Annu. Rev. Ecol. Syst. 1989. 20:331-48 Copyright © 1989 by Annual Reviews Inc. All rights reserved

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

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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

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334 KARBAN & MYERS

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

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INDUCED RESPONSES 335

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 pheno­

lics. 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,

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336 KARBAN & MYERS

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

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INDUCED RESPONSES 337

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.

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338 KARBAN & MYERS

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 pop­

ulations 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.

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INDUCED RESPONSES 339

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).

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340 KARBAN & MYERS

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

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INDUCED RESPONSES 341

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

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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 p�ilnt 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

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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

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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.

Literature Cited

I. Akazawa, T. , Uritani, 1., Kubota, H. 1960. Isolation of ipomearamone and two coumarin derivatives from sweet potato roots injured by the weevil, Cylas

formicarius elegantulus. Arch. Biochem. Biophys. 88:150-56

2. Baldwin,1. T. 1988. The alkaloidal re­sponses of wild tobacco to real and sim­ulated herbivory. Oecologia 77:378-381

3. Baldwin, 1. T. 1990. Damage-induced alkaloids in wild tobacco. See Ref. 84. In press

4. Baldwin, I. T. , Schultz, J. C. 1983. Rapid changes in tree leaf chemistry in­duced by damage: evidence for com­munication between plants. Science 221: 227-79

5. Baltensweiler, W. 1985. On the extent and the mechanisms of the outbreaks of the larch bud moth (Zeiraphera diniana Gn., Lepidoptera, Tortricidae) and its impact on the subalpine larch-cembran pine forest ecosystem. In Establishment and Tending of Subalpine Forest: Re­search and Management, ed. H. Turner, W. Tranquillini, pp. 215-219 Proc. 3rd IUFRO Workshop Birmensdorf, Swit­zerland

6. Baltensweiler, W. , Benz, G. , Bovey, P., Delucchi, V. 1977. Dynamics of larch bud moth populations. Annu. Rev. Entomol. 22:79-100

7. Benz, G. 1974. Negative Ruckkoppe­lung durch Raum- und Nahrungskonkur­renz sowie zyklische Veranderungen der Nahrungsgrandlage als Regelprinzip in der Populations-dynamik des Grauen Larchenwicklers, Zeiraphera diniana (Guenee) (Lepidoptera, Tortricidae). Z. Angew. Entomol. 76: 196--228

8. Benz, G. 1977. Insect induced resis­tance as a means of self defence of plants. In EUCA RPlAflOBC Working Group Breeding for Resistance to In­sects and Mites (Bulletin SROP 1977), pp. 155-59

9. Bergelson, J., Fowler, S. , Hartley, S. 1986. The effects of foliage damage on casebearing moth larvae, Coleophora serratella, feeding on birch. Ecol. En­tomol. 11:241-250

10. Broadway, R. M., Duffey, S. S., Pearce, G. , Ryan, C. A. 1986. Plant proteinase inhibitors: a defense against herbivorous insects? Entomol. Exp. Appl. 41:33--38

Ann

u. R

ev. E

col.

Syst

. 198

9.20

:331

-348

. Dow

nloa

ded

from

ww

w.a

nnua

lrev

iew

s.or

gby

ET

H-

Eid

geno

ssis

che

Tec

hnis

che

Hoc

hsch

ule

Zur

ich

- B

IBL

IOT

HE

K o

n 03

/29/

11. F

or p

erso

nal u

se o

nly.

