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The concept ofwholeness in nature has its scientific foundations in the theory
of ecosystems. When agriculture came into being, parts ofnatural ecosystems
were replaced by agro-ecosystems. The differences between natural and man-
made ecosystems in complexity and stability, in energy supply, and in trophic
structure are outlined. The ecological view of plant disease gives pathogenic
fungi a natural place in ecosystems. Disease exists in natural host populations,
usually in the endemic state; it becomes epidemic in uniform pioneer vege-
tations. Crops are just like the latter and thus favor epidemics. With effective
control systerns, crop diseases tend to become endernic, yet still causing
losses that may be intolerable, and still necessitating conscious efforts to
keep them at low leveI. Agro-ecosystems developed in pace with social and
economic developments; concomitantly, the epidemiologic situation devel-
oped into what it is now. A short outline of agro-ecosystems today and their
diversity is given, and their epidemiologic implications are indicated.


I (). r. 1 The Concept of Wholeness

llu 11'1'11) ecosystem represents the concept 01 wholeness in naturc 111111
IIII~ d,'vt·loped in biologic thinking since about 1900. It reflects 11hll,.h
Itll'lI 111"l'ology: that in a natural community (Section 7.1.2), bel'IIII"" tI'
111 •. 111111'"lt'rclations among organisms and between organisms 1I11t1III1~il
1II1111h vuvlroument, a change in one component wi11have reVl'1h"1111
1'111'1111 11I1I1Il~h()lItthe community. A natural community 01' 1111'1111'''111
I"''''H'~'U'II nurlhutcs of a system: components and functionnl 1,,111111111
IIIIIIII~. 1IIIIIIHIIH'lIls. The community is the next higher level nl 1IIIIIIIuh
I I,/fi unol' Iht; poplllllllolI 111111
11111111."1101 11/11/11 11,11111111 \\'111111()ur use must be wise and our manipulations muxt l'l\lll~1I11I
1I11"l lt's, plant and animnl, OllllpylllH 11jlllllllllllll 11111 111" II~ hllsbandl11an, despite the pressure of growing populatioux 111111
'!lIlIlIlly, such as the cornmunlry 01 olf&jIlIlIlIlIM!lV/1I1-l 111 11111 rtlllll ti 011bchalf ofthem. Only by understanding the natural ecosystem
11111111I11111. I i nllcd a biocenosis. Cornmunities 01' IIII'I-Il'Ni:t.c 1111' 11111wc slIlisfy ali the demands and responsibilities that are ours.
lnluw). The largest single community is 11ll'IJIO,l'fJhl'I'l' , Ikosystcms have evolved, that is, progressively changed, to incIudc
1/"11~o expccially the farming populations, are part» 01 1IIIINlderable complexity, as measured by various indices. Man, through
1IIIIIIIIIIIies, both social and ecologic. IIHIlculture, interrupts or stops this evolution, and agricultural systems are
jlOlu 111"01' an ecosystem consist of the abiotic-cIimate alld ItINScornplex when measured by the same indices. Some agricultural prac-
H" 1111'hiotic-the autotrophic, heterotrophic, and decay 01 Ikcs are severely damaging to the natural world or disregulate natural
IId. II t 1IIII0l1samongcomponents are seen when analyzingenergy tuhilizing mechanisms. Epidemics of plant disease are often a result of
illl IlIdns, diversity patterns in time and space, nutrient cycles. 1111I1disregulation. Is there a middle way, a moderate way, by which
11101II uud evolution, and control (Odum, 1971, p. 8). The com Iwiculture might cause little or, at most, acceptable levels of damage? Can
111íhcr large or small, has a definable taxonomic composition, li we rninimize damaging disregulations of natural control mechanisms? In
ti l/tll' uppearance, and a definite trophic organization. Cornrnuni- Chapter l l , we suggest concepts and practices we think willlead to more
0111II'osystems, are the basic functional units of the natural world. huelligent and efficient plant disease management.
/11, \ iurvc at least the minimal numbers and kinds of interrelations to
I, 11ftVI'lndependence through interdependence.
I /lu ecosystern concept is useful in identifying and understanding thesc 10.1.3 Succession, Clímax
11IlIliolls and their bases. The concept helps to understand agriculture as Only 200 years ago the western world believed that the earth had been
11systern, the natural place and function of plant disease, the evolution of .reated as it was. Modern sciences-geology and biology-see it differ-
fllI,hogenicity and of resistance, the effects of agricultural or man-made sntly: the world has always been changing and changes still. Demonstra-
ccosystems on host-parasite relations, and the role of man as a part of (ions of evolution have often been difficult, as evolution is a nonrepeatable
processo Ecologists found their way by observing what happens to a site
In Section 7.4.1, the pathosystem per se was introduced as an item. (hat has been seriously disturbed by nature or man; they studied repeatable
Here, we regard the pathosystem only as a subsystem, as a component of processes. From these studies have been discerned sequences in time
a larger ecosystem. As an identifiable component it has, on the one hand, Icading from a pioneer community through a series of developmental
characteristics of its own, and on the other hand, it undergoes the effects stages to a more or less stable system sometimes called "rnature" (van
of and responds to other components of the ecosystem such as cIimate Dobben & Lowe-MacConnell, 1975, p. 155). The sequences involve
and, foremost, mano orderly processes that produce changes in the number and kind of species,
lhe population structure, and the community processes at the disturbed
10.1.2 Complexity, Change, and Stability Nite. The rates, limits, and patterns of these changes are highly subject
10 lhe physical environment; a community of populations modifies its
Most major biomes,like tropical rain forests or northern deciduous foresrs OWII environment. Habitat changes make it more difficult for some and
have been as they are now for a long time. Some, like the tundra, have I'il'lkl' for other species to establish themselves and survive. This process
rnuch smaller plant and animal densities and varieties oflife forms. Biomes 111dill't:tional, nonrandom change is called succession. Generally, but not
also vary in the complexity ofinteractions among populations, for instance, 111"\ I',pmrily, as succession continues, the community becomes more
material cycIes and energy flow. Changes are constantly occurring; lhe llllllpll'" und diverse.
stability is dynamic rather than static. The pace of change may be dillcren! I)IVI'I'1l1yis subject to several definitions.Lt may be the number of spccics
in different biomes. We will try to relate some of these 111111lt;1'1I 10 111:1111111 111'01-1,
the variety of life forms in the community, the number and
agricuIture and epidemics in this chapter. 1""'"Mlly uf'rclations between species in a community, or a cornbination of II1
We start from the premise that naturallaws which govern nnture l11uSI 11111111'o 1'1IIll1gists measure diversity (Section 4.2.3), but these measures are
be observed by man if he is to produce food and fiber for ti growing 11111 !I'!t-vIIIII hcrc. Since succession usually leads to diversity, and mature
population while at the same time maintaining or at Icast nor irrcparably 111111111111111111/'1
nppcar stable, the idea developed that complexity yields
damaging the health of the biosphere. We are users, manipulutors of th 111111111\ WI'II' thut the case, then almost ali of man's perturbations of

294 295
m1\l1""""""' r i i.f ti" .fW'AWP l

I~I" 1111111111 nIlKYK(1!1l1S01' lIgro-eCOsYS((!/IIS. \I is I!vldl'lIl

IlIlii!1 111111111 IIlIlq"l!, is to be regarded as an integrated, nallll'lIl \.'1"'1
IIdlll, IIlIlSt 11\'\1'."'"1111 dl'I 1I11~tl ~lllhlllly. Mllvh 111 11
, uf t'llIl'IyNtOtllS, ir his role is to be fully understood" (Jacobs, I\)'/~,
Ílilll ut the rcccur cuvluutunutul 11\\111 I'111'1/1 H 111wl'sll'llI
" ••,,""1\1 (111111 Ihls idea. Rcccutlv, 111111'1111"1'11 1I1»lIml 111111 tllt,
11\I! 111114 \'IIHlly overlooked fact we will continually emphasize.
í "I 1 11:l:hHracter ofan agro-ecosystem has numerous determinants:
111'11, 111 Whiuakers (197~, (l. l(tl») WllnlN : "('omplt-\ 11111
IIlllIfI dlllHllic-edaphic factors, native flora and fauna, adapted plants
111\111\purticularly vulnerablc to dlsllll'hlllH:llM sucl: IIN lhe)'
11'-'IIIIIIIIIIN,tino tnan with his social, economic, and cultural activities in
Ili 1111\11 111their evolution; they may be dynnmicully fragilc."
i11IH.lllllily 01' complex ecosystems must be bccausc lhe envi
lho 1'11111111"present. The natural deciduous forest biomes of Europe ands and
illl 1II NOl'lh America became mixed farrriing areas, extensive grassl
(í lntlvcly reliable during their development and rernains 80.
IWIIIIII l ercal and grazing areas, Oriental flood plains becatne rice areas.
IlIi, nulonale, simpler systems might be expected to be less
I 1111111' enduring. \I 1111'IIllln-maintained agro-ecosystems. They stay as we know them
lHtlVIll'l'lIl1se of the continuous application of our agricultural techniques.
1Ii'IIII 01' ecological succession uses the concept of the climas
I lhe final community which, whatever its degree of diversity, MIIII IlIllI his activities replace natural components and functions.
\w n_cCOsystetns are usually less complex than the natural ones they I
II 110 1I1l1tllalingand in equilibrium with its physical environment, with
III'IIIIII\t. They are less diverse in numbers and kinds of species andnsso \
11'I IllIhllily derived from equilibrated interactions among its severa I
1111 VI't'l!wer interactions among species populations. The largest populatio
"I dhms. Each biome would, under this idea, be moving toward a
1111IIIIIlbers are usuallv those managed by mano Unwanted species beco me
11.1111íoristic climax community coveringalarge areaofthe earth 's surface.
WI'CUS" or "pests" and are eliminated or controlled in numbers. Plant
\ 1 IlIls point the theory oversimplifies, for within each biome there are
,,1.11 \'1' where local variations, particularly of water, soil, and topography,
are such an unwanted group. Agro-eCosystems and the plant 1i \
"",m'atioOS in them have attributes that often increase the probability of
l'itlVént the community from reaching its theoretical uniformity. Such
,,11I1l(disease. These attributes are the direct result of man's effort to alter
\ nriants within a climatic clímax are called edaphic climaxes. The theory,
1IIIImal systems to better suit some of his purposes. It is worth our while
Ihcn, allows for specific variation within generally similar areas of climate,
III Idcntify what man has done, to examine this history. In order to under-
vegetation, and fauna. If succession can be changed in result or rate in
IlIlId why various changes occurred we have analyzed in Chapter 7 what
such long-acting natural ways, it follows that it may be modified also by
1111111 has done, identified the attributes, and examined the history from the
short-terrn variations in major limiting factors. A community may be badly
VIl'wpoint of crop husbandry. Here we will restate our views in more general
damaged by natural occurrences, like wildfire and flood. Then, succession
begins again at whatever development leveI remains after the catastrophe. Ill\systems terminology.
The activities of man and his animais are analogous interruptive factors.
Disregarding locally catastrophic effects of man, large areas of the earth's
\!l \.5 Energy Subsidies and Stability
surface have long been subject to perturbation by man, and succession in
these are as has been altered or stopped. Nonetheless, when man ceases .I\\tlr cnergy, transformed into chemical energy by photosynthesis, runs
to till and plant or to graze his animais, succession processes reestablish, 11\1l"Il~ystems. Most natural ecosystems have nothing eis e but the daily
"1'1'1y of solar energy. Other ecosystems, [ike tidal marshes or annua\ly
and the community imrnediately begins to change: the area once again
moves on toward its climatic and edaphic climax. \1I11I11\lIll!dflood lands along rivers, receive additional energy from outside
IIi,II, Inrm of minerais brought in by the floodwaters. This can be regardcdll
ili 111\llllIral energy supply to the floodland ecosystem. Such floodlllll
10,1,4 Agro-ecosystems '11i\,'111'1ll5,
with their cyc1ical disturbances, have a low diversity 01' Spl'

An are a subject to regular, repetitive disturbance, Iike annual flood, may \('I!! ..•ri. they are dynamically stable.
~ll' 11I'I'llsystems with artificial inputs of minerais and energy are 1\01
have cyclic stability. Such an area is impeded in its natural succession and
1111111,1 IIII'HCfloodland ecosystems. "Many of these artificial ecosyslCtIlS
so stays in an "immature" or subclimactic state. Ecologists call such arcas
li'(1 jl'l,IIlvl'ly stable, provided certain inputs, e.g. of fertilizers, can bc
disturbance climaxes or disclimaxes. If the perturbation is caused by 111.111,
tillliillllilll 11." says Ovington (1975, p. 239). Jacobs (1975, p. 205) slall!S that
they are called anthropogenic disclimaxes. An agricultural are a that 1111111
has maintained for a long time, where he has exercised reasonable CHI'I!in
I~)"" '''V'' ems ". . . are autotrophic and very productive, ha ve • high
lIiliu' \lIIW. rllirly high stability, fairly high organizatio , but low species
regard to soil fertility and erosion, salt accumulation, and 80 on, rnuy Iw
quite stable as long as man's activity continues. It is propcr (o trcut slIl'h


