Plant Pathology (2000) 49, 651±658
BRITISH SOCIETY FOR PLANT PATHOLOGY PRESIDENTIAL ADDRESS 1999
Theory and plant epidemiology
M. J. Jeger
Imperial College at Wye, T.H. Huxley School, Wye, Ashford, Kent TN25 5AH, UK
Introduction
I have long been fascinated by the relationship and
interplay between theory, experimentation and
empirical observation apparent in all scientific disci-
plines, including plant pathology (Jeger, 1983a), with-
out being unduly concerned about the finer distinctions
that seem to occupy the minds of philosophers and
popularizers of science. I personally subscribe to the
views expressed by the population ecologist Levin
(1981) arguing for a very broad definition of the term
theory especially in relation to modelling so that theory
and experiment form two mutually reinforcing strands
of enquiry: the DNA±molecule analogy. The develop-
ment of theoretical models is then seen as an explora-
tory rather than an explanatory activity in which the
bounds of experimental investigations are set in context.
Theory has played an important part in the develop-
ment of ecology as a scientific discipline, for example
competition theory in relation to species' distributions
(Jackson, 1981) and community structure (Hopf et al.,
1993). In their sketch of the development of ideas in
ecological phytopathology, Zadoks & Koster (1976)
pointed to the achievement of van der Plank (1963) in
providing a solid theoretical framework and giving
epidemiology its own identity as a specialism within
plant pathology; according to Gregory (1965)
.¼ giving us for the first time a coherent and
developed theory of plant epidemiology, a notable
intellectual achievement.
Most recently, Waggoner & Aylor (2000) compare
the development of plant epidemiology to a progression
`by jagged leaps in understanding patterns of plant
disease'. It is not necessary for theory to be expressed
mathematically to qualify as such. For example, there is
a large body of ecophysiological literature on variation
in inherent growth rate in plants in relation to plant
defence strategies. Evolutionary theories on plant
defence strategies have been proposed largely with
respect to insect herbivores (Tuomi, 1992; A Ê stroÈm &
Lundberg, 1994; Hoffland et al., 1998). These are
mostly conceptual in nature but do lead, for example, to
questions over the cost of defence in the absence of
herbivores or generalist pathogens (in the absence of
specific interactions described by the gene-for-gene
theory). One measure of the power of theory is in its
applicability to different disciplinary areas. Thus it was
Q 2000 BSPP Plant Pathology (2000) 49, 651±658
of interest to examine the relevance and implications of
these theories for plant±pathogen interactions,
specifically the case of the Carbon/Nutrient (C/N)
Balance Hypothesis, which postulates a trade-off
between carbon invested in growth (when nitrogen is
not limiting) rather than in carbon-based defence
(secondary metabolites such as tannins and lignins)
(Hoffland et al., 1998). For Botrytis cinerea infecting
tomato, it was found that leaf tissue C/N ratio was
positively correlated with susceptibility (Hoffland et al.,
1999), but that there was no correlation with Fusarium
oxysporum and indeed negative correlations with
Oidium lycopersici and Pseudomonas syringae (Hoff-
land et al. 2000). Thus the effect of N supply (and hence
C/N ratio) on susceptibility to fungal pathogens is not
predictable by the theories developed for insect herbi-
vores.
These studies on plant nutrition and disease suscept-
ibility have come at a relatively late stage in my career.
My background is founded equally in biology and
mathematics, and my first exposure to plant pathology
was the book edited by Jurgen Kranz on Epidemics of
Plant Diseases (Kranz, 1974), including seminal chap-
ters on mathematical modelling in plant disease
epidemiology. It was largely a consequence of reading
this book that I decided to aim for a PhD in plant
pathology, especially one involving the modelling of
disease epidemics. It gave me considerable pleasure to
contribute a chapter to the second edition of this book
published some 16 years later (Jeger, 1990). I was
eventually accepted to work on a PhD project at
Aberystwyth with Ellis Griffith and Gareth Jones on
the topic of the effectiveness of intraspecific cereal
mixtures against relatively nonspecialized foliar patho-
gens, notably Septoria (Stagonospora) nodorum and
Rhynchosporium secalis. It is of significance that during
my PhD research at Aberystwyth, Ellis Griffiths in his
Chairman's address for the Federation of British Plant
Pathologists (Griffiths, 1978) made the comment
.¼ analytical models, which may be relatively simple,
provide a means of testing the validity of assumptions
.¼ we may wish to make about the way in which hosts
and pathogens interact.
