However, obtaining such knowledge is hampered by the complex effects of climate alterations on the behavior of diverse types of vectors and the ease by which previously unknown viruses can emerge. A review written in 2011 provided a comprehensive analysis of available data on the effects of climate change on virus disease epidemics worldwide. This review summarizes its findings and those of two earlier climate change reviews and focuses on describing research published on the subject since 2011. It describes the likely effects of the full range of direct and indirect climate change parameters on hosts, viruses and vectors, virus Advances in Virus Research, Volume 95 ISSN 0065-3527 http://dx.doi.org/10.1016/bs.aivir.2016.02.004

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2016 Elsevier Inc. All rights reserved.

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control prospects, and the many information gaps and deficiencies. Recently, there has been encouraging progress in understanding the likely effects of some climate change parameters, especially over the effects of elevated CO2, temperature, and rainfall-related parameters, upon a small number of important plant viruses and several key insect vectors, especially aphids. However, much more research needs to be done to prepare for an era of (i) increasingly severe virus epidemics and (ii) increasing difficulties in controlling them, so as to mitigate their detrimental effects on future global food security and plant biodiversity.

1. INTRODUCTION Atmospheric greenhouse gas concentrations have reached levels that are unprecedented for 800,000 years. They continue to accumulate in the earth’s atmosphere at an alarming rate causing climate change to accelerate with increasingly serious consequences for mankind and the planet’s other life forms. Since the start of the industrial era in 1750, the global average concentration of carbon dioxide (CO2) in the atmosphere has increased by 41%, methane by 160%, and nitrous oxide by 20%. Atmospheric CO2 levels are currently about 400 μmol mol1 and elevated CO2 (eCO2) levels are forecast to rise to 650 μmol mol1 by the year 2100 (IPPC, 2014). The International Panel on Climate Changes’ Fifth Assessment Report predicted that: (i) the global surface temperature increase by the end of the 21st century is likely to exceed 1.5°C relative to the 1850–1900 period for most scenarios and is likely to exceed 2.0°C for many scenarios; (ii) the global water cycle will change, with increases in disparity between wet and dry regions, as well as wet and dry seasons; (iii) the oceans will continue to warm, with heat extending to the deep ocean, affecting circulation patterns; (iv) decreases are very likely in Arctic sea ice cover, Northern Hemisphere spring snow cover, and global glacier volume; (v) global mean sea level will continue to rise at a rate very likely to exceed the rate of the past four decades; (vi) changes in climate will cause an increase in the rate of CO2 production and its increased uptake by oceans will increase their acidification; (vii) future surface temperatures will be largely determined by cumulative CO2, which means climate change will continue even if CO2 emissions are stopped; and (viii) only substantial and sustained global emission reductions would help reduce climate risks (IPPC, 2014). Thus, global prospects are bleak at a time of rapidly expanding human population, increasing food insecurity in many populous mid and lower latitude regions, declining natural ecosystems, and accelerating species extinction.

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A historic international climate agreement was reached at the global climate change conference, “Conference of the Parties, 21st session” in Paris at the end of 2015. It commences in 2020 and is aimed at (i) transforming the world’s fossil fuel-driven economy and slowing the pace of global warming to well below 2°C, aiming for 1.5°C; (ii) peaking of greenhouse gas emissions as soon as possible, followed by their rapid reduction; (iii) replacement of fossil fuels by other forms of energy; and (iv) provision of US $100 billion/year from 2020 to help developing nations reduce greenhouse gas emissions (COP21, 2015). Although such an agreement would have been much more effective before the situation had deteriorated so far, success in achieving these aims would help considerably toward avoiding the dire outcomes and scenarios currently predicted should no such improvements occur. The challenge that the increasing pace of global warming and climate instability pose to mankind’s ability to manage pests and diseases of cultivated plants and natural vegetation is cause for great concern. This is because of the consequent increase in global food insecurity at a time of rapid population increase and the accompanying loss of natural plant biodiversity. Many reviews have been written about the anticipated influences of diverse climate change parameters on (i) fungal pathogens and the plant diseases they cause, and (ii) insect pest populations and the plant damage they induce. A small number of these reviews also provided examples of the likely effects of climate change parameters on plant viral pathogens or the roles of virus vectors (eg, Garrett et al., 2006; Luck et al., 2011; Southerst et al., 2011). However, only three reviews include the likely effects of climate change on plant virus diseases globally as a major focus (Canto et al., 2009; Jones, 2009; Jones and Barbetti, 2012). Canto et al. (2009) discussed probable climate change effects on hosts and vectors that influence the spread of hemipteran-borne viruses, and Jones (2009) summarized likely climate change effects on plant virus epidemics as part of an article also covering virus origins, emergence, and evolution. Jones and Barbetti (2012) used climatic and biological frameworks to establish the probable effects of direct and indirect climate change parameters on the many vector, virus, and host parameters that represent the full spectrum of plant virus pathosystems (Table 1). They also used the same approach to assess likely effects of climate change on plant bacterial pathosystems. As regards viruses, their review addressed the many multifaceted and geographically distinct ramifications of climate change likely to influence epidemics of vector-borne and nonvector-borne plant virus pathogens worldwide. Their approach

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Table 1 Frameworks Used to Analyze Effects of Climate Change Parameters at Microclimate to Regional Climate Scales on Biological Parameters of Plant Virus Epidemics Climate Change Biological Parameters Biological Parameters Parameters for Vectors and Hosts for Viruses

(a) Direct

Changes in vector distribution

Ability to survive extreme weather events within plant hosts

Mean temperature

Changes in vector abundance

Ability to survive desiccation and ultraviolet light outside plant hosts

Maximum mean temperature (including heat waves)

Changes in vector activity and behavior

Influence of greenhouse gases on virus multiplication within hosts

Minimum mean temperature (including freezing)

Methods of vector survival Entry via wounds between growing periods

Mean rainfall and altered Vector ability to survive rainfall patterns extremes of temperature

Air-borne vector transmission

Extreme rainfall-related events (including monsoonal rain, hail, flooding, and drought)

Vector ability to survive extreme rainfall-related events

Soil-borne vector transmission

Relative humidity (including leaf microclimates)

Vector ability to survive extreme high winds

Transmission by contact

Wind speed and direction Influence of increased greenhouse gases on vector populations

Transmission by windmediated contact transmission or water

Greenhouse gas concentration

Vector infestation of alternative cultivated or weed reservoir hosts

Transmission by seed, pollen, or vegetative propagation

General climate instability

Alterations to host physiology affecting attractiveness to vectors

Importance of alternative cultivated plant or weed reservoir hosts

(b) Indirect

Alterations to host physiology affecting efficiency of vector transmission

Ability to persist and multiply inside or upon vectors

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Table 1 Frameworks Used to Analyze Effects of Climate Change Parameters at Microclimate to Regional Climate Scales on Biological Parameters of Plant Virus Epidemics—cont'd Climate Change Biological Parameters Biological Parameters Parameters for Vectors and Hosts for Viruses

Altered ranges of cultivated plants grown

Alterations to plant morphology influencing attractiveness to vectors

Ability to multiply and spread within plant hosts

Alterations in regional areas cultivated

Alterations to plant morphology influencing direct virus infection

Changes in rates of systemic movement within plant hosts

Alterations in alternative Alterations to host or vector phenology cultivated or weed reservoir hosts Changes in cultivation systems

Ability to evolve rapidly and invade new hosts

Generalist or specialist Alterations in vector activity due to the presence of another vector, a predator or a parasite/ parasitoid Alterations to temperature Alterations in symptom sensitivity of host resistance expression and virus titer within single or mixed to vectors or viruses host infections Alterations in effectiveness Alterations in effectiveness of cultural control of chemical control measures measures against vectors Alterations in effectiveness Alterations in effectiveness of phytosanitary control of cultural control measures measures against vectors Alterations in effectiveness Alterations in effectiveness of biological control of biological control measures against viruses measures against vectors (such as cross-protection)

From Jones, R.A.C., Barbetti, M.J., 2012. Influence of climate change on plant disease infections and epidemics caused by viruses and bacteria. CAB Rev., 7 (22), 1–32. http://www.cabi.org/cabreviews, slightly modified to reflect climate change knowledge published since 2011.

provided comprehensive coverage of international research then available that illustrated the likely influences of climate change on virus diseases of cultivated plants and natural vegetation in different regions of the world. They concluded that (i) climate change is likely to modify many critical

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virus epidemic components in different ways often resulting in epidemic enhancement but sometimes having the opposite effect, depending on the pathosystem and circumstances; (ii) with vector-borne pathosystems and new encounter scenarios, the complication of having to consider effects of climate change parameters on diverse types of vectors and emergence of previously unknown virus pathogens added important additional variables; and (iii) the increasing difficulties in controlling damaging plant virus epidemics predicted to arise from future climate instability warrants considerable research effort to safeguard world food security and biodiversity. Numerous information gaps where future research was required were identified and ways of improving future virus epidemic management tactics proposed. This review (i) summarizes information from earlier reviews, (ii) focuses on relevant research on the likely impacts of climate change on plant viruses and their vectors published since they were written, and (iii) provides an upto-date assessment of likely future scenarios for plant virus disease as climate change progresses further.

