Induced Plant Responses to Herbivory - Terrestrial Systems Ecology
Induced Plant Responses to Herbivory - Terrestrial Systems Ecology
Induced Plant Responses to Herbivory - Terrestrial Systems Ecology
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Annu. Rev. Ecol. Syst. 1989. 20:331-48<br />
Copyright © 1989 by Annual Reviews Inc. All rights reserved<br />
Annu. Rev. Ecol. Syst. 1989.20:331-348. Downloaded from www.annualreviews.org<br />
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INDUCED PLANT RESPONSES TO<br />
HERBIVORY<br />
Richard Karban<br />
Department of En<strong>to</strong>mology, University of California, Davis, California 95616<br />
Judith H. Myers<br />
The <strong>Ecology</strong> Group and Departments of <strong>Plant</strong> Science and Zoology, University of<br />
British Columbia, Vancouver, British Columbia, V6T lW5 Canada<br />
PHENOMENA OF INDUCED PLANT RESPONSES<br />
Changes in plants following damage or stress are called "induced responses."<br />
In the broadest sense, these changes can increase the "resistance" of the plant<br />
<strong>to</strong> further herbivore attack by reducing the preference for, or effect of,<br />
herbivores on the damaged plant. It should not be assumed that these changes<br />
which provide resistance evolved as a result of selection by herbivores. In<br />
some cases the reponses may currently act as "induced defenses"; that is, they<br />
are responses by the plant <strong>to</strong> herbivore injury or the invasion of microparasites<br />
that decrease the negative fitness consequences of attacks on the plant. These<br />
terms-"induced resistance" and "induced defense"-are used by different<br />
people <strong>to</strong> mean a variety of different things. Workers in this field would<br />
benefit by agreeing upon a set of definitions, and we offer a dicho<strong>to</strong>mous key<br />
of these terms (Table 1). Note that an induced response could conceivably<br />
operate as a defense without decreasing herbivore preference or performance.<br />
Instead, it may make the plant more <strong>to</strong>lerant <strong>to</strong> herbivory. Although "induced<br />
defenses" are widely discussed, <strong>to</strong> our knowledge no one has shown an<br />
induced response <strong>to</strong> be defensive, i.e. no one has explicitly measured the<br />
influences of the change on the fitness of the plant.<br />
Not all induced plant responses increase resistance by making plants less<br />
suitable as hosts. On the contrary, an extensive literature describes increases<br />
331<br />
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332 KARBAN & MYERS<br />
Table 1<br />
A dicho<strong>to</strong>mous key for induced responses<br />
Does stress or injury change plant quality?<br />
1 NO: No response<br />
l' YES: INDUCED RESPONSE (proceed <strong>to</strong> 2)<br />
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Does the induced response decrease herbivore preference or performance?<br />
2 NO: No effect or induced susceptibility<br />
2' YES: INDUCED RESISTANCE (proceed <strong>to</strong> 3)<br />
Does reduced herbivore preference/performance increase plant fitness?<br />
3 NO: The plant is not defended by the response<br />
3' YES: INDUCED DEFENSE<br />
in plant quality following injury caused by drought (104), nutrient deficiency<br />
(70), solar radiation (66), low temperature (46), high temperature (94), air<br />
pollution (20), and previous damage caused by herbivory (107). Much of the<br />
evidence for changes in resistance associated with induced responses comes<br />
from bioassays of induced foliage under labora<strong>to</strong>ry or artificial field conditions<br />
(reviewed in 28, 84). While the proportion of cases in which induced<br />
responses act as defenses against herbivores may be uncertain, we would like<br />
<strong>to</strong> consider in this review the characteristics of changes that relate <strong>to</strong> their role<br />
as defenses. What are the changes, why and how might they occur, and what<br />
might be done <strong>to</strong> further understand their influence on plant-herbivore interactions?<br />
Specifically, which changes are likely <strong>to</strong> act as effective defenses<br />
and how might they work? Which herbivores are likely <strong>to</strong> be affected? Have<br />
these responses evolved as defenses against herbivores? Under what conditions<br />
might selection favor facultative induced defenses rather than preformed<br />
constitutive defenses?<br />
WHAT CHANGES FOLLOW DAMAGE?<br />
Secondary Metabolites and Phy<strong>to</strong>alexins<br />
Injuries <strong>to</strong> plant tissues cause a wide array of plant responses. The nature of<br />
the response varies with plant type. One area of progress has been <strong>to</strong> recognize<br />
that the way trees respond is associated with their growth pattern and<br />
nutrient status (14). A cataloging of plant responses is beyond the scope of<br />
this review, although a few representative examples are provided. Many<br />
studies of induced responses have considered changes in tannins and phenols,<br />
products of the shikimic acid pathway. Relative activity of the enzyme<br />
phenylalanine ammonia lyase (PAL) can determine the production of phenolics,<br />
including lignin (19). Induction of the phy<strong>to</strong>hormone ethylene by tissue<br />
damage may influence the production of PAL and therefore the concentration
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of secondary metabolites (110) and leaf <strong>to</strong>ughness (47). The exact role of<br />