I 1"ll'd 111' Nomeparameters, also low structural diversity." l'It,· lutorcunnected food chains of aweb can end at one place wilh ,Ir
111. '1111/11«\lund rapidly turns into bushland when no longe r Itild 01' pl'l.lY, the usual example, and at other places with fungal parasitcs
I lII~yNlt.:m
seems to be unstablc. "Yct in reality, high "I nhytophagous insects or with parasites of phytopathogenic fungi likc
ih 11 111 hlovcd in such simplitied systems by continous careful t'rnk-tlttum vermiculatum and Trichoderma spp. parasitizing Rhizoctonia
11111 luuunn rnanipulation" (Jacobs, 1975, p. 187). This point of salant (Boosalis, 1956).
•li hy Ryszkowski (1975, p. 124): "Cultivated tields are
IIllIIclully maintained at an early stage of succession with a EXAMPLE 10.1: The plant to bacteriophage food chain, A curious
[11 '"1". few possibilities of modifying the effect of climatic factors, Iood chain is on record, that of plant, rust, rust-eating bacterium
•• 1111 "vlly, low energy costs in the production of a biomass unit,
(Xanthomonas uredovorus), and a bacteriophage parasitizing the bacter-
11 h "111'11 cycles of mineral circulation. In these ecosystems the costs iurn (Klement & Király, 1957). !::,
III,If"/lIgtheir stability are borne by mano Man inftuences practically
I \I •• ,. IINystemprocesses."
Ultimately alI organisms die, and these beco me the substrate for many
!" II 111I marize , low-diversity systems can be very stable if they have kinds of decay organisms, thedecomposers, which break down the complex
,illll Itl1{h energy inputs 01' subsidies on a regular and continuing basis. organic molecules into simple materiais of the kind used by green plants
I., 'hlll way, croplands and managed forests are like tidal marshes in that in their nutrition. A fault of the concept is that organisms often occupy
ilu lI~duced numbers of species appear welI suited to efficiently utilize more than one levei (except for producers). Man is a good example, since
• I" 'NY subsidies. Where energy subsidies are low or nil, and the system he is at once an herbivore and a carnivore. When food webs rather than
uurinly solar-powered, best productivity and stabiJily is achieved by food chains are diagrammed, it is seen that many organisms may simul-
"'uhcr diversity. Rangelands would fit this category.
taneously occupy two or more levels.
A convenient way to show trophic levels is through the use of a pyramid
10.1.6 Trophic Levels in Ecosystems (Fig. 10.1) to represent numbers of individuais, or amounts of material or
cnergy, The pyramidal shape lets us see that because of conversion effi-
Our understanding of the place and function of components of ccosystem» ciencies and energy losses, each "higher" levei is decreased in numbers,
has been increased through the use ofthe trophic levei concept. Undcr this cnergy, or materiais processed. In each levei are many organisms of different
concept, each population in a community plays a role in the ftow of energy kinds, occupying different habitats and displaying the attributes of natural
and materiais through the system. In a rather general way, different kinds populations regarding density, dispersion, life form and age distribution.
of organisms can be separated into trophic levels 01' nourishment levels, 111 lhe natural system, there will be considerable complexity, and the
depending on the source of energy and materiais they use. The basic group uumifold relations between the component populations lead to an inter-
consists of the producers-green plants and some few autotrophic bacte- dl'Pl\ndency which, given a relatively stable physical environment, itself
ria-which are alone capable of bringing new energy into the system from 111111, ibutes to the stability of the system: the natural interrelations are
the sun through its tixation by photosynthesis and subsequent conversion \ "II,II/IY determinants in an undisturbed or natural environment.
into large organic molecules. Heterotrophic organisms depend on this
continual input. The heterotrophs are consumers and may be, rather gen-
eral1y, separated into levels. Primary consumers (heterotrophs, herbivores)
obtain nourishment directly from green plants; among them are cattlc, t IUIII/I l!l,' The ecological pyramid. Plant pathogens are primary con
insects andpathogenicfungi. Secondary consumers (hyperparasites, prcd- 1011111
ators, carnivores) obtain their major nutriment from primary consumcrs.
A food chain or food web is a diagrammatic representation of "whn
-~----- --- secOndary}
eats whom." Whereas the food chain representation has only one erul . consumers heterotrollh
point, the food web picture allows for more end points. Starting wilh 11 --~-----pnmary
particular green plant, there may be several kinds of prirnary consumer
---~- green ptants producers autotroph
and even more kinds of secondary consumers. Some sccondury (;OnSlIlIIlll
feed on other secondary consumers, so food wcbs cnn IH' </1I11t' complox

10.1.7 AlhllUlhll1 111I IlIphlC Structure in Agro-ecosyslOl1h
plll11tli, 111111 this value judgment was transferred to the modero period.
Whnt IH 11111'hll 11I11111111
systerns is not true in agrc-ccoxystem«. Considor (111111111 li-IiI.fically, a disease has usually been considered as bad, abnormal,
whnt Wlj ti•• I•• 11111nyrarnid. Much of our attention gouli 10 lho primury 1111I1 llIlIli unnatural, Plant pathologists have often seen themselves as the
flnllllll~í.lI! wlll 11111wc will use it ourselves or feed it to our unirnals. Hy "tlIIIIN nrotectors of man and his plants against an unnatural enemy.
Iltlll"t! \\'0 l'lllIl 11productive habitat and, adding weed control, substan- I \\'11 01' lhe most rightfully honored senior members of our profession
111111\' iln I0111"nther higher plant competitors. We plant in unusually high \\'1 fi,,: "The ultimate aim of plant pathology is to banish destructive plant
jICII~ili(!l1IllItI uivo the even-aged population a uniform dispcrsion in lhe 11I1I1'IIS0"(Stakman & Harrar, 1970, p. 541). Let us quest for a more
nlhlilniillll 111'llIlizers and soil amendments increase primary productivity, IIl1flll'al view.
lilll IlOl"" Id1111 nnd fungicides decrease the primary consumers competiu
lill iil,11I 1111'lhe primary production. The primary producer base !s
"n i 111I" d lu slze by density of planting, fertilization, and weed control, hu]
10.2.2 lhe Role of Fungi in Ecosystems
íi ill,oIl1lj1l1fllldin species numbers. This in turn restricts the kinds of prinuuy
111011111I 114hút not necessarily their numbers. Host resistance and pest icide Another field of late emergence was ecology. Indeed, the word was intro-
1I1!!11I ,II/UIISdo reduce greatly the nurnbers of pcst« and diseascs ai IlIi duced into the scientific world in 1869, and the field won general acceptance
1(1\,[I ""1 we substitute human and dornestic 11 11i11111 I consumcrs. Similnrlv, ubout 1900. Ecology has given natural science an entirely different view
!IIII 1111I Is are directed at restricting the secondnry l'OIlSIIIlwr Icvcl ro 1111111 of Ihe living world and of the interdependent organization of its inhabitants.
i lil pYl'llmid is broadened at its base and narrowed 111111 low(.jt.d IIf IfH1111': Wc now see that fungi perform several important functions ln the cycling
1IIIIIy nnd materiais flow through fewer componoutx u! ' '11111I111WI'" \11'matter and flow of energy within ecosystems. As green plants and animais
d/e of any cause, they are decomposed to reusable smaller molecules by
I host of microscopic animais, bacteria, and fungi which thus play impor-
111~ lHE NATURAL PLACE OF PLANT DlSEASE IN ECOSYSTEM tunt roles in the cycling of oxygen, carbon, nitrogen and water. The
decornposing fungi and bacteria have a key place and role in the
10.2.1 An Ecological View of Plant Disease I'l·osystem. These are the organisms commonly called saprophytes 01'

II/I)/'Obes. But some of these have developed other trophic modes and
of our task in this book has been to describe the biologic ti nd (1~'IIIII/lh111 Ihlls occupy other trophic levels. Included are the parasites of whatever
context within which epidemiology exists. Epidemiology, deflned 11141111 IlIl'ubility that exist on living green plants. They are primary consumers,
study of disease in populations, operates also at the community 01 1.\l'1I
II~I' lhe herbivores ofthe animal kingdom. There are even some fungi in
systern levei of integration (Section 1.4). An understanding of popuhulon illl thlrd trophic levei, those that gain their nutrition from primary
phenomena is the key to understanding and managing plant disease. COIIIIllI litl'"III('r~ (Table 10.1). Examples are fungi that attack insects (e.g.,
matters have clouded this perspective. The following section should rcsuu«
"II/I/,'/lllIhora spp.) and animaIs of various kinds and fungi that attack
our vision.
111(11,'IlIlIletimes plant-parasitic fungi (e.g., Penicillium, Trichoderma
Most definitions since that ofMarshall Ward in 1901 (that plant pathok I~V
jljl i
"cornprises what is known of the symptoms, course, and causes 01' tllI
i"fPI tllIlI~ plant disease is always a matter of interspecific interaction.
diseases which threaten the lives of plants or bring about injllril'lI 111
1111"1'1 ~ '. lI, nnd 7 directed attention alteroately to populations of hosrs,
abnormalities ofstructure") have been straightforward und without vulu
111I"lIlhlllll111'parasites, and their interactions. These interactions belnn
judgment. But plant pathology is a rather new ficld with syslellllllk d
ti(" t hlMIIIII' lcvel ofbiologic organization-the community orecolIYNlplI1
velopment demonstrable only since about 1850. The l'llll'I"WIlCC WIIN1111
I !t.', 11I114(j íhey are between populations of different species. '1'111'I1II
largely because of the time necessary to cast off Ihl' l'I'pl t'HHivl' 1101'11111 111 11I111 111t Irl! hiosphere is better understood if we understand 1111", I I••
spontaneous generation oflower organisms. Sludt'llfs 111~1'"II"y, I111110,,\',
and evolution will recognize that the 100-ycal' Ill'tllld IlIltlulll" 1111'"1'111 W '1III1IWSlhe position of'plant disease among all othcr jllll'lllI;ljoll
IROO was one of intellectual turmoil and coullk: 11111111111I111 tU 11'1111'11
1It1111,,111'1'plnnlS Mel of fungi with fungi. Parasitic (lllllll ,11~rl!
slowly and painfully broke away lhe vcil 01' l'I'IIUlollll IlIltI ~I'I 111111 d "I.!II111
tlll' lII'WII1VI'interuction category. Presumably, mauv 1I11t'1t1\'lhltl
'I'II~· dctails 01' Ihal pcriod havc 110 11l'1fitll.'IIl'I' hl'II', 1.1111111('f1t'1I 111111
Ilh 111111'1 1I1'~IIIlISIlISnrc ncutral. Ali others must 1'1111illlti ,í!tll !lI
11I·lIod does. PIIII1I dist'lIse WIIS 1·IIIlNldlll'l.d 11'111dl'l/IlIl'l 11111111 01 11111111'1
I !tlh'llll 11"11~'lIh'UIIIhlH, nnd wiíh 1\ 1IIIIe thouuht 1111"11.\IU1i1i1 li

Ilhll tOI l,••hIIIIV.II IIllunlll

li' 111. Trophic Leve'

i iVP"'I'IHIlHltes

IltllUl1lu parasites }
Secondary consumers
I Ol
C ~
Primary consumers o
U cd
li ultauve parasitesl ~ >-
';;' U
Ql E
Decomposers 4)
iprobes ....'"'" '"a. c
. O) õc -g

li cxamples may be found. Biotic interactions like the influence <

••E Ol

::l .•.• c
- '"
-a. .2 ::::~~ '"
I, 1 ullural fungi on pathogenic fungi ofleaf and root surfaces or in soils '(3"';::; o "O
E ti '- c.r: .- <11 I'::
" 1IIIIllTI0datedin the tables as competition or amensalism. o ~
::2 Q.. a.. ~N f/)

,/It/,\'/t;sm requires somewhat more attention. A parasite is usually llJ

" 111111(/ as an organism gaining its nutrition from a living host or from a ~
c"!' . ~~ E-o
11, frlg host cell. In Greek, a parasite is one who cats at another's table, a 0<11
o Ql s: s: ..,

111'1,1, weIcome or not. How did some fungi becomc parasites? The answer <11- Õ Õ
-Ql .o .o "E
::J > .!!! ~ ~ as êii.8 êii
not known, but it has been assumed that during cvolutionary spans of o.~
'- c·- +-t Q)
C/) .c
.8 .8 '";>,
lime, some of the decomposing fungi developed the capubility of using e 0.0l '-
:5 +.;.r: .'!:! a.
:õQl C:-:õ
S '- Ql Ql

Ilving plant substance as food and that this enhanced their survivnl capa- -=Ci Ql c
o -.:: .~ ~ a.
QlQl c<ll
eu .8 t1l

'- .r:ccQl .••• :;: 00)00 w

bility. The parasites are not a special taxon. Rather, thcy tire casily rcc- Q):;::; ~.2 c _(1)0..c::l ~ ~=iü- as
e c ca O·'!:: Q)
.~ ~ ~
oE2 c o c.~
•••. 'õ
ognizable variants of various taxonomic classes of fungi, morphologtcntly '"
_ o..c .c
3l ~ ~ ~.2 Õ .2 :õ ~
:z ()O-c :;: ,e <11'"
similar to their saprobic relatives. Indeed, some single genera hHVCboth
saprobic and parasitic members, and in some cases the same organism may
~ li>
.~ Q)
-o .- _ o..c
Q) o Q) _
w..c aj aj _ aj "'O
E '- Q) c Q; :l Q; C
li> O <11
o E o o (/) o E E
have both modes ofnutrition. Many species offungi can occupy more than CI
one trophic levei, as they are able to change their feeding habits.
There are degrees of parasitism and, inevitably, names were applied to
N o o + + o + + -
them. Those that appeared to require residence and nutrition from living
hosts were called obligate parasites. Those that could utilize either trophic

o + + + 2S
mode in experimentallaboratory situations were calledfacultative para- o.;
sites, In the natural field situation, some parasites, the biotrophs, need ui
living host tissue to live on; these may be obligate parasites (e.g., rusts, 8
mildews) or nonobligate (Phytophthora infestans and other downy mil- '"•• ~
o <!::

dews). Other parasites, the perthotrophs, are nearer to the saprobes. They
Qi '"::JQl E
.!!? ~ 1l
c c e E (ii Qi
kill the host tissue before invading and using it (e.g., leafflecking diseases :s E.2
"' '';::;
.- .•.. .•.• ::J .!!? E c
o '"
o E "O
of the Helminthosporium and Septoria type). The borderline between ob- Ci (iiQl
oU Ql (ii
:;= Ql o .!!?
Ql c
.: U
Q) '"Ql
c '(ij
ligate and nonobligate is sornewhat arbitrary, as shown by the use of refincd E
~ a:õ
o Ql

artificial media of nutrition, and the line separating biotrophs frorn pert ho-
.1<1 Ql
Zü ai .ri E
-c c, a: o
""':c-.j C"i -i LÔ <Ó ,...: có
trophs is also arbitrary. The fungi as a group exhibit a full scale of possibil-
ities from exclusively biotrophic over a perthotrophic to a fully saprobic
way of life.
Some few fungi like the rusts and the powdcry mildcwlI 11I'l.l NIICCOSIlf\.1
in nature only through their parasitic uctivitie«. Th\\y trulv 1I'lIl1il'L1 llvln