2. GENERAL CONSIDERATIONS Plant pests and pathogens must evolve or migrate to survive climate change. Accelerated evolution prompted by a changing environment drives development of variants potentially better adapted to the new conditions and changing geographic distributions bring together diverse lineages thereby increasing diversity (eg, Chackraborty, 2013). Observations on changes in crop pests and pathogen distributions over the 20th century suggested growing agricultural production and trade have been the most important factors disseminating them, but global warming is also causing them to move poleward. Poleward shifts of >600 crop pests and pathogens averaged 27 kms/decade since the 1960s (Bebber et al., 2013). Plant hosts, vectors, and viruses are influenced by (i) the direct consequences of climate change, especially altered rainfall patterns, increased temperature, greenhouse gases, drought, and greater wind speeds; and (ii) indirectly by things like regional alterations in areas cropped, ranges of crops grown, cultivation systems, distribution and abundance of vectors, and weed or cultivated reservoir hosts. In turn, these factors influence geographic ranges and relative abundance of viruses, their rates of spread, the effectiveness of host resistances, the physiology of host–virus interactions, the rate of virus evolution and host adaptation, and the effectiveness

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of control measures (Jones, 2009). To predict how all possible climate change effects might influence all the known diversity in behavior and life cycles of plant hosts, the viruses that infect them and their vectors would constitute a task of impossible magnitude. However, despite the limitations of the information then available, it was still possible to develop a general understanding of the changes likely to arise. To achieve this, Jones and Barbetti (2012) developed frameworks for (i) each important direct and indirect climate change parameter, and (ii) each significant biological (host plant, vector, and virus) pathosystem parameter (Table 1). They then cross-checked these frameworks one against the other. Their analysis revealed that: • Climate alterations are likely to modify diverse components of virus epidemics in many different ways, including altering host morphology, physiology, resistance to vectors or viruses, vector and virus life cycles, abundance, diversity, reservoirs, and inoculum. • In many instances, climate change is likely to enhance virus disease epidemics in higher and lower latitude regions. In other instances, it is likely to have the opposite effect, especially in drying mid-latitude and subtropical regions where irrigation is lacking. • As temporal and spatial shifts in their distributions cause newly introduced crops and weeds to meet indigenous vegetation for the first time, new encounter scenarios between cultivated and wild plants will inevitably increase. This will accelerate the appearance of epidemics caused by (i) new or little understood viral pathogens that emerge from indigenous vegetation to threaten newly introduced cultivated plants, and (ii) newly introduced pathogens and vectors that arrive with newly introduced cultivated plants and invade native plant communities. • Climate change is likely to diminish the effectiveness of some control measures, and virus epidemics are projected to become less predictable, causing increasing difficulties in suppressing them successfully using current management technologies. • In many cases, losses in cultivated plants and damage to natural vegetation resulting from virus diseases are likely to increase considerably with potentially serious consequence for world food security and plant biodiversity. • Successful adaptation of the global food system to future climates requires a research effort that targets the specific challenges climate variability imposes on production, such as those arising from virus disease epidemics.

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Climate change can influence the environment on micro- to macroscales that range from microclimate to local, regional, subcontinental, continental, and global. Its effects on virus epidemics need to be considered at all of these levels. The classic virus disease epidemic triangle includes interactions between plant hosts, viruses, vectors, and effects of the environment upon each of them. Each interacts with the other, macro- and microenvironments influencing both hosts and pathogens. At the microclimate level and sometimes on local scales, the environment can be influenced by the host plants themselves, and by viruses and vectors through their effects on growth of their hosts (Jones and Barbetti, 2012). Jones and Barbetti (2012) discussed critical features of virus and vector life cycles that need to be considered in order to understand likely climate change scenarios. Some of the most important of these are: • Viruses can be generalists that have broad host ranges but are often poorly adapted to individual hosts, or specialists which have narrow host ranges but are well adapted to their hosts. Also, plant hosts and vectors can be generalists or specialists. Generalists tend to be better adapted than specialists to alterations in host range under climate change scenarios. • Due to their simple genomes, viruses tend to adapt quickly to environmental changes which explains why Anderson et al. (2004) calculated that they cause nearly half (47%) of emerging infectious diseases of plants. • Host plants and virus vectors react to climate change by alterations in their physiology, morphology, and phenology. • Cultivated host plants can be moved between different climatic zones by man’s activities, but many noncultivated species face extinction because of their inability to adapt to a changing climate fast enough or disperse their seeds or other propagules to new regions. • Insects are the most important virus vectors, and the most important types of insect vectors are aphids, whiteflies, and thrips, but other insects, such as leafhoppers, plant hoppers, mealybugs, and beetles, also transmit some viruses. Mites are also important vectors. Infection with some viruses may alter host physiology or morphology, making infected plants more attractive to arthropod vectors. • Aphid-borne viruses (eg, potyviruses) are the most widespread and damaging viruses of cultivated plants in temperate regions, but whiteflyborne viruses (eg, begomoviruses) and thrips-borne viruses (eg, tospoviruses) are often the most important in regions with tropical and subtropical climates. All three insect vector types are important in protected cropping.

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Soil-borne viruses are transmitted from roots of infected plants to healthy plant roots by ectoparasitic nematodes or “fungus-like” organisms (oomycetes and protists) that are obligate root parasites. Soils infested with virus-infected vector resting spores can be dispersed by flooding activities, and some viruses are water-borne, being spreading over long distances by flooding or in irrigation and drainage channels. Contact-transmitted viruses are generally ones that reach high concentrations in the plant and have particles that are relatively stable outside the infected cell. They infect readily through wounds caused when leaves of infected plants rub against leaves of healthy ones, machinery or large animals move through partially infected crops, or via grazing and trampling by stock or mowing in pastures.

3. DIRECT CLIMATE EFFECTS 3.1 Greenhouse Gases Carbon fertilization due to increased atmospheric CO2 alters plant growth, morphology, biomass, physiology, metabolic pathways, and microclimates. It increases the growth and yield of most crop species. This increase is mainly caused by increased rates of photosynthesis and/or increased water use efficiency. Efficiency of photosynthesis depends on intercellular CO2 which is related to atmospheric CO2 concentration. However, the potential for greater crop yields arising from increasing ambient CO2 levels in temperate higher latitude regions, and cool mountainous regions in otherwise warmer areas, is unlikely to be realized fully. This is because the impact of CO2 fertilization may be limited by deficiencies in other nutrients, increased respiratory C demand due to higher temperatures, or diminished water supply. eCO2 influences secondary metabolite pathways, altering (i) the nutritious value of leaves to arthropod virus vectors, and (ii) the patterns of gene expression of defense signaling routes against both vectors and viruses. Alterations in plant growth or morphology influence vector behavior. These eCO2-induced changes all affect the way viruses and vectors interact with their plant hosts and influence the spatial and temporal dynamics of virus epidemics (Canto et al., 2009; Jones and Barbetti, 2012; references therein). 3.1.1 Viruses Canto et al. (2009) and Jones and Barbetti (2012) found little information on the direct effects of eCO2 on virus infection of plants, except that it

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decreased stunting symptoms in BYDV-infected oat plants but increased their biomass and water use efficiency (Malmstrom and Field, 1997), increased Potato virus Y (PVY) resistance in tobacco plants (Matros et al., 2006), and had the potential to suppress pathogen-induced virus resistance (Garrett et al., 2006; references therein). Two studies not mentioned by Jones and Barbetti (2012) were: in tobacco plants eCO2 increased resistance to Cucumber mosaic virus (CMV) and damage from PVY infections (Fu et al., 2010; Ye et al., 2010). Since then, several further publications have provided more information on the effects of eCO2 on plant viruses. Zhang et al. (2015) found that eCO2 lowered disease severity and modified plant defense responses in Tobacco mosaic virus (TMV)-infected tomato plants. This increased virus resistance and lowered disease incidence. Huang et al. (2012) found that eCO2 lowered disease severity and increased above ground plant height and biomass in Tomato yellow leaf curl virus (TYLCV)-infected tomato plants growing in open-top chambers in the field. It also increased resistance to TYLCV in tomato plants by modifying induced plant defense responses which lowered its incidence. Both of these studies showed that a modulated antagonistic relationship between salicylic acid and jasmonic acid signaling pathways contributed to increased virus resistance under eCO2 conditions. Del Toro et al. (2015) found that infecting Nicotiana benthamiana plants with CMV, PVY, or a Potato virus X (PVX) construct, under eCO2, caused them to grow larger and develop higher virus titers without affecting symptom expression. These higher virus titers under eCO2 were not due to less efficient suppression of gene silencing. Trebicki et al. (2015) found that under eCO2, Barley yellow dwarf virus (BYDV) titer was increased by 37% in wheat leaves and plant growth was stimulated (greater height, tiller number, leaf area, and biomass), but increased growth did not explain the increased BYDV titer and infected plants rarely developed symptoms. Thus, the studies so far show that eCO2 conditions can cause virus titers, host resistance, and biomass to increase, and virus incidence to decrease, in virusinfected plants. Disease symptoms were increased, decreased, or unaffected depending on the pathosystem. Increased host resistance to viruses would explain the lower virus incidences sometimes found. However, higher virus titers and infected plant biomass might have been expected to compensate for this effect on virus incidence by increasing the infection source for virus acquisition and transmission to healthy plants by vectors. The extent of disease damage incurred would appear to be pathosystem dependent. More such studies with different pathosystems are needed to obtain a clearer picture of the effect of eCO2 conditions on virus infection.

