L. Geagea et al. Agricultural and Forest Meteorology 101 2000 53–66 57
tape on each arm was cut into four sections, removed and mounted on microscope slides McCartney and
Lacey, 1990. Spores were counted in five horizon- tal traverses of each slide at a magnification of 200.
The spore samplers were placed 2 m downwind of the source plants and 50 cm from the floor of the wind
tunnel, at about the same height as the infected plants. As the fall speeds of the brown rust spores were likely
to have been in the order of 1 cm s
− 1
Gregory, 1973, the vertical line of the spore plume at the spore trap
would only have varied by about 3–4 cm over the wind speeds used. The spore traps sampled air from a vol-
ume several times the diameter of the arms. Therefore, it was unlikely that variations in the position of the
spore plume, caused by different wind speeds, would have affected the proportion of the plume sampled by
the spore trap.
2.2.2. Combined effect of rain and wind An experiment was done to measure the effect of
wind alone in removing spores from infected leaves. Infected plants were placed at the base of the wind
tunnel and exposed to successive 5 min periods wind of different speeds 0.5, 1, 2, 2.5, 3, 4 and 5 m s
− 1
. The rotating-arm traps were changed after each 5 min
period. The experiment was repeated three times with different source plants each time.
In a second experiment, source plants were exposed for 20 min to simulated rain of drop size 4.9 mm and
a constant wind of either 1 or 4 m s
− 1
. During the tests, the rotating-arm traps were changed every 5 min.
The change in concentration with time reflected the changes in spore removal rate from the source. The
tests were replicated three times at each wind speed Table 1.
2.3. Kinetic energy of simulated rain drops The relationship between fall speed of drops and
vertical travel from rest given by Huber et al. 1998 suggests that the water drops in these experiments
would have reached close to their terminal velocities before impact. The terminal velocity of a water drop
was calculated from V =386.6 D
0.67
m s
− 1
, where D is the drop diameter in m; Ulbrich, 1983, and the ki-
netic energy E
K
D =12ρπ D
3
6 V
2
J, where ρ is the drop density in kg m
− 3
of the drop is given by: E
K
D = 391 × 10
5
D
4.34
2 Eq. 2 gives E
K
in J when D is measured in m. This equation was used to investigate the relationship be-
tween rain drop kinetic energy and the potential for splash dispersal of the two pathogens.
3. Results
Disease symptoms developed on trap plants in all the experiments, showing that spores of P. recondita
f. sp. tritici and P. striiformis were dispersed from infected wheat seedlings by simulated rain alone.
3.1. Dispersal gradients Because of the time required to assess symptom
development, a preliminary experiment was done to assess the variability between individual tests. Sets
of source plants were exposed to 10 min of simu- lated rainfall and the dispersal gradients were mea-
sured. Three drop diameters, 3.4, 4.2 or 4.9 mm, were used and each test was replicated three times Fig. 2.
Slopes and intercepts of the linear regressions b in Eq. 1 for each drop size test were compared using
an analysis of position and parallelism Payne et al., 1993, and the coefficients of determination r
2
and the coefficient of variation cv were determined.
Spatial patterns of dispersal were analysed, assum- ing a uniform infection efficiency for each fungal
type. Under controlled conditions at optimal tem- perature, the infection efficiency of brown rust had
previously been shown to be 12 times greater than that of semi-systemic yellow rust, and variability
in infection between plants was less than 5 de Vallavieille-Pope et al., 1995. The patterns of spore
dispersal were fitted well by Eq. 1 for both P. recondita f. sp. tritici and P. striiformis Table 2.
