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Ann. Rev. PhylOpalhoi. 1977. 15:165-83

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EPIDEMIOLOGICAL
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PRINCIPLES TO ACHIEVE
PLANT DISEASE CONTROLI

R. D. Berger
Department of Plant Pathology, University of Florida, Gainesville, Florida 3261 1

INTRODUCTION

Man's early attempts to control the epidemics that plagued his crops were based
largely on methods that evolved through experience, often with little awareness of
the principles governing his success. Our increasing knowledge of the host-patho­
gen-environment disease triangle has enabled us to apply certain principles to reduce
the losses from epidemic disease. The purpose of this chapter is to categorize many
of the epidemiological principles that have recently been put to conscious use in the
control of plant diseases. When possible, particular attention is directed to quantify­
ing the epidemiological response following the application of the technique.
Three epidemiological strategies can be applied to minimize losses due to disease:
(a) eliminate or reduct?the initial inoculum or delay its appearance, (b) slow the
rate of disease increase, and (c) shorten the time of exposure of the crop to the
pathogen. Hundreds of interesting, novel, simple, and complex practices that are
used to control diseases on the world's various crops fit comfortably into one or more
of these categories. The small number of these practices listed here has been chosen
because they pointedly illustrate a particular epidemiological principle.

CONTROL OF DISEASE BY REDUCTION

OF INITIAL INOCULUM

Attempts to reduce initial inoculum have long been of concern to agriculturists in

avoiding losses to epidemics. Most of these procedures come under the general term,

IFlorida Agricultural Experiment Station Journal Series Paper No. 201.

165
 166 BERGER

sanitation, which is generally aimed at decreasing the number of propagules of a

pathogen before a crop is planted. A good exposition on various aspects of sanitation
is given by Walker ( 100). Many variations on the general sanitation theme are
available, for example: (a) treatment of seed with hot water or chemicals to kill
seedborne pathogens is used to control black rot and Phoma diseases of cabbage;
(b) seed indexing and certification are used in California and Florida to control
lettuce mosaic virus; (c) citrus budwood registration; (d) potato seed certification;
(e) crop rotation is used to control peanut leaf spot; (j) elimination of alternate hosts
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frequently is used to control rust diseases; (g) deep plowing of crop refuse is used
to minimize losses to Septoria on wheat; (h) shoot meristem culture (2) is used to
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eliminate viruses; (i) heat therapy is used to control sugarcane ratoon stunt; and
(j) chemical eradication of pathogen-overseasoning structures is used to control
peach brown rot and apple scab. The vertical resistance concept of Vanderplank (93,
95) has been described as a useful technique to reduce initial inoculum for those
host-pathogen combinations where it applies (21, 34).
Vanderplank (95) analyzed theoretical aspects of epidemics of wheat stem rust
following eradication of barberry. He also calculated the effect on epidemics of
potato late blight following sanitation of cull piles. Often, the barberry and Rhamnus
eradication programs in the United States greatly reduced local outbreaks of wheat
stem rust and oat crown rust, respectively. But the effectiveness of these programs
often was seriously negated by frequent and heavy dispersal of spores up the "Puc­
cinia Pathway" (2 1-23).
Despite the numerous examples where sanitation has been used to reduce initial
inoculum, only a little quantitative information is available on the effectiveness of
sanitation for diseases of the "compound interest" type (95). Sumner & Littrell (91)
showed how epidemics of Helminthosporium maydis on corn were delayed by
several sanitation practices. Kucharek (55) reported several situations where crop
rotation substantially reduced cercospora leafspot on peanuts; however, his conclu­
sions were based on a single disease estimate in mid-season. In another example,
Berger (IS) showed that the progress of an epidemic of Cercospora apii in celery
fields largely depended on the incidence of disease on celery transplants. The effect
of sanitation on soilborne diseases [the "simple interest" diseases of Vanderplank
(95)] has received more attention. Baker and co-workers [references given in (6)]
studied the relation of amount of initial inoculum to subsequent development of
Rhizoctonia damping-off. Wiese & Ravenscroft (104) showed that Cephalosporium
developed less rapidly on wheat when various sanitation practices diminished the
number of surviving fungal propagules.