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Canto et al. (2009) and Jones and Barbetti (2012) found no published research that examined the influences of eCO2 on mixed infections with plant viruses, or mixed infections involving viruses and fungi or other types of microorganism. Since then there have been two such investigations. In a study of the effects of eCO2 upon the synergism between PVX and Plum pox virus (PPV) infecting N. benthamiana, Aguilar et al. (2015) found that with single infection eCO2 lowered PVX titer and attenuated its virulence toward the host, but virulence was maintained when both viruses were present in mixed infection. This suggested that as the amount of CO2 in the atmosphere increases synergistic mixed virus infections may respond differently from single virus infections. Rua et al. (2013a) investigated the relationship between BYDV infection and mycorrhizal root colonization in field plots containing two grass species growing in a freeair CO2 enrichment (FACE) facility. Mycorrhizal association increased BYDV titer, and BYDV infection increased root colonization by mycorrhizal fungi reciprocally. In addition, BYDV infection decreased root biomass, increased leaf phosphorous, and modulated effects of CO2 and phosphorous addition on mycorrhizal root colonization. Thus, plant mutualists and pathogens can interact to alter each other’s success under eCO2. It is therefore important to study interactions between multiple microorganisms under different eCO2 scenarios. 3.1.2 Arthropod Vectors in General eCO2 alters insect herbivory by altering both the defense chemistry and signaling of plants, and their nutritional and water contents, but the responses of herbivorous insects to these alterations are highly variable. It increases the production of salicylic acid but suppresses the production of jasmonates and ethylene, and these differential responses affect secondary metabolite pathways (Zavala et al., 2013). The indirect effects of eCO2 on insect herbivores, such as aphid, thrips, and whitefly virus vectors, include changes in their feeding, growth rates, fecundity, and population density. These changes are mostly mediated by its effects on host plant quality including changes in host morphology, diversity, abundance, biochemistry, physiology, and composition such as increased C:N ratios, and altered concentrations of soluble and nonstructural carbohydrates, starch, and soluble proteins (Cornelissen, 2011; Finlay and Luck, 2011; references therein). There may also be direct effects of eCO2 on insect physiology, behavior, and life history parameters (Cornelissen, 2011; references therein). Canto et al. (2009) and Jones and Barbetti (2012) described the information then

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available on the effects of eCO2 on insect vectors of plant viruses. In brief, eCO2 influenced different insect vector species in different ways. It had mixed effects on aphids which were highly species specific. With whitefly vector species, it had no effect on Bemisia tabaci (sweet potato whitefly) but affected Trialeurodes vaporariorum (glasshouse whitefly) negatively. With thrips vectors, it had little effect on populations of Frankliniella occidentalis (western flower thrips), but increased the population sizes of some other thrips vector species, and may compromise host resistance to some insect vectors. Since then, there have been further relevant publications, most of these involving aphid vectors. 3.1.3 Aphid Vectors Oehme et al. (2013) examined the effects of eCO2 on the performance of the important vector species Rhopalosiphum padi (oat aphid) and Myzus persicae (green peach aphid) on plants of wheat and canola (¼oilseed rape), respectively. The relative growth rate of R. padi increased in wheat but that of M. persicae decreased in canola. An increase in the concentrations of the carbohydrates fructose and glucose occurred in the phloem sap of wheat but not of canola, but whether this or changes in concentrations of certain amino acid were responsible for the different findings with these two aphid species–host combinations was not established. In Brussels sprouts, Klaiber et al. (2013a,b) found that eCO2 increased glucosinolate levels without altering primary metabolism and this reduced the performance of the vector species Brevicoryne brassicae (cabbage aphid). Its colonies grew more slowly and contained fewer individuals. Ryan et al. (2014a) studied the effects eCO2 on R. padi performance on three genotypes of the grass tall fescue (Festuca arundinacea, syn. Schedonorus arundinaceus). Aphid abundance diminished at a slightly increased eCO2 level (700 ppm) but increased at a higher level (1000 ppm), and this effect was dependent on host genotype. Ryalls et al. (2013) investigated colonization of three alfalfa (lucerne) (Medicago sativa) cultivars by the aphid vector Acyrthosiphon pisum (pea aphid). Successful plant colonization was unaffected by eCO2 but nodulation was increased. By contrast, Johnson et al. (2014) found that colonization of alfalfa plants by A. pisum under eCO2 conditions was affected differently depending on cultivar. Resistance to this aphid was reduced in otherwise highly resistant cv. Sequel, but enhanced in otherwise moderately resistant cv. Genesis. These differences were apparently linked to alterations in foliar essential amino acid concentrations which increased in the former but decreased in the latter. Ryan et al. (2015) studied the

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performance of R. padi on barley under eCO2. Plant biomass decreased due to herbivore load. Aphid abundance and intrinsic rate of population increase rose, but there was no significant effect on aphid fecundity or development time. Amino acids essential for aphid growth increased in the phloem sap, so the aphid population increase under eCO2 could be explained in terms of nutrient translocation. In a study involving A. pisum and two cultivars of M. truncatula (barrel medic), Guo et al. (2013b) found that eCO2 increased its population abundance and feeding efficiency on cv. Jemalong but reduced both of these parameters on N-fixing-deficient mutant dnfl1. In the absence of A. pisum, eCO2 increased photosynthetic rate, chlorophyll content, biomass, and nodule number in Jemalong, but only chlorophyll content in dnfl1. Moreover, aphid infestation enhanced activity of N-assimilation-related and transamination-related enzymes promoting amino acid metabolism which increased its population growth in Jemalong, but not in dnfl1. In their subsequent study using the same aphid and host species, Guo et al. (2014) examined the N nutritional quality and aphid resistance of an ethylene-insensitive mutant under eCO2. They concluded that eCO2 suppressed the ethylene signaling pathway in M. truncatula which increased its nutritional quality for A. pisum and decreased its resistance against this aphid. When Sudderth and Sudderth (2014) examined the behavioral responses of M. persicae feeding on three different host plant species, presence of a nonpreferred host species affected feeding behavior more than changes in plant chemistry arising from growing under eCO2 conditions. However, entropy rates still increased on nonpreferred hosts even when preferred hosts were available. Da´der et al. (2016) studied the life history and feeding behavior of M. persicae on pepper plants under ambient CO2 and eCO2 conditions, and the effect of these conditions on plant growth and leaf chemistry. Pepper plants fixed less nitrogen but were taller with greater biomass and canopy temperature under eCO2. eCO2 conditions increased the prereproductive period of M. persicae and decreased its fecundity and salivation into sieve tubes, but did not alter phloem ingestion. This indicated that its diminished fitness may be due to poorer plant tissue quality and unfavorable C:N balance rather than due to impaired feeding. When effects on its ability to transmit CMV were studied, there was a twofold decrease in transmission following exposure of receptor plants to eCO2 prior to aphid inoculation. Ryan et al. (2014b) studied the effects eCO2 on the performance of R. padi feeding on tall fescue plants with or without endophyte

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(Neotyphodium coenophialum) infection. On plants without endophyte, aphid density diminished at an eCO2 level of 800 ppm. Alterations in the amino acids arginine, aspartate, glutamine, and valine in phloem sap partly explained the effects of eCO2 on aphids. The aphids were unable to colonize endophyte-infected plants at eCO2 levels of 800 or 1000 ppm. This finding illustrates the need to investigate interactions between aphid vectors and other types of microorganisms that infect plants under eCO2. Hentley et al. (2014) reported that on raspberry (Rubus idaeus) plants the escape responses of vector species Amphorophora idaei (raspberry aphid) to predation by ladybird larvae (Harmonia axyridis) were severely impaired under eCO2. This behavioral response occurred within 24 h of transfer to eCO2 conditions. It was due to reduced aphid sensitivity to the alarm pheromone (E)-β-farnesene. This finding highlights the need to study chemical alarm signaling and aphid vector–prey interactions under eCO2. 3.1.4 Other Arthropod Vectors There appear to be few recent examples of studies on the effects of eCO2 on insect vectors other than aphids. With B. tabaci biotype B (¼Middle East-Asia Minor 1), an important virus vector biotype, oviposition, nymphal survival, and reproduction were not significantly affected by eCO2 conditions (Cumutte et al., 2014). When Wang et al. (2014a) used open-top chambers to examine the effects of eCO2 on the interaction between B. tabaci and its parasitoid Encarsia formosa on plants of Bt cotton and nontransgenic cotton, significantly longer egg-adult development times and greater nymph mortality occurred on both types of cotton. However, transgenic Bt cotton made no difference to the development, survivorship lifespan, or fecundity of either insect and there were no significant effects on parasitism by E. formosa. Liu et al. (2014) studied the effects of eCO2 on the activities of detoxifying and protective enzymes in F. occidentalis. It adapted to eCO2 by increasing the activities of two types of detoxifying enzymes (carboxylesterase and microsomal mixed-function oxidases) and decreasing the activity of the protective enzyme (superoxide dismutase). Miller et al. (2015) reported that populations of Aceria tosichella (wheat curl mite), the eriophyid mite vector of Wheat streak mosaic virus (WSMV), were unaffected by eCO2. 3.1.5 Nematode Vectors In research not mentioned by Jones and Barbetti (2012), the population density of the nematode virus vector Longidorus elongatus in grass-dominated

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pasture was increased by eCO2 (Yeates and Newton, 2009; Yeates et al., 2003). However, sometimes the population densities of root-feeding Longidoridae in soil do not benefit from the increased root biomass that occurs with eCO2. This may be due to factors such as enhancement of plant defense mechanisms against root-feeding nematodes or diminished availability of soil nitrogen under eCO2 conditions (Cesarz et al., 2015; references therein). There still appears to be no published information on the influences of eCO2 on fungal virus vectors. 3.1.6 General Issues So far, most investigations of the effects of eCO2 on viruses, vectors, and plant hosts have been done in controlled environment cabinets. In the future, the scope of such eCO2 studies needs to include more experiments examining the effects of eCO2 on virus disease epidemics in field situations, especially using FACE facilities or open-top chambers (Jones and Barbetti, 2012; references therein). There still appear to be no published information on the influences of the greenhouse gases nitrous oxide or methane on plant viral infections or their vectors.

