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ACO301 - Defra Final Project Report – March 2008 (ANNEX 7)
ANNEX 7
Pest and Disease Impacts
Impact of extreme climate events on pests and diseases of crops
Climate has profound impacts on populations of pests and diseases, affecting their
development, reproduction and dispersal. Changes in environmental conditions will have
direct effects on the pests and pathogens themselves and such changes can be studied in the
laboratory and modelled mathematically to produce forecasts. Many pests will be able to
produce more generations per year in warmer conditions, many fungi are favoured by humid
conditions, and wind may assist the dispersal of both. Extreme weather events also affect
survival (e.g. intense rainstorms or wind or high temperatures are related to the mid-season
aphid population crash in several species (Karley et al. 2004)).
There may also be indirect effects of climate change on pests and disease through their hosts.
Changes in plant growth may alter the timing of events which could have critical effects. If
climate change affects a vector or a host plant in a different manner to the pest or pathogen,
their life cycles could become desynchronised. This is particularly important for
pests/pathogens with a time-limited target such as young seedlings or flower buds, with a
consequent small window of opportunity for infestation or infection. An example is
Operophthera brumata (winter moth of apple), as bud-break of its winter host Picea sitchensis
is predicted to be altered less under climate change than its own larval emergence in spring
(expected to be earlier) (Dewar and Watt 1992). Even in cases that are less time-critical, the
impact of pests and diseases is often related to the growth stage of the host (e.g. young
plants are most susceptible). Some resistance genes and pathways function only at particular
growth phases of plants, e.g. resistance to blackleg stem canker (Li et al. 2006; Marcroft et al.
2005). The effect of climate change on such interactions is difficult to study and as such is not
generally reported in current scientific literature.
Further indirect effects of climate will arise through effects on vectors, predators and
competitors. Many diseases are spread via invertebrate vectors, notably (but not exclusively)
viruses. The impact on such diseases of extreme climate events will depend to a large extent
on effects on the vector. Thus barley yellow dwarf virus (BYDV) is commoner after mild
winters due to the enhanced survival of its aphid vector. Synergistic interactions may exist in
certain pathogen combinations, for example between potato virus Y and other viruses such as
potato virus X (Hoffmann-Wolf et al. 1990) (Mayee and Sarkar 1982). The synergistic
interactions might well have their own ‘optimum’ climatic conditions that do not necessarily
reflect the optima for the individual partners (Reyes and Chadha 1972). Thus, the disease
complex of Pratylenchus penetrans with Verticillium dahliae (potato early dying disease)
(Rowe et al. 1985) is most pronounced in seasons when high-temperature stress occurred
during tuberization (Rowe et al. 1985). The effect of (extreme) climate events on the complex
web of biotic interactions is hard to assess and yet is likely to be an important component of
the outcome to crops.
Temperature
Most pests have temperature-dependent rates of development and have particular threshold
temperatures above which development can occur and below which development ceases.
Some pest species may be able to complete more generations with higher temperatures (if
these are below lethal high temperatures). There is abundant information available about the
effects of temperature on aphids. For aphids such as Myzus persicae that can overwinter as
active adults, warmer conditions in winter lead to earlier and larger spring migrations to crop
hosts (case study). Similarly, for Delia radicum it is predicted that in a climate 5°C warmer,
activity will start earlier in the spring and there will be an increase from 3 to 4 generations per
year of (Collier et al. 1991). Temporary exposure of populations to extreme temperature (e.g.
39°C) may decrease the rates of growth of surviving individuals and delay the subsequent
generation, particularly if the teneral stage was exposed to the extreme temperature (Harrison
and Barlow 1972).
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Pest behaviour (movement through soil, flight, mating) may be altered with temperature. Even
such aspects as the aphid drop response to alarm is less likely to happen under hot and dry
conditions than more benign conditions, probably due to the increased risk of desiccationinduced mortality whilst the aphid walks and searches for a new host (Dill et al. 1990).
Some pests have an ability to adapt to higher temperatures if pre-exposed. For example,
above 34°C Acyrthosiphon pisum is beyond its temperature optimum for growth and
reproduction, but periods spent previously at lower temperatures result in the aphids
undergoing acclimation and surviving slightly better (Harrison and Barlow 1973), with
implications for pest outbreaks in long hot periods.
