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THE ANCIENT Israelites feared the ‘blight and mildew’ that destroyed
their crops. The Romans sacrificed to appease a ‘rust’ god, who had the
power to smother their corn with fungal rusts. The potato blight changed
the history of Ireland in the 1840s when it destroyed the country’s staple
crop. The fungi that cause these blights, mildews and rusts reproduce by
spores. Each spore is a single passive cell, unable to move of its own accord,
yet each is capable of causing infection. Fungi produce enormous numbers
of spores, but how can such passive organisms spread so fast and cause such
catastrophes? Some spores, such as those of the fungus that causes Dutch
elm disease, are carried by insects or other organisms. Most often, however,
spores are moved by purely physical means: on the wind or in splashes from
rain.

Wind and rain are central to the life cycle of the fungi that cause
disease. The study of this transport through the air, aerobiology, has played
a large part in helping us to understand how epidemics of plant disease
take place. One practical outcome has been that scientists can now forecast
outbreaks of disease and pinpoint the best times to apply fungicides. But
the benefits go further. The principles behind the way in which wind and
rain disperse spores apply to other areas of agriculture, such as the drift
of pesticides, as well as the spread of human diseases. They are also relevant
to any assessment of the risks of releasing genetically engineered organisms
into the environment.

Many of the fungi that ravage crops are adapted for dispersal by rain.
One example is the cereal eyespot pathogen, Pseudocercosporella herpotrichoides,
which attacks the base of the stem, causing plants to fall over. Eyespot
was probably the most serious disease of winter wheat in northern Europe
in 1987. Other pathogens that spread in droplets from splashes of rain include
those that cause Septoria blotch of wheat (Mycosphaerella graminicola and
Leptosphaeria nodorum) and leaf blotch of barley (Rhynchosporium secalis).
These blotches reduce the yield of crops by killing parts of leaves, so
preventing photosynthesis and causing leaves to die prematurely. These fungi
produce their spores in a mucilage or slime, within fungal structures on
or in the host’s tissue, at times when humidity is high. The slime holds
the spores together, preventing dispersal by wind alone. The first raindrops
dissolve the mucilage to produce a suspension of spores in a thin film of
water on the surface of the stem or leaf. As more raindrops strike the infected
tissue, the splashes scatter the spores. This limits dispersal to damp periods
when conditions are best for spores to germinate and infect their hosts.

Some fungi reproduce both asexually and sexually at different stages
in their life cycle. Generally there is a single cycle of sexual reproduction
each season, but fungi may reproduce asexually several times in a year.
Often, the asexual spores depend on rain for dispersal, while the wind carries
spores produced by sexual reproduction. This means that the fungus may travel
long distances only once a year. At other times spores travel shorter distances,
with dispersal tuned to the weather. It is as though the fungus forages
for host crops, and, when it finds one, pauses to exploit it.

At the Institute for Arable Crops Research at Rothamsted, we study how
both wind and rain spread spores in a complex arrangement of a ‘rain tower’
and a wind tunnel. From simulated raindrops falling down the tower onto
suspensions of spores or infected plant material, we estimate that one splash
can produce more than 2000 spore-carrying droplets, scattering more than
50 000 spores. In theory, each spore could produce a new infection. With
an average rainfall of 80 centimetres a year, typical of the drier parts
of Britain, each square metre of ground receives as many as 8 billion (10**9)
raindrops large enough to produce a splash. The potential for spreading
disease is enormous.

As the wind tunnel shows, splash dispersal is essentially a short-range
process. In still air, few splash droplets travel further than 1 metre from
the source or reach heights greater than half a metre. The number of spores
in a droplet is roughly proportional to its volume: most spores are carried
in large splash droplets, more than a millimetre in diameter, although a
few travel in droplets as small as 50 micrometres. Wind can move the droplets
farther. With a wind speed of 2 metres a second, spore-carrying droplets
travel as far as 4 metres; a few airborne spores reach as far as 10 metres
downwind.

Observations in field crops bear out these results. Out of doors, few
spores travel farther than a few metres from their source, but a small number
of spores reach 2 metres above the ground. This suggests that most splashes
will scatter pathogens locally, usually within a crop. But if the spores
in small airborne droplets remain viable for long enough, they could spread
diseases over much greater distances.