II. Bryant, J. P. 1981. Phytochemical de­terrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees. Science 213:889-90

12. Bryant, J. P. 1987. Feltleaf willow­snowshoe hare interactions: plant car­bon/nutrient balance and floodplain suc­cession. Ecology 68:1319-27

13. Bryant, J. P., Chapin, F. S., Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-68

14. Bryant, J. P., Danell, K., Provenza, F., Reichardt, P., Clausen, T. 1990. Effects of mammal browsing on the chemistry of deciduous woody plants. See Ref. 84. In press

15. Bryant, J. P., Heitkonig, 1., Kuropat, P., Owen-Smith, N. 1989. Effects of severe defoliation upon the long-term re­sistance to insect attack and chemistry of leaves of six South African savannah woody species. Manuscript

16. Carroll, C. R., Hoffman, C. A. 1980. Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation by Epilachna tredecimnotata. Science 209:414-16

17. Coleman, 1. S., Jones, C. G. 1990. A phytocentric perspective of phytochemi­cal induction by herbivores. See Ref. 84, In press

18. Coley, P. D., Bryant, J. P., Chapin, F. S. 1985. Resource availability and plant antiherbivore defence. Science 230:895-99

19. DiCosmo, P., Towers, G. H. N. 1984. Stress and secondary metabolism in cul­tured plant cells. In Recent Advances in Phytochemistry, ed. B. N. Timmer­mann, C. Steelink, F. Loewus, 18:97-175. New York: Plenum

20. Dohman, G. P., McNeill, S., Bell, J. N. B. 1984. Air pollution increases Aphis

fabae pest potential. Nature 307:52-53 21. Duffey, S. S., Felton, G. W. 1989. Role

of plant enzymes in resistance to insects. In Enzymes in A griculture, ed. J. R. Whittaker, D. E. Sonnet, pp. 289-313. Amer. Chern. Soc.

22. Edelstein-Keshet, L., Rausher, M. 1989. The effects of inducible plant de­fenses on herbivore populations. I. Mo­bile herbivores in continuous time. Am. Nat. In press

23. Edwards, P. J., Wratten, S. D., Cox, H. 1985. Wound-induced changes in the acceptability of tomato to larvae of Spo­doptera littoralis: a laboratory bioassay. Ecol. Entomol. 10:155-58

24. Ericsson, A., Hellquist, c., Langstrom, B., Larsson, S., Tenow, o. 1985. Effects on growth of simulated and in-

INDUCED RESPONSES 345

duced shoot pruning by Tomicus piniperda as related to carbohydrate and nitrogent dynamics in Scots pine. 1. Appl. Ecol. 22:105-24

25. Faeth, S. H. 1986. Indirect interactions between temporally-separated herbi­vores mediated by the host plant. Ecolo­gy 67:479-94

26. Faeth, S. H. 1990. Inducible responses and interactions among oak folivores. See Ref. 84. In press

27. Feeny, P. P. 1976. Plant apparency and chemical defense. Recent Adv. Phy­tochem. 10:1-40

28. Fowler, S. Y., Lawton, J. H. 1985. Rapidly induced defenses and talking trees: the devil's advocate position. Am. Nat. 126:181-95

29. Gilbert, J. J. 1980. Further observations on developmental polymorphism and its evolution in the rotifer Brachionus caly­ciflorus. Freshwater BioI. 10:281-94

30. Green, T. R., Ryan, C. A. 1972 Wound-induced proteinase inhibitor in plant leaves: a possible defense mech­anism against insects. Science 175:776-77

31. Harrison, S., Karban, R. 1986. Effects of an early-season folivorous moth on the success of a later-season species, mediated by a change in the quality of the shared host, Lupinus arboreus Sims. Oecologia 69:354-59

32. Hart, S. Y., Kogan, M., Paxton, J. D. 1983. Effect of soybean phytoalexins on the herbivorous insects Mexican bean beetle and soybean looper. 1. Chem. Eml. 9:657-72

33. Hartley, S. E., Lawton, J. H. 1987. Effects of different types of damage on the chemistry of birch foliage, and the responses of birch feeding insects. Oecologia 74:432-37

34. Hartley, S. E., Lawton, J. H. 1990. A biochemical basis and significance of rapidly induced changes in birch. See Ref. 84. In press

35. Harvell, C. D. 1986. The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs, and con­sequences. Am. Nat. 128:810-23

36. Haukioja, E. 1980. On the role of plant defenses in the fluctuation of herbivore populations. Oikos 35:202-13

37. Haukioja, E. 1982. Inducible defences of white birch to a geometrid defoliator, Epirrita autumnata. Proc. 5th Int. Symp. Insect-Plant Relationships, pp. 199-203. Pudoc, Wageningen

38. Haukioja, E., Hakala, T. 1975. Herbi­vore cycles and periodic outbreaks. Formulation of a general hypothesis. Rep. Kevo Subarctic Res. Stat. 12:1-9

Ann

u. R

ev. E

col.