However, for the large drops the half-distance, α, of deposition gradients tended to be greater for brown
rust than for yellow rust. For example, after 10 min of rain, half-distances for 4.2 and 4.9 mm drops were
23 and 34 cm, respectively, for brown rust and 12 and 14 cm for yellow rust. The gradients for the 2.5
and 3.4 mm drops were slightly shallower for yellow rust half-distances 12 and 19 cm than for brown
rust 17 and 13 cm. However, densities of the brown
58 L. Geagea et al. Agricultural and Forest Meteorology 101 2000 53–66
Fig. 2. Numbers of brown rust lesions or yellow rust chloroses recorded on trap wheat plants at different distances from infected
source plants exposed to simulated rain for 10 min. Incident drop diameters used were 2.5, 3.4, 4.2 or 4.9 mm. Means and standard
errors of four replicates are presented see Section 3.
Table 2 Different regression parameters and half-distances obtained after
fitting the linear form of the exponential model Eq. 1 to the data of the Fig. 2
Rust Drop diameter a
a
b
a
m
− 1
Half-distance m r
2b
Brown 2.5 13.7 4.0
0.17 0.65
3.4 36.6 5.2
0.13 0.92
4.2 49.4 2.9
0.23 0.91
4.9 55.1 2.0
0.34 0.96
Yellow 2.5 7.8 5.5
0.12 0.91
3.4 14.4 3.6
0.19 0.93
4.2 44.7 5.7
0.12 0.93
4.9 75.9 6.7
0.10 0.95
a
a and b are the intercept and slope parameters of the linear regression.
b
r
2
is the coefficient of determination.
rust lesions or yellow rust chloroses for the smaller drops were relatively small, especially for the yellow
rust, making the gradients more uncertain Fig. 2. In general, few lesions or chloroses cm
− 2
were found by distance 84 cm from the source. The number of
brown rust lesions or yellow rust chloroses at a given distance from the source depended on both the rain
duration and the drop diameter. For a given drop diameter and for both pathogens, spore dispersal in-
creased with increasing rain duration. For example, for a drop diameter of 2.5 mm, after 5 min of rain,
brown rust lesions were recorded on plants up to 49 cm from the source, whereas after 15 min, they
were found on plants up to 63 cm from the source. The increase in distance that the spores travelled was
due mainly to dispersal of more spores. For a drop diameter of 4.9 mm, lesions were recorded on plants
at distance 84 cm after 5, 10 or 15 min of rain.
3.2. Effect of rain duration on disease severity The overall effect of rain on the dispersal of spores
was estimated by summing the total number of brown rust lesions or yellow rust chloroses lesions or
chloroses being verified as rust by sporulation which developed on the trap plants at different distances
after exposure to rain of different durations. The total number of brown rust lesions or yellow rust chloroses
was greater after 10 min than after 5 min of rain for all drop diameters. For 2.5 mm drops, the number
of yellow rust chloroses increased with increasing rain duration over the 15 min period. For the largest
drops, for both pathogens, the number was less after 15 min than after 10 min of rain Table 3. In these
experiments, the trap plants located at 14 cm were wet after exposure to 15 min of rain suggesting that
some of the deposited spores were washed off these plants to explain why fewer lesions developed after
15 min exposure, when a larger number of spores was presumably deposited. The exhaustion of the source
of spores would have resulted only in the number of lesions reaching a constant value as rain duration
increased see further. For both rusts, the total num- ber of lesions or chloroses increased with increasing
drop diameter for a given rain duration; e.g. for a rain duration of 10 min, the total number of brown rust
lesions was 247 with a drop diameter of 4.9 mm and
L. Geagea et al. Agricultural and Forest Meteorology 101 2000 53–66 59
Table 3 Effect of increasing drop diameter and rain duration on total numbers of yellow rust and brown rust spores dispersed by simulated rain
as estimated by number of lesions and chloroses produced on trap plants at different distances
a
Fungus Rain duration
Diameter Total number lesionschloroses
r
2b
cv
c
SED
d
df
e
Brown rust 5 min
2.5 15
0.96 0.16
0.12 10
3.4 16
0.79 0.21
0.39 14
4.2 28
0.81 0.66
0.40 20
4.9 54
0.77 0.27
0.26 20
10 min 2.5
35 0.65
0.76 0.62
17 3.4
59 0.92
0.26 0.32
18 4.2
156 0.91
0.09 0.22
20 4.9
247 0.96
0.03 0.10
20 15 min
2.5 25
0.93 0.13
0.33 17
3.4 57
0.95 0.31
0.32 19
4.2 100
0.95 0.07
0.15 31
4.9 199
0.78 0.18
0.26 20
Yellow rust 5 min
2.5 3
0.89 0.24
0.28 11
3.4 6
0.87 0.37
0.18 8
4.2 15
0.85 0.78
0.14 16
4.9 41
0.76 0.26
0.17 19
10 min 2.5
11 0.92
0.22 0.25
12 3.4
37 0.93
0.24 0.22
20 4.2
32 0.93
0.34 0.36
20 4.9
81 0.95
0.24 0.3
18 15 min
2.5 22
0.72 0.16
0.27 15
3.4 31
0.81 0.25
0.16 20
4.2 36
0.71 0.31
0.21 17
4.9 52
0.81 0.13
0.15 9
a
Values of r
2
are from the regression of number of lesions or chloroses over the distance.