He used as an example the rapid disease progress
following the loss of fungicidal protection against
cercospora blight of celery, more rapid indeed than
progress in fields that had not been sprayed. There was
652 M. J. Jeger
no satisfactory explanation made for this phenomenon
at the time but subsequently, using a simple analytical
model, it could be shown that the phenomenon is
explicable in purely epidemiological terms (by changing
the age structure of disease, a greater proportion of
diseased tissue was actually producing spores after
spraying stopped), and that it was not necessary to
invoke additional characteristics of the host, pathogen
or leaf microflora to explain the phenomenon (Jeger,
1987a). Returning to the present time, Gareth Jones has
recently edited the most recent and up-to-date multi-
authored book on plant epidemiology (Jones, 1998).
My career, from its beginning to the present time, has
been influenced throughout by the interplay between
theoretical and experimental approaches in plant
epidemiology. In the remainder of this address I want
to illustrate this interplay by reference to the research I
have been involved with and have published. Although I
have tried to cover most of the key theoretical advances,
I cannot do justice to the full range and impact of theory
in plant epidemiology.
Heterogeneity and crop disease
In the 1970s there had been much experimental work
undertaken on the effects of crop heterogeneity on
epidemic development of race-specialized pathogens,
either as multilines (mixtures of near-isogenic lines
differing in resistance genes) (Frey et al., 1977) or as
cultivar mixtures in which the individual cultivars carry
different resistance genes (Wolfe, 1978). Theoretical
models had been developed, for example Barrett (1978),
in which the assumptions of the gene-for-gene relation-
ship were explicitly represented. There was no equiva-
lent theoretical basis for predicting the effect on
epidemic development of nonrace-specialized patho-
gens. Very simple theoretical models were proposed that
allowed a full qualitative analysis of the possible
outcomes in such mixtures (Jeger et al., 1981a), and
these were combined with field experiments in an
attempt to quantify the benefit of such mixtures (Jeger
et al., 1981b). Two important conclusions were reached
on the basis of the models developed.
1 Disease development would normally be less in
mixtures than the arithmetic mean of the pure stands,
but in some rather specific circumstances, where the
relative ranking of the individual cultivars with regard
to infection and sporulation parameters were reversed,
the outcome could be worse.
2 Whatever the outcome in the early stages of an
epidemic, the final epidemic size would be the same
(Jeger et al., 1982), although some yield benefits might
still be expected.
Subsequently, this modelling approach was extended
by Gumpert et al. (1987), who introduced further
epidemiological parameters such as the latent period
and spore deposition frequency into the basic structure.
The prospects for the use of variety mixtures have
subsequently been reviewed (Wolfe, 1985), a decision
model has been developed (Yong & Zadoks, 1992) to
determine the optimal strategy of variety mixing and
their current use in diversified production surveyed
(Finckh & Wolfe, 1998).
Gene-for-gene recognition systems, and the under-
lying models, whether conceptual or mathematical,
have played a major role in the development of ideas
concerning resistance and its deployment (Thompson &
Burdon, 1992; Crute, 1994; Frank, 1994). Equally the
patterns of disease development in natural plant
populations, whether homogeneous or heterogeneous,
have given much insight into plant±pathogen popula-
tion interactions and the development of an associated
theory (Alexander, 1992; Roy, 1993; Knops et al.,
1999). Although a combined population ecology/
genetics approach to resistance gene management has
never featured strongly in my subsequent work, it has
nevertheless continued to inform my epidemiological
research (Jeger, 1997; Jeger & Groth, 1985) and the
need for these linkages remains as strong as ever.
Theory of epidemics
My first position as a plant pathologist was at the then
East Malling Research Station (now part of Horticul-
ture Research International) in 1978 working on the
epidemiology and management of foliar diseases of
apple. I was privileged to work with Denis Butt who
had a long history of working on quantitative
approaches to disease epidemiology and also contrib-
uted to a chapter in the book edited by Jurgen Kranz
referred to previously (Kranz, 1974). Much of our
research was directed at decision-based management of
the major apple diseases, scab and mildew, through the
practical implementation of models (Butt & Jeger,
1983, 1985), but theoretical approaches also featured
strongly as a supporting and indeed motivating element
in my research.
