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REFLECTIONS ON SPACE, TIME, AND DIVERSITY

JC Zadoks
Department of Phytopathology, Wageningen Agricultural University, P.O.B. 8025, 6700
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EE, Wageningen, The Netherlands; e-mail: JCZadoks@User.DiVa.NL
Annu. Rev. Phytopathol. 1999.37:1-17. Downloaded from www.annualreviews.org
Key Words complexity, connectivity, farmer, focus, methodology

■ Abstract Farmers motivated and inspired me to pursue a career in plant disease
epidemiology. A taste for field observation and a need for reflexion led to a theory
of disease foci, which grow in space and time. Quantitative effects are modulated by
qualitative factors such as race differentiation of the pathogen and partial resistance of
the host plant. Moving to larger scales of operation, within- and between-crop diversity
become important. Diversity may be amenable to management. Whereas reduction-
istic experimentation will remain necessary to explain details, this paper makes a plea
to use modern techniques for tackling complexity in crop protection.
EARLY STEPS
Wonder
Wonder is the emotion that has sparked many careers in biology. My wonder grew
into a passion for agriculture. Born and bred in the glorious city of Amsterdam,
I spent my primary school years in the countryside. Under my window stretched
a Dutch polder, flat and empty. In wonder I looked at a farmer who plowed his
unwieldy clay soil, the plow drawn by two horses. Black and white bodies of cattle
drifted through the morning fog. Wartime events exposed me to farm life, and I
liked it. Toward the end of World War II, as a young teenager, I was responsible
for a small mixed farm, with pasture, arable land and garden, four cows, one hog,
but no horse.
After the war, I returned to Amsterdam to finish high school, the classical
European curriculum with Latin, Greek, French, German, English, Dutch, biology,
chemistry, physics, and mathematics. I liked this broad program, which was to
stand me in good stead throughout my career. Languages appealed to me, especially
the unruly classical Greek. Mathematics fascinated me.
Lack of money stood in the way of my studying at the Wageningen Agricul-
tural University. I chose instead biology at the University of Amsterdam, with its
old-fashioned, dreary curriculum. Only the thorough training in geology provided
me with any real satisfaction and, to this very day, it helps me understand the
structure of the landscapes in which agriculture has evolved. Because of the war,
0066-4286/99/0901-0001$08.00 1
2 ZADOKS
Dutch science had fallen seriously into arrears. Biochemistry, for instance, which
was already coming of age in the United States, hardly existed at that time in
The Netherlands. Thus I chose plant physiology as my major. The Fullbright Pro-
gramme, which financed the exchange of scholars between the United States and
the war-stricken European countries, helped to repair these deficits. One Ameri-
can Fullbright professor taught population genetics and evolution—a revelation.
Impressed by the importance of statistics, I was the first biology student in Ams-
terdam to take extracurricular courses in statistics, for which there was not even a
?
regular professor at the time.
In private life, as in science, all of us youngsters wanted to make up for time
lost during the war. To compensate for what we had missed, student life was
very intense. I learned to organize dinners and rowing regattas, not to mention
bookkeeping and debt collection. Opportunities abounded to take on voluntary
organizational and managerial responsibilities, and these extracurricular activities
were very earnestly pursued. Fraternity life offered contacts with other sciences,
law and economics, philosophy and psychology, literature, and languages.
Beginnings
Phytopathology I chose as a minor, in part because of the impressive personality
of the cigar-smoking Professor Johanna Westerdijk, whose by then declining star
had once shone so brilliantly. Another woman, Professor Louise Kerling, took
over and introduced me to Wageningen, the city of agricultural research, where I
have spent my career. Professor Joan Oort was looking for a young scientist to
unravel the epidemiology of wheat stripe rust (Puccinia striiformis). The research
was to be financed by a levy on wheat farmers of one Dutch cent per 100 kg of
wheat. Wheat farmers and breeders were to benefit from the research results. My
application was accepted and, hired by the Research Institute for Plant Protection
(IPO), I was seconded to Professor Oort, a pioneer in epidemiology.
My educational preparation to date now proved useful. Hired for my knowledge
of genetics and statistics, then unusual among biologists, my linguistic interests
paid off too since I had to work in the international arena. The working hypothesis
was that stripe rust came from the south, in analogy to stem rust epidemiology in
North America. Thus, I hunted for stripe rust from Mid-Scandinavia to Southern
Spain, from Ireland to the Iron Curtain, at a rate of 40,000 km per year, to find
out that the rust did not migrate but rather overwintered and oversummered in The
Netherlands (41).
The finding was based on observation by farmers. A network of informants
provided me with odd but useful tidbits of information. One farmer said that he
finally understood where the rust came from. “Oh yes?” “Yes, it comes from the
peas.” “Very interesting, can I come and see it?” “Sure.” So off I went and saw
what the farmer had seen. The rust did indeed come from the pea field, which had
been under wheat in the preceding year. That wheat had been severely rusted.
“Under the peas” were rusted volunteer plants, from which the rust spread to
Space, Time, Diversity 3
the neighboring wheat field. So I learned that epidemiologists have to listen care-
fully to farmers, who usually are outstanding observers but often rationalize their
observations in ways different from those of scientists.
This overwintering of the rust, carefully documented by color slides to convince
my incredulous paymasters, supervisors, and colleagues, was complemented by
many observations on overwintering and oversummering. The endemism of the
rust was considered to be an important new finding around 1959. Great was the
shock when I read that Eriksson and Henning (7) had already published in 1896 on
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the endemism of wheat stripe rust in Southern Sweden. This emotional experience
led to a deep respect for the classics in phytopathology and to a permanent interest in
the geographical and historical dimensions of our profession. The key ingredients
of my early career were space and time, international space and historical time.
Inspiration From Administration