Syst

. 198

9.20

:331

-348

. Dow

nloa

ded

from

ww

w.a

nnua

lrev

iew

s.or

gby

ET

H-

Eid

geno

ssis

che

Tec

hnis

che

Hoc

hsch

ule

Zur

ich

- B

IBL

IOT

HE

K o

n 03

/29/

11. F

or p

erso

nal u

se o

nly.

346 KARBAN & MYERS

39. Haukioja, E., Neuvonen, S. 1985. In­duced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303-8

40. Haukioja, E., Neuvonen, S. 1987. In­sect population dynamics and induction of plant resistance: the testing of hypoth­eses. In Insect Outbreaks, ed. P. Barbo­sa, J. C. Schultz. pp. 411-432. New York: Academic

41. Haukioja, E., Niemela, P. 1977. Re­tarded growth of a geometrid larva after mechanical damage to leaves of its host tree. Ann. Zool. Fennici 14:48-52

42. Haukioja, E., Suomela, J. , Neuvonen, S. 1985. Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator. Oecologia 65:363-69

43. Havel, J. E., Dodson, S. I. 1987. Re­productive costs of Chaoborus-induced polymorphism in Daphnia pulex. Hy­drobiologia 150:273-81

44. Henderson, C. F., Holloway, J. K. 1942. Influence of leaf age and feeding injury on the citrus red mite. J. Econ. Ent. 35:683-86

45. Hunter, M. D. 1987. Opposing effects of spring defoliation on late season oak caterpillars. Ecol. Entomol. 12:373-82

46. Isaak, A., Sorensen, E. L . , Painter, R. H. 1965. Stability of resistance to pear aphid and spotted alfalfa aphid in several alfalfa clones under various temperature regimes. J. Econ. Entomol. 58:140-43

47. Jaffe, M. J., Telewski , F. W. 1984. Thigmomorphogenesis: callose and ethylene in the hardening of mechanical­ly stressed plants. See Ref. 19, 18:79-95

48. Jones, C. G. , Coleman, J. S. 1989. Plant stress and insect herbivory: toward an integrated perspective. In Integrated Responses of Plants to Stress, ed. H. A. Mooney, W. E. Winner, E. J. Pell. New York: Academic. In press

49. Jones, D. A. 1972. Cyanogenic glyco­sides and their function. In Phvtochemi­cal Ecology, ed. J. B. Harborne. pp. 103-124. New York: Academic

50. Karban, R. 1983. Induced responses of cherry trees to periodical cicada oviposi­tion. Oecologia 59:226-31

51. Karban, R. 1985. Resistance against spider mites in cotton induced by me­chanical abrasion. Entomol. Exp. Appl. 37:137-41

52. Karban, R. 1986. Induced resistance against spider mites in cotton: field veri­fication. Entomol. Exp. Appl. 42:239-42

53. Karban, R. 1987. Environmental con­ditions affecting the strength of induced

resistance against mites in cotton. Oeco­logia 73:414-19

54. Karban, R. 1988. Resistance to beet armyworms. (Spodopter a exigua) in­duced by exposure to spider mites. (Tet­ranychus turkestan i) in cotton. Am. Midi. Nat. 119:77-82

55. Karban, R. 1990. Inducible resistance in agricultural systems. See Ref. 84. In press

56. Karban, R . , Adamchak, R., Schna­thorst, W. C. 1987. Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 235:678-80