ethylene in this process remains controversial (72). Many agents of environmental<br />
stress correlated <strong>to</strong> herbivory can also cause increases in secondary<br />
metabolites (71). Patterns often vary depending on the his<strong>to</strong>ry of the plant.<br />
The balance between many primary and secondary metabolites influences the<br />
response of plants <strong>to</strong> stress and also the effects that these plant responses will<br />
have on herbivores. Herbivore damage often affects the concentrations of<br />
available nitrogen and other important nutrients in foliage (7, 97). A major<br />
problem facing workers in this area is determining which of the many<br />
secondary plant chemicals and plant nutrients that change following damage<br />
or stress are responsible for the overall effects on herbivores. The range of<br />
induced changes is so great that it is impossible <strong>to</strong> investigate all these fac<strong>to</strong>rs<br />
and difficult <strong>to</strong> determine rationally which are worthy of study.<br />
In some instances, herbivores elicit plants <strong>to</strong> synthesize phy<strong>to</strong>alexins (1,<br />
68, 100). Phy<strong>to</strong>alexins are low molecular-weight, antimicrobial compounds<br />
(63) usually present in plants at extremely low concentrations prior <strong>to</strong> infection.<br />
These can be synthesized de novo by plants following microbial infection,<br />
and effectiveness is determined by the speed and magnitude at which<br />
they are produced and accumulated (62). Limited evidence suggests that<br />
phy<strong>to</strong>alexins may be active against insects as well as plant pathogens (90, 95,<br />
74, 32).<br />
Physiological and Morphological Changes<br />
The response of plants <strong>to</strong> herbivores can be more extensive than simply<br />
modifications of secondary metabolite concentrations. For example, spider<br />
mites cause widespread changes in the cy<strong>to</strong>logy, his<strong>to</strong>logy, and physiology of<br />
their host plants, including modifications of pho<strong>to</strong>synthetic and transpirational<br />
rates, and they can inject substances that can act as plant growth regula<strong>to</strong>rs<br />
(reviewed by 59).<br />
Herbivores can influence the morphology of their food plants by causing<br />
increases in the density of prickles, spines, and hairs (reviewed by 79), by<br />
causing the return <strong>to</strong> juvenile growth form (11), or by affecting the phenology<br />
of plant processes such as leaf abscission (106). Many herbivores are "specialists"<br />
on plant tissue of a particular physiological age, so that altering the<br />
synchrony between plant and insect could act <strong>to</strong> make the plant appear more<br />
resistant. All of these changes could have an influence on herbivores, or on<br />
the extent of further herbivory.<br />
DYNAMICS OF PLANT CHANGE FOLLOWING<br />
HERBIVORE DAMAGE<br />
<strong>Plant</strong>s respond <strong>to</strong> herbivore damage over spatial scales ranging from single<br />
leaves <strong>to</strong> whole trees and over temporal scales ranging from minutes <strong>to</strong>
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evolutionary time. Most of the studies that point <strong>to</strong> induced resistance,<br />
assayed as a decrease in herbivore performance, have found that the response<br />
was systemic at least <strong>to</strong> other parts of the damaged shoot. However, one study<br />
measuring rapid increases in foliage phenols found that this chemical response<br />
was not systemic in birch trees (99). The spatial extent of the induced<br />
response may determine whether the response acts as a defense. A localized<br />
response may encourage herbivores <strong>to</strong> feed elsewhere on the same plant;<br />
damage <strong>to</strong> the plant will be spread but not reduced. Surprisingly, no study has<br />
explicitly mapped the spatial extent of induced resistance in all parts of the<br />
entire plant. Despite the exciting suggestion by Rhoades (86) and Baldwin &<br />
Schultz (4) that plants may become more resistant in response <strong>to</strong> cues released<br />
by damaged neighbors, subsequent experiments have been few and have not<br />
supported the idea (80, 28).<br />
Some responses are known <strong>to</strong> occur within several hours after damage, as<br />
in the case of proteinase inhibi<strong>to</strong>rs in damaged foliage of solanaceous plants<br />
(reviewed in 108) or latex in damaged cucurbits (16). What component of<br />
damage signals rapidly induced responses is generally not known. Damage <strong>to</strong><br />
tissues may release cell wall fragments that are translocated <strong>to</strong> other parts of<br />
the plant where they activate genes that code for enzymes, such as proteinase<br />
inhibi<strong>to</strong>rs (91). In this case the signal is transported systemically within<br />
injured <strong>to</strong>ma<strong>to</strong> plants but is directed primarily up the stem from older leaves <strong>to</strong><br />
younger ones (69). The proteinase inhibi<strong>to</strong>rs accumulate in vacuoles of<br />
uninjured cells of injured plants and are deleterious <strong>to</strong> some caterpillars 00).<br />
<strong>Induced</strong> resistance need not involve de novo synthesis; damage may bring<br />
preformed enzymes and substrates in<strong>to</strong> contact, causing the production of<br />
active agents (21). Enzymatic activation of compartmentalized precursors is<br />
responsible for many reactions, including the cyanogenic response of plants <strong>to</strong><br />
