Induced Plant Responses to Herbivory - Terrestrial Systems Ecology

Annu. Rev. Ecol. Syst. 1989. 20:331-48 

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Annu. Rev. Ecol. Syst. 1989.20:331-348. Downloaded from www.annualreviews.org 

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INDUCED PLANT RESPONSES TO 

HERBIVORY 

Richard Karban 

Department of Entomology, University of California, Davis, California 95616 

Judith H. Myers 

The Ecology Group and Departments of Plant Science and Zoology, University of 

British Columbia, Vancouver, British Columbia, V6T lW5 Canada 

PHENOMENA OF INDUCED PLANT RESPONSES 

Changes in plants following damage or stress are called "induced responses." 

In the broadest sense, these changes can increase the "resistance" of the plant 

to further herbivore attack by reducing the preference for, or effect of, 

herbivores on the damaged plant. It should not be assumed that these changes 

which provide resistance evolved as a result of selection by herbivores. In 

some cases the reponses may currently act as "induced defenses"; that is, they 

are responses by the plant to herbivore injury or the invasion of microparasites 

that decrease the negative fitness consequences of attacks on the plant. These 

terms-"induced resistance" and "induced defense"-are used by different 

people to mean a variety of different things. Workers in this field would 

benefit by agreeing upon a set of definitions, and we offer a dichotomous key 

of these terms (Table 1). Note that an induced response could conceivably 

operate as a defense without decreasing herbivore preference or performance. 

Instead, it may make the plant more tolerant to herbivory. Although "induced 

defenses" are widely discussed, to our knowledge no one has shown an 

induced response to be defensive, i.e. no one has explicitly measured the 

influences of the change on the fitness of the plant. 

Not all induced plant responses increase resistance by making plants less 

suitable as hosts. On the contrary, an extensive literature describes increases 

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332 KARBAN & MYERS 

Table 1 

A dichotomous key for induced responses 

Does stress or injury change plant quality? 

1 NO: No response 

l' YES: INDUCED RESPONSE (proceed to 2) 



Does the induced response decrease herbivore preference or performance? 

2 NO: No effect or induced susceptibility 

2' YES: INDUCED RESISTANCE (proceed to 3) 

Does reduced herbivore preference/performance increase plant fitness? 

3 NO: The plant is not defended by the response 

3' YES: INDUCED DEFENSE 

in plant quality following injury caused by drought (104), nutrient deficiency 

(70), solar radiation (66), low temperature (46), high temperature (94), air 

pollution (20), and previous damage caused by herbivory (107). Much of the 

evidence for changes in resistance associated with induced responses comes 

from bioassays of induced foliage under laboratory or artificial field conditions 

(reviewed in 28, 84). While the proportion of cases in which induced 

responses act as defenses against herbivores may be uncertain, we would like 

to consider in this review the characteristics of changes that relate to their role 

as defenses. What are the changes, why and how might they occur, and what 

might be done to further understand their influence on plant-herbivore interactions? 

Specifically, which changes are likely to act as effective defenses 

and how might they work? Which herbivores are likely to be affected? Have 

these responses evolved as defenses against herbivores? Under what conditions 

might selection favor facultative induced defenses rather than preformed 

constitutive defenses? 

WHAT CHANGES FOLLOW DAMAGE? 

Secondary Metabolites and Phytoalexins 

Injuries to plant tissues cause a wide array of plant responses. The nature of 

the response varies with plant type. One area of progress has been to recognize 

that the way trees respond is associated with their growth pattern and 

nutrient status (14). A cataloging of plant responses is beyond the scope of 

this review, although a few representative examples are provided. Many 

studies of induced responses have considered changes in tannins and phenols, 

products of the shikimic acid pathway. Relative activity of the enzyme 

phenylalanine ammonia lyase (PAL) can determine the production of phenolics, 

including lignin (19). Induction of the phytohormone ethylene by tissue 

damage may influence the production of PAL and therefore the concentration

INDUCED RESPONSES 333 



of secondary metabolites (110) and leaf toughness (47). The exact role of 

ethylene in this process remains controversial (72). Many agents of environmental 

stress correlated to herbivory can also cause increases in secondary 

metabolites (71). Patterns often vary depending on the history of the plant. 