Sanitation Theory
There is no evidence to show that the rate of epidemic disease progress following
sanitation is the same or different from the rate in comparable crops without
sanitation. Disease progress conceivably could be faster following partial sanitation
if the number of susceptible plants, or the amount of susceptible leaf area, is a
limiting factor in the rate of infection in plots without sanitation. In such cases, the
beneficial effect of the sanitation practice could be rapidly diminished over time.
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 167

Obviously, it would be valuable to combine sanitation with practices which decrease

the rate of infection. This combination of procedures has been used successfully to
control early blight of celery (15).
Vanderplank's r (95), the average apparent rate of infection, can be used to
determine the intensity of a given sanitation practice that must be used to limit final
disease below some particular amount. The infection rate (r) is the slope of the linear
regression line determined by plotting loge [x/(l-x)] against time, where (x) is
the proportion of the crop area that is diseased. The equation loge [xo/(l-xo)] =
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loge [xt/(l-xt)] - (r . t) (Formula I) is used where Xo is the amount of disease

allowed after sanitation to achieve no more than a certain maximum allowable
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amount of disease (xt) after time (t), assuming an average infection rate (r). For
example, in a crop with a growing season of 80 days and a disease known to have
an r that usually is less than 0. 1 per unit per day, Xo should not exceed 2 X 10-5
if Xt must be kept below 0.05. For (substitution in Formula I):
loge [xo/(l-xo)] = loge (0.05/0.95) - (0. 1 ·80)
= (-2.94) - (8.) = -10.94
and calculation of (xo) gives Xo = 2 X 10-5•
To place this in more realistic terms, if a south Florida celery grower desires no
more than Xt = 0.05 early blight at harvest, he should start the season with fewer
than one Cercospora apii lesion per 1000 celery transplants.
A cautionary statement must quickly be entered here. The calculations above
were based on Vanderplank's notion that epidemics follow a straight logit-line
development (95, 96). Since many epidemics have been shown to have unusually
high (nonlinear) infection rates in initial stages (I, 7, 10, 12, 48-51), the effect of
sanitation may be quickly negated during the early stages of the epidemic. In such
cases it may be necessary to reduce the initial inoculum 100l00-fold more than
required in the calculation of straight logit-line development. That would mean no
more than one lesion per 10,000 to 100,000 transplants using the example calculated
above.
The sanitation principle can be stated in a general manner: The sanitation practice
should reduce the initial inoculum to a sufficiently low level that the normal develop­
ment of disease would not reach a high enough level in the time to harvest to cause
appreciable yield loss (provided unusual influx was avoided).

CONTROL OF DISEASE BY SLOWING THE RATE

OF INFECTION

Most disease control programs are based on techniques to slow the apparent infec­
tion rate of the developing epidemic. Many common control practices, such as
application of pesticides, use of resistant varieties, rouging, etc, fit this category.
Again, innumerable examples are available in the literature, but most fail to quantify
the change in epidemic progress through the utilization of the procedure. I divide
control methods that slow the infection rate into several categories, each of which
is treated separately.
 168 BERGER

Effect 0/ Disease Removals on Disease Development

Sanitation practices performed during the development of an epidemic serve not to
reduce initial inoculum, but act as a disease removal mechanism to generally reduce
the substrate on which the pathogen can reproduce. This practice decreases the total
reservoir of secondary inoculum and decreases the rate of infection. Rouging of
infected plants frequently has been used to reduce losses from ins�t-transmitted
diseases.
An outstanding example of the use of sanitation to decrease the rate of infection
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during an epidemic is the data of Miller, Silverborg & Campana (65) for Dutch elm
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disease in the city of Syracuse, New York; these data were kindly brought to my
attention by W. Merrill. I have adjusted their data to a 100% base of 53,618 trees
and used a logit transformation to express their results another way (Figure 1). The
sanitation measure, which consisted of removing diseased elm trees, was performed
during the seven-year period 1957-1964. Sanitation allowed the disease to progress
at the rate of r = 0.012 per unit per month. Discontinuance of sanitation measures
in 1964 led to an immediate threefold increase in the rate of disease development
(an average apparent infection rate of r = 0.039 per unit per month). The slow
progress of the disease during the sanitation was likely from escapes, trees with
latent infections that later showed symptoms, and influx of inoculum.