Ihh luuuuu IH;livity. Epidemics are largely man-induced. If they are 10
!til 111111nutrition, reproduction, and survival. Such being the 1111I\llld"d or reduced in frequency, rate or effect, we must understand
1111'1. [hrough their adaptation, created for themselves what ,,!tlll w" huve done that has induced them. In large part, this means
! IIII~cnllcd "the problem of the pathogen, existence without dell IllIlulllg how our modern agricultural activities depart significantly
111111 illl host. " Were an obligate parasite to evolve a perfectly !'!'1I111 thc conditions of the natural systems where disease is a normal,
illlllllll, it would, in effect, commit suicide by eliminating its own Ili li111 Il'l.!d, functioning element. Future crop management must better
I,IIIIIIV lood source. Such parasites are now viewed as one partner , /11 1//11 li' lhe natural systems in order to achieve disease management
ti ' , ulvlng host-parasite association. It is assumed that these asso-
l'I'onomically and efficiently.
!!ií~ 111'evolutionarily very old and that the host has had ample time
!I'.'I I lhe evolution of the fungus and vice versa. Thus, they have
III,h mcntary genetic systems, a matter discussed in Section 7.5.3.
10.2.3 Disease in Natural Host populations
I '1llllgical theory holds that negative interactions also achieve a kind of
IIld'lIl1l' between the two species, given sufficient periods of time. The We have described how disease is a natural component of ecosystems. The
1IIIIIIIvcly affected population is not eliminated, and the benefiting popu- Iungi that cause it have found a method of nourishment different from that
1'1111111 does not destroy a nutritional source. Both populations are capable uf their saprobic relatives. In some important cases, their trophic depend-
111j,\clletic change. Most parasitic interactions must be very old so that host .ncy is obligate, but in any case, it appears that natural interactions and
11I11 parasite have co-evolved, each affecting selection of the other, and interdependencies engender a homeostasis or dynamic stability. lf the
1'lIch responding to the other's genetic changes. Some of the most strik- fleriod of interaction has been sufficiently long for host ahd parasite to
IIg epidemics have come about when a pathogen has been introduced ovolve together, disease is manifested at low levels .
luto a host population with which it had not co-evolved. In modern What is the evidence for such a postulate-not the derivative evidence
agriculture, imperfect understanding of the principIe of co-evolution has Irorn ecology, but the direct evidence from plant pathology? If such evidence
caused serious disease (and control) problems in another way, The first exists, what practical value might the scientific conclusion have? Is there
introductions of resistant cultivars were done with the assurnption that medem evidence where plant pathologists have studied disease in natural
a gene or two would impart lasting resistance. From this was learned populations and made observations that support the ideas just presented?
something about the capability of fungi to adapt genetically. 1t is the 'I'hcre are exceIlent examples in diseases offorest trees like that of chestnut
opposite of introducing a pathogen to a new area. In effect, we now hll~ht in the United States (Example 10.2). But what about annual crops?
introduce new hosts (i.e., resistant cultivars) into populations of poten- Whnt can natural pathosystems teach us? Examples are given in Section
tially virulent pathogens, putting survival stress on those populations. \0 \4.
The latter situation is now a major concern of epidemiologists and plant
breeders. But there is one very serious deficiency in our knowledge that 1'\ AMPLE 10.2: Chestnut blight in the United States. This epidemic of
will continue to retard rational deployment of new cultivars-we simply ,'",/,1/11/(/ parasitica on American chestnut (Castanea dentata) in the east-
know almost nothing about pathogen fitness, adaptiveness, and persist- j 11,llItI i'\outheastero U nited States must hold the record for sheer biomass
ence, particularly in the absence of highly susceptible hosts. Population 1I,.,\lIIVI'd in a single, continuous epidemic wave. Discovered in 1904, bv
genetics of pathogenic fungi is a field of the future. hh~It IIIlIl' il had already reached high levels in the discovery focus, a rUI
Summing up, we have seen that fungi are largely saprobic in mode. Over liI NII' \I\rk City, the epidemic must have begun during the 1890", I
evolutionary spans of time, some have adapted and evolved into parasites llillll 1'1\tI, it had encompassed the entire Appalachian Mountain 1"11"
of severallevels of capability. The development of saprobes to parasites Ii,ihlll1111.1 \VIIi'!mopping up the smaller populations of the west. S(\III~ !lI
is an evolutionary experiment that has been repeated several times in !' lho dOI'II",11I1 ion is given in the statistic that in the southern AP1'1I11Il1lil1l1
several fungal taxa. No matter what their trophic mode, fungi are normal, IIIH1!!i,1111 IINllring 1.3 million hectares, chestnuts made up fuun .'" 111 1
natural, functional, interdependent members of ecosystems. Plant diseases li' illill ,tIlIlPVt rcc population. With this epidemic we learned whllll!Wl'hl1íll
caused by [ungi are therefore parts of these natural systems, When 1111111 III\\'II\ ' II"ltI ht, wrought by introduction of a parasite by whh li II illIl
has entered the picture, he has had strong effects on the natural sysrcms. !III'" 1111111111"1011 h"tI never been stressed. The lesson hlls !'llllll' 1
crcating simplified systems (agro-ecosysterns), manipuluting lhe gCIH.'lk liill'\I"~" Ill'plll,1I in lhe stringent plant introdllctiotl 1l'I.\Itllllhit\
01' hosts and therewith, indirectly, the genetics 01' co-cvolving pllI'llsilm~,
IIII!II'II 'd ,ti,.. \
Sll'ong epidemics, as far as is known, havc alwuvs 1'IlIlIlWI'd-.01111'Idl'lIlll

iij'''I' 11111
i:orollary discovery during the chestnut blight
1111'1111 111our present concern, which was overlooked by V"dllll/l vegctauon types are interrnixed and co-exist in an interrclutcrl,
1"" "'l!I'I' \ 111lho lime. An obscure North American relative of E. "Yllllllllc' system ofspatial arrangement, species composition, successionul
I uvercd during the massive research program stimuJated dl·vl·IlIp.llenl, species dispersion, and species density. Within these sys-
1/"1'1ürngus, Endothia virginiana, causes a minor disease, Ir,IIIM,"ungi have several roles, including one as parasites. Pure stands are
d'''"1I1 Is evidentJy controlled by the resistance of the host 1'111
c' /" ali but pioneer vegetation, and even then, large intraspecific varia-
jil' uunubly deveJoped,under its stimulus during the co-evolu- dlll! cxists (Section 7.2.4). Against this background of low species density
'111"/parasite pai r (Anderson & Anderson, 1912). SimiJarly, IIltI gcnetic diversity, parasites have co-evolved, using diverse variability
",II/f/ca was traced to its origin in China, it was found that it rucchanisms to maintain themselves against changing resistance capabil-
1'11 li' /I relativeJy minor, endemic persistent canker disease of itics of their hosts. The resistances themselves have evolved in response
, , ''''/Ilnut species (C. mollissima and C. crenata) with which it to the parasites. For these reasons, in natural ecosystems, explosive
' , \ ulvcd (Shear & Stevens, 1913). epidemics are rare and are restricted in time and space. This is truly
111l'hH'(Wery of oak wilt disease in the United States in the 1940s kindled endemic disease: in the long run the product iRe averages 1, and
I, ,11111111 America would Jose to this disease the climax oak vegetation fluctuations of i R; are small. In the oak wilt example (Example 10.3) we
111,'I IlIId succeeded the chestnuts over much of the chestnut blight area. may be seeing one of the expected yet unpredictable outbreaks, restricted
11' wllhin about 10 years, it was seen that the disease was not strongly in time and space, which are part of this dynamic balancing of co-evolving
I'IIIUIessive and that the fears had little scientific basis. host-parasite systems. In the chestnut blight examples, the Chinese
situation is comparable: the host and the parasite have long been
, \I\MPLE 10.3: Oak wi/t in lhe United SIC//e,\'. Onk wilt , caused by rcsponding to each other. The proof for the idea is the epidemic that
, 'ratocystis fagacearum, affects severa! oak spccies, UIllOII~ which lhe occurred when the Chinese parasite, which had evolved in one gene
fllost prominent are the red and black oaks, Quercus 1'1I/)1'11, O. 1'1'111//1/11, center (China) of the host genus, was inadvertently introduced into
2- nigra, and Q. ellipsoidalis. Both parasite and host are jlldl~l'"OIIS IIlItI unother gene center (United States) never before stressed by that
have presumably co-evolved. The disease outbreak obscrveu WIIS (IIU' particular virulence genotype. There the native host population had no
ofthe cyclic episodes to be expected when, in accordance with lho Ihl't~Nh defenses available to combat the raid and, in a time period infinitesimal
old theorem (Section 6.2.8), the product iR, exceeds 1 for a short ,)(.'llod .ompared to the evolutionary time necessary to evolve defenses, the
of time, probably because of unusually favorable environmental COII- invader was totaIly successful.
An interesting example of what can happen in a natural situation was
After the excitement had died away, MerriU (1967) conducted a quiet, published in a paper that described forest and concomitant fungus succes-
reasoned epidemiologic anaJysis of disease development in the states of lon in the lower Yukon VaIley of Alaska.
PennsyJvania and West Virginia during the period 1956-1965 and found
that, provided that the rate of increase of foci remained the same, the 1% IIXAMPLE 10.4: Willow rust in Alaska (Baxter & Wadsworth, 1939).
leveI of infection would not be reached in West Virginia for 25 years or in lloulcring the great wild Yukon River are large areas of Salix pulchra and
Pennsylvania for 50 years, Although this rate of disease progress would , "/11 sensis in almost pure stands. This is the pioneer vegetation thal
yield the 50% infection level in West Virginia in 40 to 57 years, a statistic !II I "pios the bank areas which are repeatedly flooded and scoured durin
worthy of attention and perhaps alarm, it seems as likely that the slill i11" 11I1""UIice breakup of the river. Within the first year, Melamps
unknown small-scaJe physica! and biologic factors supporting this eruption 'r,"'1I nppears in the willows, and many are killed as seedlin
may cycle, as suggested by Vanderplank (1975), and that this natural/y jlllll'w/llll higher ground, where flooding is much less frequent, wlll
endemic disease wilI not reach such levels because its rate offocus extcn
sion and establishment will decline.
I!~r"''''IIIi pure stands for 40 to 45 years. At about this age, whlt •• !til I 11
IIIMil/., rl/"oI'kana) enters the succession, to be foIlowed 20 YCII r" h!hll I
Iltl' '/'{I glaucay and stilllater by black birch (B. kenaica) '" t111} II
10.2.4 Natural Endemic Disease liol!! I/~ ycars, a climax spruce-birch forest is in place, wllldl 111111
II"i"lII ~IIIIICrclict willows. During the succession, as the wllhl\\'fj li
Over very long periods of time (thousands of ycars), 1111111I111
l't'OSySfI'lIl !tiI,1 !hll 111111)/1 /t'ss prevalent. Simultaneously, age, crowding, 111111I 111111
have evolved to produce a balanccd interactioll 01' ('OlllpOIlI'1I1 spc'vh il!ÍlIIIIIIIIIlIII""lll'lInkcrs and hcart rots of willow. Many 1lI011'IIh' 111111
liiíillh '''II'NI, III~I Is 11 minor disellsc of li minur spccics, 1I0W lílli'Hilll iI

d~~lIlil'IIIJ.lilN011111lhe hi~hl !t'lfl'V!'I' Ils R-gene makeup, there systematically appearcd vh uh-ut
11I1I0n. /\ "/IIIIII/I/lIIIO/'o races.
111IltIl curly 1950s, 4000 S. tuberosum clones, mainly from the Unill.ld
IIHJ01 lhe rare descriptions of a disCHSCht.·!.'Olllillgnaturally 1111111 1111<.1 Europe, containing various R-gene combinations, were sub-
11111 .1 1111
CSI succession that includes lhe hosl spccics in tho 1(11111Mexico to natural infection and to inoculation with Phytophthora
li" li til ,Iillllll íuken from native S. demissum. As postulated, all were suscep-
1111114cxarnples related to tree species, and wc should now ill\1. "Imrnunity" from S. demissum, the breeder's expectation of the
"I! ,,1I1·lsin annual crops. None of our major food plants is 01' IV10ll, was seen as a clear impossibility. Some isolates from S. demissum
I IIi 'tllll Scveral have been subjected to human selection for 5000 Ifllll'kl.ld allclones of both species showing that if S. demissum had, as
111"111, There are few records of devastating epidemics until lhe I"'l'ted, more R-genes than already identified, they too could be
liI "llltftl ln northern Europe in the 1840s, If this was truly the firsl 111ru-orne (Niederhauser, Cervantes & Servin, 1954; Niederhauser &
, .tlll epidernic in human history, the reasons are fairly c1ear. The ~tfllll, 1953).
tlli'l WIISbrought from America as one of the first fruits of wesrcrn Whlll has this to do with naturally endemic disease? Other observations
jl'"I.ltllI in the sixteenth century. Subjcct only to minor diseases, in Ih" uuule in the Mexican trials not only support but also add new dimensions
111II nl'three centuries it became a major stnrchy sraplc crop, displacin 11111111' thinking about disease resistance. Even though blight lesions were
111-/11 und rye in some areas. Then, a purusiro cnpuhle of cxplosiv« I .ruunonly found on S. demissum, the plants were rarely killed. Rather, the
1"'f1l1ll1lionincrease (an investor in high N; an /' sfl'llloj.(isl, wilh shorl /,) II ,,10m; tended to be slow in growth and with limited sporulation (Jong p,
IppeHred and produced an epidemic with terrible l~llllllllltll' IIlItI NIIl'1II1 111'" N). These alone will strongly retard the rate and depress the result of
I Ikcts (Example l.l). But this was not the end 01' thu 1'11111111, di ••illU 1111 111upidemic. Add to these the genetic diversity of the natural populations
ccntury since then, the plant has been continued arul 111111 I' \'1'11I", 1I'1I'II'd ,tf S. tlemissum in Mexico, which acts to suppress effectiveness (E), and
n use; it has been subjected to intensive study and dCVI'llIpllII'lIf IIlIrI 1111 111'sec in an annual species the phenomenon of true endemicity again.
been a major subject of resistance breeding, Ali lhe decade of the 1950s closed, a clear picture emerged. Mexico is
In the last quarter-century, much has been learned about how 1111'I"'IIII!' IIIII'ly lhe center of origin of both Phytophthora infestans and Solanum
has survived and about the fungus' pathogenic variabiiíty, 1111.'111I11111' llli ,',II//.I'sum. During their long period of co-evolution the potato had devel-
pertinent lesson of the fungus' and the disease' s behavior in iIId Iw 11ti 11 "IH.d li wide array of resistance genes in response to a genetically based
Solanum populations. Good evidence exists that the pre-1850 lilllOIH'11I1 Iltll!to~enic plasticity of the fungus. The extraction of major genes from
potato was S. tuberosum ssp. andigena, a native ofthe Andes, which WII 1111'1\hnckground in S. demissum and the incorporation of these in S.
imported to Europe about 1570 and selected there for over 200 years fOI 1/II,I'IIIn, that is, re1iance on vertical resistance, was not a viable pos-
altitude and latitude adaptation. If Phytophthora infestans was prescru lu lillIly. But the observations of retarded lesion growth and sporulation
the Andes then, it was not imported into Europe until the ninetecm 11 liI\III'l'd observations being made simultaneously in some other crops
century, when it caused an epidemic not unlike the chestnut blight-s-wide 111,11'II'lIses.This phenomenon was called by various names, and we have
spread, rapid destruction of genotypes that had never before encountcred 11••" li purtial resistance (Section 3.7.6). It can have and often has él
the fungus genotype, if, indeed, the fungus at alI. Between 1850 and IIll' ••Ir hnse that provides partial resistance to many if not all physiol
1920s, the potato continued to be an important and relatively reliablc crun II\lI'~ 01' the pathogen. The natural population of S. demissum
through use of sanitation, rotation, chemical treatment, and according fll IIllllly dlverse, individual plants carrying strong resistance gcnoN 111
recent evidence (Grun, 1976), introduction ofS. tuberosum ssp. tuberosum jjlt I unthinations in a "background" of other genes that also illll'lIll
from likely but as yet unconfirmed South American sources. Betwecn flll 111~'~IIIIIt:eat one or more subphases of the infection cydc' I li
1920s and 1940, it was discovered that some Mexican clones 01' S, Illth," fins a range of survival mechanisms so dispcrscd 'li 111
demissum were completely resistant to U.S. and Europcan isolares 01 t'. l!t,,, Ihlll cven the most virulent isolate cannot be 1'IIII1pl!.'I{l1
infestans due to resistance genes ("R-genes") which coukl bc Intnsl't.'III'd ."" •.••"••1'''1111ncccssary condition of the host' s continued cx 1'111'111,(1, 11 li 11,
to S. tuberosum ssp. tuberosum. Use of these new culf ivur», fo~l'fIlI'1 ' '"11 IIIIVI'"Icarned" to live together.
with other control procedures, greatly aided pouuo pl'Odllrt /111101' qllllJ/f Y Iflillly 1111'snmc story has been developed in regard lo !lIIfM('\1
But it was also seen that, soon after inlrodllcfillll 01 l'Udl 1'1111 IVIII'. !tI it, 11·11111111110crown rust (Puccinio coronata) in m 111'111 il