The balance between many primary and secondary metabolites influences the 

response of plants to stress and also the effects that these plant responses will 

have on herbivores. Herbivore damage often affects the concentrations of 

available nitrogen and other important nutrients in foliage (7, 97). A major 

problem facing workers in this area is determining which of the many 

secondary plant chemicals and plant nutrients that change following damage 

or stress are responsible for the overall effects on herbivores. The range of 

induced changes is so great that it is impossible to investigate all these factors 

and difficult to determine rationally which are worthy of study. 

In some instances, herbivores elicit plants to synthesize phytoalexins (1, 

68, 100). Phytoalexins are low molecular-weight, antimicrobial compounds 

(63) usually present in plants at extremely low concentrations prior to infection. 

These can be synthesized de novo by plants following microbial infection, 

and effectiveness is determined by the speed and magnitude at which 

they are produced and accumulated (62). Limited evidence suggests that 

phytoalexins may be active against insects as well as plant pathogens (90, 95, 

74, 32). 

Physiological and Morphological Changes 

The response of plants to herbivores can be more extensive than simply 

modifications of secondary metabolite concentrations. For example, spider 

mites cause widespread changes in the cytology, histology, and physiology of 

their host plants, including modifications of photosynthetic and transpirational 

rates, and they can inject substances that can act as plant growth regulators 

(reviewed by 59). 

Herbivores can influence the morphology of their food plants by causing 

increases in the density of prickles, spines, and hairs (reviewed by 79), by 

causing the return to juvenile growth form (11), or by affecting the phenology 

of plant processes such as leaf abscission (106). Many herbivores are "specialists" 

on plant tissue of a particular physiological age, so that altering the 

synchrony between plant and insect could act to make the plant appear more 

resistant. All of these changes could have an influence on herbivores, or on 

the extent of further herbivory. 

DYNAMICS OF PLANT CHANGE FOLLOWING 

HERBIVORE DAMAGE 

Plants respond to herbivore damage over spatial scales ranging from single 

leaves to whole trees and over temporal scales ranging from minutes to




evolutionary time. Most of the studies that point to induced resistance, 

assayed as a decrease in herbivore performance, have found that the response 

was systemic at least to other parts of the damaged shoot. However, one study 

measuring rapid increases in foliage phenols found that this chemical response 

was not systemic in birch trees (99). The spatial extent of the induced 

response may determine whether the response acts as a defense. A localized 

response may encourage herbivores to feed elsewhere on the same plant; 

damage to the plant will be spread but not reduced. Surprisingly, no study has 

explicitly mapped the spatial extent of induced resistance in all parts of the 

entire plant. Despite the exciting suggestion by Rhoades (86) and Baldwin & 

Schultz (4) that plants may become more resistant in response to cues released 

by damaged neighbors, subsequent experiments have been few and have not 

supported the idea (80, 28). 

Some responses are known to occur within several hours after damage, as 

in the case of proteinase inhibitors in damaged foliage of solanaceous plants 

(reviewed in 108) or latex in damaged cucurbits (16). What component of 

damage signals rapidly induced responses is generally not known. Damage to 

tissues may release cell wall fragments that are translocated to other parts of 

the plant where they activate genes that code for enzymes, such as proteinase 

inhibitors (91). In this case the signal is transported systemically within 

injured tomato plants but is directed primarily up the stem from older leaves to 

younger ones (69). The proteinase inhibitors accumulate in vacuoles of 

uninjured cells of injured plants and are deleterious to some caterpillars 00). 