-I

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x

__ OBSERVED

........ PROJECTED

9
-
19h5=3�--��--��----��----��----��--��----��----�'69

Figure J Removal of infected trees (sanitation) slowed the rate of spread of Dutch elm
disease. Average apparent infection rates (r) calculated as per unit per month (95). [Data
adapted from Miller et al (65).] See text for explanation.
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 169

If we assume that the original epidemic without sanitation would have progressed
at the same rate as that observed after sanitation ceased (r approximately 0.04
=

per unit per month), then 50% mortality [x = 0.5; loge (x/(1-x)] = 0) would
have been expected by 1963. The seven-year sanitation program delayed the 50%
mortality date five years (1968). If sanitation would have been continued without
interruption, the 50% mortality date would have been reached about 1978 (assum­
ing r 0.012).
=

Van Sickle & Sterner (97) also showed that sanitation resulted in a two- to three­
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fold decrease in the infection rate of Dutch elm disease in New Brunswick, Canada.
A portion of their data (kindly provided by the authors) was transformed by logits
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and is presented in Figure 2.

A similar slowing of disease progress with sanitation was observed in the lethal
yellowing disease of coconut palms in Florida (84). Unfortunately, the program to
remove diseased palms was not carried out as stringently as the Dutch elm disease
sanitation program. It was conducted somewhat intermittently, thereby masking
much of the suppressive effect.
Sanitation performed during an epidemic also can be an effective control measure
against leaf spotting organisms. For example, covering a portion of Helmintho­
sporium turcicum infected corn leaves with soil during the final cultivation (lay-by)
-

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-7

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Figure 2 Sanitation slowed the rate of spread of Dutch elm disease. Infected elm trees
removed only in the Fredericton site. Average apparent infection rates (r) calculated as per
unit per month. [Data provided by Van Sickle & Sterner (97).]
 170 BERGER

delayed an epidemic by 5-7 days ( 16). Generally, the earliest infections occurred on
the lower leaves and the lay-by cultivation acted in this case as a disease removal
mechanism.

Reduction in Inoculum Transport and Inoculum Arrival

Restrictions on inoculum transport and arrival by physical or natural means can
also affect epidemic development. If these restrictive measures are applied prior to
the occurrence of disease in the field, they would be considered a sanitation proce­
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dure. When the same restrictive measures are used to reduce continuing or intermit­
tent influx of inoculum in a developing epidemic, they reduce the infection rate. Few
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actual examples have appeared in the literature. Nevertheless, this approach re­
mains a fundamental practice in the control of several diseases. For example, the
generally recommended procedure for transplanted crops is to locate seedbeds at
some distance from field plantings to reduce the chance of inoculum influx into the
seedbeds. The use of barrier crops and the interplanting of unrelated host types are
aimed at reducing arriving inoculum. Sequential plantings of a crop in monoculture
increases its vulnerability to disease because inoculum from older plantings fre­
quently threatens the most recent plantings. Some of these control techniques have
found special favor as attempts to reduce movement of vectors for viral diseases (oil
sprays, repellents, aluminum foil, etc). Caution is suggested in the use of wind
barriers, because these sometimes alter the microclimate and may result in increased
disease (33). Fumigation to halt the lateral spread of Dutch elm disease through root
grafts can also be included here. Reducing inoculum transport within a crop fre­
quently is used as a control measure. Avoiding the movement of personnel or'
equipment through fields, particularly when foliage is wet with rain or dew, reduces
the spread of many pathogens. Mechanical topping of plants to restrict the size of
transplants is practiced in the general culture of some crops. If disease is already
present in the plant beds, this topping practice should be avoided because it often
results in extensive disease outbreaks from the massive disperal of inoculum.

Interruption of Pathogen LIfe Cycles

Intentional interruption or alteration of a pathogen life or disease cycle is another
means of disease control which works to decrease the rate of infection. Browning
(21) suggests that the eradication programs for barberry and buckthorn force Puc­
cinia graminis and P. coronata to cycle in the uredial stage. In effect this breaks the
life cycle of this pathogen. Royle (79) reports that such an interruption of the disease
cycle evidently provided control for powdery mildew in hop orchards in the United
Kingdom where mechanical cultivation prevented the maturation of c1eistothecia.
Upon the advent of chemical herbicides, the discontinuance of soil disturbance
around the plants allowed the fungus (Sphaerotheca humuli) to complete its life
cycle and become a serious problem.