of evol 11 111111 I I 1111,1 llalll Nlory has been admirably surnrnarized by Brown- IIl11ycause pandemics, as potato late blight did (Example 1,1),
in~(l'fI"l 111111111
V suggcst that you consult this intercsting and detailed HlIcclive endemic has a geographic connotation, but there is 11\1
IlTlIlIlI1 111II'IISÓ111cxtensity. Periodic changes in intensity are not excIuded, how-
WI} w!l! !HI\Ü til' l"l'Se matters again in the next chapter, For the moment, \'1 I I ( IlIcumann does not say that endemic disease ceases to be epidemic.
11111 liJllliI!Ii 'I! I" d,uwn comes from comparing the result of disease in the , IId"llIlc disease is not necessarily, according to Gaeumann, low-level
li 111with the all-too-common result of disease in the artificial tJI 111'11
Ne,The severity of disease may cycIe with a smaller or larger amplitude
11.1111111the first case, disease is always present, but the host's 1\""" Xmln) [1] and wavelength [T]. If an epidemic fiares up and dies
111,,1'1'1111,lhe population's genetic diversity, and the dispersion of IIIIWII pcriodically, annually for instance, it is termed a cyclic epidemic.
lilt\llit ' I .uubine to prevent extreme disease growth rates. In the latter 11", progressive epidemic is seen when disease spreads to new regions.
lu I' I ,,1"l1ts with simple genetics ofresistance are densely aggregated, """1' having reached high severities during the early years of conquest
iHI 1111IIIIIHII8soon develops a virulence capability that the host cannot Ihl~ discase will settle down to a moderate, constant value, recurring year
!ÍI ,I,"hl without further help from mano Agro-ecosystems are so young '''1'1' year. It has then beco me endemic. If an endemic disease at any time
I' J, I111til to natural ecos ystems that there has been insufficient time to tll,yclops explosively, affecting a large number of individuals, it may
111,1111 IIllIbility. "The instability of so many man-made agricultural mono- 1'111I10to a new region where it will have the character (once again) of
IIIIIII"S is likely to stem not from their simplicity, as such, but rather from I I'lIIsressive epidemic. Yellow rust on wheat, endemic in the Netherlands,
1111 II iuck of any significant history of co-evolution with pests and patho- .unetimes follows this pattern, becoming progressive whenever a new
IIIH" states a prominent ecologist (May, 1975, pp. 165, 167), who adds, I'hYNioJogic race appears.
l'hc thing which destabilizes man's agricultural mooocllllllrOH is not so l'hc newer term polyetic epidemic (Section 10.4,6) is limited to epi-
IIllICh their simplicity per se, as their lack of an cvolutiouru Y IH'dàl.ll'e~," Ikulics whose increase in intensity takes many years. Sometimes they
11111I0t easily recognized if the amplitude of the annual cycle of x due to
I IIl1dllions of host and weather is so large that it obscures the gradually
10.2.5 Epidemic, Endemic, and Related Concepts
!til rcusing annual mean severity.

Disease in natural populations, where host and parasite have luul 1111111 111sumrnary, epidemic, used as a noun, refers to an increase of intensity
interdependent association, is the most natural form of discuse 111111 1111 11 wcll as of extensity of disease, in accordance with medical usage.
most truly endemic. Disease levels may be expected to be low and to VIII I I'hh'mic and endemic, used as adjectives, refer to the states ofthe disease,
little over time. Does this mean that such disease is never eruptive showin 1\1'1(' IRe = 1 (averaged over a certain and relatively long period) marks
a sigmoid progress? Is endemic disease different from or even the opposite ilil' Iuterface between the two states. The use of the word "endemic" as
of epidemic disease? Some investigators use the words as if this were the 11111111 if) not recommended.
case. The time comes to make some definitions cIear.
We have borrowed the words--epidemic, endemic and pandemic=-frorn
111ti 1\ Natural and Managed Endemicity
human medicine, but there are differences between medicine and phyto-
pathology that necessitate adjustments, A generation ago, Gaeumann I!I d..,llIllIg the word "endemic," we have kept to the usage ofGaeumann
(1946) provided definitions, discussions, and examples. They are worth 11I1.llvnrccd ourselves from the dictionary definitions, based on medicine.
reviewing. 1111 11HII~Bcsta separation into two classes: epidemics and endemics. AI
Disease in a population must be concentrated in either time or space 10 1 11I1'1'l'às general agreement that endemic disease is always preMO'"
be called an epidemic. Epidemics may be explosive or tardive, and disease 11I"'lIudns the question of whether the several kinds of disense 1'1'\
progress may reach low levels ofseverity (as in the oak wilt, Example 10,3) .Jt'11tlbed-compound interest, sirnple interest, and cyclic 111.111
or high levels. Only in the last case does popular parlance use the word II!lUInpply to endemics. That brings us back to the l1"hll 111111
"epidemíc"; scientific usage is wider. The noun epidemic refers to 1111 ililr, dll'lclISCis not only always present but also occurs 111111111111' "I

increase ofintensity as well as of extensity of disease; it is the combina! 1011 IPi."V cyclc of values, in accordance with Gaeumann. 111111'11'1111111\
ofthese two aspects in one term that creates misundcrstandings. WIH'IIIII\ llhH'IINllon deciduous parts would follow the rulc 111I 111111I111111
epidemic increases in extensity, that is when thc fungus illl'll'lISCS ils (1/'/'// II""""NI' 011 twigs or trunks, which is not so easily "'III11VI,tI \Iv
of activity, it is called a progressive epidemic. When [ho 111"1\Is 01' ""111 11'111\I'Hi'4I'Mlike ICIII'-/':lII,01' by harvest, may actually \11'1'0\VI'lIl 111
continental size, the progressivo cpidcrnic is l'IIII"d 11/'t/II'/"/11II', tII'\ 11111\1111 lncreusc itli \11cvcry ycur.


II'Llllh ('xprcssed his view Iltul cndcmic disease is lhul luJa 1111 1lI1VELOPMENT OF AGRO-ECOSYSTEMS
1111I lU" (Scction 6.2.8) tends to oscillate about 1, so lhal
'"11 I('sion or infected plant produccs onc new lesion 01 1'11111I I1iseu se occurs wherever plants grow but comes to prominence ai mos I
li "",llIg its lifetime. He added that lhe amplitude of tho e I« luxivcly in agro-ecosystems, those man-maintained simplified ecosys-
uuill, which implies that endemic disease severities rnust II 111/1explained earlier. Since plant disease occurrence is different in these
!I'" Vnnderplank's description fits only that kind of endernic ~IIIll'Il1S,it is important to the general understanding to know something
IIH!! 1'/111be expected in large di verse natural populations o/ til Iheir evolution and of the major determinants in that evolution. We will
01 11I,~ls(lhe willow rust example of the Yukon river), but it does dl'll'\JSS some of the biologic, environmental, social, and economic factors
I I 1II1t'llIi<.:disease of annual crops (yellow rust of wheat in thc 111111 played a role in the evolution of various agricultural systems and
li. IIId,~). PIIII'liccs. This willlead to a brieflook at agro-ecosystems today and will
'10" 'fI'w echoes that of Gaeumann. Disease from an introduced path lulfl 10 understand how the disease-influencing factors brought about by
" ,IIler its initial explosive phase with increase in both intensity anil I IIlflping regimens (Section 7.2) are displayed on a worldwide scale.
I, "dly, will settle down to an annual cycJe, usually at some lower levei,
1/11xmaller or larger annual amplitude of x. The levei of endernic disell/"l' I f) a, I Cropping Zones of the World
""IY he high or low, and local eruptions are always possible as a result 01
11I1\'lOscalefactors. On this 1ast point, Vanderplunk agrccs, « llnmtologists have detailed ways of characterizing climates and their
We suggest that there are two kinds 01' Clldl'nlkily 10 hc recognizod .urlnnts. Such detail forms an important part of agro-climatology, a field
untural and managed. NaturaL endemicity is Ihul 1'011,,1111111111111'1I1 pOpll ttll'l'Cal use to agriculture and epidemiology. For the purposes ofthis book,
lations of coevolved hosts and pathogens, and Ihl' I'Xlllllplt- 111111110. wil: 111 11111 y 1\ general idea is needed of where particular crops might be grown. We
the eastern United States is a perfect one. SirnilurIy, "\'"''11/1111,'' 111111 I.•, ,\III\Jse the six classes ofagro-climates of Duckham and Masefield (1970).
constantly cycJing around some relatively low avcrnge , In tltl til ", ••••/1
severity are to be expected in natural annual plant popllllllillllÍl !II II uipcrate agro-climates:
infestans-S, demissum example (Section 10.2.4). Mal/lIHI't! , lIi/eli/l. (f' 001, humid: Europe, Canada.: China, U nited States, Tazmania,
that seen in the blue mold (Peronospora tabacina) of tobucco 111"tlIIIJlt'l New Zealand, parts of Siberia, northern Japan, and southern Chile.
where, after the initial explosive epidemic, the disease was 11I11Il'"Ily 11 Cool, dry: continental Canada, United States, Australia, Argentina,
combination of techniques and kept at a low cycJing leveI, flrs: <':11111>111 Uruguay, USSR. These areas have low summer rainfall.
high incidental and later acceptable regular loss (Section 8.1.5). It is po Warm, humid: southeastern United States, areas ofSouth America,
tulated that if ali agricultural practices were to be stopped so that host 11111/ '\outh Africa, Australia, China, and Japan.
pathogen could once again take up their natural self-regulation, such di Wurm, dry: These areas are semiarid to arid, with hot, dry summers.
eases would gradually reduce themselves to the constantly recurrinu 11111 I hl'y occur in southern Europe, North Africa, South Africa, central
low levels of natural endemic disease if given sufficient time. 11111western Asia, southern South America, Californiaand the south-
In concJusion, natural endemicity appears when the pioneer vegctuuou \\ 1'"lcrn United States, Mexico, and southern Australia. Winters are
with low diversity is replaced by a succeeding vegetation with higltl" 1I~lIlIlIywet.
diversity; managed endemicity appears when man succeeds in domuuu
ing a disease in his low-diversity crops by a variety of methods (inchultu "I ltnuues, the humid ones are generally reliable for crop producllou
increases of diversity). To this time, managed endemicity has 111'1'1\ I~ 1111'rlry ones may need water supplements through irrigatlon
achieved by application of standard control practices without thc dl'll'
of conscious planning implied by the term "integrated control" (Hl'l'lhur
11.1.1). Endemicity of a specific cultivar-race cornbination rcsult 'I IfI I t'hcsc are defined as areas where rainfall is high and di""1 ,IIIII,'d
constant cycJing levels of disease severity, with small 01' líll'gl' IIIII"llIlId Ili" 10 II110wcrop growth throughout the year.
of the cycJe. The levels may be low or high, but thcy 111'(' sl'hhllll VI'" 1~lllIlIlIy dry: These are areas within the tropical /11111'wlll'lI
high except when environment in the short terrn favors 1')(plll'lIVI' dl'vlII 11111111
I~ It'ss than about 12 inches annually; unlcss lu h.tlllhlll I
opment. These ideas can be applicd in discasc 111!\IlIHWIIII'111 11111"11',',,":h nrcas III'C usually used only for graziu

312 ,li.;