herbivores (21, 49). Damage <strong>to</strong> tissue may release ethylene that stimulates the<br />
production of PAL and increases in phenolics (110, see also 72). Phenolics<br />
are not transported from damaged <strong>to</strong> undamaged birch leaves; rather, they are<br />
synthesized in undamaged leaves following increases in PAL activity (34).<br />
The mechanisms of responses that occur over several years are also poorly<br />
unders<strong>to</strong>od. <strong>Plant</strong> tissue that dcvelops in the growing season after marked<br />
defoliation often shows increases in phenolics and fiber, declines in nutrient<br />
concentrations, regrowth of juvenile tissue, and changes in plant morphology<br />
(rcvicwed in 102, 79).<br />
MECHANISMS: ACTIVE RESISTANCE OR PASSIVE<br />
DETERIORATION?<br />
While enzymatic activation of precursors and synthesis of phy<strong>to</strong>alexins and<br />
proteinase inhibi<strong>to</strong>rs are clearly active processes, changes in plant chemistry
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following defoliation may result from a passive rearrangement of resources<br />
within the plant. The distinction is that active responses involve de novo<br />
synthesis or energetically costly enzymatic processes, whereas passive responses<br />
involve only the consequences of tissue removal. Passive responses<br />
have been described as nutrient stress by Tuomi and coworkers (98, 99), as<br />
carbon-nutrient imbalance by Bryant and his associates (13, 14), and as<br />
passive deterioration by Myers & Williams (80). According <strong>to</strong> this hypothesis,<br />
a tree growing in an area with abundant soil nutrients (a fast growing<br />
tree) loses proportionately more nitrogen and other nutrients and less carbon<br />
during defoliation because it had proportionately more nitrogen in its leaves.<br />
Subsequently, carbon may be replaced in the leaves at a faster rate than<br />
nitrogen, and the surplus allocated <strong>to</strong> carbon-based allelochemicals (terpenes,<br />
resins, tannins, and other phenolics) and fiber. These foliar changes are<br />
expected <strong>to</strong> reduce the preference and performance of herbivores on trees that<br />
were previously defoliated. On the other hand, trees growing in nutrient-poor<br />
conditions or which s<strong>to</strong>re proportionately more carbon in their leaves (evergreens)<br />
may respond in the opposite way; defoliation may reduce the concentrations<br />
of carbon-based chemicals and increase the palatability of leaves<br />
of these slow-growing trees in the next growing season (14, 15, 24, 98).<br />
This model leads <strong>to</strong> several testable predictions (see also 98). (a) Nitrogen<br />
fertilization of defoliated trees should negate the nutrient imbalance and<br />
cancel the induced response; (b) carbon stress should result in a collapse of<br />
carbon-based resistance; (c) if herbivory and plant crowding reduce the same<br />
nutrients, then the effects of these two stresses should be qualitatively similar<br />
(57). Experimental N fertilization of birch trees increased foliar nitrogen and<br />
reduced phenolics, while root damage, which reduced nutrient uptake, reduced<br />
foliar nitrogen and increased phenolics (97). Larsson et al (64) found<br />
similar patterns between carbon availability (light) and carbon-based phenolics.<br />
Shading (reduced C) increased the palatability of willows <strong>to</strong> snowshoe<br />
hares, presumably because of reduced carbon-based defenses (12). Clipped<br />
and shaded willows produced regrowth shoots with lower concentrations of<br />
carbon-based secondary compounds, that were more preferred than clipped<br />
and unshaded trees.<br />
The resource rearrangement model does not explain all observations,<br />
however. Nitrogen fertilization of artificially defoliated birch trees did not<br />
negate the induced resistance as assayed by autumnal moth caterpillars (39).<br />
Crowding cot<strong>to</strong>n plants reduced their suitability <strong>to</strong> spider mites; however,<br />
crowding and herbivore damage did not act additively <strong>to</strong> reduce foliage<br />
quality for mites or verticillium fungus (57). On the contrary, induced resistance<br />
was only apparent when plants were not crowded, suggesting that<br />
resources are required for the induced response <strong>to</strong> occur.<br />
These tests of the passive model are not easy <strong>to</strong> interpret. For example,
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nitrogen fertilization and carbon stress could produce the result predicted by<br />
the model for many reasons having nothing <strong>to</strong> do with the hypothesized<br />
nutrient stress. Nitrogen fertilization could cause ratios of specific amino<br />
acids <strong>to</strong> become unnaturally lopsided or levels of nitrogen <strong>to</strong> become higher<br />
than optimal for herbivores (82). More convincing tests of the model would<br />
cause changes in nutrient ratios by means other than herbivory (by plant<br />
crowding or more careful fertilization treatments). The effects of these treatments<br />
on both plant chemistry and plant quality for herbivores could be<br />
measured.<br />
Tissue removal by herbivores may alter the plant physiologically, making it<br />
more resistant in the process. Pruning commonly causes shoots <strong>to</strong> exhibit<br />
juvenile characters compared <strong>to</strong> unattacked shoots of similar plants. Juvenile<br />
growth is often characterized by greater concentrations of secondary chemicals<br />