Restlessness and curiosity led me to change my field of action regularly. I alternated
periods of research with intensive periods of administration at the university and
national levels. The student activism of 1968/9, which initiated reorganizations of
university life worldwide, also touched the Wageningen Agricultural University.
After the reorganization, I was elected to serve a term of three years as the first
Dean of the University, with responsibility for all teaching and research. After
the relative isolation of the junior scientist, I would be able to widen my view on
agricultural science, including social and basic sciences. I was thrilled since it
connected with interests nascent since my youth.
For many newly hatched university officials of the time, re-entry from high-orbit
administration into down-to-earth research was difficult. Discussing the re-entry
problem in front of a Pennsylvania fireplace, inspired by the warmth and good
cheer, a solution was found. Richard D. Schein and I decided to write an in-
troductory textbook on plant disease epidemiology. It worked (51). His intimate
knowledge of ecology and my interest in methodology merged and a book ap-
peared. In the course of time many students, especially from the United States,
complimented the authors on the contents and writing style. For me, used to Dutch
students less outspoken on anything positive, it was a pleasant surprise.
The holistic outlook of the administrator induced a change of interest toward
plant protection at large rather than phytopathology in the strict sense. The EPIPRE
(EPIdemiology, PREdiction, PREvention) project, computer-based recommenda-
tions for pest and disease control in wheat, was one of the outcomes (46). The
project was designed in close collaboration with Dutch farmers, over 600 in all,
who were quite articulate about their requirements. The farmers, spoiled by the
recipe approach of the chemical industry and the extension service, the latter
knowing exactly what was good for farmers, were ushered back to their fields to
look and decide for themselves. Most of the farmers loved it. Some of them even
bought a hand lens for better inspection. Many applied the new approach to other
crops.
4 ZADOKS
The EPIPRE project resulted from a conjunction of three planets: the availabil-
ity of much unexploited knowledge about the dynamics of fungal disease; the fear
of undesirable side effects caused by widespread use of systemic fungicides; and
the application of computer technology. Interestingly, the support for the EPIPRE
project came primarily from wheat farmers. My colleagues at Wageningen thought
me crazy because, as one (who had never even seen a computer) explained to me
in all seriousness, everybody knows that computers and phytopathology cannot go
together.
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EPIPRE had unexpected side effects. At a time when biochemistry was the
uncrowned queen of the sciences (molecular biology was as yet unknown), it made
field-oriented science fashionable again. No doubt, the glamour of the computer,
then feared as much as admired, contributed to the visibility of EPIPRE. Several

Western European countries tested the system and used elements of it for their own
purposes, but Switzerland was a special case. Dr. Hans-Rudi Forrer picked up the
message when he was a guest researcher in Wageningen, extended and improved
the system for wheat, and adjusted it to barley and potatoes. In The Netherlands,
EPIPRE changed the attitudes of farmers and extension workers, left its imprint,
then vanished. Transposed into modern terminology, the attitude propagated by
EPIPRE was internalized. In the letter accompanying the research proposal for
EPIPRE in 1976, I expressed the hope that EPIPRE would make itself superfluous
in the long run. It did!
CONSOLIDATION
Three themes, of a very different nature, continued to appear throughout my profes-
sional career. Intensive field work aroused a persistent interest in the phenomenon
of disease foci. A desire to create order in a bewildering multitude of observations
and ideas stimulated a taste for methodology. Curiosity and an innate restlessness
compelled me to answer the call of international agriculture. To explore these
themes I ignore chronology.
Foci
Among the field phenomena observed during the early years, foci of stripe rust
intrigued me. With the help of many technicians, students, and colleagues, fore-
most among whom were biomathematicians, a theory of focus development was
constructed that covered the total range of small-scale primary foci to pandemic
spread of focal disease (34).
The focus, beginning with a single spore successfully introduced from outside,
can be explained mechanistically and studied quantitatively in replicated epidemi-
ological experiments. The effect of cultivar mixtures, once propagated by Borlaug
(4), could be explained in part as a form of focus suppression (9, 21). Organic
farmers in The Netherlands did not need the explanation and applied the principle
of cultivar mixtures to their profit.
The study of foci has a historical dimension. The first solid description of foci of
a soilborne disease dates from 1728 (43). The author, Duhamel, added a remedy:
isolation by trenching. The phenomenon of foci obviously has existed as long as
pathogens have existed. Early experiments were conducted with stem rust of rye
around 1810, but the term focus is of recent vintage. In the older literature the
wording may differ from today’s language, but the facts are straightforward. Un-
fortunately, the researcher today has time only for the latest relevant review paper
instead of digging down to the oldest source. Loss of the historical perspective
?
may damage our science.
Basic studies on foci brought me into contact with similar trends in general
ecology, which offers a body of knowledge hardly tapped by phytopathologists.
Even a great thinker like JE Vanderplank (35) did not refer to general ecological
literature in his book, although some of his ideas were congruent with ecolog-
ical findings. In turn, the phytopathologist, who focuses on managed ditrophic
systems, might contribute to general ecology. Contacts with ecologists stimu-
lated an interest in wild, unmanaged pathosystems, where human intervention has
been minimal (45), and also in tritrophic pathosystems (38). The going is slow
in these areas. Progress in wild pathosystems is made in ecological rather than in
phytopathological research institutions.
Methodology
Obviously, wheat stripe rust was endemic in The Netherlands. Annual migration
from other countries to The Netherlands was excluded as a possibility because
the stripe rust in The Netherlands was usually found much earlier than elsewhere.
To complete the reasoning, I had to demonstrate in a quantitative manner that the
amount of overwintering stripe rust inoculum could fully and quantitatively explain
the observed epidemics, without having recourse to immigration as an additional
source of inoculum. The dynamics of the disease had to be quantified and the
resulting variates and parameters handled mathematically. Thus I developed my
own version of quantitative epidemiology in which, ideally, the epidemic to be
explained follows quantitatively from relationships established at a next lower
integration level, the explanatory level.
When I presented my first results in public, simple logistic growth of stripe
rust epidemics, my erstwhile professor, the highly respected Louise Kerling, ap-
proached me wringing her hands, half way between anger and despair, saying,
“Mathematics in biology? That’s impossible!” Such was the state of Dutch bio-
logical science in 1960.
Methodology, the art of how to do research, and mathematics, the art of making
logical inferences, have been prime interests ever since (42). Methodology is not
necessarily highbrow. Two colleagues and I developed a simple methodological
tool for research in cereals, the Decimal Code (50), describing the growth stages
of wheat, following an illustrious example (10). The Decimal Code became a
citation topper, translated from English into Dutch, French, German, Swedish,
Portuguese, and Russian, among others. It became the standard for Union pour
6 ZADOKS
la Protection des Obtentions Végétales (UPOV) and U.N. Food and Agriculture
(FAO) descriptions. One reason for its unexpected success was the Code’s careful
description of early growth stages, very important for timing of the herbicide
applications that came into fashion in the early 1970s.
Much time was spent on qualitative matters, especially on race analysis of stripe
and leaf rusts of wheat. Several colleagues had observed that seedling wheat plants
in the greenhouse and adult wheat plants in the field differentiated races differently.
I found that the race identification work, traditionally done in the greenhouse on
?
seedlings, did not explain the observations made by farmers in commercial fields.
Thus, I developed a system of “race nurseries,” planted in the field, that permitted
race identification on adult plants (41). The system worked well for stripe and leaf
rust, because the European winter wheat varieties contained many unidentified
major genes for resistance that were expressed by adult plants only. My system
was publicly condemned by a President of the British Mycological Society (22), but
other British researchers later reinvented this laborious but indispensable system
of race identification.
Inadequate mastery of analytical mathematics drove me into the arms of her
numerical sister as applied in computer simulation. Dynamic simulation allows
many variables to be incorporated, various fancies to be followed, and the con-
sequences of ideas in time and space to be tested (even ad absurdum), with or
without temporal and spatial diversity. Such simulations may lead to insight, but
they never prove a point. For rigid proof one has to return to parameter-sparse
models, which can be handled analytically. Fortunately, Frank van den Bosch
(33, 34) came to the rescue, and several papers on focal epidemics were published.
The current mathematization of phytopathology pleases me, because it deep-
ens the understanding, enhances the generalization value of the findings, and gives
more status to the discipline. I realize that good phytopathologists who do not have
a knack for mathematics may feel excluded from the game, but they can compen-
sate by interaction and collaboration. One danger is that mathematics become
overemphasized, as exemplified in many published regression analyses where an
R of 0.95 is not good enough because it can be pushed up to 0.99, and then to
0.995, by introducing a more complex function with still another variable. Such
exaggerations have little meaning when a mechanistic explanation of the correla-
tion cannot be provided. Alas, finding such an explanation takes far more time
than finding another correlation and regression program in your computer package.
The third decimal of R has high bogus value.
The Call of International Agriculture