111111'"111'"" 1'111lil 111111 '.lU

I!~I Ilrlll,' iong-term genetlc 1111""'11111111"111'11'11'11111'\\'III.!I
ItO/I'"W'1. Elevation plays ti Jllldlll I,,1r /11 1111tlllt-lllllul"ii\1
Iljjl{lll uud particularly ofagro-<..:lllllllluH 111"U 1111,,11:11,'\111111
ill!IIIIIf /IIl.-tat higher altitudes, whcre 1~'IIIjIlIIlIIlIl' 111111 IIIt1hl li! ~
,u.III1"~ illli\t 1,,- tll1ducdIy temperate, can be grown wlIlIllIl1I I!INh 11"1I1f1"1111
11Ii//II'Iy, since the earth's highest lCOlIWI'III'"I\H til( 111 I" 111
It, "llIlIls of equatorial origin can be grown 11111 lllO/ld 1111'111
!tIl 11""US provided that moisture or some other faclor'lN 1101","11111
i/I 'op plants like the starchy staples, cassava and 1'1111111111111, I'
,," 111lraditional tropical agriculture; others, the hlgh-vulu« 1'\lil
I' Ilkc bananas, coffee, cacao, and many spiccs, II/'l' ('1'0111111111 111/
ti I 111'1IIUve only when tropically grown. Teu, however, dllt'S wl'lIl1ll1lWh
1.lIlIlIdcs, matching the climate of its highllllld Impk orlN/1I ('II!lVI',,,,'1
I '''I's of temperate zone origin can be growu /11 I. 111'1l'I ri 1\1"IIN /I 1111
1 1101cnough by virtue of their altitude and IUlVI' 1111"1'1"111',11111' 111'"11I\111
tII/llraIl. A look at the map in Figure 10,2 ShOWM 1111I1\\1111'/\ 'íI'IIIIII"(''' 111
01' lhe world can be given the same agriculturul I /lII"llh_1 l~III!iljiflt'lIllllI
Allowing for local variation, similar crops CUlI 111'~IIIWil in jlH'1I1j 111••Imll
Farming is practiced in all parts ofthe world wlu-u- ~1I1\\,jj.
long enough and where moisture, including lhlll 1111111li I
limited during the growing season. Of course, wluu I 'III'~ 111
strongly affected by local, national and internationul CI.'llIllIltri, 1,1!..!lIi
well as by social pressures of local nature and by pcrsount 111li I 'I: 11
As agriculture developed, domesticated plants were cxl~\lIdl'\l '" "O,
and di1fused from their several centers of origino In latcr SIIIHIIN. 1'"' !iUI
larly during the age of western European expansion, mnuy "'1111'111
zone species were taken to new areas like N orth America und A 'I'd ,"1
and tropical annuals were successfulIy established in highl.\" 11111111\1
Old World species were taken to the New World, and Ncw Wmld 1If1
were brought back to the Old World.
Special efforts in plant breeding and selection have been and wil/ 111'111
to adapt crop plants for use in the opening of new agriculunnl "'1'"
to introduce new crops in old areas. It should be realized Ihlll lu tlu- I
a country like Brazil, about as big as Europe, brings about I 11I11111111
virgin land under the plough annually,
Sooner or later the pathogens folIow crop range CXII'Il/jlllllll. ",,,viII
seed, tubers, scions, cuttings, or plants, somctimes wuh Ih'Vllltllllh
sults, When Phytophthora infestans reached RUI'OIll' 111t /rO IlIId IIltu"
century, it found vast areas of potatocs which, '\l'florl"11 111li ••. IIh"llll
the pathogen, had very little resistance 10 O/l'l'l. HIIIIIIII.IV. IIl11lft\ ;11
had little resistance against tropical '"I1I~I' '"'11 (1'/11111110 li/l",~jl/'III
it arrived there around 1950, anil l'IIIIc'(' 111 111'111'11111111IIU 'Il'lilhlllll


"" 1111 11' nround 1970. In gcncrul rerrns, it can be said 111't hc soclcra! unit from the family or tribe through viIIages <11\\1III\~II~ I
11I'"111Ilmrue compatible, so will ils pathogens The most lhe modcrn city and nation. Agricultural organization and pracílco IIIIVI
"'lIhlll during the cropping season is moisture, but even ihungcd collaterally, increased agricultural efficiency allowing grad 11111 1\
1III-IIIIIonoften provides sufficient moisture to support lcasc of people from direct agricultural employment. The proportions nlll~\
U-l~,elions 7.2.3 and 7.6.4). The greatest obstacle in thc írorn all persons in the primitive unit to less than 4% of the populations i1\
10 "I l/tc pathogen, just arrived in a foreign environment, may western nations.
!J\ll, I1I ""itable hosts to bridge the gap between two successiv
!l11 I" IImls (Sections 7.2.7 and 7.2.8). A specific disease may
I' I""m'cntly in different areas. 10.3.3 Relations Among Agricultural Practices, Economics
111 IIIIIy studying the agro-climatic requirements of the host crops and Societal Organization
11111 u101'their pathogens, epidemiologists are able to predict with what
'I'he earliest villages were affinity groups of free individuaIs, and land was
llll j \, probability a pathogen can be expected in new areas where th
divided in two ways: grazing land was separated from cropland, and
"'I' I~ yet grown without that pathogen. This branch of epidemiology has cropland was apportioned in very sma1l units to individuals or families.
li, I li cnlled geophytopathology (Weltzien, 1972).
Primitive, semisedentary village groups, like today's Amazonian Indians,
persisted in a collectional, natural husbandry or shifting cultivation, but
10,3,2 Steps in the Development of Agro-ecosystems more stable villages developed fallow system agriculture. Villages estab-
lished market places for bartering (and late r, selling) excess production
111 Section 7.1.5, six stages in the evolution of fl\/'Il\in~ nructiccs wcre nmong families within the village. As relative societal stability increased
outlined. It was pointed out that agriculture origillUIt.ld 1IIIIllIWIHIl'IIIIyIn n lhrough authority exercised by military, political, or ecclesiastical hierar-
number of places, but that the rate of development hud VIIIh'lI 1111I11 pllll'l chies, production efficiency was sometimes sufficient to allow some persons
to place and that aII stages coexisted in today's woríd, ','IH' 1I"vl'IIII'IIII'"1 10 follow pursuits other than agriculture. The seats of authority, usually
of cropping practices is intimately interwoven with that 01' '"11111111 HIHh-t v villages on crossroads, river fords, or sheltered harbors grew in size and
The availability of land and of suitable crop plants are but IWII 11111111111 hccame towns. Towns often had a group of satellite, subservient villages.
determinants in this development. Economics and societal ()1'~IIIII:t,IIIIIl" l'owns also had daily commerce, located in shops or shopping areas, and
are equally important. In this section, we outline the interdepelldelll'U 01 contained a new nonagricultural class, the merchant. Villagers sti1l traded
agriculture, economics, and societal organization in order to gain UIl llll lucally, but there was economic incentive to produce more food, fiber, and
derstanding of the forces that shaped today's agriculture and, with it, tho products of cottage industry for sale in the towns. Villages closest to towns
environment for disease. Increasing agricultural efficiency has allowed hlld an economic advantage but were also subjected to production pressures
further development of human society; but as society has progresscd, 110111 townspeople. During this stage, the legume rotation developed. An-
economic incentive and constraints on agriculture have become more III hcr development was the loss of individual ownership and choice of
complex. These, in turn, have been determinants of the practices uscd, lnrming practice and crop. Slavery and serfdom were part ofthe later stages
Six general stages of economir development have been stated (Grus. 111development.
, "'I'tain towns, again advantageously located, continued to develop jf
1. Collectional economy, i111'V wcre the seats of major authority-political, military, ecclesiasticul.
2. Nomadic, natural husbandry econorny, 11111 1'\ unomic. A greater proportion of their populations was nonagricul
3. ViIIage economy, 1111111mcrchants, clergy, soldiers, administrators, artisans, bulhlrl
4. Town economy, ii'llI 111'111, nnd so forth. In some striking cases, they established inum-u
5. Metropolitan economy (including the city/state), IIIO,,~ "I lníluence, like the Roman Empire or the city-states 01 1111"'
6. Modern international economy (including the nation/sltlle). ilícdlt-vlllllurope. Cities traded with each other the commoditicx 1I11I""•..Cd
hy l!t., ItllhHcrvient villagers. The pressure for salable goods WII•• 1.,11It
In this progression, as the economic unit increases, thcre is n CO/1<':OIlIIIIlIlI ri
I/hi 111111'1 III the bottorn of the hierarchy. More productive fUI 1111"111111
increase in the numbers of persons included, thc divl'I'S/ty ol'lhell' m01'11 1\',0.1 I'ombining grazing and cropland into field gras/I hu ••11I1I1I11
pations, the size of the affected agricultural arCII, 111111111"1.'II111pluxllv"I liilllllll 11111.illl'l'llllsing [icld size, specialization of crops aml 111'1' IIHII'il
relations. In the above progression, Ihcre can Iw dlsl'I'IIHI!I 11dl'v\"",IIIII'1I1 IIl1l1nl I" l!t\' qllesl for grcatcr productivity, rotations 111'1111111 111111

"I'PI"'" to have countercd t hc disease increasing I1II111 ~ 1'llIduotlvlly Df major crops (in kg . ha-1)
111 UIC other practices. lncreasingly, farms were
I ,,1t'11~111IIÇÇ
units to producers of significant income. Developed Cenlrally Planned Developlng
\" II'WII village economies became prosperous-England, I;II~I" Nalions Nalions Nalions
I1I I'lIhlk of Venice, Portugal, and Spain are striking exam-
111 10 see greater horizons of profit, afHuence, and power. 2183 1313 1295
5834 3203 1980
li" I li IIl'Wareas of the earth, established military and economic 4834 3033 1325
III!qlll U ""ti began what were to beco me large colonial domains. The 21807 12466 9129
!li"". 111' lhe colonies was much influenced by the international trad- 906 966 515
1111 \1./lIllIlics. They were the sources of desirable, and therefore
illl 111, exotic products, such as spices, cane sugar, tobacco, tea, .,o\lrcc: FAO Production Yearbook, Vol. 29, 1975.
"" I , IIIIU cacao, and cheap sources of food and fibers like cereaIs,
1'/11111. nnd jute. Many crop plants began to be developed and grown in
loms only with the onset of intensification. Intensification is a function of
li. W ureas within the adaptation range-bananas in Central America, ocioeconomic forces. It is not a product of the last century, although
1111lhe,. and sugar cane in Indonesia, cereaIs in Australia, and so on. conomics and population pressures during that period have accelerated
Mllrkets were not only national and continental but also intercontinental, lhe process greatly. Agricultural science carne into being in the eighteenth
IIIlUfarmers far removed from the sites of consumption reacted to distant ccntury but had an impact on intensification only during the last 100 to 150
.conomic demando cars.
The possibility ofhigh profits creates apressure 011 Ill-\I'kll11urc W produc
'I'he intensification that has accompanied the growth of agriculture and
with efficiency what the market will accept. Markcis hnvc ~'1l11l1}{l,d ~I'l'nlly
society has increased several agricultural practices that favor plant disease,
in the last 150 years as a result of exponential population ~l'l)wl li Illul Ml'Illltly
IS explained in Chapter 7. These include:
increased levels of disposable personal income in the indust 111111",(,11 111111011
To achieve increased production, agriculture has used two tlJl'llldqlll' I. Enlargement of fields,
new land has been brought under tillage and old and new land hnvc beon 2. Aggregation of fields,
subjected to intensified farming. :I. Increase in the density of hosts,
This brief overview reveals that as agriculture has progressed, socictul ~. Increase in the uniformity ofhost populations or decrease in diversity
change and the division of labor in society have increased. ln turn, at the specific and at the varie tal levei,
changes in the organization and economics of society have causcd Increase in specialization, which encourages, if not continuous
agriculture to change crops and farming practices. The size of the monocropping, short rotational patterns,
influencing market has increased from the village to the town to the natiou li, lncrease in exchange of contaminated plant parts.
to the continent and finally to the world. Today, demands for cereaIs in
I "tlfthcrmore, intensification and specialization include other agriculturul
Russia and China affect the crop choices, rotations, and practices 01'
prnctk-ex -fertilization, irrigation, and crop environment modifications
Canadian and American farmers; demand for coffee has similar effects 111
which, 10 the presence of susceptible hosts, increase Xo and/or r.
South America and Africa. Yet in many parts of the world, farming goc
Natural husbandry includes none ofthese practices. In the fallow sy/ll
on at the subsistence or at the village economy level. These areas are t111
snd in the legume and field grass husbandry rotational schemcs. W
targets of current agricultural development schemes. The great disparií y
flnd the bcginnings of these cropping practíces but have been IIllIthl
in production efficiency is shown in Table 10.3 which cites FAO datu 11\
find the records or indications of any but regional disease olllh
order to compare production of a few important crops in the so-culkxl
most. For most of agricultural history, food was used wl1t'lI' NlliWII
developed, centrally planned, and developing areas of the world.
produced for local markets. There was Iiltle pressure towuul Ih'.lll
uhove. Even in places like the Oriental rice ureas, where Iht'1 r Wl!ill'l
10.3.4 Societal Development and Disease Determinants til lncrcnse the size or at least the aggreguílon of fields IIlId lu í/ill
dt'lINlly of hosts, selection for host gem-íle homog<.l!H·lIyI1IHI lliiI
The foregoing review of societal and agricultural dcvclopmeut cuu 111' II/il'd 11'i'I'lIl1y,rcuchcd the point where large 1I~"IIlIIN luul 1111' IIIIII\~11111
to construct the thesis that serious rcpcritivc cpidl'lIlicN h"l'lIlIl\l 1'01111111.11 Althlllllth NIH'hnrcas'had species monocultru u, IIl1'y dltllllll hll\<H I iili