Chemical Techniques for Slowing the Progress of an Epidemic

Disease increase is slowed by the application of efficacious chemicals. Critical analy­
sis of disease development using fungicides likely began with the work of Barratt
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 171

(3) and later followed by Large (60). Vanderplank (94) has given a more recent
analysis. In time and complexity, chemical techniques range from the early topical
applications of bordeaux mixture in vineyards to the recen. advances of injection
of systemic fungicides and antibiotics.
The art and science of timing fungicide applications to achieve the maximum
control effect has received considerable attention over the years (13, 15-17, 43, 46,
52, 71, 81, 88, 89). The techniques of accurately evaluating fungicide effectiveness
deserve mention (40--42, 95). James et al (40, 42) and Vanderplank (95) provide
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helpful techniques to determine adequate plot size, to reduce and determine the
amount of interplot interference, and to avoid representational errors. James (41)
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has also provided guidelines for disease assessment. The following are some general
epidemiological criticisms of most published fungicide tests: the disease estimates
are frequently begun too late in the epidemic (date of onset and features of early
epidemic stages are missed); disease estimates are made at too great an interval (the
erratic advance of disease cannot then be correlated to weather); many estimates are
not accurate enough for epidemiological studies (see 45, 90); the latent period of the
pathogen is often disregarded in interpretation; and host growth is often neglected.

SIMULATION OF FUNGICIDE APPLICATION The effect of a fungicide on disease

progress has been simulated by Zadoks (105). The response of an epidemic of a
leaf-spotting pathogen to application of a fungicide differs from the theoretical curve
proposed by Zadoks because enlargement of lesion size, the appearance of delayed
latent infections, and escapes cause substantial increase in amount of disease after
the effect of the control measure begins (Figure 3). Also, actual disease progress
following the loss of fungicidal effectiveness appears to be much faster than depicted
by Zadoks' simulation and the parallel delay in time proposed by Vanderplank (95)
(curve B, Figure 3). A more realistic curve describing the effect of a fungicide is
shown in curve C, Figure 3. The rapid advance of disease following loss of fungicidal
effectiveness usually exceeds the infection rate in comparable plots that are not
sprayed. Over time, this rapid advance of disease greatly reduces the beneficial effect
of the control treatment. When several epidemics in sprayed and unsprayed fields
were compared, disease severity was less in sprayed fields during the period that
fungicidal protection was provided. However, when spray applications ceased, dis­
ease sometimes reached greater severity in the previously sprayed areas than in the
unsprayed areas because of the rapid disease progress following the loss of fungicidal
effectiveness (10; Berger, unpublished). This is depicted in curve D, Figure 3.
The foregoing observations incidate that once spraying for disease control has
begun, the crop should continue to be sprayed, that is, until such time as any rapid
disease progress would no longer significantly affect yield or quality or until there
is reason to believe the disease may be considerably slowed by environment. The
calculation of the area under the disease progress curve for these conditions may
provide a better correlation of disease effect upon yield than would the final disease
percentage (41, 43, 44, 82).
Fungicide sprays applied early in the epidemic when the number of arriving
spores is relatively small may be more effective than sprays applied later. For many
 172 BERGER

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Annu. Rev. Phytopathol. 1977.15:165-181. Downloaded from www.annualreviews.org

:;;:
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Figure 3 Progress of a leaf-spotting disease following a fungicide application. A Unsprayed.