Induced resistance need not involve de novo synthesis; damage may bring 

preformed enzymes and substrates into contact, causing the production of 

active agents (21). Enzymatic activation of compartmentalized precursors is 

responsible for many reactions, including the cyanogenic response of plants to 

herbivores (21, 49). Damage to tissue may release ethylene that stimulates the 

production of PAL and increases in phenolics (110, see also 72). Phenolics 

are not transported from damaged to undamaged birch leaves; rather, they are 

synthesized in undamaged leaves following increases in PAL activity (34). 

The mechanisms of responses that occur over several years are also poorly 

understood. Plant tissue that dcvelops in the growing season after marked 

defoliation often shows increases in phenolics and fiber, declines in nutrient 

concentrations, regrowth of juvenile tissue, and changes in plant morphology 

(rcvicwed in 102, 79). 

MECHANISMS: ACTIVE RESISTANCE OR PASSIVE 

DETERIORATION? 

While enzymatic activation of precursors and synthesis of phytoalexins and 

proteinase inhibitors are clearly active processes, changes in plant chemistry




following defoliation may result from a passive rearrangement of resources 

within the plant. The distinction is that active responses involve de novo 

synthesis or energetically costly enzymatic processes, whereas passive responses 

involve only the consequences of tissue removal. Passive responses 

have been described as nutrient stress by Tuomi and coworkers (98, 99), as 

carbon-nutrient imbalance by Bryant and his associates (13, 14), and as 

passive deterioration by Myers & Williams (80). According to this hypothesis, 

a tree growing in an area with abundant soil nutrients (a fast growing 

tree) loses proportionately more nitrogen and other nutrients and less carbon 

during defoliation because it had proportionately more nitrogen in its leaves. 

Subsequently, carbon may be replaced in the leaves at a faster rate than 

nitrogen, and the surplus allocated to carbon-based allelochemicals (terpenes, 

resins, tannins, and other phenolics) and fiber. These foliar changes are 

expected to reduce the preference and performance of herbivores on trees that 

were previously defoliated. On the other hand, trees growing in nutrient-poor 

conditions or which store proportionately more carbon in their leaves (evergreens) 

may respond in the opposite way; defoliation may reduce the concentrations 

of carbon-based chemicals and increase the palatability of leaves 

of these slow-growing trees in the next growing season (14, 15, 24, 98). 

This model leads to several testable predictions (see also 98). (a) Nitrogen 

fertilization of defoliated trees should negate the nutrient imbalance and 

cancel the induced response; (b) carbon stress should result in a collapse of 

carbon-based resistance; (c) if herbivory and plant crowding reduce the same 

nutrients, then the effects of these two stresses should be qualitatively similar 

(57). Experimental N fertilization of birch trees increased foliar nitrogen and 

reduced phenolics, while root damage, which reduced nutrient uptake, reduced 

foliar nitrogen and increased phenolics (97). Larsson et al (64) found 

similar patterns between carbon availability (light) and carbon-based phenolics. 

Shading (reduced C) increased the palatability of willows to snowshoe 

hares, presumably because of reduced carbon-based defenses (12). Clipped 

and shaded willows produced regrowth shoots with lower concentrations of 

carbon-based secondary compounds, that were more preferred than clipped 

and unshaded trees. 

The resource rearrangement model does not explain all observations, 

however. Nitrogen fertilization of artificially defoliated birch trees did not 

negate the induced resistance as assayed by autumnal moth caterpillars (39). 

Crowding cotton plants reduced their suitability to spider mites; however, 

crowding and herbivore damage did not act additively to reduce foliage 

quality for mites or verticillium fungus (57). On the contrary, induced resistance 

was only apparent when plants were not crowded, suggesting that 

resources are required for the induced response to occur. 

These tests of the passive model are not easy to interpret. For example,




nitrogen fertilization and carbon stress could produce the result predicted by 

the model for many reasons having nothing to do with the hypothesized 

nutrient stress. Nitrogen fertilization could cause ratios of specific amino 

acids to become unnaturally lopsided or levels of nitrogen to become higher 

than optimal for herbivores (82). More convincing tests of the model would 

cause changes in nutrient ratios by means other than herbivory (by plant 

crowding or more careful fertilization treatments). The effects of these treatments 

on both plant chemistry and plant quality for herbivores could be 

measured. 

