Structure and Function in Agroecosystem Design and Management - Chapter 9 pot

CHAPTER 9
Plant Diseases and Plant Ecology
Nikolaos E. Malathrakis and Dimitrios G. Georgakopoulos
CONTENTS
Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
Effect of Diseases on the Structure of Plant Communities and Plant
Population . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
Age Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
Spatial Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
Plant Density. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186
Temporal Structure-Succession . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
Competition. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188
Diversity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
Diversity within Plant Communities . . . . . . . . . . . . . . . . . . . . . 189
Diversity within Plant Populations . . . . . . . . . . . . . . . . . . . . . . . 189
The Effect of Pathogen Attributes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
Type of Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
Wind Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
Rain Dispersal. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
Insect-Transmitted Inoculum . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
Virulence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
Pathogen Survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
Effect of the Type of Epidemic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
Some Major Plant Epidemics: Ecological Aspects . . . . . . . . . . . . . . . . . . . . . 195
Dutch Elm Disease [Ophiostoma (Ceratocystis) ulmi] . . . . . . . . . . . . . 195
Chestnut Blight [Cryphonectria (Endothia) parasitica] . . . . . . . . . . . . . 195
Dieback Caused by Phytophthora cinnamomi. . . . . . . . . . . . . . . . . . . . 196
Potato Late Blight (Phytophthora infestans) . . . . . . . . . . . . . . . . . . . . . 196
Tristeza . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 196
Other Pandemics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197
183

0-8493-0904-2/01/$0.00+$.50
© 2001 by CRC Press LLC
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 183
184 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
Weed Control with Fungal Pathogens. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198
Epilogue. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
INTRODUCTION
Plant pathogens are among the main biotic factors of any ecosystem and
may play a major role in its dynamics. However, over the greater part of the
history of plant ecology it has been convenient to assume that the structure
and composition of plant communities is mainly determined by macro- and
microclimate, soil conditions, and interactions among the plants themselves
(Harper, 1990).
In natural ecosystems the role of plant pathogens has tended to be neg-
lected. Recently, however, attention has been paid to the importance of
plant pathogens and the relevant diseases on the pattern of plant com-
munities (Dobson and Crawley, 1994). Dinoor and Eshed (1984) number sev-
eral reasons for the growing interest in diseases in the wild. The dramatic eco-
logical impact of several plant pandemics, such as Dutch elm disease, was
probably the most important. However, there are other diseases with less evi-
dent, but no less important, effects on plant communities that merit great
attention.
In agroecosystems, on the other hand, there has always been a great deal
of concern about plant diseases, but they were mostly considered from a
directly economical viewpoint. Well-known examples of destructive diseases
in agricultural systems include the great potato famine, which devastated the
population of Ireland from 1846–1851, and the 1943 great famine in Bengal
due to rice blast (Strange, 1993), but we know much less about the impact of

these, and several other epidemics, on the ecology of their hosts. This is prob-
ably due to the difficulty in studying this aspect of the consequences of dis-
ease and man’s interference, which jeopardizes the potential interactions of
plants and plant diseases.
Harper (1990) questioned the existence of convincing evidence with
respect to the role of pests and pathogens on plant communities and posed
fundamental questions which should be answered. Although those questions
are far from being answered, several publications, which have appeared
since then, provide increasing evidence that plant diseases may affect plant
ecology through the innumerable interactions taking place in any plant com-
munity and plant population.
The present chapter approaches the following aspects of the subject: (1)
the effect of diseases on the structure of plant communities, (2) the contribu-
tion of some major pathogen attributes and the type of epidemics, (3) the eco-
logical impact of selected plant pandemics, and (4) the effect of weed control
by pathogenic fungi on regulation of weed populations.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 184
PLANT DISEASES AND PLANT ECOLOGY 185
EFFECT OF DISEASES ON THE STRUCTURE OF PLANT
COMMUNITIES AND PLANT POPULATION
Studies to elucidate plant-disease interactions and their effect on plant
ecology are few. Data from such studies supporting the potential effect of
plant pathogens on several aspects of the structure of plant communities and
plant populations are presented below.
Age Structure
In the wild, it is assumed that newly established populations are more
susceptible to diseases than are older ones (Harper, 1970). Carlsson et al.
(1990) carried out comparative studies of many populations in areas where
population age can be estimated to test this assumption. They compared dis-
ease incidence caused by three host-specific systemic fungal pathogens on

host plant populations of Valeriana sambucifolia, Trientalis europea, and Silena
dioica. They found that in all three pathosystems, disease incidence was higher
during an early-intermediate phase of population development. Populations
of individual species with an estimated age of over 50, 400, and 300 years
respectively showed low disease incidence (Ͻ10%). In other pathosystems,
natural infections depended upon environmental conditions. Armillaria spp.,
for instance, is a well-known group of root rot-inducing pathogens world-
wide. They may cause both primary infections of healthy trees as well as sec-
ondary infections of stressed trees. Primary infections tend to diminish with
stand age of over 20–30 years. Since only a small proportion of the total pop-
ulation is usually infected, aged trees may prevail in infected areas. However,
in drier, inferior forests, continuing mortality in all age classes is common in
many stands (Kile et al., 1991). Trees infected by Dutch elm disease may sur-
vive for some years after infection. Elms planted in the areas where the dis-
ease is prevailing usually survive for less than 20 years. Given the destructive
effect of the disease, old trees in such stands should be rare.
In agroecosystems, plant diseases affect the aged structure of standing
crops in two ways. First, an established plantation is maintained as long as it
is healthy enough to produce a good yield. Second, in several cases early cul-
tivars are grown in order to avoid plant diseases. The theory behind this is to
reduce the time of the epidemic’s progress, as shown in Vanderplank’s equa-
tion describing disease progress,
X ϭ X
0
e
rt
(where X denotes the amount of
disease at time t, X
0
the amount of initial inoculum, and r the rate of disease

progress), and keep infection at a low level.
Spatial Structure
The effect of abiotic factors on the spatial structure of plants within plant
communities is much more evident than is the effect of plant pathogens. It is
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 185
186 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
well known, for instance, that soil acidity and soil salinity, among others, are
major factors that determine the spatial structure of plant communities. The
role of plant pathogens is sometimes hidden under the effect of the disease
that may be exacerbated by abiotic factors. For instance, in soils with high
pH, potatoes often fail to thrive not because of the soil pH per se but because
potato scab, which is favored by such soil conditions, becomes a production
constraint. Mal secco disease of citrus, caused by Phoma tracheiphila, is deter-
mining which citrus species are grown in several areas in the Mediterranean.
Lemon, the most susceptible species, is grown only in the least windy areas
where infections of wind-damaged shoots are fewer.
In the wild, one of the most extensively documented cases is the disaster
caused in Australian forests by the fungus Phytophthora cinnamomi. It pro-
duces a typical epidemic which may worsen over approximately five years,
but, about three years after infection, field-resistant species colonize the floor
of the diseased forest, thus completely changing the spatial pattern of plants
in the community (Weste and Mark, 1987). Due to its wide host range, the
invasion of this pathogen in an area exerts a definite regulatory effect on an
entire set of plants which may be the main component of the local flora. Other
plant diseases with a large range of hosts may play a similar role. Xylella fas-
tidiosa, a xylem-limited bacterium, is the principal factor preventing the
development of high quality Vitis vinifera and V. labrusca grapes in the south-
eastern U.S. where it is endemic (Hopkins, 1989). It is assumed that because
of its very large host range of cropped and wild plants favored by the same
environmental conditions, the structure of entire plant communities in the

