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AMER. ZOOL., 21:853-864 (1981) Defense and Dynamics in Plant-Herbivore Systems1 LAUREL R. FOX Biology Board of Studies, University of California, Santa Cruz, California 95064 SYNOPSIS. Recent theory about interactions between plants and their herbivores focuses on properties of individual plants that affect their resistance to herbivores, and it extrapolates from these individual properties to those of whole communities. In this paper I question three major assumptions of this approach—costs of defenses, basic differences between classes of defenses, and step-wise coevolution—and recast the theory from a different community perspective. I propose that major differences in defenses between plants with very different life-history characteristics arise from differences in community structure, especially the numbers of herbivore species involved in the interactions. In particular, because of the diffuse pattern of herbivory on persistent plants, a new model of coevolution—diffuse coevolution—becomes appropriate when many species are involved. Complex interacting assemblages have special properties that cannot be derived just by summing up all of the simple interactions that occur. types of prey. This second approach deals with chemical and structural properThere have been two very different apof individual plants that affect their ties proaches to the study of interactions between plants and herbivores. The older resistance to herbivores, and generated a approach arose from concern with herbi- theory to explain how these properties vores as pests in agricultural and forest function as defenses against the plants' ecosystems, and had a strongly quantita- natural enemies, how evolutionary changes tive basis. It focused on the population dy- in these properties are induced by herbinamics of consumer species, and assumed vores, and how changes in the plants' dethat classical predation theory could be ap- fenses affect the abilities of herbivores to plied directly to herbivory. Plant proper- adapt further. This theory is non-matheties (e.g., growth rates) directly affecting matical and was developed to explain difamounts of food available to herbivores ferences that had emerged in the patterns were often included, but, with few excep- of defenses observed in different types of tions (Austin and Cook, 1974; Caughley, plants. It is a theory that proposes mech1976; Harper, 1969; Noy-Meir, 1975), this anisms to explain these different patterns, approach did not consider either dynamics and also provides an explanation for the of the plant populations or special prop- apparently small amounts of damage erties of individual plants that might mod- caused by herbivores in natural plant comify direct analogies with predator-prey munities. models. In large part, this approach reUltimately, a comprehensive theory flected the prevailing perception that, un- about plants and herbivores must be able der natural conditions, herbivores did little to unite the two approaches, plant defendamage to individual plants and thus were ses and dynamics (of both plant and herunlikely to affect dynamics of natural plant bivore components of communities). This populations. is particularly important since recent studIn contrast, the second and more recent ies of natural populations of plants demapproach largely ignored dynamics of con- onstrate that herbivores influence plant sumers and focused on individual plants, population levels, geographical distribuparticularly on qualitative properties tions and community structures, even if showing that plants are indeed special damage seems to be low (Batzli and Pitelka, 1971; Bentley et ai, 1980; Borchert and Jain, 1978; Cantlon, 1969; Green and Palmbald, 1975; Kinsman, 1978; Louda, 1 From the Symposium on Theoretical Ecology pre-1978; Morrow and LaMarche, 1978; sented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1980, at Seattle, Rausher and Feeny, 1980; Thompson, 1978). This paper evaluates the current Washington. INTRODUCTION 853 854 LAUREL R. FOX TABLE 1. Synopsis ofdefense theory as proposed by Feeny (1975, 1976), Rhoades and Cates (1976) and Rhoades (1979). Unapparent plants Plant features Life-history Short-lived Community Diverse Low Chance of detection Evolutionary consequences of herbivory Defense Toxin = qualitative Concentration and cost Effective against Counteradaptation Examples Low Generalists Easy by specialists Alkaloids, cardiac glycosides, cyanide, glucosinolates, nonprotein amino acids, terpenes status of the second approach to plant-herbivore interactions, by focusing on one of its most interesting aspects: that it extrapolates from arguments about properties of individuals to understand properties of whole communities. After outlining major assumptions and predictions of defense theory, particularly those involving defensive chemistry, I will examine the theory in the light of very recent data, and recast some of the arguments from a different community perspective. While many of the assumptions of defense theory need to be modified, I conclude that the framework is still reasonable. By building a different community context for that framework I suggest another model for coevolution between plants and herbivores. DEFENSE THEORY Theories of plant defenses were formalized independently in the mid 1970s by two different groups, one at Cornell (led by Paul Feeny), and the other at the University of Washington (Gordon Orians, David Rhoades and Rex Cates). Although these groups used slightly different assumptions and arguments, they arrived at very similar predictions. Their models made very good sense in