or physical resistance (14, 79). Although these responses cause an<br />
increase in less palatable tissue, they are probably examples of generally high<br />
protection of the juvenile stage.<br />
INFLUENCE OF INDUCED RESPONSES ON<br />
HERBIVORES<br />
Field studies on the effects of induced responses on herbivores have yielded<br />
extremely variable results among plants within a population, and among<br />
populations (reviewed in 26, 34). Much of this variation may be the result of<br />
differences in species, age, genotype, his<strong>to</strong>ry, and environmental fac<strong>to</strong>rs (17,<br />
26, 48). Despite this variability, we can make preliminary generalizations<br />
about the timing and spatial extent of induced responses, and specificity of<br />
their effects on herbivores.<br />
Timing of <strong>Induced</strong> <strong>Responses</strong><br />
The rate at which induced changes occur and the rate at which they are relaxed<br />
determines whether they affect particular herbivores. The critical distinction<br />
between rapid or short-term responses versus long-term responses is neither<br />
the rate at which the response occurs nor the rate of relaxation of the response.<br />
Rather, these rates must be compared <strong>to</strong> the relevant events of attack and<br />
resultant damage. Short-term responses occur during the attack such that the<br />
attacking individuals experience the consequences of the changes they induce.<br />
Long-term responses occur following the attack and have little effect on the<br />
attacking individuals but can influence herbivores that attempt <strong>to</strong> use the plant<br />
at later times. The effect of an induced response must be considered in terms<br />
of the life his<strong>to</strong>ry and mobility of particular herbivores. The same plant<br />
response may affect only subsequent generations of short-lived herbivores<br />
such as spider mites, or it may affect the attacker in the case of a longer lived
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caterpillar. Less mobile herbivores, such as leaf miners, gall formers, and<br />
bark beetles are more likely <strong>to</strong> be affected by localized responses than are<br />
herbivores that constantly move.<br />
The distinction between responses that influence the attacking organisms<br />
and those that influence only later challengers <strong>to</strong> the plant is important<br />
because, in theory, the consequences of these two effects should be quite<br />
different. <strong>Induced</strong> resistance effective against the organisms causing the<br />
response is more likely <strong>to</strong> reduce the local population of this herbivore species<br />
(37). <strong>Induced</strong> resistance activated only after the attacker has left works as a<br />
negative fac<strong>to</strong>r with a time delay and is much less likely <strong>to</strong> have a stabilizing<br />
effect (37, 73). However, increased instability caused by a delay in the<br />
induced response could still be accompanied by a reduction in mean herbivore<br />
density. Using simple models of induced resistance involving mobile nonselective<br />
herbivores with continuous generations, Edelstein-Keshet &<br />
Rausher (22) argued that increasing the rate at which plants respond or<br />
decreasing the rate of decay of the response make it more likely that induced<br />
resistance will affect an herbivore population.<br />
Both common sense and mathematical theory suggest that the rates of<br />
induction and relaxation will influence the consequences on herbivores.<br />
Nonetheless, we know relatively little about these rates because the appropriate<br />
experiments are difficult, involving several treatments that must be subsampled<br />
at several different time intervals. Most of the studies that followed<br />
the time course of the induced response have found that the organism that<br />
causes the damage also suffers the consequences [caterpillars on birch trees<br />
(9, 41, 109), beetles on cucurbits (16, 96), spider mites on cot<strong>to</strong>n plants (55),<br />
caterpillars on <strong>to</strong>ma<strong>to</strong> plants (10, 23), mites on avocado trees (75), beetles<br />
and fungi on pines (83), aphids on cot<strong>to</strong>nwoods (106), cicada eggs in cherry<br />
trees (50), and caterpillars on oaks (89)]. However, three studies which<br />
showed evidence of induced resistance found that the response was delayed so<br />
that it had less chance of affecting the individuals (not the species) that caused<br />
the induction [mammals on acacias (111), hares on birches (13), and caterpillars<br />
on larches (6)]. The extent <strong>to</strong> which these individual herbivores are<br />
terri<strong>to</strong>rial or otherwise feed on the same individual plants in successive years<br />
determines the likelihood that they will suffer the consequences of their<br />
previous feeding. Some induced effects can accumulate if the stress continues<br />
for several years. For instance, performance of gypsy moth caterpillars on<br />
black oak trees decreased as the number of years that the trees had been<br />
defoliated increased from 0 <strong>to</strong> 3 (101). Several studies have found that<br />
induced resistance increased as the level of injury <strong>to</strong> the plant increased [mites<br />
on citrus (44), mites on cot<strong>to</strong>n (Figure 4 in 53), caterpillars on birch (Figure 1<br />
in 40)]. These results suggest that induced resistance should probably be<br />
thought of as a graded response rather than as an on/off process.