B Theoretical, adapted from Zadoks (105). C Observed response in actual epidemics. CER­
COS simulations gave similar curves (see Figure 4). D Disease severity of sprayed treatment
sometimes surpasses unsprayed. The delay in time from spray application (arrow) to initial
response is one incubation period.

diseases, as the incidence approaches x = 0.05, all vulnerable host tissue is essen­
tially showered with spores so that the slightest break in fungicidal coverage subjects
the tissue to possible infection. The expansion of the numerous existing lesions and
the accompanying physiological deterioration of affected tissues at x > 0.05 com­
monly mask any positive fungicidal effect. It is at this point in the epidemic that most
growers (and many pathologists!) frequently fail to consider the incubation period
of the fungus. A person must wait at least one incubation period to observe any
slowing of the rate of disease increase brought about by an effective fungicide
application.
The epidemic simulator CERCOS (8) aptly depicted the differential disease control
achieved with a fungicide when the fungicidal effect was initiated in various stages
of an epidemic (Figure 4). With environmental conditions held constant and favor­
able for disease development, a simulated spray applied when the observed disease
was very low (x = 0.0003) slowed the epidemic for about seven days. A similar
spray applied when more disease was observed (x = 0.03) slowed the epidemic by
only about three days. The rapid disease progress following loss of fungicide effec­
tiveness was also clearly simulated.
Some systemic fungicides, e.g. benomyl, in addition to preventing spore germina­
tion, penetration, and infection, provide some theraputic effects on existing latent
infections. In CERCOS-simulated epidemics during constant disease-favorable envi­
ronment, 99.5% cure of latent infections which occurred in the previous 6 days (of
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 173

4 -.------,

e-e NONE
c--C SPRAY-DAY 10
2- 1:.-6 SPRAY-DAY 35

0-
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.::::.
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DAYS

Figure 4 CERCOS sim ulation offungicide application. Environment held constant at 25°C
day,17°C night, 12 hr leaf wetness per night and no rain. A single simulated spray was applied
when observed disease was x = 0.0003 (day 10) or x = 0.03 (day 35).

a total latent period of 12 days) slowed disease development only slightly. Under
actual field situations a real benefit for the curative effect of a fungicide occurs when
the timing of a protective spray may have been delayed on a day of high disease
hazard.

Slowing the Progress of an Epidemic by Host Resistance

The use of horizontally resistant varieties (93, 95) to slow epidemic progress has long
been a favorite technique with pathologists and plant breeders. It is perhaps the
simplest, and often the most effective means of control available for many diseases.
Numerous examples can be found in the literature (20, 93, 95), and entire books and
lengthy reviews have been written on host resistance (34, 67, 74, 93). The multiline
approach using several genetically similar host lines (isolines) was covered in a
recent review (21).
The various mechanisms of host resistance affect different stages of the pathogen,
or disease cycle. The end result of using horizontal resistance in an epidemic is
 174 BERGER

slower disease development on the resistant varieties. There are several ways to
characterize the specific actions of disease resistance. In epidemiological modeling,
host resistance is commonly handled in the following ways: (0) reduction in the total
number of infections; (b) reduction in the rate of lesion expansion; (c) reduction of
pathogen fructification; (d) lengthening of latent or incubation period; (e) reduction
of spore deposition; if) shortening of infectious period; and (g) increase in number
of propagules necessary to establish infection. Each of these effects is examined in
some detail.
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REDUCTION OF TOTAL NUMBER OF INFECTIONS Most successful cases of

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plant resistance are likely to result from fewer infections on the resistant variety
compared to a more susceptible variety under the same conditions. The resistance
ranges from complete immunity (including nonhost) to barely perceptible tolerance.
This type of resistance is frequently altered by climate, host nutrition, and other
predisposing factors. Vanderplank (95) gives numerous examples; see also (14, 18,
22, 23, 30, 34, 57, 58, 61, 62, 69).

REDUCTION OF LESION EXPANSION Reduction in lesion expansion includes

the appearance of only small lesions on resistant plants as well as slowing of lesion
growth over time. The small lesion reaction types in corn as a result of infection by
He/minthosporium spp. (38) are good examples of this class.

REDUCTION OF SPORULATION Some plant resistance is expressed as a reduc­

tion in sporulation by the pathogen despite a lesion size similar to that observed in
susceptible individuals (61, 62). In those cases where host resistance limits lesion
size, fewer spores are formed per lesion on the resistant types compared to the
susceptible types simply because the total lesion surface available for sporulation is
reduced. Reduction of pathogen reproduction in resistant varieties has also been
observed in a bacterial incited disease (4).