terms of general ecological theory, and their predictions convincingly explained both experimental data and observations made in natural systems up to that time. Because these theories so well reflected the real world, they were widely and rapidly accepted, and Apparent plants Persistent Simple High Digestibility-reducing, dosedependent = quantitative High All species Very difficult Silica, tannins, terpenes, toughness have served as important frameworks for many studies during the past few years. These recent theories have been called "optimal defense theory" by Rhoades (1979), but in this paper I will refer to it simply as "defense theory," both to distinguish it from theories about herbivore population dynamics, and because some recent data lead to questions of whether these interactions have been optimized. Defense theory assumes that the kinds of defenses in a plant reflect both the lifehistory characteristics of plants and the structure of plant communities (Table 1). Both Feeny (1975, 1976) and Rhoades and Cates (1976) made their arguments initially by considering two extreme types of plants and the chances that each will be found by their herbivores. The model also considers two types of herbivores: specialized ones that are primarily insects, and more generalized consumers, including insects, mammals and molluscs. At one extreme are plants with relatively low chances of detection by their herbivores. These include early successional plants, those in which individuals are available to herbivores for only a short time, or those that live as relatively rare members of diverse communities (e.g., some annuals and herbaceous perennials). As a result of this temporal and spatial heterogeneity, herbivores may find these plants relatively difficult to locate. Feeny (1976) called these plants "unapparent": that is, unapparent to their herbivores. Of course, the average PLANT-HERBIVORE SYSTEMS: DEFENSE, DYNAMICS apparency of a given plant depends on such factors as patch sizes, relative abundances of other plant species (host and non-host) and on the predictability of local plant distributions and abundances. Typical unapparent plants grow very rapidly and invest a large portion of their nutrients and energy in reproduction. Defense theory predicts that they will be defended by "low cost" defenses, such as poisons like cyanide that are very effective in low concentrations, and have specific biochemical targets. Two consequences of these specific and very toxic defenses are that they exert strong selective pressures on specialized herbivores to evolve appropriate counteradaptations and that completely effective counteradaptations may arise quite readily. These toxins have been called "qualitative" defenses, because of their all-or-none effect on herbivores. Unapparent plants reduce damage from such adapted consumers by being unpredictable in space and time. On the other hand, these same toxins may well remain effective against more generalized herbivores which may locate a particular unapparent plant while feeding on neighboring plants, with other types of defenses, that are present in the same community. Generalists are much less likely than specialists to evolve counteradaptations to specific defenses. Defense theory contrasts the properties of spatially and/or temporally ephemeral, unapparent plants with large, long-lived persistent plants, like oak trees, that typically live in communities of very low diversity (Table 1). Each individual plant is almost certain to be found by specialized herbivores during its life span, and such species are called "apparent" plants. Herbivorous insects on apparent plants would probably evolve counteradaptations to toxins very easily because they have much shorter generation times than their hosts. Instead, selection has favored generally debilitating defenses that affect very basic animal functions (e.g., digestion). One important proposed consequence of such generalized defenses is that they are difficult to overcome and so remain effective 855 against both generalist and specialist herbivores. Because of these general properties they were called "digestibility-reducing" defenses (Rhoades and Cates, 1976); and since such defenses have greater effects on herbivores as concentration increases, they were also called "quantitative" or dose-dependent defenses (Feeny, 1976). Therefore, to be effective, these compounds may be present in high concentrations: defense theory assumes that their production and storage is "expensive," but that high costs can be tolerated by these long-lived plants. Plants that are persistent as individuals but are part of low density populations in diverse communities may have characteristics of both apparent and unapparent plants. As examples, herbaceous perennials and rain forest trees within diverse communities may have high risks of being found even by more specialized herbivores that may establish localized resident populations, as well as by more generalized consumers in the community. These types of plants may have qualitative defenses such as specific toxins which may be particularly effective at increasing chances of seedling establishment, as well as quantitative defenses that enhance persistence for long-lived tissues (Feeny, 1976; Futuyma, 1976; Gilbert, 1979). Defense theory also predicts that herbivore pressure on unapparent plants selects for both intra- and interspecific variation in defenses, including both novel defenses which would be effective even against specialists, and modifications on the dominant theme which are useful primarily against generalists. On the other hand, defense theory predicts interspecific