Tissue removal by herbivores may alter the plant physiologically, making it 

more resistant in the process. Pruning commonly causes shoots to exhibit 

juvenile characters compared to unattacked shoots of similar plants. Juvenile 

growth is often characterized by greater concentrations of secondary chemicals 

or physical resistance (14, 79). Although these responses cause an 

increase in less palatable tissue, they are probably examples of generally high 

protection of the juvenile stage. 

INFLUENCE OF INDUCED RESPONSES ON 

HERBIVORES 

Field studies on the effects of induced responses on herbivores have yielded 

extremely variable results among plants within a population, and among 

populations (reviewed in 26, 34). Much of this variation may be the result of 

differences in species, age, genotype, history, and environmental factors (17, 

26, 48). Despite this variability, we can make preliminary generalizations 

about the timing and spatial extent of induced responses, and specificity of 

their effects on herbivores. 

Timing of Induced Responses 

The rate at which induced changes occur and the rate at which they are relaxed 

determines whether they affect particular herbivores. The critical distinction 

between rapid or short-term responses versus long-term responses is neither 

the rate at which the response occurs nor the rate of relaxation of the response. 

Rather, these rates must be compared to the relevant events of attack and 

resultant damage. Short-term responses occur during the attack such that the 

attacking individuals experience the consequences of the changes they induce. 

Long-term responses occur following the attack and have little effect on the 

attacking individuals but can influence herbivores that attempt to use the plant 

at later times. The effect of an induced response must be considered in terms 

of the life history and mobility of particular herbivores. The same plant 

response may affect only subsequent generations of short-lived herbivores 

such as spider mites, or it may affect the attacker in the case of a longer lived




caterpillar. Less mobile herbivores, such as leaf miners, gall formers, and 

bark beetles are more likely to be affected by localized responses than are 

herbivores that constantly move. 

The distinction between responses that influence the attacking organisms 

and those that influence only later challengers to the plant is important 

because, in theory, the consequences of these two effects should be quite 

different. Induced resistance effective against the organisms causing the 

response is more likely to reduce the local population of this herbivore species 

(37). Induced resistance activated only after the attacker has left works as a 

negative factor with a time delay and is much less likely to have a stabilizing 

effect (37, 73). However, increased instability caused by a delay in the 

induced response could still be accompanied by a reduction in mean herbivore 

density. Using simple models of induced resistance involving mobile nonselective 

herbivores with continuous generations, Edelstein-Keshet & 

Rausher (22) argued that increasing the rate at which plants respond or 

decreasing the rate of decay of the response make it more likely that induced 

resistance will affect an herbivore population. 

Both common sense and mathematical theory suggest that the rates of 

induction and relaxation will influence the consequences on herbivores. 

Nonetheless, we know relatively little about these rates because the appropriate 

experiments are difficult, involving several treatments that must be subsampled 

at several different time intervals. Most of the studies that followed 

the time course of the induced response have found that the organism that 

causes the damage also suffers the consequences [caterpillars on birch trees 

(9, 41, 109), beetles on cucurbits (16, 96), spider mites on cotton plants (55), 

caterpillars on tomato plants (10, 23), mites on avocado trees (75), beetles 

and fungi on pines (83), aphids on cottonwoods (106), cicada eggs in cherry 

trees (50), and caterpillars on oaks (89)]. However, three studies which 

showed evidence of induced resistance found that the response was delayed so 

that it had less chance of affecting the individuals (not the species) that caused 

the induction [mammals on acacias (111), hares on birches (13), and caterpillars 

on larches (6)]. The extent to which these individual herbivores are 

territorial or otherwise feed on the same individual plants in successive years 

determines the likelihood that they will suffer the consequences of their 

previous feeding. Some induced effects can accumulate if the stress continues 

for several years. For instance, performance of gypsy moth caterpillars on 

black oak trees decreased as the number of years that the trees had been 

defoliated increased from 0 to 3 (101). Several studies have found that 

induced resistance increased as the level of injury to the plant increased [mites 

on citrus (44), mites on cotton (Figure 4 in 53), caterpillars on birch (Figure 1 

in 40)]. These results suggest that induced resistance should probably be 

thought of as a graded response rather than as an on/off process.