LENGTHENING OF LATENT PERIOD Host resistance that operates by increasing

the latency or incubation time of the pathogen has received only scant attention but
this is one of the most effective types of resistance to decrease the infection rate.
When the latent period of the pathogen is extended, the pathogen can complete
fewer cycles of reproduction in a single crop season. This results in less disease at
harvest. Resistance that extends the latent period has been reported for cereal rust
(27) and bacterial soft rot (5).

REDUCTION OF SPORE DEPOSITION There are few reports in the literature

whereby host surface characteristics affect disease progress. Leaf position, orienta­
tion, or size could significantly affect light penetration into the crop canopy and alter
leaf microclimate. These factors also could have a direct effect on the phenomenon
of spore deposition or catch. Leaf surface characteristics (smooth or setiose, waxy
or rough, etc) also could have an effect on catch. The plant would show outward
resistance (reduced disease incidence) simply because of the reduced catch capabili­
ties.
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 175

SHORTENING OF INFECTIOUS PERIOD A shortening of the time that infectious

propagules are produced on diseased host tissue (sporulation) also would slow the
progress of an epidemic because of the reduction in the total number of infectious
units over time. A good example of this type of host resistance is the reduced "zone
of sporing" described by Lapwood (57, 58) for Phytophthora infestans on potato.

HIGH INFECTION THRESHOLD In some resistant varieties of plants a minimum

concentration of pathogen propaguJes appears to be necessary for infection. In such
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cases, the infection rate would be slower on varieties that become infected only at
high spore loads. This type of resistance apparently is partly responsible for "late
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rusting" (by Puccinia coronata) in oats (63). The concentration of arriving spores
determines the disease incidence. Plants with this type of resistance normally would
have little or no disease even though neighboring susceptible plants could be consid­
erably blighted. This type of resistance may break down under the pressure of a large
influx of inoculum from nearby susceptible individuals. Whether the resistance
brought about from a high infection threshold differs from the resistance of reduced
number of infections discussed above remains to be determined.

SIMULATION OF RESISTANCE Natural host resistance of the horizontal type

could involve one or more mechanisms of the resistance described above. If several
types of resistance were present in a given variety, the resistance would be additive
since the several resistance mechanisms would individually contribute to decreasing
the infection rate. The epidemic simulator CERCOS (8) was used to illustrate
graphically the effects of several resistance types (Figure 5). When catch, spore
production, lesion size, or percentage of successful infections was reduced by 50%,
the infection rate in initial epidemic stages was reduced by about 25%. When two
types of resistance were used simultaneously in the model, the infection rate was
reduced 50% over the susceptible. The most beneficial individual effect (67% reduc­
tion of rate) came from lengthening the latent period (20 days vs 10 days). It was
interesting that all types of resistance failed to decrease the infection rate as the
epidemic progressed beyond x = 0.01. The failure of resistance to decrease the
infection rate when disease incidence was x > 0.01 has been observed in a natural
epidemic (14).

Inhibiting the Progress of Disease by Management of the Environment

Although man can do little to alter the climate in which he lives, several agricultural
practices have been used to alter the microclimate of a crop and coincidentally
influence the development of epidemic disease.
Hallaire et al (36) treat the influence of irrigation and measurement of the micro­
climate in excellent detail. Rotem & Palti (77) reviewed the effects of irrigation on
the increase of disease. Recently, overhead-sprinkler irrigation has been shown to
increase fire blight of apples (87). Leaf or soil moisture does not always increase the
amount of disease. Lapwood and co-workers (56, 59) have shown that irrigation can
reduce common scab of potatoes.
 176 BERGER

4 .-----�
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(RES F a LESIZE)x.s
2- <>-<> LATENT PO x 2

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"-
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Figure 5 CERCOS simulation of resistance mechanisms under the same constant environ­
mental conditions as in Figure 4. NONE = no resistance. RESP = resistance function
determining percentage of successful infections. CATCH = number of spores present on
leaves. SPORES = sporulation parameter. LESIZE = lesion size. LATENT period was 10
days for n o resistance. Numbers i n parentheses are average apparent infection rates for
indicated slope and intervaL See text for explanation.