The blights, mildews and rusts that have periodically devastated crops
since ancient times are all caused by windborne pathogens with asexual spores.
These spores are produced in vast numbers on the infected leaves of host
plants. The layer of air next to the surface of a leaf, the boundary layer,
is very still. So the spores are borne in chains (mildews) or on the ends
of stalks (blights, rusts), which hold them away from the leaf, where a
gust of wind can detach them and carry them away. The wind also transports
sexual spores (ascospores), which are expelled from fungal structures on
the host. The ejection mechanism propels the spores a few millimetres into
the turbulent air beyond the boundary layer. There, larger eddies may sweep
them up, carrying them through the crop or above the crop, often for long
distances. For example, the wind spread coffee rust hundreds of kilometres
throughout South America in the 1970s.

This sort of spread convinced aerobiologists that some fungi had a sexual
phase that no one suspected before. Light leaf spot (Pyrenopeziza brassicae)
is a serious disease of oilseed rape. The asexual spores commonly found
on infected plants are produced in mucilage, so researchers assumed that
the disease was spread in rain splashes. Recently, Alastair McCartney and
Maureen Lacey at Rothamsted collected many spores of P. brassicae up to
4 metres above and 18 metres downwind of infected crops: the concentration
of spores decreased with increasing height and distance from the crop. Splash
dispersal could not have been responsible for this pattern. McCartney and
Lacey also detected spores when it was not raining. And although they were
similar in shape to the asexual spores, some of the airborne spores were
in clumps of four or eight, suggesting that they might be the sexual spores
of the fungus, which had never been found in Britain. The researchers found
the sexual stage of the fungus on infected leaves decaying in the debris
under the crop. In experiments in the wind tunnel, they showed that this
debris was the source of the airborne spores.

The discovery of the windborne sexual stage of the light leaf spot fungus
has important implications for farmers and growers. Calculations suggest
that windborne ascospores can travel several kilometres from infected fields
of oilseed rape and threaten other brassicas such as cabbages and Brussels
sprouts. And if its sexual stage is common, the fungus will have a greater
potential for genetic variation. The more variation there is within a species,
the greater the chance that a strain will emerge that is resistant to fungicides.

Similarly, in experiments at Long Ashton Research Station, near Bristol,
we have shown that epidemics of Septoria leaf blotch in newly sown wheat
are almost certainly started each autumn by sexual spores carried in the
air. This means that populations of the fungus over large areas are likely
to be genetically mixed, and explains the otherwise puzzling finding that
resistance to the fungicide carbendazim does not depend on whether a farmer
has used this fungicide before.

Many fungal diseases appear first as patches of intense infection in
crops that are otherwise free of disease. Such patches may result from the
topography of the field or they may reflect the initial distribution of
sources of spores. For example, the first infections in a field may be caused
by spores blown in from outside. As the pathogen on each infected plant
produces further generations of spores, these set off new infections. To
begin with, the infection becomes less severe the further you go from the
source.

The classic empirical models that describe how spores or disease decrease
in concentration with distance from a source were developed by the late
Philip Gregory with his wife Margaret. A useful model, which fits much of
the data, is the negative exponential model. Taking the analogy with the
half-life of radioactive decay, we can describe the spread of infection
as the half-distance, the distance in which the number of spores or amount
of disease decreases by half. The problem with these models is that they
give no information about the physical processes underlying dispersal, and
it is difficult to generalise from one case to another. But theoretical
physics can help us to devise more general models. In the air above a crop,
turbulent wind eddies can disperse spores or bacteria hundreds of metres:
we can describe this movement by models developed to track the diffusion
of air pollutants from a source.

More complex models are needed to explain how spores disperse within
a crop. Brian Legg and Peter Walklate, now at the AFRC’s Institute of Engineering
Research at Silsoe, in Bedfordshire, recently simulated the way in which
spores (or rain-splash droplets carrying spores) fly and settle, using information
about the structure of a crop and the turbulence within it. They found that
many spores are deposited closer to the source than the scale of turbulence
would suggest, and so standard diffusion theory does not apply within the
crop itself.