Many ecologists became interested initially in induced responses because 

they provided a potential mechanism to explain multiyear population cycles 

of forest insects. The hypothesis presented by Haukioja & Hakala (38) and 

Benz (8)-that plant quality decreases after defoliation and then increases 

gradually after a lag of several years-provides a delayed density-dependent 

mechanism that could potentially drive population cycles of herbivores (11, 

36, 87). 

To explain regional synchrony of population fluctuations of forest Lepidoptera, 

we must test whether host trees respond in a consistent manner to insect 

attack. This basic premise does not seem to be supported: Induced responses 

of trees have been found to vary among species, among populations, among 

years, and across environmental gradients (81a). On the other hand, changes 

in the fecundity and survival of fluctuating populations of forest Lepidoptera 

often show consistent patterns through the cycle, even when caterpillars feed 

on different species of host plant, in different areas, and following different 

histories of attack (77, 78). 

Although the variation in response of trees to herbivore damage seems to 

make inducible changes in food quality an unlikely explanation for the cyclic 

population dynamics of forest Lepidoptera, we list in Table 2 further predictions 

of the hypothesis that can be tested. Observations on cyclic populations 

of tent caterpillars and other forest Lepidoptera do not support 

these predictions (77, 78). The importance of inducible changes in food 

plant quality to population dynamics of nonoutbreak species has not been 

studied. 

Table 2 

Testable predictions arising from the hypothesis that population cycles of forest 

Lepidoptera are driven by deterioration in food plant quality following feeding damage from 

increasing numbers of herbivores. Species and populations of host trees must respond in a 

consistent manner to herbivore damage for the fluctuations of different populations of insects to 

remain in synchrony within a region. 

1. Fecundity and survival of herbivores will be related to the history of attack on trees. 

2. If the response of trees is density dependent, fecundity and survival of herbivores will decline 

with increasing density (level of attack) and deterioration in food quality. 

3. Decreasing fecundity and survival of herbivores following damage to host plants will be 

translated into a decline in the population density. 

4. Cropping of herbivore density to reduce damage will prolong the outbreak phase of the 

population. 

5. Introduction of herbivores to suitable foodplants in sites with no previous herbivore damage 

will lead to an outbreak out of synchrony with natural populations.




The Specificity of Induced Resistance 

Most vertebrate immune responses are highly specific. We can ask two 

questions regarding the specificity of induced resistance against herbivores 

and other plant parasites: (a) Are plant responses triggered specifically by 

particular parasites or injuries? and (b) do plant responses have activity only 

against specific challengers? 

Many studies have found that artificial damage causes responses in plants 

that affect herbivores. However, these tell us little about whether the responses 

caused by artificial damage are physiologically the same and similar 

in strength to those caused by herbivores. Studies that include at least three 

treatments (plants damaged by herbivores, plants damaged artificially, and 

undamaged controls) are more informative. Several such studies found that 

artificial damage caused effects similar to those resulting from actual herbivory 

(30, 51, 81). However, several studies found that the effects of injury 

inflicted by herbivores and by artificial means were different in extent (42, 

39,25, 2) or in quality (33, 81). In a particularly elegant experiment, Hartley 

& Lawton (34) found that insect feeding stimulated increased concentrations 

of PAL and phenolics more than cutting the leaves with scissors. Fungi or 

some component of insect saliva may stimulate the response since cutting 

with scissors and applying caterpillar regurgitate produced a response similar 

to that of insect damage. When designing experiments of induced responses, 

investigators should not assume that artificial damage will produce results 

similar to actual herbivory, unless this hypothesis is experimentally tested. 