same area may be affected (Newhook and Podger, 1972).
Plant Density
In natural systems, plant density is the result of the established interac-
tions of all the biotic and abiotic factors. Generalizations about patterns of
density-dependent mortality and reproduction are a subject of plant popula-
tion ecology (Harper, 1977). However, there is limited information on the
effect of plant pathogens on the relevance of these generalizations for plant
populations growing in the presence as opposed to absence of different plant
pathogens (Mihail et al., 1998). Dense stands contribute to increased disease
infection because of the establishment of microclimatic conditions such as
high relative humidity, which favor pathogen infections, increase root con-
tacts that enhance transmission of root diseases, etc. (Burdon and Chilvers,
1982), indicating the regulatory effect of diseases on host populations. Several
fungal pathogens and all bacteria require free moisture to produce disease,
while infections by most other fungal pathogens are favored by high relative
humidity (Harrison et al., 1994). The spread of root diseases, such as white rot
of onions caused by Sclerotium cepivorum, is positively correlated with plant
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 186
PLANT DISEASES AND PLANT ECOLOGY 187
density and can be controlled by spacing the host to eliminate root contact
between adjacent plants (Scott, 1956). Mihail et al. (1998) reported that
Rhizoctonia solani and Pythium irregulare reduced the number of plants and the
total biomass of the annual legume Kummerowia stipulacea. Reduction was
higher in plots with higher sowing densities. Burdon (1978) claims that “the
interaction between plant density and disease has certain features of a self-
regulatory feedback system and as such has special interest in the considera-
tion of all plant communities. Thus, because of its faster rate of dissemination,
a pathogen is likely to kill more plants at high than at low plant densities.
This death of plants reduces plant density and this in turn tends to curb the
pathogen through its effect on transmission from plant to plant.” In some

pathosystems, thinning has been adapted as a standard practice for disease
management, indicating the regulatory effect of pathogens on plant density.
For example, thinning of high risk trees (over 50% girdle) is recommended for
management of infected mature plants of southern pines infected by fusiform
rust caused by Cronartium quercuum f.sp. fusiforme in the U.S. (Powers et al.,
1981). Evidence of the regulatory effect of diseases on host population can be
found in several other studies (Augspurger, 1988). Ingvarsson and Lundberg
(1993), using a mathematical model to study the effect of Ustilago violacea on
the population density of Lychnis viscaria, found three different outcomes of
this interaction: (1) extinction of the fungus, (2) a stable coexistence between
plant and fungus, and (3) extinction of both plant and fungus. Virus particle
numbers may decrease with increasing host density due to the difficulties of
insect vectors in spreading disease in dense stands (Boudreau & Mundt,
1997). Hence, it appears that diseases are an important regulatory factor for
plant densities, but their effect seems to be disease specific.
Temporal Structure-Succession
Succession is the process whereby one plant community changes into
another. Although the deterministic concept with respect to succession in
plant communities was initially accepted, the role of randomness in succes-
sion is rather universally adopted now (Crawley, 1994). Stemming from this
new concept, the role of plant epidemics, which appears as an accident rather
than as a sequence of events, could also be considered. It is reported that dur-
ing primary succession in areas where no life pre-existed, the first colonists
are cryptogams (Crawley, 1994). However, we are not aware of any report
that plant pathogens may interfere in primary succession. There are several
models on pathways of secondary succession, but all have an intrinsic deter-
ministic concept. Models based on the facilitation of succession of one organ-
ism by another, such as the replacement of fast growing species by slower
growing ones, etc., nearly predetermine plant succession in the community
on the basis of plant characteristics and available resources. None of these

920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 187
188 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
models consider the possible effect of plant pathogens. Nevertheless, several
recent publications regard disturbances mediated by host-specific pathogens
as underlining factors that determine successional relationships in a commu-
nity. Holah et al. (1997) studied the effect of Phellinus weirii, a native root rot
pathogen of Pseudotsuga menziesii (Douglas fir), an early species during suc-
cessional development of infected forests in the lower Cascade and Coast
ranges of western Oregon. They found that the presence of P. weirii in these
sites appears to push changes towards the late successional species, Tsuga het-
erophylla, Thuja plicata, and Taxus brevifolia. At least in the Cascade mountain
sites, not only was there an increase of the late successional species within
infection centers, but the trajectory along which disease had “pushed” within
these sites was common to all three areas studied.
Competition
Nutritional resources are the most studied factors affecting competition
in plant communities (Tilman, 1994). However, there is increasing evidence
of plant pathogen interference on interspecific competition among plants in
the wild. The main evidence is the flourishing of species introduced into
areas in the absence of their pathogens. Chondrilla juncea, a common but not
dangerous weed in Mediterranean countries, became a noxious weed
throughout Australia. As soon as the fungus Puccinia chondrillina, a pathogen
of this plant in its origin, was introduced, C. juncea populations declined
(Hassan, 1988). Several other reports indicate that rust fungi and other
biotrophic pathogens reduce the ability of infected plants to compete with
healthy ones. Burdon and Chilvers (1977) found that mildew reduced the
competitive ability of barley when grown in mixtures with wheat. Paul and
Ayres (1987) noticed reduced competition of Senecio vulgaris infected with the
species-specific rust fungus Puccinia lagenophorae over lettuce (Lactuca sativa)
when grown in mixtures. Finally, Paul (1989) studied the effect of the same

fungus on the competitive behavior of S. vulgaris versus the weed Euphorbia
peplus and found that infected S. vulgaris was less competitive than the
healthy. There are fewer, but not less important, examples from soil-borne
diseases. Van der Putten and Prters (1997) found strong evidence that when
Ammophila arenaria was exposed to its soil-borne pathogens, it was out-com-
peted by Festuca rubra spp. arenaria, especially under nutrient limitation.
The main issue is how pathogens affect the competitive ability of infected
plants. Many factors are involved, such as the number of competing geno-
types, pathogen type, infection time, and environmental factors, making it
difficult to draw an overall conclusion. Reduction of seed production due to
pathogen infection might reduce the competitive ability of the infected plant.
In S. vulgaris infected by P. lagenophorae, seed production decreased by 60%
over that of the healthy plants (Paul and Ayres, 1986). It seems that in each
pathosystem the reaction is different and not always easy to identify.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 188
PLANT DISEASES AND PLANT ECOLOGY 189
Diversity
Diversity within Plant Communities
The role of plant pathogens in plant community diversity, neglected for
a long time, has recently been recognised both for aerial (Alexander et al.,
1996; Burdon, 1987) and root-infecting pathogens (Bever et al., 1997; Burdon,
1987). Peters and Shaw (1996) executed an experiment on plots of rough
grassland dominated by Holcus lanatus. Plots were cleared of vegetation in
three successive years and allowed to regenerate. One third of plots was left
untreated, one third of plots was regularly sprayed with propiconazole to
reduce fungal diseases, and the last third was inoculated with urediospores
of Puccinia coronata f.sp. holci on the second and third years of the study and
with conidia of the leaf-spotting fungus Ascochyta leptospora in the third year.
Vegetation cover and disease severity were regularly monitored. The authors
concluded that, in communities dominated by grasses, foliar pathogens