The stripe rust work was international. Farmers and breeders were visited in over
12 European countries, where greetings in the national language opened many
doors. Numerous presentations were given in German, in (then) West Germany
where important wheat breeders resided, English, and French. Later, consultancies
took me to the tropics to study diseases of bananas and rice.
The Crop Loss Conference organized by FAO in 1967, at which I repre-

sented The Netherlands, opened a new box of interesting problems, with semantic,
technical, economic, and social dimensions. The conference did not produce spec-
tacular results but rather a trickle-down of ideas, a framework of thinking for many.
EPIPRE absorbed several ideas born in Rome. For example, EPIPRE was the first
computerized advisory system with a financial algorithm to calculate costs and
benefits of any intervention. FAO’s conference generated a life-long interest in
economic and social aspects of plant disease and crop protection.
?
The Netherlands warmly supported another FAO initiative, studies on horizontal
resistance (HR). Several Dutch researchers became involved, and some chose me
as their supervisor. The original idea, launched by Vanderplank (36), was translated
into a manageable program by Robinson (26). Slowly, Vanderplank’s imaginative

power and Robinson’s hands-on approach began to change the outlook of plant
breeders and pathologists. Assessment of Partial Resistance (PR), as we call
HR now, was essential to EPIPRE. I feel that PR resistance is still neglected
in entomology, where it fits well with biological control (32). In nematology,
assessment and utilization of PR are promising (2).
An evaluation mission of the FAO Inter-Country Programme on Integrated Pest
Control in Rice in South and South-East Asia, 1986, left me deeply impressed
by that large-scale, farmer-oriented program (13). It reminded me of EPIPRE,
but it had different roots and took a different course, perfectly adapted to small
farmers in developing countries. As a sequel to the Green Revolution, these farmers
were under heavy pressure from representatives of the chemical industry and their
own governments to use more pesticides, notwithstanding the known or suspected
adverse side effects (15). Around 1986, the tide turned, largely because of the FAO
Programme. High-ranking South-East Asian officials (Presidents and Secretaries
of Agriculture) declared that IPM was to be the official crop protection policy
(49).
As a member of the FAO/UNEP Panel of Experts on Integrated Pest Manage-
ment, I had a front seat to watch the changing international scene. The contribution
of phytopathology to IPM was and is impressive but barely recognized. American
phytopathologists prefer to speak of “plant health” (6), pointing to the end rather
than to the means. At times, there was a Babylonian confusion of disciplinary
tongues. There were serious conceptual constraints to mutual understanding of
entomologists, phytopathologists (virologists included), and herbologists. In sys-
tems terminology, we might describe the problem as one of “time constants.”
Whereas the time constants of the entomological problems then discussed could
be measured in days or weeks, the time constants of the relevant phytopathological
processes had to be expressed in weeks to years, and the time constants of weed
control actions had to be measured in years.
Conceptually and logistically the FAO Programme was and is a great innovation.
The input of the social sciences was crucial. Since we have left threshold IPM
behind us (44), I may say with little exaggeration that the most advanced IPM of
today belongs more to the social sciences than to the natural sciences (39). The
8 ZADOKS
statement is not meant to belittle the contribution of the natural sciences, which is
as impressive as it is indispensable, but it marks a necessary transition.
SPACE, TIME, AND DIVERSITY
Epidemiology dealt primarily with disease progress in time, very seldom with
regress. Since about 1980 disease progress in space has come in vogue. The
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modifying effect of diversity is largely neglected. A discussion of space, time, and
diversity will cross the border separating phytopathology from sister disciplines
such as entomology, and intrude into the domain of nature management.
Space
Vanderplank (35) in his epoch-making treatise did not care about space. His space
had zero dimension; it was a mathematical point. The only exception was his
treatment of interplot interference. In later work, Vanderplank (36) discussed and
illustrated his “horizon of disease spread,” a concept related to the “focal front” of
an epidemic.
Mathematics broke the spell of the point-space. Epidemiology began to borrow
concepts from meteorology and physics, such as the concept “time constant” that
measures the pace of an epidemic process. Dynamic simulation techniques were
applied to spatial aspects of epidemics (12, 17). Others analyzed meticulously
performed field experiments. Replicated focus formation experiments were used
independently by several researchers to test models and also to measure minor
differences in partial resistance, minor but effective in polycyclic disease, which
multiplies tenfold per generation (29).
Whereas foci often result from within-canopy spread of disease, new foci are
usually initiated by propagules that leave the canopy temporarily, drifting in ed-
dies of air, to be deposited again some distance away in the same field or just
over the fence or ditch, into the next field. Experimentation on field-to-field spread
of disease is difficult, expensive, and usually unethical. A mock-up experiment
using a miniaturized design with a source field and target fields showed that focal
spread and between-field spread are two distinct processes, with different scales
of distance and different frequencies (28). The same was found in a potato growing
area with Phytophthora infestans (53). Circumstantial evidence from various
pathosystems is in agreement with that view.
Simulation models show that two mechanisms of spread, one with short dis-
tance and high frequency and the other with long distance and low frequency, are an
optimal strategy for a polycyclic foliar pathogen (52). The point had already been
made by Vanderplank (36) who stated that short-distance spread serves the mul-
tiplication of the pathogen with the penalty of self-destruction by host depletion,
whereas long-distance spread was needed to find new hosts.
A combination of descriptive epidemiology using records of introduced patho-
gens, descriptive regional epidemiology, and small-scale experimentation showed
that plant disease spread takes place at more than one scale of distance. Distance
must be characterized by a “distance constant,” “critical distance,” or “mean free
path” (52), in analogy to the “time constant.” Whereas the “distance constant” of
foci is in the order of 1 m, “jump spread” within crops is in the order of 10 m,