The theory underlying the dynamics of epidemics of
plant disease had been developed by van der Plank
(1963), summarized succinctly later in a much shorter
paper (van der Plank, 1965). Basically, with little
reference to the literature in human/animal epidemiol-
ogy, a mathematical model was developed, a single
differential-delay equation, that specifically recognizes
that disease can be categorized into three components ±
that which is latent (not yet infectious), that which is
infectious and that which is removed (postinfectious).
The equation includes three key epidemiological para-
meters: an infection rate based on infectious diseased
tissue, and latent and infectious period durations. From
this equation, given numerical values for the para-
meters, it is possible to predict whether an epidemic will
occur (the so-called epidemic threshold), the initial
growth rate (during exponential disease increase) and
the final size of the epidemic (with removals this is
always , 100%). This equation, it turns out, is a special
case of the Kermack±McKendrick integro-differential
equation derived in medical epidemiology (May, 1990),
Q 2000 BSPP Plant Pathology (2000) 49, 651±658
 Presidential Address 1999
but as is the case in so much of van der Plank's writings,
reference to the nonplant literature was rare.
The approach generally followed in deterministic
models of human epidemics (Bailey, 1975) has been to
represent the categories of host individuals explicitly
and to derive linked equations for each of these rather
than a single equation. Thus susceptible (S), exposed (E)
(equivalent to latently infected), infectious (I) and
removed or postinfectious (R) categories of host
individuals are recognized. If all four categories are
modelled (the so-called SEIR epidemic), then a system
of four equations would be specified. The advantage of
this type of approach is that qualitative analysis is
simpler, aspects of host growth and development can be
included, and parameters describing control practices
can be incorporated directly into the system of
equations. In 1982, I published an alternative approach
to that of van der Plank, based in part on the SEIR
model (Jeger, 1982). For much of the 20 years or so
since I have been concerned with showing the relation-
ships with the van der Plank model (Jeger, 1986, 1987a;
Jeger & Van den Bosch, 1994a) and the ways in which
new approaches offer more power and flexibility (Jeger
& Van den Bosch, 1994b), and can still be linked to
strategic but practical approaches to disease manage-
ment (Jeger, 1998). Over the same period the classical
epidemiological models for infectious disease in
human and animal populations have been influenced
and invigorated by population ecological concepts
(Anderson & May, 1979; May & Anderson, 1979).
The theoretical advances made are increasingly being
integrated into plant epidemiological models (Michael,
1993; Swinton & Anderson, 1995; Truscott et al.,
1997). Particularly impressive is the way in which
combined theoretical and experimental approaches
have been linked in investigations of plant pathogen
associations in natural plant populations, for example
of the anther smut Ustilago violacea system (Thrall
et al., 1993a, b; Ingvarsson & Lundberg, 1993; Thrall
& Jarosz, 1994; Thrall et al., 1995; Alexander et al.,
1996).
Soil-borne plant pathogens
Although van der Plank gave many examples of soil-
borne pathogens and viruses in illustrating his approach
to analysing epidemics, it has mostly been applied for
fungal foliar pathogens. The theory he developed is
arguably more relevant for the latter, but the lack of a
theoretical input into the epidemiology of soil-borne
plant pathogens and of viruses has as much to do with
the opaqueness of and difficulties of working with the
soil medium and the added complication of a vector
involvement for most virus diseases.