tended to decrease the abundance of perennial herbs and, therefore,
decreased the diversity in regenerating plots by favoring grasses.
Mills and Bever (1998) assume that soil community as a whole can con-
tribute to the maintenance of diversity within plant communities. They claim
that negative feedback occurs when the presence of a plant alters the soil
microbial community in a manner resulting in growth reduction of that par-
ticular plant species relative to other species, with the potential interference
of soil-borne pathogens. Assuming that the negative feedback was related to
the species-specific soil pathogens, they tested the effect of Pythium spp. on
the growth of plant species in which negative feedback through soil commu-
nity had previously been observed. Their results suggest that accumulation
of species-specific soil-borne pathogens could account for this negative feed-
back and conclude that soil pathogens may themselves contribute to the
maintenance of plant species diversity.
Diversity within Plant Populations
The effect of plant-pathogen interactions on pathogen populations has
been well studied in great detail in a number of agricultural and natural
pathosystems. Little work has been done, however, on the long-term effect of
disease on plant populations, although this situation has started to change
with the use of modern molecular genetic techniques, such as the various
electrophoretic methods for detection of DNA polymorphism or allozyme
analysis.
Plant resistance to pathogens has long been explained by the gene-
for-gene theory (Flor, 1971), where a single plant resistance gene interacts
with a matching pathogen avirulence gene to produce a resistance reaction.
This type of resistance was based on specific interactions between certain
plant cultivars and pathogen races. Several plant resistance and pathogen
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 189
190 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
avirulence genes have now been cloned and sequenced, although their mode

of action still remains to be explained. Although the gene-for-gene theory
was initially based on an agricultural pathosystem, it has been well docu-
mented in wild plant pathosystems as well (Thompson and Burdon, 1992).
Single gene plant resistance, however, is not the only type of resistance in
nature. A broad and quantitative type of resistance to pathogens is also very
common, but it has been less studied, perhaps due to its inherent complexity.
This type of resistance also exists in natural plant populations, but its long-
term effect has not been elucidated.
In natural plant populations, plant resistance genotypes have co-evolved
with pathogen virulence genotypes, interacting in a perpetual “arms race”
where selection of resistance plant genotypes is followed by the reciprocal
selection of pathogen virulent genotypes. Although this procedure is greatly
influenced by environment (Paul, 1990) and spatial features of the surrounding
vegetation (Morrison, 1996), a few cases have been documented in which dis-
ease altered in time the composition of host plant genotypes in a population.
Murphy et al. (1982) examined the competitive ability of five oats (Avena
sativa) multilines in a mixture over four consecutive years in the presence and
absence of infections by the crown rust pathogen Puccinia coronata. Each year,
plants were inoculated with a mixture of five P. coronata races and were either
treated with fungicide during the growing season to prevent infection or left
untreated. During the course of the experiment, the frequency of certain mul-
tilines in the population started to rise while others were reduced, but no sta-
tistically significant difference was observed in treated and untreated plants.
It would be interesting to see whether this trend would be maintained if the
experiment was continued for a number of years. This study generates the
hypothesis that disease has the potential of reducing genotypic variability in
a population of plants over time.
A recent study on the effect of oak wilt epidemic caused by Ceratocystis
fagacearum is in accord with the former assumption. The genetic structure of
oak trees before and after an epidemic wave was determined with allozyme

analysis of wood samples (McDonald et al., 1998). Post-epidemic trees were
survivors of a 20-year epidemic. Allozyme analysis indicated that genetic
diversity of post-epidemic oak trees was lower than pre-epidemic diversity
for two out of the four allozyme loci tested. Data analysis considered the
effect of spatial distribution of trees and suggested that disease was the major
factor driving this shift in oak forest genetic structure.
A hypothesis proposed by Clay and Kover (1996) similarly suggests that
systemic plant pathogens may sometimes promote host plant genetic unifor-
mity. Several systemic plant pathogens are known to induce asexual repro-
duction of their host or enforce self-fertilization, thus reducing genetic
recombination. This provides the pathogen a selective advantage, because a
susceptible genotype is perpetuated in a plant population and the pathogen
can be vertically transmitted with seed. Direct experimental data are needed
to support this hypothesis.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 190
PLANT DISEASES AND PLANT ECOLOGY 191
Shifts in host plant genotypes effected by disease have been observed in
a number of cases. In Australia, an attempt to stop the spread of the compos-
ite weed Chondrilla juncea was undertaken by using the rust pathogen
Puccinia chondrillina as a biocontrol agent. Plants belonged to three pheno-
typically different genotypes, one of them being the most abundant. After
nine years of biocontrol a complete shift in genotype composition was
recorded, with the formerly most important genotype reduced to extinction
in most areas and the two other genotypes prevailing and becoming the new
target weeds for control (Burdon et al., 1981).
THE EFFECT OF PATHOGEN ATTRIBUTES
Plant pathogens share some attributes, such as type of dispersal and vir-
ulence. Each of them, alone or in combination, clearly affects the interaction
of plants and diseases and finally their effect on plant ecology. The effects of
some of these attributes are briefly discussed below.

Type of Dispersal
Dispersal of pathogens or their carriers is closely related to the spread of
any epidemic and plays a major role on disease appearance in new areas (for
reviews see Fitt et al., 1989; McCartney, 1989). Pathogens are spread in sev-
eral ways but for simplicity we mention only wind dispersal, rain dispersal,
and insect transmission of inoculum.
Wind Dispersal
Airborne spores may travel intercontinentally and cause disease thou-
sands of miles away from the original infection. For instance, spores of wheat
stem rust are transferred each year from Mexico to the U.S. and Canada as
well as from India to Scandinavia. Coffee rust, caused by the fungus Hemileia
vastatrix, is also transferred via airborne spores. It was discovered early in
1970 in Bahia, Brazil, and four years later it had spread in South America over
an area equivalent to the size of Central America. Coffee rust possibly came
to Brazil from Angola with trade winds across the Atlantic in 5 to 7 days
(Schieber, 1975).
For long distance pathogen migration by air currents, propagules should
reach high altitudes in the atmosphere by eddy diffusion. Otherwise they
remain in the lower atmospheric layers and disperse over rather short dis-
tances. Studies for dispersal of Cronartium ribicola, the causal agent of white-
pine blister rust indicated that it is spread about 0.4 km away from infected
Ribes. Other wind-borne pathogens, such as Venturia inaequalis (apple scab),
follow the same pattern (Meredith, 1973).
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 191
192 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
Rain Dispersal
Bacterial plant pathogens, as well as fungi producing mucilaginous
spores, are dispersed by rain splash since mucilage prevents dispersal by
wind alone. Distance of dispersal depends on the size of rain drops and
rarely exceeds 1 m.