3.2 Temperature Viruses have different temperature optima for multiplication within their host plants, some being adapted to warmer regions and others to cooler ones. Such optima are highest in viruses adapted to invade hosts growing in lowland tropical environments and lowest in viruses adapted to cold climates, such as those in cool temperate zones or at high altitude in mountainous regions. Different species of host plants and virus vectors (insects, mites, nematodes, fungi) also have diverse temperature optima under which they flourish, some being adapted to warmer climates and others to cooler ones. As the mean temperature increases, generalist viruses with high-temperature optima for multiplication within their host plants that are adapted to warmer regions and infect many different host species are likely to expand their geographical ranges from the areas with tropical or subtropical climates they currently occupy. This expansion would be to areas of higher latitude that were previously to cool for them and to formerly cooler higher elevations in mountainous regions within the tropics or subtropics. For vector-borne viruses, such expansion would be limited if the ranges of their vectors were to remain unchanged, but the opposite scenario is predicted for key tropical vectors of such viruses, such as B. tabaci and T. palmi (melon thrips).

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Conversely, the geographical distributions of viruses with lower temperature optima for multiplication within their host plants are likely to contract to areas of higher latitude or higher elevations in mountainous regions within the tropics and subtropics. Again, for vector-borne viruses such expansion would tend to be limited if the ranges of their vectors were to remain unchanged, but the opposite scenario is predicted for key temperate region vectors, such as aphids. Warmer winters can increase virus epidemics in regions with temperate climates by increasing overwintering virus and vector survival. By contrast, hotter, drier summers decrease virus epidemics in rainfed crops in regions with Mediterranean climates by decreasing virus and vector over-summering. Unusually high air temperatures can reduce insect vector populations so prolonged heat waves may diminish epidemics of the viruses they transmit. Thus, there are many ways by which rising mean temperature is likely to increase the scale of plant virus epidemics, but there are also circumstances where it can cause them to diminish. However, such predictions exclude protected cropping situations where plants are grown in temperature-controlled environments that include heating in cold climates and cooling in warm climates (Jones and Barbetti, 2012; references therein). 3.2.1 Viruses Increasing temperature alters host plant physiology, metabolic pathways, nutritional status, morphology, and phenology (Canto et al., 2009; Jones and Barbetti, 2012; references therein). Rising mean temperature and heat stress increase general plant susceptibility to virus infection and decrease the effectiveness of temperature-sensitive single-gene resistances. Increased mean temperature also alters rates of virus multiplication, systemic movement, and seed transmission and influences the multiplication and systemic movement of individual viruses present in mixed infection. Moreover, it modifies virus evolution rates and selection pressures which can lead to development of virulent virus strains with broadened natural host ranges, higher virus multiplication rates in reservoir hosts, and increased vector transmission efficiencies. Prolonged heat waves are likely to cause remission of virus symptoms in infected plants by reducing their virus contents. In some instances, prolonged heat waves might eliminate virus infections from growing plants where systemic invasion is already incomplete or the virus involved has unstable particles. Protracted heat waves might also sometimes be sufficiently long to inactivate seed transmission of seed coat contaminants with viruses with unstable particles (Jones and Barbetti, 2012; references therein).

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Jones (2014a) described the likely effects of elevated temperature on potato virus epidemics worldwide. Potato-infecting viruses best adapted to warmer regions (eg, Potato leaf roll virus (PLRV) and Potato yellow vein virus (PYVV)) are likely to expand from areas they occupy now to areas of higher latitude previously too cool for them, and to formerly cooler higher elevations in mountainous regions within the tropics or subtropics. Conversely, the geographical distributions of viruses adapted to cooler regions (eg, Andean potato latent virus and Potato mop-top virus (PMTV) are projected to contract to areas of higher latitude or higher elevations in mountainous regions within the tropics and subtropics, including ones previously too cold for the potato crop. A similar scenario is likely with the soil-borne viruses of wheat which include furoviruses, eg, Soil-borne wheat mosaic virus (SbWMV), and bymoviruses, eg, Wheat spindle streak mosaic virus (WSSV). Such wheat viruses are adapted to temperate conditions and mostly occur in cooler parts of Europe, Asia, North America, and New Zealand (Cox et al., 2014; references therein). Soil-borne wheat viruses also include the pecluviruses, Indian peanut clump virus (IPCV) and Peanut clump virus (PCV), which cause diseases of wheat under subtropical conditions in the Indian subcontinent (IPCV) and Africa (PCV), respectively (eg, Tamada and Kondo, 2013; references therein). When the soil moisture is sufficient for activity of the motile zoospores of their vector, the former viruses are likely to contract to areas of higher latitude or higher elevations in mountainous regions within the tropics and subtropics including areas previously too cold for the wheat crop, while the latter viruses are likely to expand to areas of higher latitude previously too cool for them and to formerly cooler higher elevations in mountainous regions within the tropics or subtropics (Jones, 2014a). Several research papers published during 2012–15 added more information on the effects of increased temperature upon virus infection in plants. Their findings are discussed in the next four paragraphs. Nancarrow et al. (2014) studied the effects of elevated (10–21°C, night/ day) or ambient (5–16°C, night/day) temperature winter growing season regimes on wheat plants infected with BYDV. Infected plants grown under elevated temperature were larger, developed virus symptoms earlier, and had higher virus titers than plants grown at ambient temperature. Chung et al. (2015) investigated the effects of different temperature regimes on the speed of systemic invasion following inoculation of Turnip mosaic virus (TuMV) to Chinese cabbage. It took 48 days for systemic infection to occur at 13°C but only 6 days at 22–33°C. Rate of systemic infection increased linearly up to 23°C. The optimum temperatures for symptom expression were 23–28°C.

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Nyalugwe et al. (2014) studied the effects of elevated temperature on TuMV resistance in oilseed Brassica species. When TuMV-inoculated plants of 18 B. napus and 14 B. carinata lines that behaved as if they had an extreme resistance phenotype when grown at 16–18°C were kept after inoculation at 25–28°C, all except one B. napus and three B. carinata lines developed other resistance phenotypes or proved susceptible at 25–28°C. Graft inoculations confirmed stable extreme TuMV resistance in the latter four lines. Also, keeping plants of the former lines at 16–18°C diminished TuMV multiplication below the level it could be detected in their inoculated leaves. An example of temperature-sensitive resistance being overcome by heat stress was provided by Zinati et al. (2012) who found that 32°C incubation of WSMV-infected wheat plants carrying temperature-sensitive WSMVresistance gene wsm1 overcame this resistance gene. Aguilar et al. (2015) studied the effects of elevated temperature upon the synergism between PVX and PPV infecting N. benthamiana. They found that the titers and virulence of both viruses decreased markedly with mixed infection at 30°C compared to 25°C. This contrasted with the situation under eCO2 where virulence of both viruses was maintained in mixed infection (see Section 3.1.1). Rua et al. (2013b) investigated the relationship between BYDV infection and fungal endophyte colonization under different temperature regimes over 3 years in grass plots dominated by tall fescue. Using a hexagonal array of infrared heaters mounted on posts, all-yearround the air temperature above elevated temperature plots was increased by 3°C above that of adjacent ambient temperature plots. Elevated temperature altered BYDV prevalence in tall fescue, although its effects varied between years and interacted with fungal endophyte symbiosis. In the final year, regardless of endophyte presence or absence, elevated temperature increased virus prevalence in tall fescue which was apparently due to increased aphid vector colonization. This indicated that as global warming progresses BYDV epidemics are likely to increase in grass pastures. Guerret et al. (2016) investigated the effects of temperature on symptom expression in subterranean clover plants infected singly or in mixed infection with Bean yellow mosaic virus (BYMV) and the fungus Kabatiella caulivora. The plants were maintained at 18°C, 20°C, or 22.5°C after BYMV inoculation and inoculated with K. caulivora once systemic BYMV symptoms developed. Mixed infection caused the most damaging disease symptoms. In single infections, BYMV symptoms were most pronounced at 18°C, but K. caulivora induced more severe symptoms at 20°C and 22.5°C. In mixed infections, disease severity followed the pattern developed with BYMV alone as

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temperature increased. Also, synergistic increase in disease severity sometimes occurred at 18°C, but increases in severity were always additive at 20°C and 22.5°C, reflecting the greater BYMV multiplication detected in infected leaves at 18°C compared with 20°C or 22.5°C. These findings indicated that as global warming progresses in subterranean clover pastures disease severity from single infections with BYMV or K. caulivora may decline or increase, respectively, and mixed infection become less damaging. Virus recognition by the host defense machinery of plants induces plant defense responses including those based on RNA silencing as well as others involving stress-response proteins and their actions to limit virus accumulation (eg, Chellappan et al., 2005; Obrepalska-Steploweska et al., 2015). Four recent studies examined the effects of elevated temperature upon the RNA silencing antiviral defense mechanism in plants. When Zhang et al. (2012) maintained Turnip crinkle virus-infected plants of Arabidopsis thaliana at the elevated temperature 26°C, vigorous virus replication causing death occurred in plants containing loss-of-function mutations and RNA methyltransferase genes, but not in wild-type plants which were able to survive and produce viable seeds. A specialized RNA silencing pathway provided the wild-type host plants with a competitive edge against this virus which still operated successfully at 26°C. Zhong et al. (2013) found increasing temperature from 22°C to 30°C inhibited transgene-induced posttranscriptional gene silencing effectively in A. thaliana. Moreover, it induced transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis. When Ghosal and Sanfacon (2014) grew N. benthamiana plants infected with Tomato ringspot virus at 21°C and the elevated temperature of 27°C, temperature-dependent recovery from symptoms occurred due to induction of RNA silencing at the elevated temperature. This recovery was associated with reduced levels of RNA2-encoded coat protein and movement proteins but not of RNA2 itself. Silencing of Argonaute1-like (Ago1) genes prevented both symptom recovery and RNA2 translation repression. They concluded that recovery of infected plants at 27°C was associated with an Ago1-dependent mechanism that represses RNA2 translation. Del Torro et al. (2015) examined the effects of growing N. benthamiana plants infected with CMV, PVY, or a PVX construct at 25°C or 30°C on virus accumulation and symptom expression. CMV accumulation and symptom expression remained similar, but PVY and PVX construct accumulation decreased markedly at 30°C and there were few or no symptoms. With PVY and PVX, the diminished virus accumulation and symptom expression at 30°C were not due to less efficient suppression of gene silencing.