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Many ecologists became interested initially in induced responses because<br />
they provided a potential mechanism <strong>to</strong> explain multiyear population cycles<br />
of forest insects. The hypothesis presented by Haukioja & Hakala (38) and<br />
Benz (8)-that plant quality decreases after defoliation and then increases<br />
gradually after a lag of several years-provides a delayed density-dependent<br />
mechanism that could potentially drive population cycles of herbivores (11,<br />
36, 87).<br />
To explain regional synchrony of population fluctuations of forest Lepidoptera,<br />
we must test whether host trees respond in a consistent manner <strong>to</strong> insect<br />
attack. This basic premise does not seem <strong>to</strong> be supported: <strong>Induced</strong> responses<br />
of trees have been found <strong>to</strong> vary among species, among populations, among<br />
years, and across environmental gradients (81a). On the other hand, changes<br />
in the fecundity and survival of fluctuating populations of forest Lepidoptera<br />
often show consistent patterns through the cycle, even when caterpillars feed<br />
on different species of host plant, in different areas, and following different<br />
his<strong>to</strong>ries of attack (77, 78).<br />
Although the variation in response of trees <strong>to</strong> herbivore damage seems <strong>to</strong><br />
make inducible changes in food quality an unlikely explanation for the cyclic<br />
population dynamics of forest Lepidoptera, we list in Table 2 further predictions<br />
of the hypothesis that can be tested. Observations on cyclic populations<br />
of tent caterpillars and other forest Lepidoptera do not support<br />
these predictions (77, 78). The importance of inducible changes in food<br />
plant quality <strong>to</strong> population dynamics of nonoutbreak species has not been<br />
studied.<br />
Table 2<br />
Testable predictions arising from the hypothesis that population cycles of forest<br />
Lepidoptera are driven by deterioration in food plant quality following feeding damage from<br />
increasing numbers of herbivores. Species and populations of host trees must respond in a<br />
consistent manner <strong>to</strong> herbivore damage for the fluctuations of different populations of insects <strong>to</strong><br />
remain in synchrony within a region.<br />
1. Fecundity and survival of herbivores will be related <strong>to</strong> the his<strong>to</strong>ry of attack on trees.<br />
2. If the response of trees is density dependent, fecundity and survival of herbivores will decline<br />
with increasing density (level of attack) and deterioration in food quality.<br />
3. Decreasing fecundity and survival of herbivores following damage <strong>to</strong> host plants will be<br />
translated in<strong>to</strong> a decline in the population density.<br />
4. Cropping of herbivore density <strong>to</strong> reduce damage will prolong the outbreak phase of the<br />
population.<br />
5. Introduction of herbivores <strong>to</strong> suitable foodplants in sites with no previous herbivore damage<br />
will lead <strong>to</strong> an outbreak out of synchrony with natural populations.
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The Specificity of <strong>Induced</strong> Resistance<br />
Most vertebrate immune responses are highly specific. We can ask two<br />
questions regarding the specificity of induced resistance against herbivores<br />
and other plant parasites: (a) Are plant responses triggered specifically by<br />
particular parasites or injuries? and (b) do plant responses have activity only<br />
against specific challengers?<br />
Many studies have found that artificial damage causes responses in plants<br />
that affect herbivores. However, these tell us little about whether the responses<br />
caused by artificial damage are physiologically the same and similar<br />
in strength <strong>to</strong> those caused by herbivores. Studies that include at least three<br />
treatments (plants damaged by herbivores, plants damaged artificially, and<br />
undamaged controls) are more informative. Several such studies found that<br />
artificial damage caused effects similar <strong>to</strong> those resulting from actual herbivory<br />
(30, 51, 81). However, several studies found that the effects of injury<br />
inflicted by herbivores and by artificial means were different in extent (42,<br />
39,25, 2) or in quality (33, 81). In a particularly elegant experiment, Hartley<br />
& Law<strong>to</strong>n (34) found that insect feeding stimulated increased concentrations<br />
of PAL and phenolics more than cutting the leaves with scissors. Fungi or<br />
some component of insect saliva may stimulate the response since cutting<br />
with scissors and applying caterpillar regurgitate produced a response similar<br />
<strong>to</strong> that of insect damage. When designing experiments of induced responses,<br />
investiga<strong>to</strong>rs should not assume that artificial damage will produce results<br />
similar <strong>to</strong> actual herbivory, unless this hypothesis is experimentally tested.<br />
<strong>Induced</strong> responses in plants can influence a variety of different herbivores.<br />
The inducer and the affected species may belong <strong>to</strong> very different feeding<br />
guilds and be taxonomically unrelated. For instance, cot<strong>to</strong>n seedlings damaged<br />
by spider mites become more resistant <strong>to</strong> the symp<strong>to</strong>ms of a fungal<br />
disease (56). Similarly, seedlings that had been infected by the fungus became<br />
less suitable hosts for spider mites. Many studies have found "crossresistance"<br />
between different herbivore species [many different herbivores on<br />
cot<strong>to</strong>n (58, 52, 54), insects on larch (5), caterpillars on lupines (31), insects<br />
on oaks (103, 25, 45)]. However, several studies found that different species<br />
reacted idiosyncratically <strong>to</strong> induced plant changes. For example, birch leaves<br />
damaged by leaf mining were avoided by four species of caterpillars, whereas<br />
leaves damaged by chewing caterpillars were avoided by one caterpillar<br />
species but were equally preferred by another two species; leaves damaged<br />
artificially were preferred by two caterpillar species and were preferred<br />
equally by another two species (33). Unlike the antibody-antigen model of<br />
immune responses in vertebrates, induced resistance in plants against herbivores<br />
is characterized by low specificity. Interestingly, plant pathologists<br />
have reached the same conclusions about the lack of specificity of induced<br />
resistance against pathogenic organisms (61, 62).