Insect-Transmitted Inoculum
The majority of viral diseases and many bacterial and fungal diseases are
transmitted by insects or other animals, such as nematodes. Many of the
known catastrophic pandemics are animal-dispersed. Chestnut blight is
spread by birds and insects, Dutch elm disease by the beetle Scolytes spp. and
tristeza by several aphids such as Toxoptera citricida (Agrios, 1997). The dis-
tance of animal-dispersed diseases depends on many factors, including ani-
mal activity, type of crop, plant species and pathogen strain. T. citricida, for
instance, is 25 times more efficient in transmitting the tristeza virus than
Aphis gossypii. Although some strains of the virus are more easily transmitted
by A. gossypii than others, their transmissibility, by either species, is markedly
affected by the source plant used for acquisition feeding (Raccah et al., 1978;
Bar-Joseph, 1989). Most viruses spread within crops and cause diseases of the
“compound interest” type. However, the ultimate proportion of infected
plants and the rate at which new infections appear vary widely among dif-
ferent viruses and for different crops. Viruses that infect annual crops spread
more rapidly than those of trees and shrubs. In a typical orchard in California,
the citrus tristeza virus spreads to an average of two citrus trees a year for each
infected one already present. By contrast, cauliflower mosaic virus spreads
from a single infected plant to as many as 131 in one season. Invariably,
viruses such as citrus tristeza, cacao swollen shoot, and plum pox take several
years to spread throughout plantations. Nevertheless, their ecological impact
is important since trees are far larger and take longer to grow (Thresh, 1974).
Long distance transport of several wind-borne diseases is one of their
main characteristics with respect to their epidemiology and their effect on
plant ecology. Coffee rust, a wind-borne disease, spread to South America
within four years, 1971–1974 (Schieber, 1975), but it took approximately two
decades for Dutch elm disease, another fast-spreading insect-borne disease,
to spread across Europe (Gibbs, 1978; Ingold, 1978), while chestnut blight
spread in the U.S. at a rate of about 37 km/year (Anagnostakis, 1987).

Man himself also acts as the main long distance transporting agent of
many diseases. Several pathogens have been transferred to Europe from the
New World during the last century and changed the structure of several
crops as well as of natural plant communities. For example, potato late blight
and downy mildew of grapes were introduced in Europe around 1845 and
1875, respectively, from America (Strange, 1993; Agrios, 1997), and chestnut
blight was introduced in the U.S. probably from Japan or China. Citrus
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 192
PLANT DISEASES AND PLANT ECOLOGY 193
tristeza is probably the most sound example of disease spread by man.
Although insect vectors are able to disseminate the virus short distances, dur-
ing the last 60 years the disease moved to almost all citrus-growing areas,
probably by propagating material transferred by man.
Virulence
Virulence is one of the main factors that determine the aggressiveness of
any epidemic. There are several examples both from natural and from agro-
ecosystems. Spread of Dutch elm disease in Europe was rather mild until the
late 1960s when a strain of O. ulmi more virulent than the local ones was
introduced from Canada. By 1976, it was estimated that 9 million out of a
population of 23 million trees had died in England. In France the area of the
country affected by this outbreak increased some threefold every year
between 1972 and 1975 and doubled again in 1976. Gradually, the aggressive
strain spread all over Europe and by 1977 it was noticed in Iran (Gibbs, 1978).
Moreover, European strains of C. parasitica were less virulent than American
strains. Chestnut blight in the U.S. expanded much faster and devastated the
local chestnut Castanea dentata. However, a remission of the epidemic
appeared in the 1950s in Italy and other European countries.
Virulence can easily be modified by several factors. Apart from mutation
and recombination, other factors with severe consequences on pathogen vir-
ulence have been studied during the last years. The presence of viruses and

unencapsidated dsRNAs has been reported in several fungal plant
pathogens (Nuss and Koltin, 1990), which are related with reduced or
enhanced virulence of the host fungus. The dsRNA genetic elements associ-
ated with hypovirulence of some strains of C. parasitica have recently
received considerable attention. A consistent correlation exists between the
presence of the dsRNA, hypovirulence, transmissibility of this element, and
successful use of the hypovirulent strains to control chestnut blight
(Anagnostakis, 1988; Griffin, 1986). Recently, considerable progress has been
made in characterizing structural and functional properties of the dsRNA
associated with North American and European hypovirulent strains, GH2
and EP713, respectively, and determining the potential of its use for more
effective control of chestnut blight (Nuss and Koltin, 1990). Segments of
dsRNA have also been found in the Dutch elm pathogen O. ulmi. There is
evidence of the potential application of this phenomenon for biological con-
trol of the disease (Brasier, 1986)
Satellite viruses may also modify the virulence of a helper virus. Most
viral satellites attenuate disease symptoms, although exacerbation of the
symptoms has been reported as well. Satellite viruses that attenuate disease
symptoms have been effectively tested to reduce virus diseases (Collmer and
Howell, 1992). Galliteli et al. (1991) reported a twofold increase of tomato
yield in plants treated with a satellite containing a mild strain of CMV over
the nontreated ones, as well as a slowed spread of disease in untreated plants
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 193
194 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
in the same field. Similar results were reported by Tien and Gusui (1991) in
China against CMV in several vegetables. Given the aphid transmission of
CMV and the large range of CMV hosts, we assume that this protective agent
may spread further, in crops as well as in wild hosts, with considerable con-
sequences on the ecology of both types of plants.
Pathogen Survival