lu. i.1I1111,nlung with scusouu] lulluw 11I' sccond croppin Whcrc mnn has geared the ecosystem to his own needs as a 1.:1111""1111:1
1"1 "'N, irucrrupted pathogeu 11111111IIp und rcprcssed IIlld 111 doing so has made himself dependent on and part of the ecosys« 111
he has created an agricultural ecosystem, or agro-ecosystem, Thc tlI-\III
II I I!lU'IS lhe wheat trade ofthe ROIlIlIIl HlIlpirc. To fecd the ccosystern has many components: soil, climate, crops, pathogens, rnun
I' "'1111,Ihc provincial towns, and the garrisona at thc fronticr, li imself, and so on. Definition and delineation of an agro-ecosystern dependa
"'11 /11ali parts of the empire and shippcd ovcr hundreds 01' o largely on the purposes of those describing it that unless the objective
1'11\lopulhologists cherish the poetic record 01' a folkloristic s clearly specified, there is apt to be a confusing arbitrariness in agro-
I",I/IV mcant to appease the rust god Robigo (Ovide, about 8 A.'),) ccosystem boundaries.
11'111.1.'Illal rust was important at that time. Present-day evidence The farming systems of Sections 7.1 and 10.3 are subsystems of agro-
I 1IIIIl'cd that black stem rust coming from barberry bushes ncur ecosystems. They have spatial and temporal boundaries and the cornpo-
! 'li Itls was important then as now, at a local scale. However, no ncnts of soil, climate, crops, pathogens, man, markets, and social patterns.
Illl11" has been found for any major breakdown of the Roman whcnt Noncrop plant species and their pathogens are excluded. Whereas farming
11M li result of large-scale epidemics. ystern refers to ali crop and domestic animal species encompassed by it,
with some emphasis on managerial aspects, a cropping regimen refers to
1 single crop species only, again seen from the manager's point of view
(Scction 7.2). Cropping regimens are, then, subsystems offarming systems.
The next subsystem is the one ofmost interest to us. It is the pathosystem
Ali stagesofagro-ecosystemsdevelopmentco_cxisl jllIIlIlIlY'/'I Wlllld '1'IIlIl' (Scction 7.5.1), the combination of one host population and one parasite
is a large potential for increased productivity by Ill'l'l''''I'' I/IIU 1111111I., 01 population with their mutual interactions as described by population dy-
agricultural development. But not alI lands and clilllllftlN \VIII /'1111'11111
I 111 unmics and population genetics. The pathosystem is subject to the effects
tensive, specialized agriculture. Some are more suituhk- ItI di v. 111/'1111_'111 111' climate and man. When appropriate, the pathosystem includes hosts,
than others; some reached advanced stages centuries ugo, SOIIIl 111111(1 IIIHI vectors, and other items.
century, and some are being pushed in that direction at this 11101111111 ~(lIllill 'I'he above can be reduced to an outline:
epidemics are more probable in the advanced areas. Is it pOHslhh' 10 dIlNI,~1I
a picture of world agriculture that lets us identify the high tllld luw I/lil; Agro-ecosysterns (1, 2, ... , n)
areas? Farming systerns (1, 2, ... , n)
To do that, we must be very c1ear in our approach. A reconsidcrntlnn oi Cropping regimens (1, 2, . , . , n)
agro-ecosystems and their components wiII assist in achieving this clurií Pathosystems (1, 2, ... , n)
A uiodel is a simplified representation of a system or subsystem made
10.4.1 Agro-ecosystems: a Reconsideration !I-" IIH' purpose of demonstrating or calculating a function of the system
I~'.·III!' simulation models discussed in Sections 6.5 and 6.7).
The word "systern" is currently used in various connotations. To avokl , 111'lutcrest ofthe epidemiologist is not so much in the agro-ecosystern
confusion, we use "systerns" in the modern sense of systems analysis. 1 I•• 11111 in how its components and subsysterns affect the subsystem of
A system is a part of reality separated from the outside world by clem Ii '.\ lntcrcst to him, the pathosystem, and conversely, how pathosy
boundaries (Section 6.5.2). The outside world can influence the SYStCIII, ,111'1I lhe agro-ecosystern.
but the system cannot change its outside world. By definition, a SYSIi'III
consists of subsystems separated from each other by clear boundurlca,
subsystems can and must mutually influence each other, SO Ihlll 11chuu
in one subsystem produces reverberations in ali othcrs, AIIY slIhsYII'I'1I1 l;htU/IOSot Agro-ecosystems
can be regarded as a systern and be subdivided, and so 011 111'11uhovc, it is difficult to define an agro-ecosysum willllllll
An ecosystem is an ecological system, lirnitcd in 1I'IIl' IIlld Plfllllll, w/III 111
"f11II.~IIi~ lell rurlncss and confusion. Consequently, it is difllnl!l I" iJovi
species-each with its own pattern of distributinu 111slIml' 111111 111111'li I, 11111111 01 1I1-\1'()-Ccosystems. But an intellectually 1I1I1"1I1!t~111t1
its components, and a recognizable .\'lruNIII'(· l'oll/'lINfillU 01 1/1111 !I,'I/III, li "'"1 111IIlIlIh· hy dillcrcnuating among subsystcm •• 11111111)11[I~i
lations among these component S (Sl.l~'1iou I(), I, I ) !lill"'''' oU. IlIltI luuctional structurc. Hence, 1'''"1\1111'••V~ft'iil


11,'lI.lilll1 10 thcir' dt'I-\IIII' 01 "11111111111I11011

IIlld 1111
e "'~ @)
,- :::l
111111111I, ~ü >'",Q)'"
" ,~ '" '-cCicn
e u!~
o o....
~'§~ ~
I I 1I11'111Hln.:
of inputs to thc SyN/('1I1 HH' Mkllls; 1lIIIIIIIIId ~< CJ) ';::
• " 111111\'
IIlId industrial conlribllliollM. 1111'11'('hlloloHY 111 > "
õ< o ui u..
::::l'i: .cai", '-0)0>
IH'Nls, nnd weeds; the pracuccs (1IIIPloYi'd 10 11I11I1IId/1 o C])
o e,- o 'ã. :::l,~
:::l '" m ~0.0l0.
IIIIIHI'N 011 and off the farm; and cnCl'gy NuhNldkN, MOII OlE ~o< -:.= ~ a.
:E ' .. ~w .,'-
Q) L:. Q)
o I

1111 111111111
y gcnerally has lower inputs of each o/' thc1'wexcep: 1111 ,~ g>crj e o, o o

ii:' ii:'
". ---j ~ "'81
!I\L 'til. II hkh is usualIy much higher. Energy and machine Nubslilllllllll ceCI)

Illiii'llIlIlIlI nnimal labor is not essentialfor intensification, as thc dou"" @lI @lI ~~ @I
ti 111ICIlIaI rice-legume system exernplifies. Nonetheless, this SYNli'lI1 ~
11I1l'IIsivethan maize or soybean production in the United SllIli''', 'E Q)
a. Cl)Ui
C]) "
.c ce
m Q)

/tio 1INllhstitutes machines and fossil fuel energy for human and uIlllllltl
o ~ e:::l
:::> :õ
ãí CI)
Ilill,tI nnd utilizes numerous other inputs as well. e :::>g-o.ãí C]):::>
~., '" Qi ~
e cn:;e~
Q) ..

\I",,'i(llization is a measure ofthe degrce 10which 11singlc Iarm OrH!I'lI/hlll Do

~ êií o.... Eai
~ E
Q) C])
='" ~m ~UJtIl~ Uig-
," " regional are a of farms is modified toward pro(/lIl'fjon of ti NinHIt· fll j .,
e ~ C])~ ,C])CI)Qi::;
••.. E'O
C]) C]) e
~ m o.... '"
""eQ) '" ~'~'E:::>~UJ
1I1I1I'yproduct. Flower bulb production in lhe Nl'lh('1 IrllldN 111IlhvlllllHlv Ri :::> ,- o Z ,,'- ai o m s: '"
li! Ui~~
CI) Ui :fl ~ 0.;;::: o o e C])
.c "'.c
IIlghly specialized, but so is the mixed farm of 111(,i'lINfl'l1l "1\/11'" HIII/t"", '':: Q)'" (ij C).8 à)Cõ.sQ;euf8 em_
where the primary salable product is rnilk. Thcre IN1111111111'11I)1',1111\\1'\ 1'1 :!2

m C])
o.... '" .~~s -t ~:9 ~ Q) ~Q)
lI!.c Z
lhe bulb farm is intensive in inputs, whereas thc dll" V /111111. "1'1110111"'11 ~ o ü a.. ~c3~~ ~~ Clü

as it may be in its herd management, is extcnslve

husbandry support.
111II~ iI!l" 1.1111 e m e '"
.g (tj
'00 l'"i! < ,_
~ o .-
o.... e
o '"
Table 10.4 shows, to some degree, the relation of intl'IlN/1 VIII, IIli I\fUi -c
~~ ~ ~ ~ m ~ ~ ~
to disease risk. The table shows thatlarge areas of agricuttun dllllOI " -g.g
Ui '" .g
- •..
0.0Q) ,-
'" ü",<
Ui~§ ~
Ri ';:: ~ .~~ e,-'-
o ,-... .-o '" «Í'OORi
a high disease risk. In the tropics, this is extremely impOIII,,1I IlIdol u oQ)C]) '-- .- c Q)
'ii. ~ E E <:::l ::c,'ã.rl .-
Q) ~ ãi cn·-
c •...
pressures will change that picture. Two hundred million pcople NII""I,! II1 e '0« C]) §
~crjcrj E zs ~.. o 'E<~~~
shifting cultivation, but they use 30% of the world's exploitable Noil/CUh, aoen
•..• '"crja. ,- a.
& Greenland, 1960). The trends are to intensify the growing 01'l/lu tl'lul
'" o
o «Í ;,.§ ~
'õ.. .. "52:0> ..:g g ~
.s .;::.~ g jl § ~,~
tional crops like cassava, applying practices that increase disease 1'01('11
0. ••.. e
0<'- :::l
rl a.~ ,e.,g ál õ g a.. 's
'" -
a. e

~ O '" o
üü ,_
o>'" üüü O ~~ ~
tial, and to use these largely tropical soils more intensely, often ror l'lOII
with which there is no experience in large-scale cropping or intcnslv.
e e @) <§)
tn e
«Í ~Q)E
:::> o.~ e 0.",
:::> 's
'e" Uiet:
«Í .. C
'O _

a..o e 'O m :::l C])

CI) 'õ ~UJeCl) '':: Em Ol
.. :::> e
13'- UiUi:::> o
10,4.3 Major Influents co t) m
00'" u::: >.:::lm ~Z
C]) E:J.. oo
U oo....oUJ .
"O c
_ Q)!D
c 'O
o.... ;;:::
~ '>." ,-
ãí CI). x'"

~1iimUi C])
'" ,-
'" ':;
:::l .c
To paraphrase prominent authorities (Duckham & MIIIWllcld, 1(70), Ou =o';::
'" oo m
Q) ca 'i:: -o a.~c ai Vi E .~ ca ~ Q)
a. ,- '" a. -0>C])00.
"agricultural systern" in any area reflects efforts fo ('Ollll1il1(' 10(:111 1'lIvl o
'O o e_CI)
C]) C]) :::l
Ui:::-o"E- e
::J m c o ::J m
ronrnent with local socioeconomic conditions in 01'(/('110NIIIINl'y 1111' 111111 ~I'I o<~ce
C ~õ::>
~ o,~w
ü Cl o
demand with maximum domestic, social, or 0<':011011111 NIIII/jI'III'lioll 'I Ir
ecological infiuents limit the range of possible 1'1111'1 I'lilll'lI, 11111 IIrl' \tI, /, I C]) C])
economic infiuents determine which of scvcrul "'IU,/"'" 1'lIh'qlllljl'" 111
m I '00
farrner chooses. In less developed arcas, cl'llloj4kllllllJ1II1'III11 IIIIVI' j,lII'ulel
Q) tlj
importance than i~ advanced CC0I101lIil~S,wlu-u- li..,,,
il'lh fto •• 111j'II\11111i il!

ment like poor soil fcrtiliry 01'lack of'WIII('1 1111'0\'1'11111111' li, 11111'11,,1/11 tllllljj I I~
.., '


10 4 VllhllllllbilllV 10,4 , Polyetlc Epidemics

,"1111'I'llpllllltion and economic prcssurcs, many areas of the l'ulyctic cpidemics occur in pathosystems in which the build-up 01' Ih
1IIIIItlOlllycalled the less developed 01' developing areas, are ,'pkJcmic takes many years. Each year, or growing season, Xo is higher,
\11111111\ tuwurd specialized, intensive agriculture. Concomitant Annual or seasonal amplitude may be large or small.
I lia \'1 lupment can be an increase in epidemic risk. The risk 'I'hcre are many examples of polyetic epidemics with small seasonal
li..lllllld hy the growing of a genetically uniform crop over large unplitude. Several insect and nematode infestations build up this way.
1111"bccn termed genetic vulnerability (Committee, 1972). The Among the fungi, those soil-borne pathogens causing the Fusarium wilts,
tllll IINk to a crop increases with the loss of genetic diversity and poluto wart disease, and club root of crucifers have this characteristic.
'1IIIIIIlIity in space. The area under a genetically uniform crop and
lli '11'1'1I1I'lItionof fields enhance continuity and, thus, risk. Zadoks and liXAMPLE 10.5: Club root around Petrograd. Woronin's (1878) classic
\llll'lIltlUCr (1977) tried to describe vulnerability quantitative!y giving it tudy of Plasmodiophora brassicae, the causal organism of club root of
li! \\ dlmension, so that it can be calculated, but their approach is toa crucifers, was done in response to a serious social and economic problem.
1111\ ti) have been tested for general acceptance. 111castern Europe, cabbage was and is a major constituent of the diet.
,'lic story ofthe southern corn leaf blight (Section 10.5.2) shows how the l'his was also true for the rapidly growing population of late nineteenth-
lllidzc crop in the United States becarne vulnerable by way of a then r outury Petrograd, now Leningrad in the USSR. Because of inadequate
uuknown and unpredictable genetic mechanisrn. Several of the "green üu'm-to-market transportation, the cabbage gardens needed to feed the
Ievolution" crops are quite vulnerable, as Safcculla «(977) rightly pointed
IIIWIl'S populace were concentrated in a narrow ring around the city. Lack
out. By the same token, the wheatcrops of'the Rornan Empirc, as irnpressive uf rotation in these market gardens led to a disastrous accumulation of
to the conternporaneous traveler then as are lhe whcut crons of North nuculum with time. The same situation pertained to several other cities
America and the USSR now, seem to have had a low VIlIII~l":Ihlllty. 'I'hc IllItside Russia. I:::,
major protective mechanism was probably the betwecn- IIlId withill fi~'ld
'I'hc polyetic disease pattern is common among diseases of perennial
I IIlpS as well: Panamadisease ofbananas (Example 7.2.2), clove wilt(Valsa
, 111/"lIia), fusiform rust of pines (Section 10.5.1). Such epidemics in tree
10.4.5 Continuity in Systems
I II'PNproceed slowly when compared to epidemics on annuals, as measured
The foregoing sections afford an opportunity to bring up and ilIustrate two li, luwer values of r (Table 10.5). But these values are partly an illusion.
attributes of systems that are important from a systems standpoint and 'I I~uue that r is low in calendar time units, but it is not low if we relate
epiderniologically: continuity in space and in time. ti 111lhe growing of the crop.
Continuity in space is easy to grasp. One of the largest pathosystems is 1\ I'IIISS of special interest is the polyetic epidemic with large amplitude
the "Puccinia path" described in Example 7.21; it covers an area of 1111111111 crops. The case of yellow rust in Chapter 7 is a good example.
500 x 2000 km, or about 106 krn". The risks incurred are those indicated ". hlllhlllp of a severe epidemic usually takes more than one season,
in the last section. hlllhlM 111. least one aestivation. Attempts have been made to simulnl
If continuity of pathosystems in space increases vulnerability, what 11 1",lví'lic epidemics (Rijsdijk, 1975), taking into account the 1111
can be said of continuity in time? Continuity in time was partially dealt ",'11111114 in the host population (Fig. 7.7) and devising special rui
with earlier as an important aspect in the discussion of endernicity .I!tlll (ljxample 7.6).
(Sections 10.2.5 and 10.2.6). When disease is endemic, there is continuity '111'Iurcgoing, only population dynamics is involved. A 1111il\ill
in time, over the years. Usually there is also stability, iR; averaging I. !11I1I11~(lOCt involves the population genetics ofthe polycuc l'l'hlt'inl
with low amplitude oscillations. But there is the chance of fiare-uns 01 jjll" /.7.3, annual and polyetic aspects offungicide 1011'111111 'oI!1il!!
epidemics. In many pathosystems, such flare-ups may OCClIr only ill'l'lI II~IIIIHH.ltl.Kiyosawa (I 976) has made calculations of 1111' 1IIIIIIIItI\111I1
sionally, while in others, they may occur every year; rnost 01' this hOIl~ li '"III'IISl' of new physiologic races ofrice blast. Durlnu li,,! 11('\111\111
deals with these pathosystems. '1111'I11111uí'cxist ing and ncw strains (to bc cornpared w'11 li 1111)II Wllll