b
r
2
is the coefficient of determination.
c
cv is the coefficient of variation.
d
SED is the standard error.
e
df is the degree of freedom.
35 with a drop diameter of 2.5 mm. Generally, the number of brown rust lesions was greater than the
number of yellow rust chloroses; e.g. after 15 min of rain with drop diameter of 4.9 mm, the total number
of brown rust lesions was 200 compared to 52 yellow rust chloroses. This difference could be partially at-
tributed to differences in infection efficiency between the two rusts.
3.3. Effect of rain duration on source depletion Except for P. striiformis with 2.5 mm incident drops,
the total number of brown rust lesions or yellow rust chloroses was always greatest on plants exposed to an
initial 10 min period of rain, but decreased for plants exposed to subsequent 10 min periods of rain Fig. 3.
For P. striiformis with 2.5 mm incident drops, the num- ber of chloroses increased and then decreased with
sequential exposure periods. Between 83 to 98 of brown rust lesions or yellow rust chloroses which de-
veloped on all the trap plants used in each test were initiated during the first 20 min of rain. Few lesions
or chloroses were found on the trap plants exposed to 10 min after 30 min of rain and almost none were
recorded after 40 or 50 min, even with 2.5 mm diam- eter incident drops, suggesting that all spores on the
source plants had been removed.
3.4. Effect of interrupted rain on restoration of sporulation
For each rust, the three replicate sets of trap plants to only one 30 min period where brown rust lesions
and yellow rust chloroses were produced after the
60 L. Geagea et al. Agricultural and Forest Meteorology 101 2000 53–66
Fig. 3. Decrease in numbers of brown rust lesions or yellow rust chloroses produced on the trap plants with continuous exposure
of source plants to rain. The Y-axis shows disease symptom pro- duction on trap plants exposed to splashed inoculum for 10 min
periods. Trap plants were changed every 10 min. The number of lesions or chloroses is the sum of lesions or chloroses recorded
on plants at all distances. The diameters of incident drops used were 2.5, 3.4, 4.2 or 4.9 mm.
first 30 min of rain were used to estimate experimen- tal variability. The standard errors of the total number
of lesions or chloroses produced at all distances were equal to 3.73 and 0.26 for brown and yellow rusts, re-
spectively. These estimates were used to test the dif- ferences between the unreplicated treatments after the
period allowed for restoration of sporulation.