In 1983 I moved from East Malling to take up a
position at Texas A&M University to work on the
epidemiology of soil-borne diseases, notably phymato-
trichum root rot of cotton and other annual and
perennial dicotyledonous plants. This fungal pathogen
Q 2000 BSPP Plant Pathology (2000) 49, 651±658
653
forms very characteristic hyphal strands that have the
ability to grow from plant to plant in soil. Again my
interests developed along both theoretical and experi-
mental lines. Experimentally, simply plotting out the
spatial positioning of plants killed by root rot with time
gave indirect evidence of plant-to-plant spread of the
fungus (Jeger et al., 1987b). Spatial analysis techniques
were then being developed and applied in plant
epidemiology but software for the analysis of spatial
pattern was poorly developed, leading to a rather ad
hoc suite of different statistical techniques being used,
including spatial autocorrelation. Today a whole range
of space±time statistical procedures to analyse agricul-
tural and environmental related phenomena are avail-
able and have recently been used to re-analyse the same
root rot data collected in the early 1980s (Stein et al.,
1998). These include geostatistical techniques not only
to analyse spatial pattern but also to design optimal
sampling or monitoring strategies for such a disease. In
recent years there have also been major advances in
elucidating the theory underlying the statistical proper-
ties of assessed disease incidence (Madden & Hughes,
1995), and the uses of this theory in determining
sampling strategies and sizes (Madden et al., 1996;
Madden & Hughes, 1999).
In a sense, these sophisticated statistical procedures
do little to advance our understanding of the mechan-
isms of observed disease spread unless we have an
underlying conceptual model that could be refined into
a mathematical model of spatial dynamics. From a
purely temporal point of view I became interested in
how inoculum density in soil and root growth with or
without lesion expansion on roots might affect the
dynamics of root disease epidemics (Jeger, 1987b). One
possibly counterintuitive outcome of this analysis was
that a low rate of root extension, relative to the rate of
root infection, would lead to less root disease develop-
ment, and thus could form the basis for a root disease
control strategy. This outcome was counterintuitive in
the sense that normally rapid plant establishment and
early growth is considered a good indicator of plant
health. Adding the further complication of the ability of
the fungus to grow through soil to encounter a
developing root system adds another layer of complex-
ity that presents a severe challenge to modelling if it is to
retain some parsimony both in the numbers of variables
and parameters.
This challenge remains today. The group of Chris
Gilligan at Cambridge is at the forefront (Bailey &
Gilligan, 1997; Gilligan & Bailey, 1997; Otten &
Gilligan, 1998) both in theory development and in
design of experimental systems to monitor growth
pathogens and biocontrol fungi. Many novel
modelling approaches are possible, including the
development of morphometric or pattern formation
equations (Gilligan, 1995), scaling from individuals to
populations (Kleczkowski et al., 1997) and attempts to
simulate the complexities of horizontal and vertical
growth distributions of a fungus such as Armillaria
654 M. J. Jeger
(Lamour & Jeger, 2000). The starting point for a
rather different approach has its origins with another
pioneering plant pathologist, Denis Garrett, and the
concepts of inoculum potential and competitive
saprophytic potential (Garrett, 1970). These concepts
continue to be controversial in terms of their appli-
cation to the epidemiology of root diseases, partly
because `potential' has a physical definition not
originally intended by Garrett. There is also perhaps a
reluctance on the part of plant pathologists to deal with
a physical term such as energy, and there are few
examples of exploring its use in the epidemiological
literature.
At Wageningen University, to which I moved in 1994,
we developed a model of the dynamics of a fungal
mycoparasite and its host (the host being in this context
a sclerotial-forming plant pathogen) based on energetic
considerations (Stolk et al., 1998) and applied it to
laboratory and field data on the dynamics of Sclerotinia
minor (causing lettuce drop) and its mycoparasite
Sporidesmium sclerotivorum. The main conclusion
from the theoretical analysis was that expansive growth
of the mycoparasite did not depend on its initial
inoculum density or on the energy content of its
propagules, but rather on the density of the target
sclerotia and their energy content. This was largely in
agreement with the experimental data (Adams et al.,
1984; Fravel et al., 1992). Using the model and
experimental data it was possible to estimate realistic
values for the model parameters, except for energy
content of a microscelerotium which was considerably
overestimated compared with laboratory measure-
ments. Gubbins & Gilligan (1996, 1997) also developed
a model for the Sclerotinia±Sporidesmium system by
extending a predator±prey model into one in which
the prey (the plant pathogen) was either uninfected
and capable of causing an infection of the host, or
infected supporting further reproduction of the hyper-
parasite. The same data may then serve for different
modelling purposes and lead to potentially different
interpretations.