Another kind of epidemic, the polyetic cpidcrnic, muy IIIlW 111I dl'sl,.lhnl 1"1'"1'" Hll"iIllIS in Scction 7.7) changc, so that thc ".,,1'


kinds 01' disruptive events occur; man is a source of di.\·r(/N/I/llfl"1/ III

~ '"
.~... ,IIi".'.'
~"III h,I.'11I1I1I'ftle 01 some epidemia. I" rell.llon 10 lhe growlng or rotallon
11111lCIuUhand only ordera 01 mllgnltude ,naller) simplificd agricultural disclimax ofthe agro-ecosystern is stablc ollly \\'111111
I man continually intervenes to maintain regulation.
Estlmated Orowlng An example of disregulation induced by forestry practices is provided
Apparent Inlection Perlod GP or
Rate r in Units Proportion by the fusiform rust ofpine trees in the southeastern United States. A case
Rotallon Perlod x 1000
per Unit per RP 01 host of sudden man-induced disregulation followed by prompt regulation due
to fast and adequate human intervention is found in the story ofthe southern
r r
corn leaf blight epidemic of 1970 in the United States.
d y GP RP

/nfestans 10.5.1 Fusiform Rust of Pines
tomato 0.17 120 /1.4
potato -0.40 / / 150 / 2.7 An appropriate example ofthe effects of disturbance is found in the fusiform
ruuolnie striíformis
barley 0.27 150
rust disease (Cronartiumfusiforme) ofpine trees in the southeastern U nited
winter wheat
/II/()cystis fagacearum
0.10 I 270 / 0.4 States. The following is adapted from Dinus (1974). Cronartium fusiforme
is a macrocyclic rust alternating between pines (pycnial and aecial stages)
oaks (0.0021) 0.771 I 60 I I 13 und oaks (uredial, telial, and basidial stages). Damage to oaks is small
ronartium fusiforme
slash pine (0.0011) I ~0.40 I I 30 I I 13 und of little economic importance, but infected pine needles and the
Fusarium oxysporum lusiform aecial galls on pine shoots can kill trees less than five years old,
banana (0.0014) ~0.501 I ilO I I • 25
rcduce growth of older trees, predispose branches and stems to wind
Swollen shoot virus
cacao (0.0008) I 0.301 I 20 I I 10 hreakage, and cause deformity and death of older stems. Heavily infected
tands may be abandoned, harvested prematurely, 01' used for low-value
nroducts. Nursery losses can be high if rigorous fungicidal control is not
values for the following season differ from those of the fOI'(.:golll~ IIIll' 11 practiced.
polyetic effect. Kiyosawa (1976) caIculated the mean longcvlty uf IH'W The coniferous forest of the southeastern United States comprises
cultivars with vertical resistance: it was 5 years. /H X 106 ha and produces about one-third of softwood timber and two-
Few authors have yet studied polyetic problems, but the tools IIIHI thlrds of pulpwood in the United States. Much of the forest is in the
methodology are now at hand; polyetic epidemiology is a challenge for 111" II!llstal plain and other lowlands, but it extends through the Piedmont
next generation of epidemiologists. unto the Appalachian ridges. Historically, wildfire played a large role in
Control ofthe polyetic epidemic has consisted ofbreaking the continuity uutintaining the area as a mixed coniferous-hardwood forest. Control of
of the pathosystem in time. The methods are c1assic--cultivar change, lIilllfire results in succession toward a mixed hardwood forest. Today the
chemical disinfestation, and particularly, long rotation periods. But thc 1IIIl'sl is largely artificial, a factor to be reckoned with in accounting for
socioeconomic pressures now pushing more farms to specialization and ,111'stcady increase in fusiform rust in the last 50 years. Three species of
intensification often preclude wide rotation and foreshadow the need for 1'1111' huve been the important commercial woods: Pinus palustris (Iongleaf
greater study ofpolyeticism to aid future disease management (see Chaptcr ,,1111"), P. taeda (Ioblolly pine), and P. eLLiottii var. elLiottii (slash pine). 1n
11). 1111fl\ll'sl as first encountered by Europeans, longleaf pine covered 11
!d. 1111'11 (Fig. 10.3). This species is quite fíre-resistant and so was 111111
'1Ihllsh itself in drier sites in the Piedmont where tire was conuuuu
10,5 TWO HISTORICAL EPIDEMICS " plllll, 110tfire-resistant, was limited to lowlying and swarnpy 1111'11
li J..llllIlly, also not fire-resistant, had a wide range but was flI01'I1dl'lI
In the long run, disease levels in natural systcrns WWIIIIIIl'II11ow Illllplllndt I. Ihl' longleaf area. Although wildtire interrupted !-tIHI 1111,,11111
around an iR; value of 1, except when tcrnpouu y rhllll»t'N ucvur /11llONl, 11111•• W('I'Cprcsent in the understory to varying degrccs dl"lll"lIlIllI
pathogen, or environment. Natural pHlhosysh'IIIM IIl1vl' 11 hllllllloStllNIN 111 IIIIIIIIM 111111 flrc frcquency. Among these were munv 1111111 ,'li
intrinsic self-regulation, some pioncer vl'/-IclllllllllN I'H'I'pIl1d Whl'll 111111I' .1 (11/1'11 I/.\', which are alternate hosts to C. fusifunn« 111",,111
actions are supcrimposed on lhe dlNCIISC 1IIIIIIIoIk(1I1HIIII' I I), viu lou 1111,111 ""Ii4IllIIlIi\l1l of' nines and oaks, carly reporta 1IIIIIIIIk 111111

liA 11I()/iYHII M MANflW MI N I

stands were infected. This area was all in the COIII'I11l1
0, ~l-vcre disease Ievels had been reached across a rnuch
1111klcnce remained low in poorly drained areas unfavorablc
I'J/I 1973, the range had extended and the general severity
l1ii"ll throughout. Average infection has been increasing
I" 1 VI'lIr with much greater rates in high incidence areas. A
I IIIU" incidence now spans six states; in four of these, it lies
'I '1I1~lIionzone from the originallongleaf area into the loblolly
11I1I1h.This phenomenon is no accident; here is where dis-
," !t" cxpected to have its greatest effect, as will be explained

I~" in importance of the disease can be ascribed largely to

l'hc situation is complex, requiring an analysis of past and
1 managernent practices .

. 500 km .

Figure 10.3 Natural ranges of three pine tree species in the southeastern
United States. (After Dinus, 1974.) Longleaf pine, Pinus palustris; slash pino,
Pinus elliottii varo elliottii; loblolly pine, Pinus taeda.

fusiform rust disease was rare prior to 1900, even in second growth anil
planted forests, and of no practical importance until 1930, from which
date the disease has increased in range (extensity) and intensity to l/H
point where, in 1972, it caused losses of 2.8 x 106 m" of wood valucd 111
$28 million.
Fusiform rust began to be noticed in the 1920s, when a survcy 111I 1011hHII11I1
showed an incidence ofless than 5% in an eight-year-old p/nnllllH '1'/11'IIno
regional survey in 1938-1939 showed that in Louisinnu, 111111111,'111 MI".~/
sippi, and Alabama (Fig. 10.4), in areas whcrc lun VI'IIIIIIH111/IIIlH"'11Ipl,,~ Ulll
had been especially destructive, 20 to 50% 01' IlIhlllllV lI"tI "1,,••11pllll'" 111


I 111I" IHllldence (1775-17H.I), IIwklllturc was extcndcd wlth the more resistant longleaf pine, which gave l'll
I~'Ü 1\11·11íructs were later allowed to revcrt to forest. Lar 1I11~111first, are now seen to increase the damage from pitch
\111I "mlcd during the Civil War (11HII•. IH65) and the World 1/11/ lateritium f. sp. pini) to which loblolly is resistant.
,i'IH, 11)\9-1945) and then allowed to revcrt. These disturh
.l luhlully and slash pine to invade longlcaf arcas; hardwoods,
Corn Leaf Blight
ti I, WCI'Creleased from competition and prospered. Clearing,
11_. IllIdllBlc harvesting, particularly oflongleaf pine, so reduced th ••• ,••Iml \' Pl/O, an alert plant pathologist in Belle Glade, Florida, found
III,tI Ity 1930, 90% of the naturallongleaf pine had been harvestcd, it 11 lenf blight on maize hybrids which in previous years had
"IIIIII'ldul planting had become common. Loblolly and slash pinos 11II ~INtllnce despite the common occurrence ofthe causal fungus,
1,1'11I1'tIin commercial planting because oftheir ease of planting-and ',"/111111/1/1 maydis. The fungus was causing serious leaf disease
nhl I ui ly growth. But, by this time, fusiform rust was severe enough I~ 1111,IIS well as an unexpected symptom, ear rot. The affected
IlIíli 111une plantation as many as 23% of seedlings planted had gall« "IIHiugh possessing different genes for resistance to H. maydis,
!til 11xerved to provide inoculum to nearby oaks from which more pinos , 11 produced through use of the cytoplasmic male sterility tech-
.\ I li' infected. Reforestation required fire control that favored natural ,,'" IIbservation was particularly disturbing since it was to be
IIVIINionof loblolly and slash pines into longleaf pine areas. Fire control 111111 IIS much as 85% of the total D.S. com acreage that year
IIlso allowed improved establishment and growth 01' oaks. By about 1950. 1'IIIIIIcuin such lines. The pathologist may not have known that
much of this huge forest area had been convcrtcd from ti longlcaf forcst 111111" ubservations had been made only a few months before, in
into a loblolly-slash pine-oak forest. The two subSlitlllcd pincs are nol 11111 Hl'ptember of 1969, a thousand miles to the north, in the great
only the most susceptible species, but the practiccs whlch l)I'oll~hl abOll1 /I l'hc pathologist's report, the first of the new season, had
their substitution also favored a great increase in thc ouk IIII~\IIIIII,' hosls. 111,11 ~1"Ilj(icance in that it carne from one of the southernmost com
The forest management practices attendant to commcn.:11I11'11t1l1111/4 "ItVI lill "I IlIe U nited States, where sweet and seed com are grown in
played a large role in the increase of disease. Almost 400,O()() IH'lll!!"" 1111 "11 11I1I'Illernmarkets.
planted annually on sites which are mechanicalIy prepared in<.:l\ldlllll l'IlIIP "1\ W, lhe disease was well established in the South. Disease
ping ofbrush. The latter practice retards oak growth for a few ycurx, dlll'hll· 1I0wn in Figure 10.5. Two paths formed. One disease track
which time the pine seedlings beco me established. But the chopped ollks 1'''\ 111»"r> the East Coast while the other, across the mountains in the
are not killed, and ultimately they sprout prolifically; sixfold incrcascs in I" 11I'lIlllldfor the Com Belt. In August, the greatcorn states ofIllinois
oak stems per hectare have been measured. Exclusion of wildfire favors ", ,I li11 11widespread infection. By the first of September or earlier,
the fire-sensitive loblolly and slash pines, but controlled burning as 11 Irlll ""II'es were affected.
postplanting, cornpetition-reducing treatment must be delayed for some I\'~I"111'wcather patterns showed that conditions favorable for the
years until the pine seedlings are less sensitive and their growth has becn Itmlll\\l,11d uunsport ofinoculum occurred six times during the period frorn
sufficient to allow burning to be controlled. After such burning, oaks sprout 1I~IINI,including one tropical storm which moved from the Gulf
prolifically, again increasing the density of alternate hosts. But most darnagc ,,111 III the Midwest in mid-July. Probably, massive amounts arrived
has already been done by that time. 1111"'ml'Íously affected northern areas during the normally moiNI
The effects ofthese practices are strongest in the transition zone betwecu 1~lIl1l1l1cr weather of late June, favoring disease establishmcnt nn
longleaf and loblolly pine areas. This zone in the Piedmont is suboptirnal •••••• ItH\ ,h'vl.lopment. In some parts ofthe Com Belt-southern Iml
for both pine species and more favorable for oaks; loblolly is mixed with i~',11 cxample=-inoculum arrived early enough to find w,,"11
longleafpine, and oaks are more abundant. The populations have a naturnl "'"'.hl •• /111pulycyclic development. Such areas registered the "'M'
instability and species structure not unlike that induced by rnan in 01hl~1 1i1ill'II/1111111the North as well as the greatest loss. In oth('1 1111111
areas. Smaller disturbances produce greater effects and, spcciftcnlly, 111 !Ihly Ihal sccondary development was impeded by l'lUll Wrllíl
creased fusiform rust. liillll' ,,, rclntcd not only to the time of onset of discuw !tlll 111
The outlook for the future is not bright. Resistuuce hll't'llIlI~ is 011 II 111"111 dl'vclopmcnt, crop loss was rnost severe in uuur lI\iI!íI
way, but genetic disease management is still in Ih,' lutllll' nml wlll 111 li' IlIm'III\1111urrivcd curly and whcro wcather gIlK'III1I~',llli
impeded because of the high potcntial for hClt'I'Of..IIIYlIlk IIlId "1'X 1111 I 11' ••••••••• li •• "'IIH 11I·,lllds, SlIl'h 1!I'casoftcn hnd cunsidcrnbíe cu: I li'
cotnbination ofthe rust and thc lonu time req 111111I11111",,·,·dlllu IIlId 111",1111 1"11'01,,,111'111dlNt'IIN,' IWitll1lrl'IIIIivl'ly tlllt' IIlld Whl'l