57. Karban, R., Brody , A. K., Schnathorst, W. C. 1989. Crowding and a plant's ability to defend itself against herbivores and diseases. Am. Nat. In press

58. Karhan, R., Carey, J. R. 1984. Induced resistance of cotton seedlings to mites. Science 225:53-54

59. Karban, R., English-Loeb, G. M. 1988. Effects of herbivory and plant condition­ing on the population dynamics of spider mites. Exp. Appl. Acar. 4:225-46

60. Kogan, M., Paxton, J. 1983. Natural inducers of plant resistance to insects. In Plant Resistance to Insects, ed. P. A. Hedin, pp. 153-71. Washington, DC: Am. Chern. Soc.

61. Kuc, J. 1981. Multiple mechanisms, reaction rates, and induced resistance in plants. In Plant Disease Control, ed. R. C. Staples, pp. 259-72. New York: Wiley

62. Kuc, J. 1987. Plant immunization and its applicability for disease control. In Innovative Approaches to Plant Disease Control, ed. I. Chet, pp. 255-74, New York: John Wiley

63. Kuc, J., Rush, J. S. 1985. Phytoalexins. Arch. Biochem. Biophys. 236:455-72

64. Larsson, S . , Wiren, A . , Lundgren, L., Ericsson, T. 1986. Effects of light and nutrient stress on leaf phenolic chemistry in Salix dasyclados and susceptibility to Galerucella lineola (Coleoptera). Oikos 47:205-10

65. Levins, R. 1968. Evolution in Changing Environments: Some Theoretical Explo­rations. Princeton, NJ: Princeton Univ. Press

66. Lincoln, D. E., Mooney, H. A. 1984. Herbivory on Diplacus aurantiacus shrubs in sun and shade. Oecologia 64:173-76

67. Lively, C. M. 1986. Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40: 232-42

68. Loper, G. M. 1968. Effect of aphid in-

Ann

u. R

ev. E

col.

Syst

. 198

9.20

:331

-348

. Dow

nloa

ded

from

ww

w.a

nnua

lrev

iew

s.or

gby

ET

H-

Eid

geno

ssis

che

Tec

hnis

che

Hoc

hsch

ule

Zur

ich

- B

IBL

IOT

HE

K o

n 03

/29/

11. F

or p

erso

nal u

se o

nly.

festation on the coumestrol content of alfalfa varieties differing in aphid resis­tance. Crop Sci . 8 : 1 04-6

69. Makus, D . , Zuroske, G . , Ryan, C. A. 1 990. The direction and rate of transport

of the proteinase inhibiting factor out of wounded tomato leaves. Plant Physiol. 65: 1 50 (Suppl . )

70. Mattson, W . J . , Addy, N . D . 1 975 . Phytophagous insects as regulators of forest primary production. Science 1 90: 5 1 5-22

7 1 . Mattson, W. 1 . , Haack, R . A . 1 987. The role of drought in outbreaks of plant­eating insects. Biuscience 37: 1 1 0- 1 8

72. Mauch, F . , Hadwiger, L . A . , Boller, T. 1 984. Ethylene: symptom not signal for the induction of chitinase and b- 1 ,3-glucanase in pea pods by pathogens and elicitors. Plant Physiol. 76:607- 1 1

73. May, R. H. 1 98 1 . Models for single populations. In Theoretical Ecology: Principles and Applications, ed . R . H . May, pp. 5-29. Sunderland, Mass: Sinauer. 2nd ed.