340 KARBAN & MYERS<br />
WHY INDUCED RESPONSES RATHER THAN<br />
CONSTITUTIVE ONES?<br />
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Some fraction of the induced responses elicited by damage result in greater<br />
resistance <strong>to</strong> herbivores. If these changes increase the resistance of plants <strong>to</strong><br />
their herbivores, why are they inducible rather than constitutive? The problem<br />
becomes more perplexing for those cases in which induced responses are<br />
general reactions <strong>to</strong> many stresses and have activity against many different<br />
herbivores and parasites. The problem applies only <strong>to</strong> active responses since<br />
passive deterioration can only be inducible, by definition. We consider four<br />
hypotheses.<br />
Phy<strong>to</strong><strong>to</strong>xic <strong>Responses</strong> and Packaging Problems<br />
If the products induced by damage are <strong>to</strong>xic <strong>to</strong> herbivores and plant diseases,<br />
they may also be <strong>to</strong>xic <strong>to</strong> the plants themselves, and self-<strong>to</strong>xicity may increase<br />
if the effect is maintained for an extended time. For example, some phy<strong>to</strong>alexins<br />
are <strong>to</strong>xic <strong>to</strong> plants at concentrations that inhibit microorganisms (62).<br />
Repeated applications of fungus-derived elici<strong>to</strong>rs of these phy<strong>to</strong>alexins <strong>to</strong> the<br />
foliage of beans caused severe necrosis and stunted growth. This au<strong>to</strong><strong>to</strong>xicity<br />
is avoided by a system in which the phy<strong>to</strong>alexins are only produced when<br />
needed. Many plant products that are released following herbivory are locally<br />
<strong>to</strong>xic <strong>to</strong> the plant. However, precursors may be s<strong>to</strong>red safely in vacuoles so<br />
that enzymes and substrates are mixed only after the vacuoles are ruptured by<br />
feeding damage (reviewed in 21).<br />
<strong>Plant</strong>s Are <strong>Induced</strong> Much of the Time<br />
For some plants, the induced state might be the most common one. For<br />
example. <strong>to</strong>ma<strong>to</strong> plants must be carefully protected in the greenhouse <strong>to</strong><br />
prevent the induction of high levels of proteinase inhibi<strong>to</strong>rs. <strong>Plant</strong>s in the field<br />
are likely <strong>to</strong> be in the induced state most of the time following stimulation<br />
from wind (R. M. Broadway. personal cummunication). This argument<br />
probably does not apply <strong>to</strong> those examples of induced resistance in which an<br />
effect on herbivores has been demonstrated in the field. This is not really an<br />
explanation for why a particular response should be inducible but rather an<br />
observation that the distinction between induced and constitutive traits may be<br />
largely semantic. in some cases.<br />
The <strong>Induced</strong> Response Creates a Changing Target<br />
Most studies measure induced responses by looking at only a restricted group<br />
of chemicals or by doing a bioassay. Even so. results often vary considerably
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among parts of plants, and among different plants within a population. The<br />
responses <strong>to</strong> damage of different plants and different parts within an individual<br />
plant may be quite idiosyncratic. The plant may not simply be in an<br />
"induced state." Rather, induction likely involves differential changes occurring<br />
in different types of organs of a plant, and in different organs of the same<br />
type (leaves on a tree). <strong>Induced</strong> responses include many traits that affect<br />
herbivores, all of which can change, rather than the turning on of a single<br />
"defensive chemical." Each of these traits in each plant part may respond with<br />
its own rate of induction and relaxation. A changing, heterogeneous target<br />
may allow for a more rapid response and may retard or prevent the adaptation<br />
of herbivores or diseases <strong>to</strong> the plant defense (105). A changing plant<br />
phenotype may allow the plant <strong>to</strong> respond more rapidly <strong>to</strong> herbivores and<br />
other parasites than it could if it relied on constitutive defenses that changed<br />
only in evolutionary time. Constitutive defenses have no lag time at all, but<br />
also no ability <strong>to</strong> change when herbivores circumvent them. <strong>Induced</strong> responses<br />
may allow the plant <strong>to</strong> respond <strong>to</strong> unpredictable environmental<br />
variability (65). Phenotypic plasticity in resistance is expected <strong>to</strong> be more<br />
effective than genetic adaptation in response <strong>to</strong> selective fac<strong>to</strong>rs, such as<br />
herbivores and plant pathogens, that may vary during the life span of an<br />
individual plant. This hypothesis predicts that induced resistance will be most<br />
common for plants that experience unpredictable selective pressures from<br />