Pathogenic micro-organisms are rarely limited to one life cycle per year but will complete as
many as conditions allow. Whilst temperature optima are often studied, temperatures above
30°C are not routinely tested for temperate organisms. Consequently there are less data
published about the likely effects of periods of unusually warm weather on UK pests and
diseases.
For those pathogens which use invertebrate vectors, temperature can have additional effects
on the interaction. For example, when phytoplasmas (e.g. aster yellows MLO) are acquired by
leafhoppers from infected plants, there is a latent period before the vector is able to transmit
the micro-organism to new hosts. The latent period reduces under high temperatures,
meaning faster turnover of infectious pathogens through the vector (Baker et al. 1996).
Temperature can also affect the retention time of non-persistently-transmitted viruses on
aphid mouthparts, with implications for the spread of viral epidemics (Jurik et al. 1987).
Extreme temperatures and increased frequency of heatwaves may be deleterious to some
current UK pests. For example, Peronospora viciae, Hyaloperonospora parasitica,
Synchytrium endobioticum, Plesiocoris rugicollis and Deroceras reticulatum are all examples
of organisms that prefer cool temperatures.
Water
The availability of free water is extremely important in the life cycle of many micro-organisms.
Many types of fungal spores require free water for periods of several hours for germination
(e.g. Botryotinia fuckeliana (Broome et al. 1995), Alternaria brassicae (Collier and Finch
1983)), and zoospores (produced by many fungal pathogens) spread through swimming (e.g.
Phytophthora, Pythium (Smilde et al. 1996)). Bacteria are also often actively motile in water.
Rain splash is used by many pathogens as a passive means of physical dispersal of spores
or other propagules (Pielaat et al. 2002). Modelling leaf wetness is consequently of great
importance to disease forecasting (Anon 2005). The absence of water affects pest behaviour.
In conditions of drought, aphid vectors of viruses may be encouraged to travel further, visit
more plants and hence exacerbate disease spread (e.g. BYDV (Smyrnioudis et al. 2000)).
In contrast, too much water can be devastating for some pests. Raindrops can physically
dislodge the pest from its host plant (Mann et al. 1995). Behaviour patterns can be disrupted,
such as the ability to fly and spread to new crops, or an inability to hide and feed (Esbjerg
1988). Water-intolerant pests include cutworms (Agrotis segetum) (see case study),
wireworms (Agriotes spp.), potato tuber nematodes (Ditylenchus destructor) and diamondback moth larvae (Plutella xylostella) (Clarkson et al. 2004; Esbjerg 1989; Wakisaka et al.
1991).
The effect of water is often incorporated into modern forecast models for pathogens using
measurements of relative humidity or leaf wetness rather than rain measurements.
Unfortunately there is no simple mechanism to calculate these parameters from the rainfall
data predicted by climate change models. Consequently it has been very difficult to integrate
the climate and pathogen models to predict the effects of extreme weather on diseases (see
case study on Phytophthora).
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Wind
Wind is important in the dissemination of sex pheromones by several pest insects, and in
locating potential hosts by their volatiles (e.g. (Antignus et al. 1996)), although it is hard to
envisage an extreme climate event that would affect these behaviours to any great extent. On
the other hand, wind direction, and high altitude wind in particular, is important to the flights of
migratory pests. The spread of Cydia pomonella (codling moth) is very dependent on wind
direction (Mani and Wildbolz 1977). The arrival of diamond-back moths (Plutella xylostella)
(see case study) is known to be determined by wind direction (Chapman et al. 2002; Coulson
et al. 2002; Kohno et al. 2004). Autographa gamma (silver Y moth) is a migrant which uses
high-level north winds to return to North Africa/the Middle East in autumn (Barasubiye et al.
1994; Kohno et al. 2004). It is possible that some insects are able to select their vertical
altitude to pick appropriate wind directions for migrations (Reynolds et al. 2005; Wood et al.