Induced responses in plants can influence a variety of different herbivores. 

The inducer and the affected species may belong to very different feeding 

guilds and be taxonomically unrelated. For instance, cotton seedlings damaged 

by spider mites become more resistant to the symptoms of a fungal 

disease (56). Similarly, seedlings that had been infected by the fungus became 

less suitable hosts for spider mites. Many studies have found "crossresistance" 

between different herbivore species [many different herbivores on 

cotton (58, 52, 54), insects on larch (5), caterpillars on lupines (31), insects 

on oaks (103, 25, 45)]. However, several studies found that different species 

reacted idiosyncratically to induced plant changes. For example, birch leaves 

damaged by leaf mining were avoided by four species of caterpillars, whereas 

leaves damaged by chewing caterpillars were avoided by one caterpillar 

species but were equally preferred by another two species; leaves damaged 

artificially were preferred by two caterpillar species and were preferred 

equally by another two species (33). Unlike the antibody-antigen model of 

immune responses in vertebrates, induced resistance in plants against herbivores 

is characterized by low specificity. Interestingly, plant pathologists 

have reached the same conclusions about the lack of specificity of induced 

resistance against pathogenic organisms (61, 62).


WHY INDUCED RESPONSES RATHER THAN 

CONSTITUTIVE ONES? 



Some fraction of the induced responses elicited by damage result in greater 

resistance to herbivores. If these changes increase the resistance of plants to 

their herbivores, why are they inducible rather than constitutive? The problem 

becomes more perplexing for those cases in which induced responses are 

general reactions to many stresses and have activity against many different 

herbivores and parasites. The problem applies only to active responses since 

passive deterioration can only be inducible, by definition. We consider four 

hypotheses. 

Phytotoxic Responses and Packaging Problems 

If the products induced by damage are toxic to herbivores and plant diseases, 

they may also be toxic to the plants themselves, and self-toxicity may increase 

if the effect is maintained for an extended time. For example, some phytoalexins 

are toxic to plants at concentrations that inhibit microorganisms (62). 

Repeated applications of fungus-derived elicitors of these phytoalexins to the 

foliage of beans caused severe necrosis and stunted growth. This autotoxicity 

is avoided by a system in which the phytoalexins are only produced when 

needed. Many plant products that are released following herbivory are locally 

toxic to the plant. However, precursors may be stored safely in vacuoles so 

that enzymes and substrates are mixed only after the vacuoles are ruptured by 

feeding damage (reviewed in 21). 

Plants Are Induced Much of the Time 

For some plants, the induced state might be the most common one. For 

example. tomato plants must be carefully protected in the greenhouse to 

prevent the induction of high levels of proteinase inhibitors. Plants in the field 

are likely to be in the induced state most of the time following stimulation 

from wind (R. M. Broadway. personal cummunication). This argument 

probably does not apply to those examples of induced resistance in which an 

effect on herbivores has been demonstrated in the field. This is not really an 

explanation for why a particular response should be inducible but rather an 

observation that the distinction between induced and constitutive traits may be 

largely semantic. in some cases. 

The Induced Response Creates a Changing Target 

Most studies measure induced responses by looking at only a restricted group 

of chemicals or by doing a bioassay. Even so. results often vary considerably




among parts of plants, and among different plants within a population. The 

responses to damage of different plants and different parts within an individual 

plant may be quite idiosyncratic. The plant may not simply be in an 

"induced state." Rather, induction likely involves differential changes occurring 