01' lhe seed corn planted was of hybrid types (a plll~'lh I

lu 1I1111cd States in the 1930s and intensified greatly after Wol'ld

11t11l~1 lhe entire U.S. corn crop was greatly changed. Probably,
111lrercrogeneity was given up in return for greatly increased
1111:11 But the methods of maize breeding differ from those of
di. I1l1dcultivars with vertical resistance are practically un-
1111,bccause the U .S, corn-producing area is so large, with
".""!lh'I'lltll vnriation in growing season, ecology, and cropping practices
" , IlIlsiderable diversity of plant diseases, and because seed corn
Ihllluml sale is a highly competitive and lucrative private business,
111111101' maize types is deployed. In this way, the national crop still
1I1~ldl'I'lIblegenetic diversity, although evidence indicates that in
Sept. 1
k:::;;;::lj:;::;j 111111' 71% of the crop derived its resistance from only 6 of 119
Aug. 15 11" lubrcd lines. Nonetheless, it becomes even more puzzling how
~ July 15 IIIW race could attack 80% of this national population.
!11m June 15 I'llultlction for a hybrid corn crop is itself a highly controlled and
lIl'II"" I 1,IIIdof agriculture. Seed sufficient for one year's crop must be
101lhe.' previous year by the crossing of the selected parents. The
1I1IHIlld parents must be protected from pollinating each other. For
1111 N, emasculation by detasseling was accomplished by hand and
11\' uuwhine, at a cost of $120 to $450 per hectare, In the 1950s, male
Figure 10.5 The 1970 epidemic of southern corn leaf bllgllt (1111/111111111" '11\ \\IUSdiscovered. Male sterile lines produce pollen incapable of
sporium maydis) in the United States. Disease progress map. i""
'11 1i was quickly seen that ifthe fernale, or seed, parents possessed
1'111,(hey could not pollinate themselves. And, if the male parent
.'I\'I,~~1t1 1\ pollen restorer gene, the hybrid, when grown the following
development may have been small, damage was cornmensuratcly less, '"11111(Ince again be self-fertile. So, through genetics, expensive
Losses ranged from 100% in some southern fields, through an average loss 1,111111& WHSeliminated with benefits to both the seed producer and
of 20 to 30% (with instances of 50 to 100%) in Indiana and Illinois, [o I 1III'I'l' are now a number of genes known that give male sterility,
negligible losses in some northern and eastern areas. Losses could be only Íll'd ull production depended on but one gene, Tcms, Texas cytoplas-
estimated for such a widespread epidemic. The best available data placc 11,~II'I'i1e. As the name implies, the character is cytoplasmically
the loss at about 15% of the total American crop (2.5 x 107 hectares), I IIV lhe mid-1960s, almost 80% ofU.S. corn acreage was planted
amounting to some 20 million metric tons, worth at that time about 1111'II'od produced with this technique.
1,000,000,000 dollars. Such a loss had strong effects on reserves and 011 l hl I lcur vision of hindsight, it can now be seen how the 19711
international prices, as well as on supplies for on-farm and industrial use. II'III\lIl'cd so suddenly and how pathologists and breeders ov
How did such an epidemic appear so suddenly? Given the statc 01 I h lndications. The many hybrids in use in the various 1.'11I1
knowledge about the risks of widespread display of uniform germplasm, IIIINhad been severely tested for disease resistance. SUI"h"l"
howdid ithappen thatas much as 80% ofthe U .S. corncrop was susccptihlc' hllWhl had been reduced to a relatively minor diseasc; 1111
The answers bring forth an explanation of a previously unforcsccn hU:1I1I11 """4,"U iil/II lcuf blights together produced an average IONN111'IIllllill
in modern plant breedirig. 1111/1'(/1,1' was not static, or uniracial. In 1961, it WIIIIItlfil.!!Wíl
Maize is a cross-pollinated plant and so has more ~l'Ill'lk hl'It'l'oHI'llI'ilY hlllJlJllrll's IhHI Iwo lines with Tcms character wcre 1I1I~1)'IHlhl
than self-pollinated or clonally propagated crops. W(' wuuhl 11011'''111'1'111 IIh II'sislllllCC gcncs. In 1968, 100,000 kg of s~'l'Illlilii \\'lll
to be uniformly susceptible to single races ofpulhoHI'II"1 Blllltn Ulllil' 111111/1 IIlldl'lIlV IIfllwllrin~ ('.11'rol; only during the 197() t'1,hh'''Ill: \\lU
exhibits hybrid vigor, breeders learncd 10 pl'Oíltll'l' !lVIIl1111(1'1'""V 1'1111'111I111 •••••• 11111111111I ""Ii l'UIISt.'d hy 11new racc, In 1969, somo MI't'll1\i.l1í.1" i
inbred lines, a technique that rcquircs P1'l'Vl'1I1h1l111111111'111'111111111111111 11'1111'1111111\1\11I111111
NIISl'('Plihilily thut WIISIIlwIIV~1I111i1iljlt''I,1


!II( , 11I11I1I.'ICI'. '1', WIiMevcntually describcd,

The ncw 1"111.'(\, Ih" ,',' IIIIINlrates, although with an interesting variation, the dan-
!\\H I1 pIII'ls did not reach lhe Iilí.lI'llIlIl'C until August and iol, 'Pll"III genetic uniformity 01', conversely, the value of subspe-
;;,'0, when the epidemic was linisllillg, Aftcr the epidernic, H:I "I" !lei j y in disease management. It may have been the most
!lIIII!IIHlllií' I 1111 Hí.lworld collection of H. maydls mude between 195~ Ij" •• IItHIc.!season epidemic ever experienced and certainly it was
I 1)1111kly controlled one. Note that the only human intervention
ilu" I ti "Ice T to have been present in many parts of the world
\I 11I'l'ol'cthe epidemic but mainly on gramineous hosts, not
'11I " •• W, H. maydis got its foothold and encountered the right
'11 I" umnipulation,
inl 111I1·11 multiplication.
rapid, on large scale, using the winter season

" ,'11'111before it was fully realized that alI plants with the Trlll"
I, I wore susceptible and that this factor overweighed any resistance
.I, flloyed, with the result that 80 to 85% of V.S. com acreage WHS 11111111\11 Intervention: Regulation and Disregulation
1,ltI, uly" susceptible to a single race.
'" Ip/t'SS to combat the ongoing epidemic, plant pathologists spent thc 1111IIINI was but a mino r disease with natural endemicity, but with
""11111'"and autumn of 1970 piecing together the picture outlined abovc, 1I'IIiH'of human disturbance, it "crept upon us," imperceptibly at
\\1111111 lhe epidemic repeat itself in 1971? Would it be worse by virtue 01' illllllppllble now. Originally, ali tree species had more 01' less their
IlIm'II/um which would overwinter in the grcat northern corn regions, "I,,, I' 'l'he amount of dangerous slash pine-oak overlap was limited
, uming forth early to initiate disease which would have a whole season to 111""111 hound distribution. Fire control and the unrestricted planting
.lcvastate the crop? The seed companies took SICps 10 provido as rnuch 1,,-11plnc changed the subtle natural balance, and the disease has run
sced without the Tems character as possible. In 1970, I lu-y had produccd , , 111111'01. Chernical treatment and oak eradication are impossible for
some for areas where yellow leaf blight (Phvllosücta 1//(/,1,,/1,\') WIIMIhl'oal h·1\ 1\1' reasons. Resistance breeding of slash pine offers some per-
ening, because an association between Phyllosticta susccntthill! y III1I!'1',,"," , 111 lhe long run, if the longevity of the resistance is satisfactory.
cytoplasm had just been reported. Attempts were madc 10 im'l ('IINI' NI'I'd \ II V long run, commercial pine growing will be possible only when
supplies with normal cytoplasm during the winter of 1970-/971 1111"111111111, 111111 írom ecology are learned and translated into action; rapid
Hawaii, the Caribbean Islands, and in Central Arneriça. Arncricnn hylll 11/ , 111111I1 with immediate results seems to be out of questiono
grown in Argentina, Hungary, and Yugoslavia were imported, nOI IIlwllys 11111110m com leaf blight offers a story contrasting in many ways.
with successful results. In the spring of 1971 it was thought thcre WIIS , WI'I'Odealing, not with a natural ecosystem and creeping human
enough normal cytoplasm seed to plant only 25% ofthe acreage and cnough 1011111 li, but with a stable agro-ecosystern and sudden disregulation.
of blends of normal and Tems seed to plant another 40%. The rest would ,I \\ 11Mrcgained nearly as fast as it was lost. Genetic manipulation
have to be of Tems, open-pollinated varieties, and F2 normal cytoplasm IIII1WCI',made possible by an enterprising and highly skilled corn
seed from 1971 hybrid production tields. 1111dlsí.lHSewas brought back to its state of managed endemicity ai
Despite ample overwintering of the fungus in the South and weathcr li!\'{ I
conducive to disease development in the early summer, blight did not once
again reach high levels. In the Com Belt, inoculum survived, even in some
northern -areas, but the disease failed to develop significantly, with some
few exceptions, partly because of unusually cool wcaiher in July and dlnu
August. Stands of com planted with normal or blcndcd seed probabl
dampened disease development. In the East, despite lho limited supplies I \ 1974. Relevance of knowledge about natural ecosysl
of normal seed, and overwintering of the fungus, ouly lilllall arnounts 01 .UIIII'lm.l.1I1 "I ncst management programs for agro-ecosysterns. 1'111
disease occurred. The largest missing factor in 1971 WIISprobuhly lho hllijl'
",.1111",111111 HII\~, I: 191-199.
. I1 VIIII,1975. Natural biological communities and intl'l "'Ifill
amount ofinoculum blown northward, a result of Iho Il'dlll'l'd disollso IL'VI'I
111110'11111'11 Nitrogenous Fertilizer Rev. No. 18: 22-32.
in the South.
, N, ""ti G. B. Mascfield. 1970. Farming systerns 111IIr
During 1971, seed producers convertcd 1\111101'11 1'lllIldy '''"III'llllIll'yll WII"III~. I .ondon, 542 pp,
plasm, and despite accumulating cvidcnce Ihlll '"1' l1l1lW1II1 1'1111
OVi" WIIIII'I " 1'1/ \ 'I '.'OP"-:II
I IIA"ill'Cosyslems. Scicncc 182: 1211 1.'I
in the North and that the pathogcn with l'III'Ir I'"".'IIH VI'1I11/1IIm'ulIlllI I I III'IIIV01'pllll1ls lu 111\,tronic», Sludios in hiologv N"
more fit, southern corn leaf blhdll 1MIIIH'I' 1110111111 ,I 11111 •• " 111""11 1'1'

P/\ 1IHlfiVll1 1 M M 1 NI

til! J~ !lHI! t! 111"111111111111 01' the agro-ecosystern? Ir SO, why?

III I, \\'11,11 I~ IlIi. I ,111' trophic level(s) of (a) Erysiphe graminis, (b) Penicillium IDI MIOLOGY ANO PLANT OISEASE
/11/'. (c) Phytophthora infestam', (d) Septoria nodorum, and (e)
li' vlrtde? MANI\GEMENT
t, ,I ,lIlIlollowing was the key factor in promoting fusiform rust (Section
I' 111'LlI'IllSof comparative epidemiology: xo, p, i, N, or E?
lul ""I~dcnces operate at various integration leve/s, and so does epide-
I1"'I/lI You are familiar with Phytophthora infestans and you have an
"I. ,,1"IIl' knowledge of the disease caused by that fungus. Mention 2 or 3
IlIh Il/llllon levels and describe for each levei some facts (phenomena, proc-
I "fllN) Ihat can be studied at the integration levei mentioned and not at the
IIIll(l lower level.

111I 'huptcr 9 we divorced ourselves from the scientifically well-established

, jlhll'llIlologic theory and pointed toward larger vistas, therewith introducing
1111' h'ltlent of speculation. The area of epidemiology was revisited in Chapter
IfI IItllI viewed in a wider perspective. Systems .terminology was chosen as
I vrhlclo of thought, but this choice, and the statements made in that ter-
1IIIIIIIIo"y,reflect more the authors' opinions than established scientific truth.
1111 ~lIllle can be said, a fortiori, of this chapter, which outlines some
"II"II'q\lCnCes of epidemiologic reasoning, It shows where the chosen trail
,I I11,11 I(o(h I may lead when it is followed toward implementation in practice.
I 1I'''lIllIlogists set the example by cutting out a similar trail, which leads along
"" 1\11111·11 control toward pest management. Through hindsight, we may say
l!till IIIIIIf.llllted control of funga! diseases and fungal disease management
11\1' IH'IIII, to some extent, applied by phytopathologists as long as phyto-
li,IIIIIYhas existed. The present and possible future position of integrated
1111111,,1' lungal diseases and fungal disease management are sketched. The
111'I1'I~ 01' ihresholds of damage, action, and warning are defined. SOIllI'
h'tlil~1 1IIIIIIIIgement systems have led to serious problems: vicious cycl
Illh'lI" ulleys. Some ofthese-the breeding cycle, the chemical cyclr , 111111
I~i!i"111'I'lImulation of inoculum-are examined in the hope 111111 .lIl'I
11'1I1~1'1I1ibe avoided in the future. Some feedback, both plI"III\'1I ••li
I~.·I~hullcated. Biologic control offungal disease, yet lu I,~l!if.11I
.'lIlllIillv becornc another useful alternative in plant diNt'1I

1111•• 11I1I(l11'1 I,. 1111'11""1\' 1111I111I1-\1'1111'111 11

1IIIIIIIIIlV 111111I111111 11 1IIl'IIIIIIIbllll' 111111111111