herbivores sporodically in relation <strong>to</strong> the generation time of the plant. This<br />
argument would be strengthened if we knew that phenotypic plasticity in<br />
resistance <strong>to</strong> herbivores was heritable, as plasticity of some other plant traits<br />
appears <strong>to</strong> be (92).<br />
<strong>Induced</strong> Defenses Are Less Costly<br />
Much of the recent theory concerning the evolution of plant defenses has<br />
centered around the notion that defenses are costly (18, 27, 76, 85, 88).<br />
Accordingly, plants should allocate resources <strong>to</strong> defenses only when and<br />
where such allocation will result in increased fitness.<br />
This leads <strong>to</strong> several testable predictions: (a) <strong>Herbivory</strong> should reduce plant<br />
fitness and induced plants should have greater fitness than noninduced plants<br />
when herbivores are present. (b) <strong>Plant</strong>s without induced defenses should have<br />
higher fitness in environments without herbivores. (c) <strong>Plant</strong>s that are well<br />
defended by constitutive defenses against a particular herbivore should not<br />
allocate resources <strong>to</strong> induced defenses against that same herbivore. If constitutive<br />
defenses are effective, induced defenses, which are presumably<br />
costly, would be redundant. In other words, these two should be negatively<br />
correlated.<br />
These predictions have not been tested adequately. Cot<strong>to</strong>n plants that were<br />
induced at the cotyledon stage supported smaller populations of spider mites
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during the remainder of that field season (52). However, growth and yield of<br />
these induced plants did not differ from plants that were not induced, contrary<br />
<strong>to</strong> prediction (a). Either spider mites did not reduce these aspects of plant<br />
fitness or else the reduction in fitness <strong>to</strong> control plants caused by greater<br />
herbivory was offset by the costs of inducing resistance. Since cot<strong>to</strong>n has<br />
undergone intense selection as an agricultural crop this may not be an<br />
appropriate model system. In native <strong>to</strong>bacco plants, both constitutive levels of<br />
alkaloids and increases in alkaloid titers induced by damage were negatively<br />
correlated with seed output, suggesting a cost <strong>to</strong> this presumed defense (3).<br />
The best examples of estimates of costs of induced resistance come from<br />
small invertebrates in fresh water and marine environments. Some of these<br />
organisms respond <strong>to</strong> preda<strong>to</strong>rs through morphological modifications such as<br />
the production of helmets in daphnia (43), heavier shells in barnacles (67),<br />
and spines in rotifers (29) and bryozoans (35). <strong>Induced</strong> resistance for rotifers<br />
did not reduce survival, fecundity, or population growth, but for barnacles,<br />
daphnia, and bryozoans, these induced morphological changes reduced<br />
growth and/or fecundity. When preda<strong>to</strong>rs are not present, unarmored individuals<br />
have the fitness advantage.<br />
CONCLUSIONS<br />
The initial observations of changes in chemical composition of plants following<br />
stress or damage seemed obvious examples of plant adaptations against<br />
herbivores. If, in a bioassay, the quality of foliage was reduced (as indicated<br />
by poorer survival and fecundity of the herbivore), then an impact on the<br />
future density of the herbivore seemed an obvious conclusion. Many studies<br />
have now found that induction causes changes in performance of bioassay<br />
herbivores. However, all stages in the interactions between plants and herbivores<br />
have been found <strong>to</strong> vary; insects vary in their choice of damaged and<br />
undamaged foliage and in their growth and survival on damaged and undamaged<br />
tissue. Some plants respond <strong>to</strong> damage, some do not; some improve<br />
as hosts following damage, others deteriorate. After a decade of work, there<br />
are few generalities concerning the effects of induced plant responses on<br />
population dynamics.<br />
The hypothesis outlined by Haukioja (36) and Rhoades (87), in which<br />
changes in food pilnt chemistry were proposed as the driving mechanism<br />
behind large-scale cyclic fluctuations in folivorous insects, has met with<br />
equivocal support. In some instances, variation among populations of trees is<br />
<strong>to</strong>o great <strong>to</strong> provide the consistent impact on the insects sufficient for widespread<br />
cyclic declines. More work is needed <strong>to</strong> examine the effects of induced<br />
host changes on populations of herbivores in natural and agricultural systems.<br />
The variation that may have surprised ecologists searching for simple
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answers and general patterns will perhaps come as little surprise <strong>to</strong> plant<br />
physiologists. Recognizing that fast- and slow-growing trees will respond <strong>to</strong><br />