and between crops in the order of 100 m. The “distance constant” of continental
spread must be expressed in 1000-m units. Can one model really describe disease
spread at so many scales of distance?
?
Time
“Polycyclic disease” of foliar pathogens has been so well studied that many pub-
lications do valuable gap-filling without contributing new ideas. One notable

exception is the renewed thinking on lesion growth, an underestimated parameter.
Bergamin & Amorim (3) argued that pathosystems in the tropics depended more
on lesion growth than in the temperate zone. The point is worth considering in
detail. At one time, we in the temperate Netherlands wondered why a wheat stripe
rust epidemic continued to develop during a prolonged dry spell without dew, and
hence without reinfection. With the primitive simulation technique then available
about 1980, we found that about 50% of the epidemic progress could be attributed
to semisystemic lesion growth and the other 50% to the establishment of new
lesions.
Polycyclic disease, with dispersal of propagules as an essential element of
the monocycle, is well documented in annual crops. We may think of rusts and
mildews, but also of aphids, white flies, and planthoppers as injurious agents.
These insects also transmit viruses, but should we consider these viruses as poly-
cyclic pathogens? I doubt it. In the case of early infections of barley yellow dwarf
virus in barley, one can recognize the flight path of the transmitting aphid. In such
cases, the virus is a polycyclic pathogen, but is it in all cases? A single wheat
stem with a foliar area of 100 cm2 may carry 1000 mildew lesions but it represents
only one virus lesion. Is the concept of polycyclic disease applicable when a lesion
coincides with a plant?
Monocyclic and polycyclic have been useful terms, but, apparently, they cannot
be applied to all diseases. Soilborne diseases are another point in case. Even useful
concepts have limited applicability. A concept has a domain of validity. Scrutiny
of the borders of such a domain will pay off.
Polyetic disease covers many years. Stripe rust on wheat may multiply by a
factor 1010 during a single season, and be reduced by a factor 1010 during the next
off-season. If, however, the reduction factor is only 108, the net result is a build-up
of inoculum so that every following year the epidemic is worse than the preceding
year. Such phenomena happen, certainly in soilborne diseases, but documentation
is poor. Difficulties arise with diseases of perennials where the pathosystem is
clearly subjected to seasonal cleanup. Coffee rust (Hemileia vastatrix) in Brazil
builds up to levels that are sometimes very damaging, but the next season it begins
again from scratch. The decline of an annual epidemic at the end of the season
10 ZADOKS
has received scant attention (19). More research in polyetic disease is needed,
including the annual disease decline or epidemic regress. Information on this
score will eventually help to avoid surprises.
Quantitative studies in polyetic disease are quite rare. The methodology is un-
derdeveloped and protocols for experimentation are practically nonexistent. Ex-
ceptions are the long-term agronomy experiments as at Rothamstead Experimental
Station, England (20), and the classical lattice experiments once used in nema-
tology. The phenomenon can be illustrated by means of simulation, provided
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sufficient empirical parameters are available. Analytical mathematics have been
applied to polyetic pandemics (34). Important work on polyetic disease caused
by potato cyst nematodes in potatoes is in progress in The Netherlands. Using an
enormous data base and a sophisticated probabilistic approach, this work provides
the farmer with useful management alternatives, among which are chemical con-
trol, partial chemical control, crop rotation, and use of appropriate cultivars with
specific and/or partial resistances (2).
Diversity
Diversity has many faces. One face is the multiplicity of pests and diseases in a sin-
gle crop. Farmers encounter this diversity daily, as they have told me emphatically.
EPIPRE is one answer, though not necessarily a definitive one. Agroecosystems
analysis, as taught in the Farmer Field Schools of the FAO Programme (see below),
is another valid answer.
Another face is diversity between crops. This refers to the mosaic pattern of
different crops within a region, and it should include managed noncrop vegetation,
bunds, verges to roads and ditches, rough and wastelands, and natural nonmanaged
vegetation. With respect to spatial diversity, phytopathology and entomology seem
to stay in opposition to each other. The maintenance of environmental diversity in
the surroundings to fields is crucial to conserve the beneficials that help to control
insect pests. The best demonstration is the story of spiders in and around rice fields,
fast migrants with a voracious appetite for plant and leafhoppers (14). It would
be interesting to come to grips with the underlying problems of how to manage
so-called nonproductive farm areas.
Two problems might be addressed systematically. One is the influence of the
environment of a field on diseases and pests in that particular field. How large
should a field be to prevent pathogens residing outside the field from infecting
the center of the field? How small should a field be to allow beneficials living
outside the field to reach the center of the field in time to be efficacious? The
other is how to design the environment of the field to be least threatening and
most profitable? Should the bunds between the rice fields be broad and covered
by asphalt to avoid hosting any living organisms, weeds included? Should they
be narrow and mud covered, which is good against rats but provides no refuge
to spiders when there is no rice in the fields? Should a refuge for beneficials be
long and narrow, similar to the highly praised field hedges in traditional European
landscapes? Or should the refuge be a village with its gardens and a rich variety
of trees, as often seen on Java in Indonesia (31)?
Modern nature conservation and landscaping in highly industrialized coun-
tries has to cope with the fragmentation of the landscape by construction, roads,
railways, and waterways. The remaining biotopes may become too small for the
survival of various species of plants and animals that were once common and now
are rare or even extinct. If biotopes become too small and too far apart, species
become extinct in each biotope separately and the usual recolonization from one
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biotope to the other is no longer possible, e.g. because traffic on the highway
separating two biotopes kills the animals that attempt to cross. The connectivity
between a source and a target population is expressed as the function of individuals
leaving the source and arriving at the target (37).