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In a study of the effects of temperature on plant proteome differences, Obrepalska-Steploweska et al. (2015) compared the effects of keeping Peanut stunt virus-infected N. benthamiana plants at 21°C and 27°C on accumulation of this virus and its satellite RNA. The rate of accumulation of both virus and satellite RNAs was faster at 27°C initially but then declined. At 21°C, the initial rate of accumulation of both was slower but eventually exceeded that at 27°C. At 27°C, proteins involved in photosynthesis and carbohydrate metabolism decreased in abundance, but proteins involved in metabolic processes were all more abundant than at 21°C. This was especially evident in plants infected by the virus alone where proteins involved in protein synthesis, degradation, and folding all increased in abundance. Stress-related differentially regulated proteins were increased in plants infected with virus alone but barely increased in plants infected with both virus and satellite. 3.2.2 Arthropod Vectors in General Temperature is the predominant climatic influence on insect herbivores modifying their development, survival, fecundity, distribution, and abundance. Considerable shifts in the distribution and abundance of insect vectors of plant viruses can result from small alterations in average temperatures. Increased mean temperature alters plant physiology by influencing secondary metabolite pathways, thereby altering the nutritious value of leaves to insect vectors. It increases stomatal conductance which influences efficiency of photosynthesis. This alters virus multiplication within cells, thereby influencing virus systemic movement and acquisition by vectors. In addition, increased temperature also alters the patterns of gene expression of defense signaling routes against some insect vectors. Increased mean temperature can increase the efficiency of virus transmission from infected to healthy plants by insect vectors. Such enhanced transmission efficiencies could enable viruses they transmit to expand their ranges to areas formerly too cold for them to be transmitted effectively. However, distributions of some other viruses might contract from regions with increased temperatures due to diminished virus transmission efficiencies at higher temperatures. Also, prolonged heat waves can diminish vector numbers thereby decreasing virus epidemics (Canto et al., 2009; Jones and Barbetti, 2012; references therein). In a review of the likely effects of climate change on potato virus epidemics, Jones (2014a) discussed the general effects of global warming on potato virus vectors. As aphid, whitefly, and thrips vectors add areas to

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their global distributions that were formerly unfavorable to them because they were too cold, the risk of serious epidemics of the potato viruses they transmit is projected to increase. For example, such a shift in vector populations is projected to result in aphid-borne PLRV becoming more widespread in cool temperate regions under increasing mean winter and summer temperature scenarios. It is also likely to cause the ranges of damaging potato-infecting tospoviruses transmitted by T. palmi (eg, Groundnut bud necrosis virus) to expand into regions formerly too cool for them, and of T. vaporariorum vectored PYVV moving to higher altitudes in the Andean region of South America. Moreover, rising temperatures in formerly cooler regions are likely to have serious implications for potato seed production. This is because of (i) increased aphid vector activity and (ii) factors like greater survival of volunteer potatoes arising from milder winters or introduction of other Solanaceous crops that act as infection reservoirs for aphids or potato viruses but require warmer summer growing conditions than were available formerly (eg, tomato, pepper). Seed potato production areas in some parts of the world may become unsuitable for high-quality seed tuber production necessitating moves away from formerly cooler regions, such as ones at lower altitude or in windswept coastal areas, to cooler higher altitudes in highland regions or to higher latitude regions formerly too cool for potatoes. 3.2.3 Aphid Vectors Aphids react strongly to small changes in mean temperatures due to their mobility, low developmental threshold temperatures, short generation times, high capacity for reproduction, and ability to make rapid life history and behavioral changes. An additional five generations of aphids/year are predicted in temperate zones from a warming of 2°C. Thus the risk of serious epidemics of aphid-transmitted viruses increases as their populations and activities increase. In temperate regions, survival of aphid vectors is expected to increase with milder mean winter temperatures, and higher mean summer temperatures are likely to increase their development and reproductive rates. Fewer days with frost and shorter cold spells increase their ability to overwinter, permitting them to expand their geographic ranges and increase the period in which they are active each year. Increased winter temperatures induce earlier starts to aphid annual life cycles, increase the proportion of winged aphids, and stimulate their flight activity. Although the actual rate of advance varies with aphid species and region, over the next 50 years in Europe the overall date when aphid species are first

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caught is anticipated to advance by an average of 8 days. Many aphid-borne virus diseases are likely to become more widespread in temperate regions under increasing mean winter and summer temperature scenarios (Canto et al., 2009; Jones, 2009; Jones and Barbetti, 2012; references therein). Many additional research papers about different aspects of the effects of rising mean temperature, heat waves, and unusually cold periods on aphids or their parasitoids were published in 2012–15. The next seven paragraphs provide examples of these. Gao et al. (2012) studied the effects of rearing the vector species Acyrthosiphon gossypii (a cotton aphid) on cotton plants at 18°C, 21°C, 24°C, 27°C, and 30°C: the average longevity of adult females was 16, 12, 8, 5, and 3 days, and the average number of offspring per female was 46, 38, 20, 14, and 0 at these temperatures, respectively. The optimal temperature range for its growth was 21–27°C, while 30°C was beyond its upper limit for reproduction. Gillespie et al. (2012) found that the population growth of M. persicae was lower under heat waves (32°C and 40°C maxima) compared to environments with periodic hot days. Heat waves also decreased the proportion of winged aphids in the population. Ryalls et al. (2013) investigated the ability of A. pisum to colonize three alfalfa cultivars when temperatures were raised from 26°C to 30°C. Successful plant colonization was unaffected by the increase to 30°C, but root nodulation was severely reduced. Using the same aphid species and plant host, Ryalls et al. (2015) found that although increased foliar amino acids stimulated increased aphid population growth under eCO2 conditions at ambient temperature (26°C/18°C day/night), this effect was neutralized when they were kept under eCO2 at high temperature (30°C/22°C day/night). This was because, although elevated temperature increased plant biomass, it decreased the foliar amino acid concentrations that mediated increased aphid numbers under eCO2 at ambient temperature. Therefore, incorporating both eCO2 and elevated temperature factors together in climate change studies is likely to provide greater insight into how aphid vectors will be affected by climate change. Ma and Ma (2012) found that an aphid usually stays at one feeding site for a long time but heat stress can make it decide to move on. These authors created a wheat leaf temperature gradient based on microhabitat temperatures, and used it to study the behavioral responses of Sitobion avenae (grain aphid) and R. padi to heat stress. Their results suggested that aphids make a decision to avoid heat stress based on the combination of temperature and exposure time and escape before they are hurt by high temperatures under

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the conditions of climate warming. However, avoiding high temperatures costs considerable time and resources, and so is likely to reduce their growth, development and reproduction. Ma et al. (2015) focused on changing maximum daily temperatures while holding night time temperatures constant to study high-temperature effects on demographic parameters and fitness in S. avenae. They concluded that daily maximum temperature will play an important role in regulating aphid population dynamics especially when considering the expected increase in extreme temperature events likely to occur with climate change. Two papers investigated the effects of fluctuating extreme climatic events on aphids. Chen et al. (2013) examined the effect of elevated temperature on the performance of the vector species Aphis craccivora (cowpea aphid). The aphids were reared at four temperatures: current midsummer mean of 28.6°C in subtropical Taiwan, +1.4°C, +3.6°C, and +6.4°C. The aphids experienced either constant or daily oscillating (from 2.9°C to +3.6°C) temperatures. As temperatures increased, so did negative effects on life history traits and demographic parameters. Also, compared with those reared at constant temperatures, aphids reared under oscillating temperatures developed more slowly and had longer mean generation times, but their net reproductive rate was higher. Thus, in midsummer in Taiwan global warming is likely to exceed A. craccivora’s thermal optimum for growth and affect life history traits and demographic parameters differently. Jeffs and Leather (2014) assessed the effects of simulated heat waves and unusually cold periods on the survival, development period, and fecundity of the vector species S. avenae. Exposure to 16 h at 30°C (ie, heat stress) diminished fecundity and increased physiological development period causing reduced population growth rate. Exposure to 15°C for 1.3 h (ie, cold stress) did not affect fecundity or physiological development period but elongated the development period which reduced population growth. Maternal experience of heat stress reduced nymphal birth weight, suggesting that the cross-generational effects may occur on population growth rates. Using nine anholocyclic clones collected along a latitudinal line from Spain to Sweden, Alford et al. (2012) examined the effects of intra- and intergenerational acclimation and latitude on the activity thresholds of M. persicae in Europe. Low-temperature (10°C) acclimation for one generation depressed the cold movement threshold and chill-coma temperature. High-temperature acclimation (25°C) for one generation increased heat movement threshold and heat coma temperature. Two Swedish clones expressed low heat coma temperatures consistently and three Spanish clones