convergence of defenses among apparent plants, though even in these, intraspecific variation remains advantageous. EVALUATION To evaluate current defense theory, I will concentrate on three major topics that underlie most of its arguments: costs, basic differences between qualitative and quantitative defenses, and coevolution. Digest- 856 LAUREL R. FOX ibility-reducers will be referred to simply as DRs. Costs Cost arguments are intuitive, convenient and pervasive in ecology. But for plantherbivore interactions, as well as other areas of study, there are very few direct measurements of costs, or data suitable for testing these assumptions in a critical way. Cost arguments are difficult to assess because pathways for production, costs of storage, translocation or breakdown, and functions of the compounds other than defense, are rarely known, while effects of these compounds on a plant's overall fitness are difficult to measure. Finally, costs of defensive compounds also reflect other features of a plant's environment besides herbivores. For example, environmental stresses such as low water or light levels, or competitive interactions with other plants, may modify the ratio of costs to benefits even for the same plant species in different habitats (Mooney and Gulmon, 1979). The best evidence for the existence of costs is indirect: defenses of some plant species are reduced, or even completely absent, in individuals growing in areas with reduced herbivore pressures (Janzen, 1973, 1975). In one of the surprisingly few experiments designed to test the assumption of costly defenses, unpalatable (and presumably defended) wild ginger plants were smaller and had fewer seeds than palatable ones (Cates, 1975); unfortunately, these results are difficult to interpret because the mechanisms of unpalatability are not known, and since the morphs came from different habitats, the results could be explained in terms of ecotypes adapted to different physical environments. Despite the fact that existing evidence remains largely circumstantial, it still seems reasonable to assume that defenses have some associated cost and that, in the absence of herbivores, their production will have negative effects on plant fitness. However, quantifying these costs, and justifying assumptions of cost differentials between different types of defenses, are very difficult. Concentration of a defensive chemical by itself is not a good indication of cost; other factors which must be considered include a) the amounts of energy, carbon or nitrogen that are used, b) the cost of special structures that may be required for production or storage, and c) whether molecules involved in defense are produced once or whether they are turned over and have to be produced constantly. In addition, defenses may have other functions that may be advantageous to plants, irrespective of their effects on resistance to herbivores. Contrast production of DRs such as tannins, with toxins such as alkaloids. There may be a 50-fold difference in concentration: tannins may comprise 15% of leaf dry weight, and alkaloids much less than 1%. On the other hand, tannins accumulate and probably do not turn over, whereas alkaloids may cycle daily. Over the course of a growing season, each tannin compound may be produced only once, but the alkaloids may be produced 100 times to maintain their low levels: thus there may be no difference in their cumulative costs to the plant (Swain, 1978). For evergreen leaves that stay on the plant for several years, the balance of costs may even favor tannins. In addition, producing high concentrations of tannins and other phenols may actually cost plants very little if they are growing in soils where nitrogen is limiting, because phenols may serve as carbon sinks for excess photosynthate (Phillips and Henshaw, 1977). Thus, while production of defenses may be "costly" in an absolute sense, there is little evidence for the major cost differentials required by defense theory. Qualitative vs. quantitative defenses The distinction between qualitative and quantitative defenses is not absolute. First, some compounds fit definitions in both categories. For instance, in several species of mints and rain forest trees, terpenes occur in low concentrations, with high intraspecific variation, as expected for qualitative defenses (e.g., Lincoln and Langenheim, 1976; Langenheim et al., 1978). In some Eucalyptus trees, however, terpenes appear to be quantitative defen- PLANT-HERBIVORE SYSTEMS: DEFENSE, DYNAMICS ses because they make up as much as 20% of the dry weight of leaves (Morrow and Fox, 1980). Second, some adapted herbivores can effectively detoxify or tolerate quantitative defenses such as tannins, without reducing feeding efficiency, growth or K reproduction (Fox and Macauley, 1977). Recent work on 15 species of grasshoppers from many parts of the world showed that the range of responses to tannic acid (a hydrolyzable tannin) is closely linked to the presence of tannins in the herbivores' normal diets (Bernays et al., 1980). Those grasshopper species that typically ate grasses, which do not contain tannins, were very severely affected by tannins; but those grasshoppers that normally ate tanniniferous plants were all adapted, and some of these species even performed better on high tannin plants. These data are particularly important because tannins have been considered the most effective barrier against herbivores in terrestrial plants (Harborne, 1978): they are widespread through the plant kingdom and were thought to be virtually impossible to overcome. Although mechanisms of accommodating tannins are poorly known, the peritrophic membrane in midguts of the grasshoppers absorbed much of the ingested tannin (Bernays and Chamberlain, 1980). Alkaline midguts of herbivores also may reduce tanning (Feeny, 1970, 1975; Berenbaum, 1980) but the grasshoppers' midguts were neutral (Bernays, 1978), and, in fact, tannin-protein bonds may remain strong at high pH levels if the isoelectric points of proteins (such as digestive enzymes) are also high (Hagerman and Butler, 1978). In addition fungi such as Aspergillus and Penicillium produce an inducible enzyme, tannase, that breaks down hydrolyzable tannins (Haslam and Tanner, 1970). 