2006). Reproduction by some aphids is inhibited in wet and windy conditions, but the adults
become unsettled and inclined to move to new locations (Mann et al. 1995; Narayandas and
Alyokhin 2006). Wind delays take-off by Aphis fabae (black bean aphid) (Kennedy 1990), and
Ceutorhynchus assimilis (cabbage seed weevil) prefers low wind speeds (Achar 1998;
Antignus et al. 1996).
Over land, a significant proportion of airborne particulate material is biological, including
pollen, fungal spores, bacteria and plant debris (Jones and Harrison 2004). The wind speed
necessary to disrupt material (e.g. spores) is less on a plant surface than on the ground
(Jones and Harrison 2004) and wind determines the spread of numerous fungi. The vertical
concentration of bacteria declines less than fungal spores (Jones and Harrison 2004),
indicating perhaps a greater potential for long-distance spread. Erwinia amylovora (fireblight)
is believed to have spread through Europe (Behalova 2004; Billing and Berrie 2002). Many
other bacteria, e.g. Pseudomonas syringae pv. syringae, are known to be spread by wind/rain
(Hayward and Waterston 1998).
Although the current climate models do not contain a wind component, wind is likely to have a
strong influence on extreme pest and disease events, both in the arrival of immigrants (and
the timing of such occasions) and in their eventual spread within the UK.
Solar radiation
Cloud cover and solar radiation are components of climate that could change in future, but
which have not been modelled. Photoperiod is known to be important in regulating the timing,
activity and synchronisation of many events for insects (Anon 1960; Ansari et al. 1989; Bale
et al. 2002) but it is hard to foresee a weather event affecting this. Some airborne spore
concentrations have been correlated with solar radiation (Adams et al. 1986) (sunny dry days
had most spores). Conversely, bright light can inhibit fungal spore germination (e.g. Alternaria
solani (Rotem et al. 1985; Stevenson and Pennypacker 1988)) or even kill spores (e.g.
Phytophthora infestans (Mizubuti et al. 2000))
Bright light can be deleterious to some pest eggs e.g. Tipula paludosa (Ahn and Hahm 1998).
It has also been implicated in the control of the timing of diapause in some insects (Axelsen et
al. 1997) and behaviour such as searching for mates (Hirota and Obara 2000). Complete or
partial absorption of solar UV can disrupt some fungal life cycles (Al-Dahmashi and Khlaif
2004) and alter the visual behaviour of some insect pests (Bylemans 1998), useful in
glasshouses but unlikely to be of importance in field crop situations.
It is becoming clear that light has a role in the correct functioning of the classical plant
resistance response to pathogens (Roberts and Paul 2006), with weakened resistance in poor
light levels (Staub and Williams 1972) although it is inconceivable that an extreme event
would result in so little light as to abolish resistance.
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Effects on ability to control pests and diseases
The most economically important pests and diseases are often controlled through
combinations of monitoring and forecasting, applications of pesticides, natural resistance, use
of scheduling times and good husbandry. In considering the effects of extreme climate events,
it should not be forgotten that such events may also affect the efficacy of current control
measures.
Control by chemicals (pesticides/fungicides/biocides etc.) can be affected by weather, for
example high temperature is reported to reduce the effectiveness of some chemical controls
(Paiva et al. 1995; Palm 1975) or increase others (Grafius 1986; Yadwad and Kallapur 1988;
Zhu et al. 2006). Humidity levels can also modify the efficacy of some pesticides(Imai et al.
1995), as can the timing and the amount of rain following the application of pesticides (Suss
et al. 1994). On a simpler level, rain can affect the ability to apply the control chemical at the
time of most need, e.g. Aculus schlechtendali (apple rust mite) was reported to be numerous
in the Netherlands after a wet spring when conditions prevented the usual sprays (Bylemans
1998), possibly an increasingly likely scenario.