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expressed high heat comma temperatures consistently, but otherwise, there was no relationship between latitude and activity thresholds. This suggested that clonal mixing limited local population adaptation to areas where temperature conditions enable long-term persistence of populations at the two latitudinal extremes. Bell et al. (2015) used 50 years of aphid data from suction traps dispersed around the United Kingdom to examine long-term phenological trends, elucidate mechanisms that advance aphid phenology under climate change, and explain these mechanisms using life history traits. Linear and mixed effect models estimated the average rate of change per year since 1965, and effects of climate on annual counts, first and last flights, and lengths of flight season. All 55 aphid species studied had earlier first flights, and 85% increased the durations of their flight seasons, but there was little overall effect on the timing of their last flights. The North Atlantic Oscillation index (NAO) and accumulated day degrees above 16°C (ADD16) drove patterns of aphid phenology, the winter NAO determining when aphids first migrated and the ADD16 predicting later aphid flights. Permanently parthenogenic and nonhost alternating aphid species advanced their phenology faster than species with complex life cycles involving alternation of sexual and asexual generations and host plant alternation. Temperature thresholds for flying were established for several aphid species. For example, the low-temperature threshold for S. avenae takeoff was 16°C which was similar to that for Aphis fabae (back bean aphid). The extent to which aphids fly over very long distances (over hundreds of kilometers) may have been overestimated in the past due to methodological difficulties in tracking them. When landing, the aphid repeatedly lands and probes plants (so-called trivial flights) before it settles (termed the settling period). Their trivial flights and settling periods are highly significant in transmission of nonpersistently and persistently aphid-transmitted plant viruses, respectively (D€ oring, 2014; references therein). There is an urgent need for more detailed knowledge of how aphid vector behavior in the field is likely to be affected by temperature alterations and how these affects are likely to influence spread of plant viruses under field conditions under different climate change scenarios. Temperature influences the activity, abundance, and distribution of parasitoids that suppress aphid vector populations, and this knowledge is important in relation to aphid transmission of viruses under projected increased temperature global warming scenarios. Several recent papers examined the effects of elevated temperature on aphid parasitoids. For

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example, Gillespie et al. (2012) studied the effects of daily maxima of 32°C and 40°C on the parasitoids Aphidius matricariae and Aphelinus abdominalis. When they parasitized M. persicae under heat wave conditions, their development times were longer and the numbers of A. matricariae diminished, while the numbers of A. abdominalis did not. When both were present together their impacts on aphid populations were greater under heat wave conditions than when there were periodic hot days. In two further examples, (i) Romo and Tylianakis (2013) found that with the parasitoid wasp Diaeretiella rapae, although warm temperatures decreased parasitoid longevity, they increased their successful emergence and ability to reduce B. brassicae populations, while (ii) Bannerman and Roitberg (2014) found that increasing the frequency of warmer than average days only exerted impacts on aphid–parasitoid dynamics when daily temperatures were sufficient to produce temperature-dependant mortality. 3.2.4 Whitefly Vectors As with aphid vectors, whitefly vectors also react strongly to climatic changes due to their short generation times, high reproductive capacity, and ability to make rapid life history and behavioral changes. B. tabaci and T. vaporariorum transmit different whitefly-transmitted viruses. Both flourish under warm conditions but B. tabaci is less cold tolerant than T. vaporariorum. With B. tabaci, 25–28°C is optimal for development, and much shorter adultto-adult generation times occur at high (31–33°C) than low (17°C) temperatures. For B. tabaci to flourish, an average monthly temperature of at least 21°C in the hottest month of the year, and a dry season with a period of 4 months of monthly rainfall of less than 80 mm, is needed. As climate change progresses, these conditions are occurring over increasingly wide areas. Because of increasing mean winter temperatures in places formally too cold for it in winter, B. tabaci is tending to displace T. vaporariorum which is increasing its distribution in formerly cooler regions. In turn, this shift in vector distribution is influencing whitefly-transmitted virus distributions in different parts of the world, and damaging epidemics of B. tabaci-transmitted begomoviruses are becoming more widespread (Jones and Barbetti, 2012; references therein). In 2012–15, several additional research papers were published about the effects of rising mean temperature, heat waves, or unusually cold periods on B. tabaci (but only one for T. vaporariorum). The next three paragraphs provide examples. With the Q biotype (¼Mediterranean biotype) of B. tabaci, Pusag et al. (2012) found that the total lifespan from egg to adult death was 63 days

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with nonviruliferous whiteflies reared on healthy plants, but 53 days for whiteflies reared on TYLCV-infected plants. When they exposed whiteflies to 1 or 3 h at 4°C, 25°C, and 35°C, the mortality of nonviruliferous whiteflies was significantly smaller than that of viruliferous whiteflies at 4°C and 35°C, but at 25°C there was no difference between the two. Thus, TYLCV acquisition reduced whitefly fitness, reducing their longevity and increasing their sensitivity to cold and heat stresses. This research on exposure of T. tabaci to brief periods of temperature stress in the presence or absence of TYLCV has implications over future TYLCV epidemics in tomato crops as its spread might be diminished by reduced vector fitness during heat waves caused by the global warming process. Guo et al. (2013a) compared the survival, development, and reproduction of the biotype B of B. tabaci over five generations at 27°C, 31°C, and 35°C. At 27°C, its survival, development, and fecundity were stable, but its fecundity declined in the fourth and fifth generations at 31°C. At 35°C, egg hatching, immature survival rate, and fecundity all declined in the fourth and fifth generations. When held at 37°C for one generation fecundity was 700 mm

– Area cropped shrinking, crop failures increasing

Rainfall 450–700 mm Rainfall 225–450 mm

NORTHAM

Rainfall 175–225 mm

PERTH

– Rainfall in annual cropping period decreasing rapidly

Rainfall < 175 mm 17 5m

MANDURAH

700 mm

m

225 mm

– Growing wheat barely viable in driest areas

BUNBURY BUSSELTON ESPERANCE

45 0m

m

450 mm

ALBANY

700 mm

Based on data provided by the State of Queensland (Dept. of Environment and Resource Management) [2014] Produced by Geographic Information Services DAFWA, October 2014 Job No: 2012234

C Western Australian Agriculture Authority, 2014

Fig. 3 A region suffering less from aphid-borne virus diseases as it rapidly dries due to climate change. The wheatbelt of southwest Australia is a semiarid, mid-latitude region without irrigation in which annual crops grow in winter/spring (Jun.–Nov.). During this period, south-westerly cold, rain-bearing fronts pass from the Indian Ocean inland, the rainfall declining with distance from the coast, giving rise to high, medium, and low rainfall, rainfed cropping zones. Due to a rapid reduction in size and penetration of rain-bearing fronts in the last 14 years, the low rainfall zone expanded markedly, while the medium and high rainfall zones contracted toward the coast. Due to insufficient moisture at sowing time, a sharp reduction in crop diversity and rapid increase in areas of land left uncultivated followed. The decreasing green-bridge that both virus and aphid vector require to persist through the increasingly hot, dry summer, and autumn period (Dec.–May) is the main cause of the significant decrease in aphid-borne virus diseases, eg, of BYDV in cereals. Map with kind permission of Western Australian Agriculture Authority and Dr David Stephens, Department of Agriculture and Food Western Australia.

As the ranges of cultivated plants currently restricted to warmer regions expand due to temperature and/or rainfall increases, the distributions of their viruses and vectors are projected to expand through introduction of infected seed and vegetative propagules, contaminated soil or dust, or infectious arthropod vectors carried on wind currents. Climate change would then be accelerating an already existing process as such dispersion increases in momentum due to expanding trade in plants and plant products, and movement of plants away from their centers of domestication. The result

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is exposure of native plants to new encounters as they meet newly introduced viruses and vectors spreading to them from introduced cultivated plants. Similarly, introduced cultivated plants become exposed to new encounters as they meet with indigenous viruses from native plants. Such new encounters provide new opportunities for rapid, adaptive virus evolution and host species jumps, thereby increasing the rate of invasion of (i) introduced plants by indigenous viruses emerging from native plants and (ii) native plants by introduced viruses. Damaging epidemics are likely to arise because these viruses did not coevolve with the plants they encounter. Generalist viruses adapt to new hosts better than specialist viruses as the geographic ranges of their plant hosts and vectors change and new encounters occur with host plants they never met before, so climate change is likely to favor their epidemics over those of specialists. Also, when viruses and vectors that native vegetation has not been exposed to are introduced to it through new encounters, the natural control measures that operate to limit virus epidemics in wild plant communities are likely to be rendered less effective by stress caused by climate change, which would aggravate introduced virus epidemics in native vegetation. In contrast, in drying middle latitude and subtropical, arid, and semiarid regions, climate change is likely to decrease new encounters between indigenous viruses and introduced hosts, and introduced viruses and native plants. This would occur as diminishing rainfall and more frequent droughts decrease land used for cropping and lessen the fragmentation of remaining native vegetation. New epidemics in introduced plants caused by viruses emerging from the local flora, or in native vegetation caused by newly introduced viruses, would then diminish (Jones, 2009; Jones and Barbetti, 2012; references therein). Although their main focus was not on climate change, several important reviews and opinion pieces have been published since 2010 on the subject of new encounters and virus emergence (eg, Alexander et al., 2014; Elena et al., 2014; Fereres, 2015; Gilbertson et al., 2015; Jones and Coutts, 2015; Navas-Castillo et al., 2011; Roossinck and Garcia-Arenal, 2015). In addition, two reviews addressed the subject in relation to climate change (Jones, 2014b; Krishnareddy, 2013). Two of the most recent articles approached the subject from the perspective of introduced insect vectors as drivers of virus emergence from native vegetation (Fereres, 2015; Gilbertson et al., 2015). Vectors impose strong bottlenecks between host-to-host virus transmissions during which much virus variability is lost so vectors strongly influence their potential for successful emergence (Fereres, 2015; references therein). Gilbertson et al. (2015) emphasized that in the last 10–20 years emergence

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of insect-vectored viruses has been disproportionally driven by the increased global distributions of two supervectors, B. tabaci and F. occidentalis. Several research papers contributed to knowledge of the alterations to virus genome nucleic acid required for a host species switch to be successful (eg, Bedhomme et al., 2012; Kehoe et al., 2014; Vassilakos et al., 2016). Inevitably, as climate change progresses the frequency of new encounters will increase, so the importance of introduced vectors in driving virus emergence from native vegetation to infect introduced plants is likely to increase with serious consequences for crops and food production (eg, Jones, 2014b; Krishnareddy, 2013). Due to their ability to host shift readily, the importance of generalist plant viruses introduced through trade is likely to increase at the same time with serious consequences for native vegetation (Jones and Coutts, 2015; Vincent et al., 2014).