Interestingly, a typical separator, the Dutch railway system, has adopted a good
conservation protocol and thereby also become a good connector (8). Some 1000
of the 1400 plant species in The Netherlands live along the rails, together with
innumerable and often highly specialized pathogens and parasites and the even
more specialized elements of the third trophic level.
We see two sides of the same coin, called habitat fragmentation. We want to
enhance one species, the beneficial one, be it bird, spider, or fungus. At the same
time we want to constrain another species, be it planthopper, weed, or nema-
tode. Whereas nature conservation and natural biological control require biotopes
(refuges) with maximum connectivity to promote desirable species, pest and dis-
ease control want to minimize connectivity to reduce the spread of noxious species.
Mathematically, the two approaches are identical.
The urgency of nonchemical crop protection by avoidance and natural biological
control and the urgency of new nature conservation technology (yes, technology
is involved in improving connectivity by digging toad tunnels and building game
bridges; it works!) is of the same order. We talk about relatively small scales, say
a distance constant of 1 km and a time constant of 1 year. Much scientific effort
will be needed in the future to harmonize conflicting demands on land use, e.g. a
benevolent nature in an industrial environment.
A SOCIOECONOMIC DIMENSION
Answers to classical questions such as why so many New York policemen are
Irish or why the English drink tea are rooted in plant disease epidemiology. Plant
diseases affect people in many ways.
Crop Loss
The crop loss theme, triggered by FAO in 1967, fascinated me as a non-economist.
EPIPRE taught me about farm accounts and brought me to national accounts of
crop protection. Such approaches, which disregard externalities, are no longer
12 ZADOKS
satisfactory. The approach taken by welfare economics, broad enough to incorpo-

rate social dimensions, is more satisfactory since it does consider negative exter-
nalities (16, 39). New projects on crop protection at the national or international
level should be embedded in a broad economics background (23).
Epidemiology has become strong in one-crop-one-disease issues, the simple
pathosystem approach. Farmers seldom deal with one problem at a time. The time
has come to tackle multiple pathosystems, whereby several pathogens and pest
organisms are dealt with simultaneously. EPIPRE was just an early attempt with the
?
juxtaposition of harmful agents, but without integration under due consideration
of interactions between them. Crop physiology, supported by dynamic simulation,
provides an avenue since all disease effects can be expressed in terms of measurable
injury to roots, stems, foliage, or reproductive organs of plants (1). The step from
monoetic to polyetic approaches must be made. Nematologists paved the way (2).
In soilborne diseases and pests, this year’s population increase may cause the next
year’s damage.
Sustainability
My wartime farmwork and summer job on a Swiss mountain farm between high
school and university acquainted me with the way of life of farmers and what
their thinking is. The early stripe rust work and the later EPIPRE work was
done for farmers, paid for by farmers, and executed with the help of farmers,
hundreds of them. Farmers were a part of my life. The international work, in-
cluding consultancies and reviews, brought me to countless farms in the tropics.
Among these were large estates growing rice, bananas, or oil palms, and numer-
ous smallholders growing rice, peanuts, cocoa, coffee, and a plethora of secondary
crops.
In the developing world the direction of change may differ from that in the de-
veloped world, though both worlds should move toward increased sustainability.
Farmers in the developing world had to be freed from some of society’s pres-
sures. Governments pushed the Green Revolution technology, which backfired
by overexploitation and pollution of natural resources. In the wake of the Green
Revolution, pesticides companies made handsome profits (24).
As a reaction to government and industry pressures, the “farmer first” (6) school
of thought sprang up, with emphasis on nonchemical crop protection. The FAO
Programme embodied another philosophy and applied methods from adult edu-
cation: a farmer-oriented approach aimed at empowerment of the farmer. The
Programme developed the Farmer Field School (FFS) as an instrument of exten-
sion and empowerment. Its objective was to allow the farmers, individually and
collectively, to gain sufficient knowledge of rice field ecology to make their own
decisions with confidence. As the message was brought in the farmers’ own lan-
guage, and fitted their attitudes and perceptions, irrespective of educational level,
the results were quite positive. Farmers, even if illiterate, are good observers, keen
to understand the workings of their rice ecosystems. Among South-East Asian
farmers I met, the FFS approach raised enthusiasm similar to what EPIPRE had
once done in The Netherlands. It is hoped that the empowered and self-confident
farmer will be able to resist outside pressures, including that for unnecessary use
of pesticides, and to voice his needs for research.
In the western world, there were new social pressures for farmers, as exempli-
fied by adoption of “integrated agriculture” as the new panacea in The Netherlands
(48). Integrated pointed to both integration of methods and integration of objec-
tives. The former, leading to IPM with a minimized input of pesticides, met with
?
success and disappointment. The latter, involving reconsideration of the objec-
tives of agriculture, created a mental space for cleaner production methods, a less
polluted environment, the restoration of biodiversity, better nature conservation,
pleasant landscaping, and recreation of townspeople. An abstract concept had to