74. Mcintyre, J . L . , Dodds, J . A . , Hare, J . D. 1 98 1 . Effects of localized infections of Nicotiana tabacum by tobacco mosiac virus on systemic resistance against di­verse pathogens and an insect. Phyto­pathology 7 1 :297-301

75. McMurtry, J . A. 1 970. Some factors of foliage condition limiting population growth of Oligonychus punicae (Acar­ina: Tetranychidae) . Ann. Entomol. Soc. Am. 63:406-12

7 6 . Mooney, H . A . , Gulmon, S. L. 1 982. Constraints on leaf structure and func­tion in reference to herbivory. Biosci­ence 32: 198-206

77. Myers, J. H. 1 998. The induced defense hypothesis. Does it apply to the popula­tion dynamics of insects? In Chemical Mediation of Coevolution, ed. K. Spencer, pp. 530-37. New York: Aca­demic

78. Myers, J. H. 1 988. Can a general hy­pothesis explain population cycles of forest Lepidoptera? Adv. Ecol. Res . 1 8: 1 80-242

79. Myers, J. H . , Bazely, D. 1 990. Thoms, spines, prickles and hairs: are they stimulated by herbivory and do they deter herbivores? See Ref. 84. I n press

80. Myers, J. H . , Williams, K. S. 1984. Does tent caterpillar attack reduce the food quality of red alder foliage? Oeco­{ogia 62:74-79

8 1 . Neuvonen, S . , Haukioja, E. , Molarius, A. 1 987. Delayed inducible resistance against a leaf-chewing insect for four

INDUCED RESPONSES 347

deciduous tree species. Oecologia 74: 363-69

8 1 a . Neuvonen, S . , Haukioja, E. 1 990. The effects of inducible resistance in host foliage on birch feeding herbivores. See Ref. 84. In press

82. Prestidge, R. A. , McNeill, S. 1 983. Au­chenorrhyncha-host plant interactions: leafhoppers and grasses. Ecol . Ent. 8: 33 1-339

83. Raffa, K. F . , Berryman, A. A . 1 987. Interacting selective pressures in coni­fer-bark beetle systems: a basis for recip­rocal adaptations? Am. Nat. 1 29:234-62

84. Raupp, M. J . , Tallamy, D. W . , cds. 1 990. Phytochemical Induction by Her­bivores. New York: Wiley

85. Rhoades, D. F. 1 979. Evolution of plant chemical defense against herbivores . In Herbivores: Their Interaction With Secondary Plant Metabolites, ed . G. A . Rosenthal , D. H . Janzen , pp. 4-54. New York: Academic

86. Rhoades, D. F. 1 983. Responses of alder and willow to attack by tent cater­pillars and webworms: evidence for pheromonal sensitivity of willows. See Ref. 60, pp. 55-68

87. Rhoades, D. F. 1 983. Herbivore popula­tion dynamics and plant chemistry. In Variable Plants and Herbivores in Nat­ural and Managed Systems, ed. R. F. Denno, M. S . McClure, pp. 1 5 5-220. New York: Academic

88. Rhoades, D. F. , Cates, R. G. 1 976. Toward a general theory of plant anti­herbivore chemistry. Recent Adv. Phy­tochem . 1 0: 1 68-2 1 3

89. Roland, J . , Myers, J. H . 1 987. Im­proved insect performance from host­plant defoliation: winter moth on oak and apple. Ecol. Entomol. 1 2:409-1 4

90. Russell, G. B . , Sutherland, O. R . W . , Hutchins, R . F. N . , Christmas, P. E. 1 978. Vcstitol: a phytoalexin with insect feeding-deterrent activity . 1. Chem . Ecol. 4:57 1-79

9 1 . Ryan, C. A. 1 983. Insect-induced chem­ical signals regulating natural plant pro­tection responses. In Variable Plants and Herbivores in Natural and Managed Systems. ed. R. F. Denno, M. S . McClure, pp. 43-60. New York: Aca­demic

92. Schlichting, C. D. 1 986. The evolution of phenotypic plasticity in plants. Annu. Rev. Eco!. Syst. 1 7:667-93

93. Shapiro, A. M . , DeVay, J. E. 1987. Hypersensitivity reaction of Brassica nigra L. (Cruciferae) kills eggs of Pieris

Ann

u. R

ev. E

col.

Syst

. 198

9.20

:331

-348

. Dow

nloa

ded

from

ww

w.a

nnua

lrev

iew

s.or

gby

ET

H-

Eid

geno

ssis

che

Tec

hnis

che

Hoc

hsch

ule

Zur

ich

- B

IBL

IOT

HE

K o

n 03

/29/

11. F

or p

erso

nal u

se o

nly.