Energy, either in the substrate available to a fungus or
in terms of its utilization for growth depends, of course,
on carbon and nitrogen fluxes and limitations (Paustian
& SchnuÈrer, 1987). In a complementary approach to
that described above we have tried to model the growth
of soil-borne fungi, whether pathogens, mycoparasites
or saprobes, in terms of carbon and nitrogen fluxes
from the original substrate in soil to the carbon and
nitrogen present metabolically and structurally in fungal
biomass (Lamour et al. 2000). Although a complicated
model involving seven variables results, some qualita-
tive analysis is possible in defining conditions for
establishment and persistence of the fungus in relation
to substrate supply. These conditions specify firstly
that there should be a positive carbon balance in terms
of energy invested in substrate breakdown and that
arising from breakdown; and that the energy necessary
for production of structural fungal biomass and its
maintenance should be less than this positive carbon
balance when all substrate is utilized.
Dispersal and spatial dynamics
Even given these elaborations of energy, carbon and
nitrogen fluxes, etc., it is still not possible to compose a
realistic but parsimonious description of the spatial
dynamics of root disease. Fungal growth in soil is
simply a means of dispersal of the pathogen and for this,
just as much as for air or vector dispersal, the spatial
and time dimensions must be considered simulta-
neously.
My interest in spatial dynamics returns me to another
early pioneer, Philip Gregory, who laid many of the
foundations of modern plant epidemiology. Gregory
(1968) examined in great detail how different forms of
disease gradients in space arose and how these devel-
oped over time. My interest arose in early work on the
effect of cultivar mixtures on spread of nonspecialized
fungal pathogens of cereals. I developed a simple
procedure using multiple regression to estimate the
rates of disease increase (with time) and the gradient
parameter (in space) simultaneously (Jeger, 1983b). In
reality this procedure served as a calculation tool only
and had no real theoretical or mechanistic basis. That
basis arose with the modelling work of Minogue & Fry
(1983a, b) and subsequently with the seminal work of
Frank Van den Bosch and coworkers (Van den Bosch
et al., 1988a, b) on focal expansion of plant disease
(Zadoks & Van den Bosch, 1994), a phenomenon that
can be seen not only in individual fields but also over
many hectares in tree populations or forests (Appel
et al., 1989). Focus expansion, and whether this takes
the form of a wave-like or nonwave-like expansion
(Shaw, 1995), was reconciled with biophysical princi-
ples of spore dispersal by Ferrandino (1993). Such
linkages between biophysical phenomena and the
description of epidemiological processes is an absolute
requirement for improved crop disease management
(Jeger, 1999).
Plant virus epidemics
Spatial pattern was also the stimulus for my final
example of the role of theory in plant epidemiology. In
my early career at East Malling I was aware of the
devastating effects that plant virus epidemics have in
tropical perennial crops. Mike Thresh, a previous
President of the British Society for Plant Pathology
and a colleague with whom I renewed acquaintance in
1986 when I moved to the UK Natural Resources
Institute, had written about cocoa swollen shoot and
what has probably been the most intensive attempt ever
to eradicate a plant disease (Thresh, 1980). In looking
at the effect of disease gradients and the spread of
disease in endemically diseased areas such as the eastern
region of Ghana, it seemed apparent that contraction in
the healthy area of replanted cocoa should be the focus
Q 2000 BSPP Plant Pathology (2000) 49, 651±658
 Presidential Address 1999
of attention rather than expansion of the diseased area
into the replanted area. This insight led to an analysis of
the options for replanting cocoa and the uses of a
cordon-sanitaire around such plantings (Jeger &
Thresh, 1993). From this arose the question of whether
the monitoring of replanted areas and the removal of
diseased trees (rogueing) would improve the likelihood
of maintaining a healthy population. One feature of
epidemics caused by plant viruses is that with few
exceptions (Nakasuji et al., 1985) there has been
virtually no modelling framework developed to answer
this type of question.