in different types of organs of a plant, and in different organs of the same 

type (leaves on a tree). Induced responses include many traits that affect 

herbivores, all of which can change, rather than the turning on of a single 

"defensive chemical." Each of these traits in each plant part may respond with 

its own rate of induction and relaxation. A changing, heterogeneous target 

may allow for a more rapid response and may retard or prevent the adaptation 

of herbivores or diseases to the plant defense (105). A changing plant 

phenotype may allow the plant to respond more rapidly to herbivores and 

other parasites than it could if it relied on constitutive defenses that changed 

only in evolutionary time. Constitutive defenses have no lag time at all, but 

also no ability to change when herbivores circumvent them. Induced responses 

may allow the plant to respond to unpredictable environmental 

variability (65). Phenotypic plasticity in resistance is expected to be more 

effective than genetic adaptation in response to selective factors, such as 

herbivores and plant pathogens, that may vary during the life span of an 

individual plant. This hypothesis predicts that induced resistance will be most 

common for plants that experience unpredictable selective pressures from 

herbivores sporodically in relation to the generation time of the plant. This 

argument would be strengthened if we knew that phenotypic plasticity in 

resistance to herbivores was heritable, as plasticity of some other plant traits 

appears to be (92). 

Induced Defenses Are Less Costly 

Much of the recent theory concerning the evolution of plant defenses has 

centered around the notion that defenses are costly (18, 27, 76, 85, 88). 

Accordingly, plants should allocate resources to defenses only when and 

where such allocation will result in increased fitness. 

This leads to several testable predictions: (a) Herbivory should reduce plant 

fitness and induced plants should have greater fitness than noninduced plants 

when herbivores are present. (b) Plants without induced defenses should have 

higher fitness in environments without herbivores. (c) Plants that are well 

defended by constitutive defenses against a particular herbivore should not 

allocate resources to induced defenses against that same herbivore. If constitutive 

defenses are effective, induced defenses, which are presumably 

costly, would be redundant. In other words, these two should be negatively 

correlated. 

These predictions have not been tested adequately. Cotton plants that were 

induced at the cotyledon stage supported smaller populations of spider mites




during the remainder of that field season (52). However, growth and yield of 

these induced plants did not differ from plants that were not induced, contrary 

to prediction (a). Either spider mites did not reduce these aspects of plant 

fitness or else the reduction in fitness to control plants caused by greater 

herbivory was offset by the costs of inducing resistance. Since cotton has 

undergone intense selection as an agricultural crop this may not be an 

appropriate model system. In native tobacco plants, both constitutive levels of 

alkaloids and increases in alkaloid titers induced by damage were negatively 

correlated with seed output, suggesting a cost to this presumed defense (3). 

The best examples of estimates of costs of induced resistance come from 

small invertebrates in fresh water and marine environments. Some of these 

organisms respond to predators through morphological modifications such as 

the production of helmets in daphnia (43), heavier shells in barnacles (67), 

and spines in rotifers (29) and bryozoans (35). Induced resistance for rotifers 

did not reduce survival, fecundity, or population growth, but for barnacles, 

daphnia, and bryozoans, these induced morphological changes reduced 

growth and/or fecundity. When predators are not present, unarmored individuals 

have the fitness advantage. 

CONCLUSIONS 

The initial observations of changes in chemical composition of plants following 

stress or damage seemed obvious examples of plant adaptations against 

herbivores. If, in a bioassay, the quality of foliage was reduced (as indicated 

by poorer survival and fecundity of the herbivore), then an impact on the 

future density of the herbivore seemed an obvious conclusion. Many studies 

have now found that induction causes changes in performance of bioassay 

herbivores. However, all stages in the interactions between plants and herbivores 

have been found to vary; insects vary in their choice of damaged and 

undamaged foliage and in their growth and survival on damaged and undamaged 

tissue. Some plants respond to damage, some do not; some improve 

as hosts following damage, others deteriorate. After a decade of work, there 

are few generalities concerning the effects of induced plant responses on 

population dynamics. 