Pathogens can be grouped into two main categories according to the way
they perennate: (1) those that remain in the outside environment and come
into contact with their host just before infection and (2) those that remain and
multiply on or inside the host long before infection. All major groups of plant
pathogens belong in one or both of these categories.
Several destructive rusts belong to the first category, in that they usually
have a primary and a secondary host. For example, wheat stem rust has bar-
berry as an alternate host, white pine blister rust has cultivated or wild Ribes,
and apple rust has Juniperus spp. The closer the alternate host, the greater the
damage on wheat, pines, and apples. Eradication projects applied for the elim-
ination of all these diseases were based on the assumption that the destruction
of the alternate hosts within infection distance should prevent infection of
their primary hosts. The type and the susceptibility of the alternate hosts
greatly affect disease progress. In the U.S., eradication of Ribes to control white
pine blister rust was considered worthless as soon as the very susceptible
European black currant alternate host was eradicated (Maloy, 1997).
Soil-borne pathogens differ in respect to their persistence in soil. Fungi
producing overwintering structures may persist for many years in the
absence of their hosts. Verticillium dahliae Kleban, for instance, can survive in
soil for up to 15 years in the form of microsclerotia (Agrios, 1997). Some soil-
borne fungi may survive saprophytically. Thrall et al. (1997) developed gen-
eral models of annual crops and soil-borne fungal pathogens to explore the
conditions for host-pathogen co-existence. Using model parameter estimates
from the empirical literature for Phytophthora spp. and Fusarium oxysporum,
which differ in several life history features such as saprophytic potential
(Phytophthora spp. are comparatively poor saprophytes compared to
Fusarium spp.), they found that increased rates of saprophytic growth reduce
the likelihood of co-existence.
EFFECT OF THE TYPE OF EPIDEMIC
Vanderplank (1963), based on the pattern of pathogen increase, charac-

terized plant diseases as simple interest and compound interest diseases. Do
these distinct types of diseases differentially affect their hosts? The answer is
not straightforward. Zadoks and Schein (1979) postulate that since the
progress of any disease depends on initial inoculum (Xo) and the rate of the
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 194
PLANT DISEASES AND PLANT ECOLOGY 195
disease progress (r), disease increases will be faster if the two components
have a higher cumulative effect. They further partition rate of disease
progress into its components: p ϭ the length of latent period, N ϭ the relative
rate of spore production, i ϭ the length of the infectious period, and E ϭ the
effectiveness of inoculum. It is apparent that pathogens with high Xo, short
p, long i, high N, and high E cause the fastest developing diseases and so are
termed “r strategists,” while those with the opposite variables are the slowly
developing diseases and so are termed “R strategists.” They also present
examples of compound and simple interest diseases, which are “r” and “R”
strategists respectively, but they do not generalize.
SOME MAJOR PLANT EPIDEMICS: ECOLOGICAL ASPECTS
The increased concern about the effect of plant diseases on plant ecology
is based to a great extent on the catastrophes man witnessed during the 20
th
century by a number of plant pandemics. The effect of some of them on plant
ecology is discussed below.
Dutch Elm Disease [Ophiostoma (Ceratocystis) ulmi ]
Dutch elm disease was recorded soon after the First World War in several
western European countries. Until the mid-1960s it spread all over north
Europe as well as in several areas of Asia. Damage was high, but no precise
records of the total number of dead trees are available. In England, 10 to 20%
of the elm population died between 1927 and 1960. Dutch elm disease was
transferred to the U.S. in the 1920s. Infection rates as low as 0.14 and as high
as 0.7 have been reported in different states and periods of time. In the late

1960s a new major outbreak started in Europe. High damage was recorded in
England, where 9 out of 22 millions trees died by 1976 and infection rates as
high as 0.65 were found. It was caused by a new, more aggressive strain of the
pathogen introduced from Canada. The new outbreak expanded throughout
northern Europe, as well as to Russia and Iran (Brasier and Gibbs, 1978;
Gibbs, 1978).
Chestnut Blight [Cryphonectria (Endothia) parasitica]
Chesnut blight is the best known catastrophic pandemic of the 20
th
cen-
tury. Its pathogen is native to far Asia, such as Japan and China, where the
local Castanea spp. do not suffer. It was introduced in the U.S. around 1904,
probably from Japan or China. It is lethal to infected trees and spreads
via rain-splashed ascospores and conidia. Insects and animal vectors may
also play a role in dispersal. The chestnut blight epidemic expanded at
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 195
196 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
a rate of about 37 km/year, and by 1950 most of the chestnut trees (C. dentata)
had been destroyed. It also appeared in Italy during the 1930s, and within 25
years it had spread to several other European countries from France to
Turkey, where it severely damaged the European chestnut C. sativa. It has
been reported that in Italy a remission of the disease was noticed in the 1950s,
as concluded from the observation of cankers healing. Such a remission was
not noticed in the U.S. (Agrios, 1997).
Dieback Caused by Phytophthora cinnamomi
Dieback has spread in native forests of Australia, South Africa, New
Zealand, and China, among others. The spread of the disease in Australian
forests and national parks is probably one of the most exciting paradigms of
the effect of a single disease in plant ecology. Its ability to infect over 1000
hosts, both in wild and agricultural ecosystems, indicates its potential threat

to any plant community. The pathogen spreads, among other ways, by water,
vehicles, and animals. Dissemination of up to 171 miles per year has been
reported in Australia under certain conditions (Weste et al., 1976). According
to Sea (1975; referenced by Weste and Marks, 1987), in 1975 the area of jarrah
forest affected by P. cinnamomi was estimated at 282,000 ha increasing by
20,000 ha per year. In this area, several Pinus and Eucalyptus species were
growing. Since its introduction in Australia in 1920 and until 1987 it
destroyed 50 to 75% of the jarrah forest’s flora of western Australia and other
areas of this country. The death of 59 indigenous species belonging to 34 gen-
era and 13 families has been recorded from the same area (Podger, 1972).
Potato Late Blight (Phytophthora infestans)
Potato late blight is one of the most destructive diseases of crop plants. It
has been historic due to the famine caused by the destructive epidemic in
1845 in Ireland. The origin of the pathogen is in central Mexico but now it
exists in every potato growing area. There is evidence for at least two migra-
tions of the pathogen from Mexico to Europe, one during the early 1840s and
a second before the 1980s. P. infestans is a heterothallic fungus with two mat-
ing types, A1 and A2. Mating type A1 was the only one found in Europe until
1984 when mating type A2 was also reported. The absence of hosts of P. infes-
tans in the natural ecosystems in most parts of the world outside Mexico
eliminates the ecological effect of the disease in the agroecosystems of the
large potato producing areas (Strange, 1993; Agrios, 1997).
Tristeza
Citrus tristeza virus (CTV) is one of the most important citrus diseases
for the last 60 years. Since its first appearance in Argentina in 1930, it has
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 196
PLANT DISEASES AND PLANT ECOLOGY 197
destroyed or rendered unproductive about 50 million citrus trees in various
countries, such as Argentina, Brazil, Ghana, U.S., Venezuela, Spain, and
Israel. CTV infects most citrus species, but their reaction varies considerably.