When overhead-sprinkler systems of irrigation are changed over to trickle or drip

systems, it would be interesting to see what changes this makes in the incidence and
prevalence of pathogens that require a lengthy wet period or are dispersed by
splashing water.
One of the easiest ways to decrease losses during an epidemic is to sow or plant
a crop at a time of year that is less favorable for disease. This technique also could
affect disease development in ways already discussed above. Several examples of this
technique have appeared in the literature (73, 100).
In many crops, mechanization has resulted in the standardization of plant and
row spacing. Plant spacing has sometimes influenced the rate of spread of epidemics.
Diseases generally spread faster among plants at closer spacings (9, 24).
Row orientation (compass direction) is frequently overlooked in management
systems. Haas & Bolwyn (35) showed that rows of bean plants running north-south
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 177

in southern Ontario, Canada had more disease (Sclerotinia) than in rows planted
in an east-west (E-W) direction. The prevailing winds were mostly westerly provid­
ing more rapid drying conditions in E-W rows. They also claimed that sunlight
penetrated deeper into the canopy of E-W rows. The orientation of rows also
influences inoculum dispersal patterns, particularly in sequentially planted crops.
Disease is usually maximal when crops are harvested. This disturbance can result
in tremendous influx of inoculum to younger crops downwind if fields are oriented
in this manner. Higher infection rates would result from a repeated influx of inocu­
by Moscow State University - Scientific Library of Lomonosov on 11/04/13. For personal use only.

lum. Berger (15) recommended that sequential plantings be made in a direction

opposite to prevailing winds so as to reduce losses caused by an influx of inoculum
Annu. Rev. Phytopathol. 1977.15:165-181. Downloaded from www.annualreviews.org

originating from harvesting operations.

The judicious management of greenhouse temperature and ventilation to control
relative humidity has long been a standard recommendation for control of tomato
leaf mold (Cladosporium) and similar foliage pathogens (100).

The Application of Epidemiological Principles in Disease Forecasting

A thorough understanding of the epidemiological principles as they affect specific
diseases aids the pathologist in developing more accurate disease monitoring and
forecasting systems.
Most early disease forecasting techniques involved the correlation of specific
environmental conditions with disease occurrence (15, 47, 68, 76, 80, 102). Usually,
favorable weather critically influenced one or more stages of the pathogen life cycle.
In actuality, the forecast predicts the time of likely onset or rapid increase of disease.
Sometimes forecasts identify periods when pathogens are relatively inactive. It is not
the purpose here to review all disease forecasting literature, as previous reviews (19,
53, 66, 98, 99) more than suffice. However, an update on some recent forecasting
techniques is warranted.

COMPUTER AIDS The use of computers in disease forecasting will likely increase
because of the computer's record-keeping capabilities, mathematical accuracy, and
the speed of response necessary to make the forecasting method current and reliable.
Voluminous amounts of pertinent weather and biological data can be processed
rapidly to achieve regional or local forecasts (37, 85). Plant growth, disease, and
insect simulation models rely almost entirely on computers in the handling of data.
Computers are also used in information delivery systems to make quicker and more
accurate disease management decisions (31).
The potato late blight forecasting systems of Hyre (39) and Wallin (101) found
only limited acceptance among northern US potato growers until the computer­
ized version (Blitecast) (54) was developed. A similar computerized disease fore­
casting and grower advisory system is available for cercospora leafspot on peanuts
(70).

PATHOGEN MONITORING Monitoring of pathogen activity (generally airborne

fungal spores) can provide additional information and increase the forecasting
accuracy, particularly where release of spores is triggered by specific environmental
 178 BERGER

conditions or physical disturbance of the crop (15, 28, 32, 72, 78, 83, 92, 102).
Cournoyer (29) and Roelfs et al (75) followed entire epidemics of Puccinia spp.
utilizing spore monitoring. Propagules of soil pathogens have been monitored to
determine potential disease occurrence (86, 103, 104).

REGRESSION ANALYSIS Multiple regression analysis has been used to define as

many as eleven or more independent biological and climatological variables to
describe the progress of an epidemic (25, 26). The analyses are used to predict future
disease intensity and possible crop loss. James et al (44) also used regression analysis
by Moscow State University - Scientific Library of Lomonosov on 11/04/13. For personal use only.

to predict losses of potato tubers to late blight.