The effectiveness of resistance genes can break down under changed climatic conditions,
particularly at 30°C and above. Although Fulvia fulva (leaf mould) is no longer considered to
be of serious concern to tomato growers due to the availability of resistance genes (Cf), some
of these genes break down above 30°C, for example at 33°C there is a (reversible) failure of
the necrotic resistance response (Jong et al. 2002). Several resistance genes to tobacco
mosaic virus (Tm) can also fail above 30°C (Cirulli and Ciccarese 1975; Fraser and Loughlin
1982; Pilowsky et al. 1981).There are numerous other examples of resistance breakdown at
high temperatures ((Kuginuki et al. 1991), (Huang et al. 2006), (Li et al. 2006), (Badawy et al.
1992), (Ellis et al. 1994), (Redolfi et al. 1977), (Eisbein and Haack 1985), (Celebi-Toprak et al.
2003), (Jong et al. 2002), (Cirulli and Ciccarese 1975), (Pilowsky et al. 1981), (Fraser and
Loughlin 1982), etc.). Moreover high humidity works synergistically with this breakdown
(Wang et al. 2005).
Pests and pathogen populations may themselves develop resistance to chemical or genetic
control measures. The ability to overcome resistance may carry a fitness cost to the pest or
pathogen. This may be expressed as a reduced ability to multiply in the absence of the
control measure (Jenner et al. 2002), or as a greater susceptibility to weather conditions (e.g.
Myzuz persicae with esterase-based insecticide resistance are less likely to survive a cold
wet windy winter (Foster et al. 1997; Foster et al. 1996)).
Control by natural enemies is increasingly common, particularly in glasshouses and orchards.
Parasitic insects and predators will have their own climate optima, although not necessarily
the same as their hosts (Campbell et al. 1974; Islam and Chapman 2001), e.g. Eriosoma
lanigerum (apple woolly aphid) can be controlled via Aphelinus mali but currently this is only
effective in the south east of the UK because the parasite needs warmer drier climates (Ahn
and Hahm 1998). It is a pertinent to ask whether extreme events will affect the enemies to the
same extent/in the same direction as the pests they are intended to control (Arthurs et al.
2003). For example C. pomonella can be controlled by Cydia granulosis virus at 15-30°C but
the virus has reduced mortality at 34°C (Keller 1973); control is also possible using the
nematode Neoaplectana carpocapsae agriotos which works well at high temperatures
(Rasinya 1976). Acyrthosiphon pisum (pea aphid) is more resistant to infection by the
entomopathogenic fungus Erynia neoaphidis at 28°C compared to 18°C (Stacey and
Fellowes 2002).It is difficult to predict how extreme climate events would impinge on such a
complex web of biotic interactions.
New pests and diseases
The advent of milder winters and warmer summers, more typical of other parts of Europe
today, has implications for the survival and reproduction of new pests and diseases. Nonindigenous pests and diseases may initially become established in protected crops under
glass.
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Despite national and international restrictions and procedures, sometimes unavoidable
circumstances occur that allow new pests and diseases to establish and spread. Erwinia
amylovora (fire blight of apple, probably the most important intra-European quarantine
organism (EPPO 2007)) was first noticed in the UK in 1957, then spread, possibly via migrant
starlings grounded in coastal areas of England in 1964 because of adverse weather (Billing
and Berrie 2002).
Some of the more notable agricultural alien pathogens and invertebrate pests recently
intercepted on arrival in the UK include significant numbers of Leptinotarsa decemlineata
(Colorada potato beetle), Anoplophora chinensis (Citrus longhorn beetle), Trialeurodes
abutiloneus (banded-winged whitefly), Trialeurodes ricini (castor whitefly), Thrips palmi
(melon thrips), Bemisia tabaci (tobacco whitefly), Helicoverpa armigera (Old World bollworm
caterpillars) and Xanthomonas fragariae (angular leaf spot of strawberry). Additionally, there
have been new UK outbreaks of important new invasive alien pests such as Diabrotica
virgifera virgifera (Western corn rootworm), Lymantria dispar (gypsy moth) and Cacopsylla
fulguralis (Elaeagnus psyllid).
Future novel crops may be sources of pests and diseases new to the UK, some of which may
have host ranges which overlap current UK established crops. The possible outcome of such
introductions would have to be assessed on a case by case basis. An example would be
Naupactus leucoloma (white-fringed beetle), a Schedule 1 polyphagous pest of maize that
includes brassicas, peas, and potato in its host range.
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