be given legs. To reduce pollution, levels of nitrogen fertilizer were lowered. As a
consequence, epidemics developed slower, which in turn meant that the number of
pesticide treatments could be reduced. Yields were generally somewhat lower than
with current agriculture but the financial returns per hectare hardly diminished. In-
volvement in the development and the scientific supervision of a large experiment,
“Development of Farming Systems,” in The Netherlands brought new inspiration
(47). The early beginnings led to a movement of change in The Netherlands, where
many farmers try to be smart and gain at least as much money as before but with
far fewer external effects. In other words, they strive for economic and ecological
sustainability.
Choices
Each nation has the agriculture it deserves, one option out of many placed along
the line connecting high external input agriculture (HEIA) over low external input
sustainable agriculture (LEISA) to organic farming. The choice largely determines
the type of crop protection available to the nation. Whatever the choice, there will
be consequences, both positive and negative. In a continuum of options, only a
few stand out as being feasible and profitable.
Such options can be identified by means of scenario studies. The trick is to
identify obviously different but equally feasible scenarios, each responding to a
typical political program, and to carefully calculate the consequences of each.
For the European Union, the report Ground for Choices reasons that only four
distinct scenarios are feasible. In all four, the twelve member countries of the
European Union can feed themselves, but the crop protection implications differ
widely (40). Epidemiology can assist in modeling crop protection risks incurred
by a chosen solution.
I see no single and universal solution to the problem of choosing from available
options. In an affluent, industrialized country such as The Netherlands, the choice
may be for more nature and diversity. The European Union has its roots in a choice
for relatively small family farms. In the United States, the lost prairies with their
wide vistas may still dominate the minds of planners. In South Asia, with only
14 ZADOKS
1 hectare of land per inhabitant and a teeming population, the choice must be
different. In some parts of the world, small-scale agriculture may be desirable to
avoid the migration of rural people to overpopulated towns. A thorough knowledge
of epidemiology may help to shape the chosen solution.
WHERE TO GO?
?
The three themes discussed above, with the additional socioeconomic dimension,
illustrate the development/history of a field-oriented, international epidemiologist.
They lead to some reflections which, it is hoped, will be picked up by future students
of epidemiology. Whether the label epidemiology fits their exercises remains to

be seen.
For me, the passion is agriculture and the tool is epidemiology. I see many
reasons to develop and sharpen that tool. Experimentation in the classical sense
is not impossible but it is expensive. Empirical knowledge, as distinct from ex-
perimental knowledge, can be gathered by analyzing what nature offers and, once
the mechanics are known, the modelers can synthesize such knowledge. The pro-
cedure will become more difficult the larger time and distance constants are, and
the more diversity is incorporated. I see a great future for a fundamental approach
to problems at high levels of integration, but teamwork will be needed among
researchers, disciplines, and institutions (27). Phytopathology journals must open
up their pages to nontraditional points of view, which now seems anathema, or
they will loose clientele.
The space-time continuum is not yet adequately explored, particularly not for
soilborne diseases. Great originality is demanded from the mathematically in-
clined epidemiologists and from experimenters to study dispersal at various scales
of distance, including capricious dispersal by humans, and to investigate polyetic
effects. Diversity due to discontinuities in space and time needs more attention,
since discontinuities are not empty, nor are they epidemiologically neutral. On the
contrary, discontinuities offer space and time for a multitude of synergistic and
antagonistic organisms. The decline of epidemics is a useful topic per se, but the
mathematical study has hardly begun (18).
The real challenge to epidemiologists is the diversity of the agroecosystem, es-
pecially diversity managed for optimum crop protection (25). The methodology to
tackle the problem is poorly developed at best. Small-scale replicated experiments,
Fischer style, will only be a minor technique. The survey will gain in importance
(30). Opportunistic studies of nature’s own experiments, incidental and capricious,
often one time only, will be vital (53). Scenario studies will become more promi-
nent, of course supported by solid modeling, to synthesize alternative views.
In science the road follows the traveler. That road through space will take time
because it crosses a diverse landscape, with rocks to climb and pitfalls to avoid.
Don’t get lost in impenetrable diversity. Look and listen with open eyes and ears,
and think with an open mind. You will not arrive at the “end of science” (11).
Visit the Annual Reviews home page at http://www.AnnualReviews.org
LITERATURE CITED
1. Bastiaans L. 1993. Understanding yield re- EPIMUL, a Simulator of Foci and Epi-
duction in rice due to leaf blast. PhD thesis, demics in Mixtures, Multilines and Mos-
Wageningen Agric. Univ. 127 pp. aics of Resistant and Susceptible Plants.
2. Been TH, Schomaker CH. 1998. Quantita- Wageningen: Pudoc. Simulation Monogr.
?
tive studies on the management of potato 50 pp.
cyst nematodes (Globodera spp) in the 13. Kenmore PE. 1991. Indonesia’s Integra-
Netherlands. PhD thesis, Wageningen. 319 ted Pest Management—A Model for Asia.
pp. Manila: FAO 56 pp.