4.2 Alterations in Weed or Cultivated Plant Reservoir Hosts When seeds of weed species not previously found in a region are introduced as contaminants during trade in plants and plant products, seed-borne viruses can be introduced. Weed species formerly unable to establish because they possess specific temperature or rainfall requirements may subsequently be able to establish due to altered conditions resulting from climate change. Seed contamination can introduce viruses that then invade native vegetation, and the newly introduced weeds can become infected by viruses emerging from indigenous vegetation or provide attractive hosts to new arthropod vectors. They would then be likely to provide reservoirs of viruses or arthropod vectors that accelerate spread of emerging viruses from native vegetation to newly introduced crops. In addition, the introduced weeds might provide favorable hosts for viruses or arthropod vectors already present, and the virus concerned might be damaging to an important crop grown locally. If weed control is inadequate, their presence would aggravate damaging epidemics of already occurring viruses in the vulnerable local crop. Moreover, cultivated plants introduced to regions formerly unsuited to them may be tolerant of viruses damaging to vulnerable cultivated plant species growing nearby. Their presence as major virus reservoirs would then enhance virus spread to, and virus epidemics within, the vulnerable crop which might be one grown traditionally in the region before it became suitable for plantings of the newly introduced crop. A similar situation would arise when such newly introduced cultivated plants turn out to be favorable hosts for arthropod vectors already present in the region. The increased vector population moving from the introduced cultivated plant

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reservoir would then drive an acceleration of virus epidemics in the vulnerable traditional crop (Jones, 2009; Jones and Barbetti, 2012; references therein).

4.3 Changes in Cultivation Systems The current rapid expansion in human activity and need to feed the burgeoning human population includes adopting ever more sophisticated agricultural practices. It also promotes more widespread use of monocultures. Changes in cultivation systems likely to arise in areas rendered more suitable for large-scale plant cultivation as a consequence of climate change include: agricultural intensification, extensification, and diversification; greater use of chemical control measures; use of irrigation in dry regions to provide all-year-round cropping; and increased use of protected cropping. Such changes in cultivation systems often favor frequent and damaging virus epidemics. In contrast, in arid and semiarid, mid-latitude regions, the option of growing rainfed crops without adoption of water saving measures is likely to become increasingly limited as the climate becomes drier and hotter. Dryland cropping is already difficult to sustain in many such regions and land degradation is also a serious concern. Cultivation practices that improve rainfall use efficiency involve minimizing moisture losses from soil and weeds, and maximizing the proportion of rainfall available to the crop. However, some of these practices increase crop attractiveness for insect vector landings, which can accelerate virus spread resulting in more damaging virus epidemics (Jones, 2009; Jones and Barbetti, 2012; references therein). Protected cropping environments are often highly conducive to virus epidemics because the irrigation regimes, high relative humidity, warm temperatures used, and cultural practices employed favor them or their vectors, especially whiteflies, thrips, aphids, and root-infecting fungal vectors. However, the high values of the crops grown often permit deployment of expensive, comprehensive integrated disease management (IDM) approaches so any impacts of climate change in aggravating the virus epidemics caused are likely to be limited (Jones and Barbetti, 2012; references therein).

5. IMPLICATIONS FOR CONTROL General climate instability impacts on plant hosts, vectors, and viruses alike and alters pathosystem dynamics, which, in turn, drives virus and vector evolution at an accelerated rate in response to changing circumstances. Accelerated virus and vector evolution, increasingly intense and frequent

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extreme weather events, and the generally less predictable climate are projected to increase uncertainty over the effectiveness of control measures against plant virus epidemics. This uncertainty is likely to compromise decision making over when control measures are needed, and, if so, which to employ to optimize the desired outcome. Moreover, when crops are grown in regions where the temperature has become too high for their optimal growth, they are likely to become physiologically less able to withstand virus infection. Also, when temperature-sensitive host resistance genes are deployed, these are likely to become ineffective. Predicting the timing of sprays with oils, repellents, or pesticides to coincide with peak arthropod vector flight times is likely to become more difficult. Cultural control measures would become less reliable, eg, planting upwind of infection sources, sowing nonhost barriers when prevailing winds change, and measures such as manipulation of sowing date, planting early maturing cultivars, or harvesting early when sowing dates and vector flights become less predictable. Deploying nonselective control methods would be particularly important when attempting to limit spread of unknown or little understood viruses occurring as a consequence of climate change. In such cases, it will be important to deploy tactics that employ generic information on control measures previously used effectively with related pathosystems. Moreover, as climate instability increases, predictive models will be needed increasingly to determine when and where control measures are necessary, which control measure combinations are likely to be effective, and the risk of emergence of damaging new viruses (Jones, 2009; Jones and Barbetti, 2012; references therein). In undisturbed communities of wild native plants coevolution of host plants with viruses and vectors over millennia has selected natural host resistances and tolerances to both of them, and, as mentioned above, other natural control measures also operate that help suppress virus epidemics. Fragmentation and disturbance of natural vegetation disrupt these natural control measures and therefore are likely to aggravate virus epidemics in native plant communities. Direct stresses on native plants caused by climate instability are likely to exacerbate these epidemics in similar ways. Little is known of how to control them effectively, but knowledge of the natural control measures that operate in undisturbed wild plant communities provides clues (Jones and Barbetti, 2012). Jones (2014b,c) discussed how rapidly advancing technological innovation currently underway in the world is providing many opportunities to improve virus control measures and so help mitigate the impact of climate

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change on virus epidemics in cultivated plants. Recent innovations in remote sensing and precision agriculture give valuable information about (i) virus epidemics occurring not only on continental, regional, or district scales (via satellites) but also within individual crops (via lightweight unmanned aerial vehicles or tractor-mounted sensors), and (ii) exactly where to target control measures. Improvements in information systems and innovations in modeling improve (i) understanding of virus epidemics and ability to predict them, and (ii) delivery of advice on control measures. Molecular epidemiology approaches provide insights about genetic variation within plant virus populations involved in epidemics, and how this variation drives what occurs when they develop. Improvements in virus detection technologies provide many opportunities to collect and analyze new types, and ever-increasing amounts, of data about virus epidemics, and the genetic variability of the virus populations involved. These types of advances provide the means to (i) greatly streamline collection and processing of epidemiological data sets; (ii) collect and process new types of epidemiological data; (iii) enhance knowledge of epidemics by making available new insights into why and how they develop; and (iv) provide much more effective prediction and decision support over when to deploy carefully targeted interventions that suppress damaging epidemics effectively on continental, regional, district, or within-field scales. In their analysis of the current status and prospects for plant virus control through interference with vector transmission, Bragard et al. (2013) emphasized that many gaps in knowledge about virus transmission mechanisms remain because current understanding of virus–vector–host complexes is limited to a small number of well-studied systems. Advances in genome sequencing and molecular technologies could help to address these problems and might allow development of innovative control methods through interference with vector transmission. Also, a deeper understanding of vector behavior could be used to devise new control strategies that disrupt the complex association between host plant, vector, and virus. They suggested that novel, innovative control measures were needed because of the increased risks from vector-borne virus diseases that arise from environmental change. Their approach was long term rather than focusing on technological advances with potential to be applied soon to mitigate virus epidemics currently being aggravated by climate change, as discussed recently by Jones (2014b,c). They suggested possible future opportunities for introducing new host resistance traits to control viruses and/or vectors when no resistance genes are available in related species or to reinforce partial or quantitative resistance, such as:

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(i) plants expressing complementary double-stranded RNAs or infected with virus-derived molecular vectors that induce RNAi to target specific genes necessary for insect vector survival; (ii) densovirus-mediated RNA interference for aphid vector control; (iii) a resistance mechanism that relies on a serine hydroxymethyltransferase-encoding gene for controlling nematode vectors; (iv) RNA interference to engineer resistance against plant viruses, (vi) plantibodies and nanobodies that act against viruses when expressed in plants; and (vii) specific sequences targeting vectors or viruses operating via RNA silencing. However, virus or vector resistance is just one of the many beneficial traits that farmers have to consider when selecting a cultivar to grow. Therefore, unless the virus disease being controlled is of such overriding importance they cannot do without virus resistance, farmers tend to choose a susceptible cultivar that optimizes yield and quality of product instead of selecting a virus resistant one. IDM approaches that include phytosanitary, cultural, and chemical control measures, as well as host resistance if available, provide them with a practical means to optimize virus control (eg, Jones, 2001, 2004, 2006). With high value protective cropping, biological control measures are often included too. IDM programs benefit greatly from use of predictive models which alert the farmer over the need for, and timing of, control measures (eg, Jones et al., 2010). As climate change progresses, employing a flexible and intelligent approach to controlling virus diseases in crops that uses a combination of IDM, predictive modeling, and newer technologies, such as remote sensing and precision agriculture, is likely to provide the best solution to providing effective control under an increasingly unpredictable climate. Finally, the potential for gene editing through CRISPR-based technologies to control insect vectors of human diseases, such as mosquitoes, has gained much attention recently because they are cheap and easy to use (Reid and O’Brochta, 2016; Webber et al., 2016). Their potential for inclusion as an additional component acting against insect vectors within IDM approaches seems likely to be the subject of much future research.