Each year farmers spend millions of pounds on fungicides, and not always
to much effect. For both economic and environmental reasons we need to ensure
that farmers apply pesticides only when necessary. Before we can offer the
appropriate advice, however, we must first understand the biology of these
diseases and know how and, especially, when, they spread. Forecasting disease
is useful if the disease causes damage only occasionally (if it is always
damaging everywhere then there is always a need to spray) and if the crops
can be sprayed at a time when the fungicide will have some effect. Many
forecasts are based on conditions that favour infection (often high humidity
or the presence of free water) and do not take account of dispersal, because
for many pathogens dispersal is not a factor that limits the development
of epidemics.

Researchers at Long Ashton do take dispersal into account in the forecasts
they are developing for Septoria diseases of wheat. Those diseases do most
damage when they infect the topmost leaves or the growing ear. Whether they
reach those tissues depends on rain splashes carrying spores from the lower
leaves up to the top of the crop. By placing dishes of fluorescent dye on
the ground and seeing where the dye appeared later on paper targets, Michael
Shaw tracked the movement of splashes. In general, with every 3-centimetre
increase in height, the amount of dye halved. However, the average height
the dye attains varies widely. This means that in some summers, there may
be no risk from Septoria simply because rain does not move enough spores
on to the vulnerable leaves. The Long Ashton Splashmeter allows farmers
to compare the splashes on different rainy days. It may eventually be possible
to work out just how much splashing it takes before a farmer must spray
a crop with fungicide. If so, the instrument may be simple enough to use
in everyday farming.

Walklate approaches the question of vertical dispersal from a different
angle. He applies the theory of fluid mechanics to relate the maximum height
a splash droplet will reach to the momentum of the raindrops. The theoretical
models and the observations of natural rain agree that the key point is
not simply how much rain is falling. It depends instead on the proportion
of large drops. Clearly, if we are to forecast the spread of diseases to
the upper leaves of cereal crops in the spring, we must take into account
how often short, heavy showers that are rich in large raindrops fall at
sites where susceptible crops are growing.

The general physical principles governing the dispersal of spores by
wind and rain apply equally to other particles of a similar size. Theories
that describe the spread of plant diseases will also describe the movement
of the spores and pollen grains that cause allergic reactions in people
and animals, such as the fungi that cause farmer’s lung. The same principles
apply to the way spray drifts; farmers apply most of their pesticides and
herbicides as sprays and though many droplets reach their target, others
drift, perhaps killing harmless or beneficial organisms.

The unpredictable nature of airborne transport is one of the stumbling
blocks to releasing genetically engineered microorganisms outside the laboratory.
Biotechnologists are developing novel, biological alternatives to chemical
pesticides (see ‘Genes on the loose’, New ÐÓ°ÉÔ­´´, 26 May 1988). The aim
is to control disease in a way that will do less damage to the environment.
Field trials with ‘altered organisms’ are out of the question until we know
that the organisms are safe to let loose. But anyone trying to lay down
the conditions under which organisms can be released will need to know how
they will be dispersed. Aerobiology’s role in assessing the risks will be
every bit as crucial as it is in the control of plant diseases.

* * *

THE POTENTIAL IN A SPLASH OF RAIN

THE Long Ashton Splashmeter is a crude but effective device for comparing
how far splashes from different rainstorms can move spores upwards through
a crop. Small cups on the wooden ring on the ground contain a fluorescent
dye that reacts chemically with cellulose. The plastic cylinder at the centre
holds high-quality filter paper. When a raindrop hits the surface of the
dye in a cup some dye becomes mixed into the splash droplets. If a droplet
then hits the filter paper the dye binds permanently to the paper, leaving
an indelible record. The dye is viewed under ultraviolet light in the laboratory.

After applying a correction factor, it turns out that the amount of
dye moved to a given height usually declines exponentially as height increases.
But the average height to which the dye moves differs from occasion to occasion.

Bruce Fitt and Michael Shaw are researchers in the Crop and Environment
Protection Division of the AFRC Institute of Arable Crops Research based,
respectively, at Rothamsted Experimental Station and Long Ashton Research
Station.

Further reading The Microbiology of the Atmosphere by Philip Gregory,
Leonard Hill 1973. Plant Disease Epidemiology, edited by Kurt Leonard and
William Fry, Macmillan 1986.