Some citrus species, such as Poncirus trifolliata, are resistant while others are
tolerant. Tolerance varies according to the CTV strain and varieties tolerant
to some isolates may react to others. Sweet orange, mandarin, and grapefruit
decline when grafted on sour orange root stock. Aggressiveness of CTV iso-
lates also varies considerably. Some isolates may cause quick decline while
others do not induce visible decline in susceptible varieties.
CTV is an insect-transmitted virus of the semipersistent mode, mostly
transmitted by the aphids T. citricida and A. gossypii. T. citricida is a 25 times
more efficient vector than A. gossypii. However, transmissibility and epi-
demiology of CTV are also affected by the responsible virus strains, the
source plant for acquisition feeding, and environmental conditions. CTV is
not seed-borne, and its long distance transport has been done by the intro-
duction of vegetative propagating material from infected areas.
CTV infects only species of the Rutaceae family. The preference of the
pathogen on certain rootstock-subject combinations, such as sweet orange on
sour orange, greatly affected the ecology of the citrus species cultivated world-
wide. It is considered to be the reason why attempts to use sour orange as root-
stock for citrus in Australia, South Africa, and Java were unsuccessful
(Toxopeus, 1937; Weber, 1925 referenced by Bar-Joseph et al., 1989). Later, fol-
lowing the destruction of millions of citrus trees grafted on sour orange, the
entire citrus industry was restructured; and nonsusceptible rootstocks were
used instead of sour orange. However, according to Bar-Joseph et al. (1989)
many resistant rootstocks were sensitive to citrus exocortis viroid and other
viroids which forced growers to reestablish citrus production on sour orange
rootstock. Taking into account that sour orange was, initially, used as rootstock
against Phytophthora spp. infection long ago, we have a nice picture of how dis-
eases may affect the ecology of a certain group of plants in agroecosystems.
Other Pandemics
Several other pandemics have caused tremendous catastrophes in vari-
ous areas world-wide. Oak wilt disease (C. fagacearum), known in North

American forests since the mid-twentieth century, has been a recent aggres-
sive epidemic in Texas where it causes massive losses. It is potentially the
most destructive disease of trees and should elicit concern for the resources
of Quercus world-wide (Appel, 1995). Bayout disease of the date palm
(Fusarium oxysporum f.sp. albedinis) has destroyed about 10 million trees in
Morocco and 3 million in Algeria and has accelerated desertification of
infected areas (Strange, 1993). South American leaf blight of rubber
(Microcyclus ulei), reported in Brazil in 1904, has nearly devastated Hevea trees
in South America, and now nearly 92% of rubber comes from Asia (Maloy,
1993; Strange, 1993).
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 197
198 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
WEED CONTROL WITH FUNGAL PATHOGENS
Several fungi have been used for weed control. For example, P. chondril-
lina has been used against C. juncea (skeleton weed), Entyloma compositarum
against Ageratina riparia (hamakua pamakani), and Colletotrichum gloeospori-
oides f.sp. aeschynomene against Aeschynomene virginica (northern jointvetch).
Depending on their dispersal type, pathogenic fungi are either introduced
once in a certain area (classical strategy), or they are formulated and applied
regularly like chemical herbicides (bioherbicides). Their effectiveness is, usu-
ally, high. For instance, P. chondrillina was initially introduced near Wagga,
New South Wales in Australia, and the fungus was found 80, 160, and 320 km
from the initial release site at the eighth, tenth, and twelfth generation, respec-
tively, after release. Similarly, two years after its introduction in the U.S., P.
chondrillina was found in California, Idaho, Oregon, and Washington. Weed
mortality exceeding 90% has been noticed in the U.S. E. compositarum, which
was introduced in Hawaiian forests to control the most serious weed
hamakua pamakani, reduced weed population in a 9-month period from 80%
to Ͻ5%. C. gloeosporioides f.sp. aeschynomene, is available in the U.S. as a com-
mercial product and has been used as conventional post-emergent herbicide

against northern jointvetch in rice fields. Its effectiveness may exceed 90%.
Weed control not only reduces plant/weed competition in favor of the
former, but also, in the long run, species not affected by herbicides may pre-
dominate, resulting in a change in weed community structure. In Australia,
an introduced strain of P. chondrillina was pathogenic against only the narrow
leaf form of C. juncea. The other two existing forms remained unaffected and
gradually began to increase in some areas. There is always a risk that fungi
pathogenic to weeds may increase their host range through genetic recombi-
nation. The danger is higher if the fungus is plurivorous. This is the case for
Phytophthora palmivora, used to control Morrenia odorada (stranglervine) in cit-
rus groves in Florida. In addition to stranglervine, it may infect, under artifi-
cial conditions, several other cultivated plants. We assume that the chance of
the emergence of a new strain pathogenic to the above hosts under field con-
ditions is high (Hassan, 1988).
Dissemination of weed fungal pathogens may also be a problem. All
fungi selected for weed control spread slowly in natural habitats. The long-
time co-evolution with their hosts has established constraints, such as popu-
lation diversity with respect to virulence and susceptibility of the host,
spatial isolation of the host, and environment, which mutually exclude one
organism prevailing over the other. For instance,
C. juncea is native to
Mediterranean countries, but it is not a problem due to the stabilizing effect
of P. chondrillina (Hassan, 1988). The deliberate use of a fungus for weed con-
trol is a directed epidemic with a predetermined ecological disturbance. The
pathogenic fungus is selected to fill some prerequisites (have the required
specificity, virulence, and environmental requirements). However, none of
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 198
PLANT DISEASES AND PLANT ECOLOGY 199
these characteristics can be reliably predicted. Variation is a universal phe-
nomenon and pathogens are not excepted. Once released, an organism might

not be recoverable. If the pathogen thrives and becomes self-perpetuating, it
too could become a pest itself. Also, the reduction of the target weed might
increase the competitiveness of the other plant species in the community,
which may greatly disturb the community dynamic. Furthermore, selection
pressure of the pathogen over the host may result in predomination of weed
species resistant to the pathogen (Templeton et al., 1979).
Te Beest et al. (1992) state that according to their simulation model, con-
trol of an annual weed is influenced by pathogenicity, K, of the introduced
fungus. Introduction of a pathogen with low pathogenicity (K ϭ 0.15, either
15% of the infected plants are killed or reproductivity is reduced by 15%)
results in a series of oscillations in density, followed by a stable equilibrium.
Weed density at equilibrium is determined by the pathogenicity, K, of the
pathogen. For K ϭ 0.66, a stable equilibrium is maintained at 1.4 plants/m
2
.
Periodic oscillations in plant densities over long periods of time begin with
K ϭ 0.68. When pathogenicity is high (K ϭ 0.90), weed population cycles
through relatively stable periods followed by periodic oscillations. They con-
clude that we may expect weed population to be controlled at intermediate
to lower levels rather than totally eliminated after the introduction of a
pathogen. Pathogens with higher levels of pathogenicity will not provide a
stable equilibrium.
EPILOGUE
Plant diseases are an integral part of the episodes taking place in plant
ecosystems, and as such they potentially affect plant ecology. However, plant
diseases in the wild usually have a low profile and their effect on the struc-
ture of plant communities was rather neglected. In agroecosystems the effect
of plant diseases is jeopardized by man’s interference. Hence, convincing
data of the effect of plant diseases on plant ecology, until recently, were rather
poor. However, (a) the increased concern about the effect of plant diseases on