Annu. Rev. Phytopathol. 1977.15:165-181. Downloaded from www.annualreviews.org

INFECTION RATE IN DISEASE PREDICTION When the infection rate of a patho­

gen exhibits little variability each year, then the rate can be used to predict future
epidemic development and spray timing schedules after initial disease occurrence.
Infection rate patterns for Helminthosporium turcicum in com sprayed with fungi­
cide were quite similar over several seasons (Figure 6) (12). A satisfactory disease
forecast and corrective spray schedule was developed using this information (13).
A similar approach was used to determine confidence limits for infection rates of
Uromycesphaseoli in snap beans and allowed the prediction of the amount of disease
at harvest (11). For fusiform rust (Cronartiumfusiforme) in Florida, future disease
in pine can be predicted based largely on prevalence of the alternate host (oak) (R.
A. Schmidt, personal communication).

HELMINTHOSPORIUM TURCICUM

...... 1970

-2
...... 1972
_1973

-4

X-
-6
I

�
x

�
OIl
.3 -8

-10
5 15 25 30 5 15 25
APRIL MAY

Figure 6 Epidemic progress of Helminthosporium turcicum on maneb-sprayed sweet corn

(Iobelle) for three seasons at Belle Glade, Florida. The consistent pattern of disease develop­
ment from year to year permits a prediction of disease severity at harvest so that corrective
action can be taken.
 EPIDEMIOLOGICAL PRINCIPLES FOR CONTROL 179

HOST PHENOLOGY Infection by a pathogen depends on the availability of sus­

ceptible host tissues. Therefore, control measures can be scheduled to coincide with
specific host phenological events. The seasonal development of apple bud and leaf
tissue has long been used to time fungicidal sprays opportunely to control scab
(Venturia inaequa/is). As another example, Merrill & Kistler (64) reported success­
ful control of Endocronartium harknessii on pine with fungicide sprays timed to
correspond with the emergence of needles from the bud sheath. In some row crops,
good protection against leaf-spotting fungi can be achieved by applying fungicide
by Moscow State University - Scientific Library of Lomonosov on 11/04/13. For personal use only.

sprays during the period of rapid increase in leaf area (16).

Annu. Rev. Phytopathol. 1977.15:165-181. Downloaded from www.annualreviews.org

CONTROL OF DISEASE BY SHORTENING TIME

OF EXPOSURE

Time is the third factor that enters into all equations describing growth (initial
amount and rate being the other two). Commercial growers and plant pathologists
seldom consider altering time of exposure as a possible control for disease but,
nevertheless, this can be a most effective measure.
Any practice that shortens the time of exposure of a crop to a pathogen will
decrease the risk of loss due to an epidemic. In a transplanted crop, the setting of
large, vigorous plants with a well-developed root system would insure quick estab­
lishment of the crop and shorten the time to maturity. Use of short season varieties
and maintenance of adequate soil fertility and moisture to avoid any slowdown of
crop growth are the most common techniques to shorten the exposure of crops to
pathogens. In the event an epidemic occurred, the pathogen would have less time
before the disease could reach an economic loss level. To paraphrase one of "Mur­
phy's laws," "the longer a crop remains in the field, the more likely something bad
will happen to it."

CONCLUDING REMARKS

The condensation of the voluminous literature that was available to treat this
chapter's theme was not an easy task. I was especially pleased to have had the
cooperative response from the numerous pathologists who answered my requests for
information. I am certain many individuals can think of additional important con­
trol techniques that I omitted or overlooked. Some may question my choice of
examples for the principles I categorized, particularly if their favorite disease was
neglected. The actual quantification of the epidemiological response to new, or even
long-standing, control practices is frequently neglected. Much work lies ahead. It
was my intention to treat several principles controversially so as to stimulate more
critical analysis in future experimentation. It would not be at all surprising if several
well-established theories on spread of epidemics were eventually set aside as our
knowledge of modern epidemiology increases. New modeling techniques and com­
puter simulation should simplify the assessment of specific epidemiologic events.
These techniques also can aid in determining the underlying biological and ecologi­
cal basis for naturally occurring disease phenomena.
 180 BERGER
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