The hypothesis outlined by Haukioja (36) and Rhoades (87), in which 

changes in food pilnt chemistry were proposed as the driving mechanism 

behind large-scale cyclic fluctuations in folivorous insects, has met with 

equivocal support. In some instances, variation among populations of trees is 

too great to provide the consistent impact on the insects sufficient for widespread 

cyclic declines. More work is needed to examine the effects of induced 

host changes on populations of herbivores in natural and agricultural systems. 

The variation that may have surprised ecologists searching for simple




answers and general patterns will perhaps come as little surprise to plant 

physiologists. Recognizing that fast- and slow-growing trees will respond to 

defoliation in different ways and that loss of buds in the winter or spring will 

cause different patterns of foliage quality has greatly helped interpretations of 

conflicting findings. However, still controversial is whether chemical changes 

following damage can be wholly attributed to passive changes by damaged 

plants, or if active defensive processes must be invoked. The role of microparasites, 

fungi, bacteria, or viruses in eliciting active responses in damaged 

plants following contamination by herbivores will be an exciting area for 

future research and one that may help answer questions about the mechanisms 

of induction. The controversy between active and passive responses of plants 

to herbivore damage will almost certainly be resolved by the realization that a 

combination of mechanisms are involved. We must find out what is happening, 

where, why, and how often. 

If, as ecologists, we wish to understand induced changes we should be 

prepared to devote ourselves to long-term and multidimensional studies. If we 

aim to understand the chemical mechanisms of induced resistance, we should 

consider all of the chemicals within a plant with potential activity against 

herbivores, rather than specializing on a particular subset that are easy to work 

with or are thought to bc important. Certainly, we should seek experimental 

evidence that allows us to vary only one constituent, using artificial diets and 

isogenic lines, when available. This careful experimentation must be conducted 

for all of the plausible mechanisms. At the same time we should keep 

in mind that the effects we observe in these highly artificial experiments may 

be very different from effects experienced by herbivores dealing with the 

chemicals in plants, where interactions and synergisms arc likely to be 

important. We have now learned that many plants change in response to 

herbivory and that no single mechanism will explain all of these diverse plant 

responses. 

At the other extreme, we must extend our bioassay results to field experiments 

on natural populations of herbivores. Rather than asking whether 

induced responses can be shown to affect the performance or behavior of 

herbivores we should assess the relative importance of induced plant resistance 

compared to other ecological factors that may also affect the population 

dynamics of herbivores. 

Induced responses should not be assumed to be defenses. Instead, we must 

observe whether they defend plants by comparing fitness of induced and 

un induced plants in an environment that includes herbivores. Fitness will be 

most easily measured on small, short-lived plants which show evidence of 

induced responses following low levels of herbivore damage [e.g. cucurbits 

(96), wild tobacco (3), crucifers (93)]. It should be kept in mind that results 

with these systems may have little relevance to what is happening with trees. 

Even after an induced response is shown to provide resistance against a




particular herbivore and to defend the plant against that herbivore, we should 

not conclude that it evolved in response to that herbivore. Plants are affected 

by many different selective pressures; thus, limiting our consideration to a 

single herbivore at one point in time is likely to be misleading. 

The speed with which the study of induced changes in plant quality has 

progressed from the "simple understanding" phase to the "chaos of variation" 

phase and is now entering the "patterns of variation" phase is due both to 

initially stimulating ideas and to efforts of a large number of researchers. In 

the future we should concentrate our efforts toward (a) understanding the 

mechanisms of induced responses, (b) understanding the consequences of 

induced resistance on populations of herbivores, and (c) applying what we 

learn about induced resistance and defense to protecting agricultural crops 

(60, 55). Continued progress in each of these directions will be most rapid if 

we can maintain a broad perspective and consider a wide variety of nonexclusive 

hypotheses. 

ACKNOWLEDGMENTS 

This research has been supported by grants from NSF and USDA to R. 

Karban and grants from NSERC to J. H. Myers. Joy Bergelson, Alison 

Brody, John Bryant, Greg English-Loeb, Murray Isman, and Bill Morris 

made useful comments on the manuscript. 

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