various ecological aspects of plant communities, (b) the tremendous ecologi-
cal catastrophes of plant pandemics world-wide, and (c) the use of plant
pathogens for the establishment of predetermined epidemics against weeds,
both in wild and agricultural ecosystems, all provide increasing evidence on
the important role of plant diseases in plant ecology.
ACKNOWLEDGMENTS
We thank the several colleagues who answered requests for information.
We are particularly grateful to Dr. M. Karandinos for critical evaluation of the
manuscript and to Dr. J. Peters for substantial contributions.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 199
200 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
REFERENCES
Agrios, G., 1997. Plant Pathology. Academic Press, London
Alexander, H.M., Thrall, P.H., Antonovics, J., Jarosz, A.M. and Oudeman, P.V., 1996.
Population dynamics and genetics of plant disease: a causal study of anther–smut
disease.
Ecol., 77:990–996.
Anagnostakis, S.L., 1987. Chestnut blight: the classical problem of an introduced
pathogen.
Mycologia, 79:23–37.
Anagnostakis, S.L.,1988.
Cryphonectria parasitica, cause of chestnut blight, in. Sidhu,
G.S. (Ed.)
Advances in Plant Pathology. Academic, London. 123–136.
Appel, D.N., 1995. The oak enigma: perspectives from the Texas epidemics.
Annu. Rev.
Phytopathol.,
33:103–118.
Augspurger, C.K., 1988. Impact of pathogens on natural plant populations, in Davey,
A.J., Hutchings, M.J., and Watkins, A.R. (Eds.)

Plant Population Ecology: 28th
Symposium of the British Ecological Society.
Blackwell Scientific Publications,
Oxford. 413–433.
Bar-Joseph, M., Marcus, R., and Lee, R.F., 1989. The continuous challenge of citrus tris-
teza virus control.
Annu. Rev. Phytopathol., 27:291–316.
Bever, J.D., Westover, K.M., and Antonovics, J., 1997. Incorporating the soil commu-
nity into plant population dynamics: the utility of the feedback approach.
J. Ecol.,
85:561–573.
Boudreau, M.A. and Mundt, C.C.,1997. Ecological approaches to disease control, in:
Rechcigl, N.A., and Rechcigl, J.E. (Eds.)
Environmentally Safe Approaches to Crop
Disease Control.
CRC Press, Boca Raton, U.S. 33–62.
Brasier, C.M., 1986. The population biology of the Dutch elm disease: the principal
features and implications for other host-pathogen systems, in: Ingram, D.S. and
Williams, P.H. (Eds.)
Advances in Plant Pathology, Vol.5. Academic Press, London.
55–118.
Brasier, C.M., and Gibbs, J.N., 1978. Origin and development of the current Dutch elm
disease epidemic, in: Scott, P.R. and Bainbridge, A. (Eds.)
Plant Disease
Epidemiology.
Blackwell Scientific Publications, London. 31–39.
Burdon, J.J., 1978. Mechanisms of disease control in heterogenous plant population-
an ecologist’s view, in: Scott, P.R. and Bainbridge, A. (Eds.)
Plant Disease
Epidemiology.

Blackwell Scientific Publications, London. 193–200.
Burdon, J.J., 1987.
Disease and Plant Population Biology. Cambridge University Press,
Cambridge, MA.
Burdon, J.J. and Chilvers, G.A., 1977. The effect of barley mildew on wheat and bar-
ley competition in mixtures.
Aust. J. Bot., 25:59–65.
Burdon, J.J. and Chilvers, G. A., 1982. Host density as a factor in plant disease ecology.
Annu. Rev. Phytopathol., 20:143–166.
Burdon, J.J., Groves, R.H., Kaye, P.E., and Speer, S.S., 1981. The impact of biological
control on the distribution and abundance of
Chontrilla juncea in south-eastern
Australia.
J. Appl. Ecol., 18:957–966.
Carlsson, U, Elmqvist, T, Wennstrom, A., and Ericson, L., 1990. Infection by pathogens
and population age of host plants.
J. Ecol., 78(4):1094–1105.
Clay, K. and Kover, P., 1996. Evolution and stasis in plant-pathogen associations.
Ecol.,
77:997–1003.
Collmer, C.W. and Howell, S.H., 1992. Role of satellite RNAin the expression of symp-
toms caused by plant viruses.
Annu. Rev. Phytopathol., 30:419–442.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 200
PLANT DISEASES AND PLANT ECOLOGY 201
Crawley, M.J., 1994. Plant Ecology. Blackwell Scientific Publications, Oxford.
Dinoor, A. and Eshed, N., 1984. The role and importance of plants in natural plant
communities.
Ann. Rev. Phytopathol, 22:443–446.
Dobson, A. and Crawley, M.J., 1994. Pathogens and the structure of plant communi-

ties.
TREE, 9:393–397.
Fitt, B.D.L., McCartney, H.A. and Walklate, P.J., 1989. The role of rain in dispersal of
pathogen inoculum.
Annu. Rev. Phytopathol., 27:241–270.
Flor, H.H., 1971. Current status of the gene-for-gene concept.
Annu. Rev. Phytopathol.,
9:275–296.
Galliteli, D., Vovlas, C., Martelli, G., Montasser, M.S. et al., 1991. Satellite-mediated
protection of tomato against cucumber mosaic virus. II. Field test under natural
epidemic conditions in southern Italy.
Plant Dis., 75:93–95.
Gibbs, J.N., 1978. Intercontinental epidemiology of Dutch elm disease.
Annu. Rev.
Phytopathol,
16:287–307.
Griffin, G. J., 1986. Chestnut blight and its control.
Hortic Rev., 8:291–335.
Harper, J.L., 1977.
The Population Biology of Plants. Academic Press, London.
Harper, J.L., 1990. Pests, pathogens and plant communities: an introduction, in
Burdon, J.J. and Leather, S.R. (Eds.)
Pests, Pathogens and Plant Communities.
Blackwell Scientific Publications, Oxford. 3–14.
Harper, J.L., 1970.
Plant Population Biology. Academic Press, London.
Harrison, J.G., Lowe, R., and Williams, N.A., 1994. Humidity and fungal diseases of
plants—problems, in: Blackeman, J.P. and Williamson, B. (Eds.)
Ecology of Plant
Pathogens.