defoliation in different ways and that loss of buds in the winter or spring will<br />
cause different patterns of foliage quality has greatly helped interpretations of<br />
conflicting findings. However, still controversial is whether chemical changes<br />
following damage can be wholly attributed <strong>to</strong> passive changes by damaged<br />
plants, or if active defensive processes must be invoked. The role of microparasites,<br />
fungi, bacteria, or viruses in eliciting active responses in damaged<br />
plants following contamination by herbivores will be an exciting area for<br />
future research and one that may help answer questions about the mechanisms<br />
of induction. The controversy between active and passive responses of plants<br />
<strong>to</strong> herbivore damage will almost certainly be resolved by the realization that a<br />
combination of mechanisms are involved. We must find out what is happening,<br />
where, why, and how often.<br />
If, as ecologists, we wish <strong>to</strong> understand induced changes we should be<br />
prepared <strong>to</strong> devote ourselves <strong>to</strong> long-term and multidimensional studies. If we<br />
aim <strong>to</strong> understand the chemical mechanisms of induced resistance, we should<br />
consider all of the chemicals within a plant with potential activity against<br />
herbivores, rather than specializing on a particular subset that are easy <strong>to</strong> work<br />
with or are thought <strong>to</strong> bc important. Certainly, we should seek experimental<br />
evidence that allows us <strong>to</strong> vary only one constituent, using artificial diets and<br />
isogenic lines, when available. This careful experimentation must be conducted<br />
for all of the plausible mechanisms. At the same time we should keep<br />
in mind that the effects we observe in these highly artificial experiments may<br />
be very different from effects experienced by herbivores dealing with the<br />
chemicals in plants, where interactions and synergisms arc likely <strong>to</strong> be<br />
important. We have now learned that many plants change in response <strong>to</strong><br />
herbivory and that no single mechanism will explain all of these diverse plant<br />
responses.<br />
At the other extreme, we must extend our bioassay results <strong>to</strong> field experiments<br />
on natural populations of herbivores. Rather than asking whether<br />
induced responses can be shown <strong>to</strong> affect the performance or behavior of<br />
herbivores we should assess the relative importance of induced plant resistance<br />
compared <strong>to</strong> other ecological fac<strong>to</strong>rs that may also affect the population<br />
dynamics of herbivores.<br />
<strong>Induced</strong> responses should not be assumed <strong>to</strong> be defenses. Instead, we must<br />
observe whether they defend plants by comparing fitness of induced and<br />
un induced plants in an environment that includes herbivores. Fitness will be<br />
most easily measured on small, short-lived plants which show evidence of<br />
induced responses following low levels of herbivore damage [e.g. cucurbits<br />
(96), wild <strong>to</strong>bacco (3), crucifers (93)]. It should be kept in mind that results<br />
with these systems may have little relevance <strong>to</strong> what is happening with trees.<br />
Even after an induced response is shown <strong>to</strong> provide resistance against a
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particular herbivore and <strong>to</strong> defend the plant against that herbivore, we should<br />
not conclude that it evolved in response <strong>to</strong> that herbivore. <strong>Plant</strong>s are affected<br />
by many different selective pressures; thus, limiting our consideration <strong>to</strong> a<br />
single herbivore at one point in time is likely <strong>to</strong> be misleading.<br />
The speed with which the study of induced changes in plant quality has<br />
progressed from the "simple understanding" phase <strong>to</strong> the "chaos of variation"<br />
phase and is now entering the "patterns of variation" phase is due both <strong>to</strong><br />
initially stimulating ideas and <strong>to</strong> efforts of a large number of researchers. In<br />
the future we should concentrate our efforts <strong>to</strong>ward (a) understanding the<br />
mechanisms of induced responses, (b) understanding the consequences of<br />
induced resistance on populations of herbivores, and (c) applying what we<br />
learn about induced resistance and defense <strong>to</strong> protecting agricultural crops<br />
(60, 55). Continued progress in each of these directions will be most rapid if<br />
we can maintain a broad perspective and consider a wide variety of nonexclusive<br />
hypotheses.<br />
ACKNOWLEDGMENTS<br />
This research has been supported by grants from NSF and USDA <strong>to</strong> R.<br />
Karban and grants from NSERC <strong>to</strong> J. H. Myers. Joy Bergelson, Alison<br />
Brody, John Bryant, Greg English-Loeb, Murray Isman, and Bill Morris<br />
made useful comments on the manuscript.<br />
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