6. INFORMATION GAPS AND DEFICIENCIES Jones and Barbetti (2012) emphasized that reviewing the literature on plant virus spread in relation to climate change constituted a challenging undertaking because information then available about probable alterations in most of the diverse biological parameters involved was limited, or often completely lacking. Furthermore, the emergence of previously unknown viruses in new encounter scenarios, and, with vector-borne viruses, the

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complication of having to take into account the effects of climate change parameters on the diverse types of vectors involved, added important extra variables. In the international research data then available, they identified many information gaps and deficiencies over the likely effects of climate change on plant virus epidemics. This section summarizes the gaps and deficiencies they identified but modifies them where appropriate to take into account progress made since 2011 when they were written: 1. More predictive climate change scenario modeling is required to establish (i) whether damaging virus epidemics that already occur in a locality are likely to become more damaging; (ii) where climate change is likely to result in damaging virus epidemics in regions where the virus concerned was previously of limited importance; (iii) when significant viruses or vectors are likely to invade regions where conditions were formerly unsuitable for them; and (iv) which different types of control measures are likely to remain effective, or become less effective or ineffective, and when the critical time to deploy such measures would be. 2. With greenhouse gases, information is still completely lacking on the effects of elevated concentrations of nitrous oxide and methane on biological parameters associated with plant virus infections and virus vector populations. Such information is also minimal or lacking on the influences of eCO2 on several types of insect vectors (leafhoppers, planthoppers, treehoppers, beetles, and mealybugs), and on mite, nematode, and fungal virus vectors. Also, although accumulating steadily for several important aphid vector species, it is still very deficient for other aphid vector species, viruses, and both whitefly and thrips vectors. Addressing these deficiencies should be an important focus of future research. 3. Although the influence of elevated temperature on plant viruses and their vectors has received more attention than the influences of other climate parameters, more research is urgently needed as many important issues have been neglected. These include its influence on virus multiplication inside vectors and on virus transmission efficiencies achieved by insect vectors other than aphids, whiteflies, and thrips, and by mite, nematode, or fungal vectors. Also, more research is needed on the possible effects of prolonged heat waves in mitigating or enhancing damaging virus epidemics. 4. More information is required on the effects of increased or decreased rainfall, and the extreme weather parameters drought, flooding, and

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6.

7.

8.

9.

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increased wind speeds on spread of virus diseases. Also, existing studies with different virus pathosystems gave conflicting results regarding the influence of drought, and this situation needs to be resolved. Moreover, more data are urgently needed on the influences of (i) drought and flooding on dissemination of water-borne viruses and on the probability that their epidemics would be mitigated or enhanced, and (ii) increased wind speeds on arthropod vector behavior and the extent of virus spread by them, and the extent of wind-assisted spread of contact-transmitted viruses. Very little research has been done on the effects of alterations in relative humidity on virus spread so further research is needed on this, particularly over the influence of altered relative humidity on the activity and survival of arthropod vectors and stable viruses within the critical leaf surface microclimate. Information is still lacking regarding the likely effects of climate change parameters on several biological parameters, eg, pollen transmission of viruses and their ability to multiply within vectors. There is also only minimal information on their influence on several others, eg, virus or vector survival in water or soil; virus transmission by seed; alternative cultivated or weed reservoir host infection with viruses or fungal vectors, or their infestation by arthropod or nematode vectors; and alterations in plant morphology relevant to virus infections. Addressing these deficiencies should be an important focus for future research. Research is needed to (i) understand which climate change parameters accelerate evolution of generalist viruses to become more virulent, overcome host resistances, and make host species jumps; and (ii) devise models that use this information to help identify where climate changeinduced temporal and spatial shifts in crop, reservoir, and weed host distributions are likely to foster new encounter scenarios which could result in damaging emerging virus epidemics. Research is required in wild plant communities located at the interface between natural and managed vegetation to understand the likely influences of different climate change scenarios in triggering virus epidemics arising from new encounters with introduced viruses or vectors that threaten biodiversity. More research is required on the influence of climate change parameters, especially enhanced temperature, on shifts in species balance in situations where virus spread is only occurring in an individual component species within mixed-species pasture swards and wild plant communities.

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10. Much more emphasis is required on following up information found using experiments with potted plants growing in controlled environment facilities by field experiments investigating the effects of diverse climate change parameters on viruses, vectors, and plant hosts in field situations, including in FACE facilities, open-top chambers, heated and rainfall-adjusted plots, and plots growing in regions with high temperatures or where flood or drought conditions occur. 11. Research is needed to develop integrated disease management approaches that are well validated by field experimentation, and effective against virus epidemics under diverse climate change scenarios. Such approaches would need to include nonselective control measures as these are more likely to remain effective under widely diverse climate change situations. They would also need to emphasize rapid application of technological advances that improve the capacity for shrewd and locally appropriate decision making. 12. Finally, many virus epidemics represent situations where multiple stresses occur, but few experiments address climate change scenarios where several parameters change simultaneously and continuously so limiting their usefulness in making predictions. Research is urgently required to examine not only the effects of multiple climate variables on single virus infections or single vector species but also the influences of single environmental variables on mixed infections with viruses or in multiple vector species situations. The challenge in the future would be to manipulate multiple environmental parameters across multiple viruses and vectors together on a single host species to define future expansions or contractions in individual and combined disease epidemics.

7. CONCLUSIONS In a review written in 2013, Jones (2014b) wrote “When compared with the magnitude of the worldwide research effort to assess the likely impacts of climate change on the severity of fungal disease epidemics and insect pest outbreaks, there has been lamentably little focus on research to determine the magnitude of the threat from diseases associated with diverse plant virus pathosystems under different climate change scenarios.” Although there have been encouraging signs of increased research activity and progress being made in some areas since then, this statement still holds true in many instances. The most notable exceptions concern the number of recent studies on the influences of factors like eCO2, elevated temperature,

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and rainfall-related parameters upon a small number of important viruses, eg, BYDV, CMV, TYLCV, and TuMV, and several important vectors, eg, the aphids A. pisum, M. persicae, R. padi, and S. avenae, and, to a lesser extent, the whitefly B. tabaci and the thrips F. occidentalis. There have also been encouraging signs of research going beyond small-scale pot experiments undertaken under controlled environment conditions to being undertaken in field experiments that more closely reflect real world situations, eg, with BYDV and its key vector R. padi in FACE facilities (Rua et al., 2013a) and heated and rainfall-adjusted pasture swards (Rua et al., 2013b), and in open-top chambers with TYLCV (Huang et al., 2012) and B. tabaci (Wang et al., 2014a). Other encouraging signs include several investigations that examine the effects of: (i) combinations of different climate stress parameters upon a single plant virus or insect vector, or both a virus and its vector occurring together; and (ii) a single-climate stress parameter upon mixed infections with more than one plant virus, mixtures of a plant virus and another type of plant pathogen, or a plant virus and its principal insect vector occurring together. There has also been important progress in understanding how climate stress parameters influence plant host defense machinery against viruses and insect vectors. The recent realization that spread of plant viruses through wind-mediated contact transmission and water-mediated transmission is more important than previously thought, and likely to be influenced by climate change, constitutes another example of progress. Nonetheless, the extent of the information gaps and deficiencies over possible effects of climate change scenarios on plant virus epidemics remain enormous. Moreover, the task of addressing them is becoming ever more urgent because increasing climate instability is likely to make damaging virus epidemics in staple food crops, and other economically important plants, increasingly difficult to predict and control, especially in tropical and subtropical regions where food insecurity is already a serious issue due to their rapidly growing human populations. Adding to these difficulties is (i) the projected accelerated appearance of epidemics caused by newly emerging viruses and newly introduced viruses and vectors in new encounter scenarios, and (ii) the climate-induced alterations in host morphology, physiology, resistance to vectors or viruses, vector/virus life cycles, abundance, diversity, reservoirs, and inoculum that are anticipated. As global climate change progresses and the world’s population continues to increase, the future looks increasingly bleak because of the threat posed to food production and natural ecosystems. Increasing difficulties in managing virus epidemics in cultivated plants and wild vegetation are

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expected to contribute significantly to this negative scenario. Fortunately, however, rapidly advancing technological innovation currently underway in the world has the potential to provide many opportunities to improve the effectiveness of virus and vector control, and so help mitigate the impact of climate change on plant virus epidemics. Their successful application will depend greatly on an improved understanding of how to circumvent the effects of increasing climate instability on these epidemics.

ACKNOWLEDGMENTS I thank the Western Australian Agriculture Authority, John Stretch and David Stephens of the Department of Agriculture and Food Western Australia, and Jari Valkonen of the University of Helsinki for permission to use the satellite image, aerial photograph, and maps in Figs 1–3, and Alison Mackie, a PhD student of the University of Western Australia, for permission to use the two lower photographs in Fig. 1.

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