A model of plant virus disease dynamics in perennial
tree crops was developed (Chan & Jeger, 1994) and
analysed to evaluate rogueing (removal of diseased
trees) and replanting with healthy trees as a disease
control strategy. Taking published data for three
important virus diseases ± citrus tristeza, banana
bunchy top and plum pox ± it was concluded that
rogueing and replanting could contribute to the
eradication of a disease if economically viable, and
that continuing operations could certainly maintain
disease below economically damaging levels (Jeger &
Chan, 1995). In collaboration with Frank Van den
Bosch at Wageningen, and subsequently in the UK, this
general approach has been extended to modelling a
combined nursery±field plantation system where, for
example, it may be necessary to assess the relative
effectiveness of rogueing in the nursery and the field
plantation. This analysis (M.J. Jeger, F. Van den Bosch
& M. Dutmer, unpublished data) has led to the
specification of criteria for the establishment and
persistence of a virus disease in a healthy population
and, perhaps more importantly, for the establishment
and persistence of healthy plants in an endemically
diseased population.
A crop such as cassava is propagated routinely from
stem cuttings which desirably would be virus-free. Such
an ideal is not always possible in tropical countries such
as Uganda, where there has been a recent pandemic of
African cassava mosaic disease (ACMD) (Otim-Nape
et al. 2000). It was not clear initially whether the
increased severity was due to changes in the virus or
vector (the whitefly Bemisia tabaci) biotype. Holt et al.
(1997) developed an epidemiological model that incor-
porated vector population dynamics and applied it to
the case of ACMD. This showed that with only virus-
free cuttings then either a high transmission rate by the
vector or a large population of vectors could lead to
persistent cycles in disease incidence. When frequency-
dependent use of infected cuttings was admitted, either
because of ineffective diagnosis or because of lack of
healthy material and the necessity of a famine-insurance
crop, then cycles were no longer apparent, but healthy
and diseased cassava could both persist in equilibrium
or the healthy population could totally collapse ± the
outcome depending not only on model parameters but
also on initial conditions. Those findings have major
implications for the propagation and distribution of
Q 2000 BSPP Plant Pathology (2000) 49, 651±658
655
ACMD-resistant cassava against a backdrop of fluctu-
ating disease levels, especially where more susceptible
cultivars may still be favoured by farmers.
The importance of vector movement is likely to be a
key feature in plant virus epidemics (Power, 1992).
Virus±vector associations can be categorized according
to different transmission classes, dependent in part on
the time-scales involved in acquisition and transmission,
and whether the virus moves through and even multi-
plies in the insect vector. In collaboration with Frank
Van den Bosch at Wageningen, Larry Madden at Ohio
State University, and John Holt at the Natural
Resources Institute, a general model was proposed
(Jeger et al., 1998) for analysing plant±virus transmis-
sion characteristics and epidemic development, largely
as a basis for determining the effectiveness of the
different (if limited) control options available. This
analysis has recently been extended to include vector
migration and further evaluation of disease control
strategies (Madden et al., 2000).
Other recent examples of the application of models to
the epidemiology of virus diseases include the problem
of stringent validation of spatial dynamics (Hughes
et al., 1997) and estimation of the endemic period,
during which an infectious population is subject to
stochastic dynamics (Grasman, 1998). In both cases,
more general models were applied to specific data on
virus epidemics.
Conclusion
Kermack and McKendrick's Contributions to the
Mathematical Theory of Epidemics were published as
journal papers over the period 1927±39, as cited in the
first edition of Bailey's The Mathematical Theory of
Epidemics published in 1957 (references in Bailey,
1975). The two influential papers coauthored by
Anderson and May on the `Population Biology of
Infectious Diseases' were published in 1979. It is still the
case that the theoretical basis for plant disease
epidemics has not been established to the same extent
as in human and animal epidemiology (Michael, 1993),
despite the major contributions referred to in this
Address. Clearly there are differences between epi-
demics in plant and animal/human populations: the
scope for direct experimentation rather than theory
development is one such difference that may obviate the
need for comparable theoretical development to take
place. Nevertheless, with the remarkable advances in
molecular plant pathology, the deepening understanding
of host±pathogen interaction at the genetic and
biochemical levels, and the sophisticated tools for
monitoring, tracking and quantifying pathogen popula-
tions, it is even more important in my view that we
maintain and enhance our ability to place these
advances in an appropriate epidemiological and ecolo-
gical setting. This, in my view, can only come through
the further development of theory and its interactions
with practice. As noted by Hengeveld (1992), in a
656 M. J. Jeger
different context, `we still need good theory to underpin
good practice'.
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