CAB International. 79–97.
Hassan, S., 1988. Biocontrol of weeds with microbes, in Mukerji, K.J. and Garg, K.L.
(Eds.)
Biocontrol of Plant Diseases vol. I. CRC Press, Boca Raton, FL, 129–151.
Holah, J.C., Wilson, M.V. and Hansen, E.M., 1997. Impacts of a native root-rotting
pathogen on successional development of old-growth Douglas fir forests.
Oecologia, 111:429–433.
Hopkins, D.L., 1989.
Xylella fastidiosa: a xylem-limited bacterial pathogen of plants.
Annu. Rev. Phytopathol., 27:271–290.
Ingold, C.T., 1978. Dispersal of microorganisms, in Scott, P.R. and Bainbridge, A.
(Eds.)
Plant Disease Epidemiology. Blackwell Scientific Publications, London.
11 –21.
Ingvarsson, P.K. and Lundberg, S., 1993. The effect of a vector-borne disease on the
dynamics of natural populations: a model for
Ustilago violacea infection of Lychniss
viscaria. J. Ecol.,
81:263–270.
Kile, G.A., McDonald, G.I and Byler, J.W., 1991. Ecology and disease in natural forests,
pp. 102–121. in Saw, C.G. and Kile, G.A (Eds.)
Armillaria Root Disease. Agricultural
Handbook No.691, USDA.
Maloy, O. C., 1997. White pine blister rust control in North America: a case history.
Annu. Rev. Phytopathol., 35:87–109.
Maloy, O.C., 1993.
Plant Disease Control, Principles and Practices. John Wiley and Sons,
New York.
McCartey, H.A., 1989. Spore dispersal: environmental and biological factors, in
Blakeman, J.P. and Williamson, B.

Ecology of Plant Pathogens. CAB International,
U.K. 171–185.
McDonald, B.A., Bellamy, B.K., Zhan, J., and Appel, D.N., 1998. The effect of an oak
wilt epidemic on the genetic structure of a Texas live oak population.
Can. J. Bot.,
76:1900–1907.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 201
202 STRUCTURE AND FUNCTION IN AGROECOSYSTEMS DESIGN AND MANAGEMENT
Meredith, D.S., 1973. Significant of spore release and dispersal mechanisms in plant
disease epidemiology.
Annu. Rev. Phytopathol., 11:313–342.
Mihail, J.D., Alexander, H.M. and Taylor, S.J., 1998. Interactions between root-infect-
ing fungi and plant density in an annual legume,
Kummerowia stipulacea. J. Ecol.,
86:739–748.
Mills, K.E. and Bever, J.D., 1998. Maintenance of diversity within plant communities:
soil pathogens as agents of negative feedback.
Ecol., 79 (5):1595–1601.
Morrison, J.A., 1996. Infection of
Juncus dichotomus by the smut fungus Cintractia junci:
an experimental field test of the effects of neighbouring plants, environment, and
host plant genotype.
J. Ecol., 84:691–702.
Murphy, J.P., Helsel, D.B., Elliot, A., Thro, A.M. and Frey, K.J., 1982. Compositional
stability of an oat multiline.
Euphytica, 31:33–40.
Newhook, F.J. and Podger, F.D., 1972. The role of
Phytophthora cinnamomi in Australian
and New Zealand forests.
Annu. Rev. Phytopathol., 10:299–326.

Nuss, D.L. and Koltin, Y., 1990. Significance of dsRNA genetic elements in plant path-
ogenic fungi.
Annu. Rev. Phytopathol., 28:37–58.
Paul, N.D., 1990. Modification of the effects of plant pathogens by other components
of natural ecosystems, in Burdon, J.J. and Leather, S.R. (Eds.)
Pests, Pathogens and
Plant Communities.
Blackwell Scientific Publications, Oxford. 81–96.
Paul, N.D. and Ayres, P.G., 1986. The impact of a pathogen (
Puccinia lagenophorae) on
population of groundsel (
Senecio vulgaris) overwintering in the field. J. Ecol.,
74:1085–1094.
Paul, N.D. and Ayres, P.G., 1987. Effects of rust infection on competition between
groundsel and lettuce.
Weed Control, 27:431–441.
Paul, N.D., 1989. The effect of
Puccinia lagenophorae on Senecio vulgaris in competition
with
Euphorbia peplus. J. Ecol., 77:552–564.
Peters, J.C. and Shaw, M.W., 1996. Effect of artificial exclusion and augmentation of
fungal plant pathogens on regenerating grassland.
New Phytologist, 134:295–307.
Podger, F.D., 1972.
Phytophthora cinnamomi a cause of lethal disease in indigenous
plant communities in Western Australia.
Phytopathology, 62:972–981.
Powers, H.R., Schmidt, R.A. and Snow, G.A., 1981. Current status and management
of fusiform rust on southern pines.
Annu. Rev. Phytopathol., 19:353–371.

Raccah, B., Bar-Joseph, M., and Loebenstein, G., 1978. The role of aphid vectors and
variation in virus isolates in the epidemiology of tristeza disease, in Scott, P.R. and
Bainbridge, A. (Eds.)
Plant Disease Epidemiology. Blackwell Scientific Publications,
Oxford. 221–228.
Schieber, E., 1975. Present status of coffee rust in South America.
Annu. Rev.
Phytopathol.,
13:375–382.
Scott, M.R., 1956. Studies on the biology of
Sclerotium cepivorum. II The spread of white
rot from plant to plant.
Ann. Appl. Biol., 44:584–589.
Strange, R.N., 1993.
Plant Disease Control. Chapman and Hall, London.
TeBeest, D.O., Yang, X.B., and Cisar, C.R., 1992. The status of biological control of
weeds with fungal pathogens.
Annu. Rev. Phytopathol, 30:637–657.
Templeton, G.E., TeBeest, D.O. and Smith, R.J. Jr, 1979. Biological weed control with
mycoherbicides.
Annu. Rev. Phytopathol., 17:301–310.
Thompson, J.N. and Burdon, J.J., 1992. Gene-for-gene coevolution between plants and
parasites.
Nature, 360:121–125.
Thrall, P.H., Bever, J.D., Mihail, J.D. and Alexander, H.M., 1997. The population
dynamics of annual plants and soil-borne fungal pathogens.
Ecology, 85:313–328.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 202
PLANT DISEASES AND PLANT ECOLOGY 203
Thresh, J.M., 1974. Temporal pattern of virus spread. Annu. Rev. Phytopathol.,

12:111–128.
Tien, P. and Gusui, W., 1991. Satellite RNA for the biocontrol of plant diseases.
Adv.
Virus Res.
39:321–339.
Tilman, D, 1994. Resources, competition and the dynamics of plant communities, in:
Crawley, M.J. (Ed.)
Plant Ecology. Blackwell Scientific Publications, Oxford. 51–76.
Van der Putten, W.H., and Prters, B.M., 1997. How soil-borne pathogens may affect
plant competition.
Ecology, 78(6):1785–1795.
Vanderplank, J.E., 1963.
Plant Diseases: Epidemics and Control. Academic Press. New
York, 349.
Weste, G., Ruppin, P. and Vithanage, K., 1976.
Phytophthora cinnamomi in Brisbane
Ranges: patterns of disease extension.
Aust. J. Bot. 24:201–208
Weste, G. and Marks, G.C., 1987. The biology of
Phytophthora cinnamomi in
Australasia.
Annu. Rev. Phytopathol., 25:207–229.
Zadoks, J.C. and Schein, R.D., 1979.
Epidemiology and Plant Disease Management.
Oxford University Press, New York.
920103_CRC20_0904_CH09 1/13/01 10:59 AM Page 203