For the brown rust, the total number of lesions recorded on trap plants exposed to 30 min of inoculum
was roughly similar before and after an interruption in rain of 2 h, suggesting that a 2 h time interval be-
tween periods of rain was almost sufficient to restore the sporulation rate of the lesions Fig. 4. The number
of spores dispersed tended to increase with increasing length of the interruption period; after a 6 h interrup-
tion the disease severity on the trap plants was almost twice of that before the interruption in rain 90 com-
pared to 174 lesions. Although the post interruption tests were not replicated see Section 2, the likely
variability in measurements can be estimated from the variability of the three pre-interruption tests as de-
scribed earlier. The total number of lesions after a 6 h interruption was different from the pre-interruption
value the differences were significant if the variabil- ity is assumed to be the same as for the uninterrupted
experiment. In contrast, the total number of chloroses recorded on trap plants after the 2 and 4 h interruption
treatments was much smaller than pre-interruption 59 before, 6 after 2 h, 15 after 4 h. This suggests that
these interruption times were not long enough to re- store sporulation on the yellow rust lesions. It was
only after the 6 h interruption that the number of yel- low rust chloroses recorded on trap plants increased
slightly, indicating that the lesions had begun to sporu- late again, although the numbers were about half of
those before the interruption 25 compared to 59.
3.5. Combined effect of wind and rain The flux of spores number m
− 2
s
− 1
passing the rotating-arm traps was estimated by multiplying the
spore concentration by the wind speed. This gave a measure of the rate of loss of spores from the source
plants. In the absence of rain, the flux averaged over 5 min periods increased monotonically with wind
speed Fig. 5a. Although no specific wind speed threshold for spore removal was found, faster wind
speeds were more effective at removing spores than slower ones i.e. the mean flux at 5 m s
− 1
was nearly 10 times that at 1 m s
− 1
. However, spores were re- leased at mean wind speeds as low as 0.5 m s
− 1
. When the source was exposed to simulated rain with
4.9 mm drops and a wind speed of 1 m s
− 1
, the spore flux density initially increased with increasing time
of exposure before declining Fig. 5b. The greatest 5 min average flux was observed after 10 min. In con-
trast, at a wind speed of 4 m s
− 1
, the 5 min average spore flux decreased over the 20 min exposure period
Fig. 5b, but spores were still being released after exposure to rain for 20 min.
3.6. Simulated rainfall parameters The kinetic energy E
K
of individual incident drops was calculated using Eq. 2. The total kinetic energy
per unit area of all the incident drops landing on the
L. Geagea et al. Agricultural and Forest Meteorology 101 2000 53–66 61
Fig. 4. Restoration of spore populations on brown rust 4a and b and yellow rust 4c and d lesions after a rain event. Infected source plants were exposed to simulated rain consisting of 4.9 mm diameter drops for 30 min, then incubated under optimal conditions for spore
development for 2 h
d
, 4 h
j
or 6 h
m
, before being exposed to simulated raindrops again for another 30 min. Numbers of lesions or chloroses produced on trap plants at all distances observed from the source before 4a and c and after 4b and d the incubation periods
are presented.
source plants, K
t
, was estimated for each drop size and the three exposure periods 5, 10 and 15 min, see Sec-
tion 2.1.3. The relationships between the total num- ber of brown rust lesions or yellow rust chloroses, Y,
and total kinetic energy K
t
of the rainfall is plotted in Fig. 6. For both pathogens, Y was almost proportional
to the total kinetic energy; for brown rust, Y = 0.70 K
t 1.09
r
2
= 0.8 and for yellow rust, Y = 0.24 K
t 1.15
r
2
= 0.8. These relationships mask the decrease in
the rate of spore dispersal with longer rain exposures. However, they suggest that for short durations of rain
the potential for dispersal of rust spores may be re- lated to the total kinetic energy of incoming splash,
assuming all rain droplets can contribute to splash.
The kinetic energy of drops falling at their termi- nal velocity is proportional to their diameter raised to
the power 4.34 Eq. 2. As the size distribution of raindrops depends on the type of rain Ulbrich, 1983,
the potential for disease spread may be influenced by the type of rain, as well as its duration. The relation-
ship for ND given by Ulbrich 1983 see Huber et al., 1998 and the above relationships between Y
and K
t
were used to evaluate the number of lesions or chloroses potentially produced by raindrops of a given
diameter D Fig. 7b for a 5 min duration of rain of a given type thunderstorm, shower and widespread
rain of intensity of 10 mm h
− 1
Fig. 7a.
4. Discussion