348 KARBAN & MYERS

butterflies (Lepidoptera: Pieridae). Oecologia 7 1 :63 1 -32

94. Sosa, O. 1 979. Hessian fly: resistance of wheat as affected by temperature and duration of exposure. Env. Entomol. 8: 280-8 1

95. Sutherland, O. R. W. , Russell, G. B. , Biggs, D. R . , Lane, G. A. 1 980. Insect feeding deterrent activity of phytoalexin isoflavonoids. Biochem. Syst. Ecol. 8: 73-75

96. Tallamy, D. W. 1 985. Squash beetle feeding behavior: an adaptation against induced cucurbit defenses. Ecology 66: 1 574-79

97. Tuomi, J., Niemela, P . , Haukioja, E., Siren, S . , Neuvonen, S . 1 984. Nutrient stress: an explanation for plant anti­herbivore responses to defoliation. Oecologia 6 1 :208- 1 0

98. Tuomi, J., Niemela, P . , Chapin, F . S., Bryant, J. P . , Siren, S. 1 988. Defensive responses of trees in relation to their carbon/nutrient balance. In Mechanisms of Woody Plant Defenses Against In­sects: Search for Pattern, ed. W. J. Mattson, J. Levieux , C. Bernard-Dagan, pp. 57-72. New York: Springer-Verlag

99. Tuomi , J. , Niemela, P . , Rousi, M . , Siren, S . , Vuorisalo, T. 1 988. Induced accumulation of foliage phenols in mountain birch: brauch response to de­foliation? Am. Nat. 1 32:602-8

1 00. Uritani, I . , Saito, T . , Honda, H. , Kim, W. K. 1 975. Induction of furano­terpenoids in sweet potato roots by the larval components of the sweet potato weevils. Agric. Bioi. Chem. 37: 1 857-62

1 0 1 . Valentine, H. T. , Wallner, W. E., War­go, P. M. 1 983. Nutritional changes in host foliage during and after defoliation, and their relation to the weight of gypsy moth pupae. Oecologia 57:298-302

1 02. Wagner, M. R. 1 988. Induced defenses in ponderosa pine against defoliating in­sects. See Ref. 98, pp. 1 41-55

1 03. West, C. 1 985. Factors underlying the late seasonal appearance of the lepidopterous leaf-mining guild on oak. Ecol Entomol. 1 0: 1 1 1-20

1 04. White, T. C. R. 1 969. An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905-9

\ 05. Whitham, T. G. 1 983. Host manipula­tion of parasites: within-plant variation as a defense against rapidly evolving pests. In Variable Plants and Herbivores in Natural and Managed Systems, ed. R . F . Denno, M . S. McClure. p p . 1 5-4 1 . New York: Academic

1 06. Williams, A. G. , Whitham, T. G. 1986. Premature leaf abscission: and induced plant defense against gall aphids . Ecolo­gy 67: 1 6 19--27

1 07. Williams, K. S . , Myers, J. H. 1 984. Previous herbivore attack of red alder may improve food quality for fall web­worm larvae. Oecologia 63: 1 6&-70

108. Wolfson, J. 1990. The effects and non­effects of proteinase inhibitors on insect herbivores. See Ref. 84. In press

1 09. Wratten, S. D . , Edwards, P. J . , Dunn, I. 1 984. Wound-induced changes in palatability of Betula pubescens and B. pendula. Oecologia 6 1 :372-75

1 1 0. Yang, S. F . , Pratt, H. K. 1 978. The physiology of ethylene in wounded plant tissues. In Biochemistry of Wounded Plant Tissue, ed. G. Kahl, pp. 595-622. New York: De Gruyter

I l l . Young, T. P. 1 987. Increased thorn length in Acacia drepanolobium-an in­duced response to browsing. Oecologia 7 1 :43&-38

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