3. Bergamin Filho A, Amorim L. 1996. 14. Kenmore PE, Cariño FO, Perez CA, Dyck
Doenças de Plantas Tropicais: Epidemi- VA, Gutierrrez AP. 1984. Population reg-
ologia e Controle Econômico. São Paolo: ulation of the rice brown planthopper (Ni-
Ceres. 299 pp. laparvata lugens Stål) within rice fields in
4. Borlaug NE. 1956. The development and the Philippines. J. Plant Prot. Trop. 1:19–
use of composite varieties based upon the 37
mechanical mixing of phenotypically sim- 15. Kenmore PE, Litsinger JA, Bandong JP,
ilar lines developed through backcrossing. Santiago AC, Salac MM. 1987. Philip-
Rep. Int. Wheat Rust Conf., 3rd, Mexico, pine rice farmers and insecticides: thirty
pp. 12–18 years of growing dependency and new op-
5. Chambers R, Pacey A, Thrupp LA. 1989. tions for change. In Management of Pests
Farmer First. Farmer Innovation and Agri- and Pesticides. Farmers’ Perceptions and
cultural Research. London: Intermed. Practices, ed. J Tait, B Napompeth, pp. 98–
Technol. Publ. 218 pp. 108. Boulder: Westview Press. 244 pp.
6. Cook RJ, Veseth RJ. 1991. Wheat Health 16. Kishi M, Hirschhorn N, Djajadisastra M,
Management. St. Paul: APS Press. 168 pp. Satterlee LN, Strowman S, Dilts R. 1995.
7. Eriksson J, Henning F. 1896. Die Getrei- Relationship of pesticide spraying to signs
deroste, Ihre Geschichte und Natur sowie and symptoms in Indonesian farmers.
Massregeln gegen Dieselben. Stockholm: Scand. J. Work Environ. Health 21:124–
Norstedt & Söner. 463 pp. 33
8. Ernst WHO. 1998. Invasion, dispersal and 17. Kiyosawa S. 1976. A comparison by sim-
ecology of the South African neophyte ulation of disease dispersal in pure and
Senecio inaequidens in The Netherlands: mixed stands of susceptible and resistant
from wool alien to railway and road alien. plants. Jpn. J . Breed. 26:137–45
Acta Bot. Neerl. 47:131–51 18. Kocks GC, Ruissen MA, Zadoks JC. 1999.
9. Habtu A, van den Bosch F, Zadoks JC. Survival and dwindling away of Xan-
1995. Focus expansion of bean rust in cul- thomonas campestris pv campestris in soil.
tivar mixtures. Plant Pathol. 44:503–9 Eur. J. Plant Pathol. In press
10. Feekes W. 1941. De tarwe en haar milieu. 19. Kranz J. 1968. Eine Analyse von an-
Versl. Tech. Tarwecomm. 12:523–888 nuellen Epidemieen pilzlicher Parasiten. II.
11. Horgan J. 1996. The End of Science. Fac- Qualitative und quantitative Merkmale von
ing the Limits of Knowledge in the Twi- Befallskurven. Phytopathol. Z. 61:171–
light of the Scientific Age. Reading, MA: 90
Helix/Addison-Wesley. 308 pp. 20. Leigh RA, Johnston AE, eds. 1994. Long-
12. Kampmeijer P, Zadoks JC. 1977. term Experiments in Agricultural and Eco-
16 ZADOKS
logical Sciences. Wallingford, UK: CAB Use of categorical information and corre-
Int. 428 pp. spondence analysis in plant disease epi-
21. Luo Yong, Zadoks JC. 1992. A decision demiology. Adv. Bot. Res. 21:213–40
model for variety mixtures to control yel- 31. Soemarwoto O. 1964. Rural ecology and
low rust on winter wheat. Agric. Syst. development in Java. In Unifying Con-
38:17–32 cepts in Ecology, ed. WH van Dobben, RH
22. Manners JG. 1969. Presidential address. Lowe-McConnell, pp. 275–81. The Hague:
The rust diseases of wheat and their con- Junk. 302 pp.
?
trol. Trans. Br. Mycol. Soc. 52:177–86 32. Thomas M, Waage J. 1996. Integration of
23. Oskam AJ, Vijftigschild RAN, eds. 1997. Biological Control and Host-Plant Resis-
Policy measures to control environmen- tance Breeding: A Scientific and Literature
tal impacts from agriculture. Concerted Review. Wageningen: CTA. 99 pp.
Action AIR3-CT93-1164. Workshop Pes- 33. van den Bosch F. 1990. The velocity of spa-
tic., Wageningen, The Netherlands, Aug. tial population expansion. Leiden, Nether-
24–27, 1995. Proc. Discuss. Wageningen, lands, PhD thesis. 161 pp.
Dep. Agric. Econ. Policy. 629 pp. 34. van den Bosch F, Metz JAJ, Zadoks JC.
24. Oudejans JHM. 1999. Studies on IPM pol- 1999. Pandemics of focal plant disease, a
icy in SE Asia. Two centuries of plant pro- model. Phytopathology 89: In press
tection in Indonesia, Malaysia and Thai- 35. Van der Plank JE. 1963. Plant Diseases:
land. Wageningen Agric. Univ. Pap. 99- Epidemics and Control. New York: Aca-
1:1–311 demic. 349 pp.
25. Pickett CH, Bugg RL, eds. 1998. En- 36. Van der Plank JE. 1975. Principles of Plant
hancing Biological Control. Habitat Man- Infection. New York: Academic. 216 pp.
agement to Promote Natural Enemies of 37. Verboom J. 1996. Modelling fragmented
Agricultural Pests. Berkeley: Univ. Calif. populations: between theory and appli-
Press. 422 pp. cation in landscape planning. PhD thesis,
26. Robinson RA, Chiarappa L. 1977. The In- Leiden Univ. 119 pp. Sci. Contrib. 3, DLO-
ternational Program on Horizontal Resis- Inst. Bos-Natuuronderz.
tance. FAO Plant Prot. Bull. 25:197–200 38. Verhaar MA. 1998. Studies on biolog-
27. Rossing WAH, Jansma JE, de Ruijter FJ, ical control of powdery mildew in cu-
Schans J. 1997. Operationalizing sustain- cumber (Sphaerotheca fuliginea) and rose
ability: exploring options for environmen- (Sphaerotheca pannosa) by means of my-
tally friendly flower bulb production sys- coparasites. Wageningen, PhD thesis. 164
tems. Eur. J. Plant Pathol. 103:217–34 pp.
28. Sache I, Zadoks JC. 1996. Spread of faba 39. Waibel H, Fleischer G. 1998. Kosten
bean rust over a discontinuous field. Eur. J. und Nutzen des Chemischen Pflanzen-
Plant Pathol. 102:51–60 schutzes in der Deutschen Landwirtschaft
29. Savary S, Zadoks JC. 1990. Analyse des aus gesamtwirtschaftlicher Sicht. Kiel:
composantes de l’interaction hôte-parasite Wisssenschaftsverlag Vauk. 254 pp.
chez la rouille de l’arachide. II. Mesure de 40. WETENSCHAPPELIJKE RAAD VOOR HET
la résistance intermédiaire par un essai en REGERINGSBELEID. 1992. Ground for
micro-parcelles. With translation: Analy- choices. Four perspectives for the rural ar-
sis of host-parasite interaction components eas in the European Community. Rep. Gov.
in groundnut rust. II. Measurement of inter- 42. The Hague: Netherl. Sci. Counc. Gov.
mediate resistance using a micro-plot trial. Policy. 144 pp.
Oléagineux 44:215–24 41. Zadoks JC. 1961. Yellow rust on wheat,
30. Savary S, Madden LV, Zadoks JC. 1995. studies in epidemiology and physiologic
specialization. Tijdschr. Plantenziekten 67: Year Period 1980–1984. Wageningen:

69–256 Pudoc. 90 pp.
42. Zadoks JC. 1972. Methodology of epi- 48. Zadoks JC. 1990. Management of wheat
demiological research. Annu. Rev. Phy- diseases in Northwest Europe. Can. J.
topathol. 10:253–76 Plant Pathol. 12:117–22
43. Zadoks JC. 1981. Mr. Duhamel’s 1728 49. Zadoks JC. 1993. Crop protection: why
treatise on the violet root rot of saffron and how. In Crop Protection and Sus-
crocus: “Physical explanation of a disease tainable Agriculture, ed. DJ Chadwick, J
?
that perishes several plants in the Gastinois, Marsh, pp. 48–55. Chichester: Wiley. 285
and Saffron in particular.” Meded. Land- pp.
bouwhogesch. Wageningen 81-7:1–31 50. Zadoks JC, Chang TT, Konzak CF. 1974.
44. Zadoks JC. 1985. On the conceptual ba- A decimal code for the growth stages of
sis of crop loss assessment: the threshold cereals. Weed Res. 14:415–21
theory. Annu. Rev. Phytopathol. 23:455– 51. Zadoks JC, Schein RD. 1979. Epidemiol-
73 ogy and Plant Disease Management. New
45. Zadoks JC. 1988. A salty act. Notes York: Oxford Univ. Press. 427 pp.
on the dispersal of Uromyces limonii. Z. 52. Zawolek MW, Zadoks JC. 1989. A phys-
Pflanzenkr. Pflanzenschutz 95:384–91 ical theory of focus development in plant
46. Zadoks JC. 1989. EPIPRE, a computer- disease. Wageningen Agric. Univ. Pap. 89-
based decision support system for pest and 3:1–229
disease control in wheat: its development 53. Zwankhuizen MJ, Govers F, Zadoks JC.
and implementation in Europe. Plant Dis. 1998. Development of potato late blight
Epidemiol. 2:3–29 epidemics: disease foci, disease gradients,
47. Zadoks JC, ed. 1989. Development of and infection sources. Phytopathology 88:
Farming Systems. Evaluation of the Five- 754–63

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REFLECTIONS ON SPACE, TIME, AND DIVERSITY

Key Words complexity, connectivity, farmer, focus, methodology

Space, Time, Diversity 3

Inspiration From Administration

then feared as much as admired, contributed to the visibility of EPIPRE. Several

Space, Time, Diversity 5

The Call of International Agriculture

Space, Time, Diversity 7

The Crop Loss Conference organized by FAO in 1967, at which I repre-

into a manageable program by Robinson (26). Slowly, Vanderplank’s imaginative

SPACE, TIME, AND DIVERSITY

Space, Time, Diversity 9

lications do valuable gap-filling without contributing new ideas. One notable

Space, Time, Diversity 11

leaving the source and arriving at the target (37).

satisfactory. The approach taken by welfare economics, broad enough to incorpo-

Space, Time, Diversity 13

pleasant landscaping, and recreation of townspeople. An abstract concept had to

of epidemiology. Whether the label epidemiology fits their exercises remains to

Space, Time, Diversity 15

Visit the Annual Reviews home page at http://www.AnnualReviews.org

pp. Manila: FAO 56 pp.

Space, Time, Diversity 17

specialization. Tijdschr. Plantenziekten 67: Year Period 1980–1984. Wageningen:

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