857 0 to about 2% caryophyllene (well within typical concentrations of toxins) resulted in a nearly 9-fold increase in herbivore mortality. Other toxins, such as some cardiac glycosides and glucosinolates also have both toxic and digestibility-reducing effects (Chew and Rodman, 1979). Feeny (1976) was careful to point out that toxins may have dosage-dependent effects on partially-adapted herbivores, but this distinction has sometimes been overlooked in subsequent discussions. I interpret these and other recent studies to mean that there are no fundamental dose-dependent differences in the action of qualitative and quantitative defenses, and that both can be overcome effectively by at least some herbivores. A priori chemical classifications are not sufficient to identify the mode of action in a specific context. A particular group of defenses may affect herbivores in "quantitative" or "qualitative" ways. Nevertheless, I argue below that these are distinctions between compounds acting in "toxic" or "digestibility-reducin~" ways, with major consequences for interactions between plants and herbivores. These differences in properties of toxins and DRs may affect a) the number of plant species eaten by each herbivore species, b) the ecological interactions between herbivores and their own natural enemies, c) selective pressures imposed by plants on their herbivores and, quite possibly, both d) variation and e) the rates of speciation of components of the coevolutionary system. Coevolution Coevolution is assumed to occur between two interacting species when each exerts selective pressures affecting the other's gene pool. As the term is normally used, coevolution implies ongoing stepThird, some herbivores respond to tox- wise evolution within both populations, ins in a dose-dependent way. For instance, with the properties of first one and then though leaf sesquiterpenes were toxic to the other continuing to evolve in response the very generalized beet armyworm (Spo- to specific changes in properties of the othdoptera exigua), these herbivores showed a er species. Plant defenses provide the sedose-dependent response to the cary- lective pressures for counter-adaptations ophyllene component of terpenes in their by herbivores; successful counter-adaptadiets (Stubblebine and Langenheim, 1977; tions in turn select for modified defenses Langenheim et al., 1980): an increase from among the plants. This process is repeti- 858 LAUREL R. FOX tive, although it does not imply continuous fine-tuning in every generation. Rather, the gene pools probably will not change much until an appropriate allele or recombinant enters the population, resulting in a major shift in gene frequencies in a very few generations. Evidence for step-wise coevolution and its ecological importance initially came from observations that the taxonomy of host plants could be predicted from the taxonomy of the herbivores (Fraenkel, 1959; Ehrlich and Raven, 1964). Closely related herbivores (most data were for butterflies), especially those from the same genus, tended to feed on plants within one family. This "family specialization" is correlated with secondary chemistry, because plants within the same family typically have similar defenses. Recognition of family specialization led to the idea that interacting species become locked into coevolutionary cycles, an idea inherent in the defense model. Gilbert (1979) recently described major exceptions to this pattern among butterflies. He found many genera in which species have broad diets, and use plants from different families that often are not closely related and have very different chemistries. Many lycaenids, one of the largest and most diverse butterfly families, are family generalists, and this constitutes a major exception to the hypothesis that butterflies as a whole are family specialists. In addition, among the nymphalids, species in some genera are family specialists, while others are family generalists, showing that the herbivores' taxonomic affinities and their patterns of host use are not necessarily related. Defense theory predicts that a herbivore's diet breadth depends on the apparency and mode of defense of its food plants, and on the coevolutionary history of the interaction: herbivores using unapparent plants defended by toxins will tend to be more specialized than those restricted to plants relying on generalized DRs (Cates, 1980; Feeny, 1975, 1976; Futuyma, 1976; Rhoades, 1979; Rhoades and Cates, 1976). However, in addition to many butterflies (Gilbert, 1979), other major groups of herbivorous insects (e.g., acridoid grasshoppers: Bernays and Chapman, 1978; aphids: van Emden, 1978; Eastop, 1973), as well as most mammalian herbivores, also do not fit the expected pattern of family specialization. Gilbert (1979) related diet breadth of both family generalists and family specialists to the butterflies' mating behaviors, while on a broader scale, Fox and Morrow (1981) discussed many diverse factors that affect dietary specialization of a wide variety of herbivorous insects, independently of plant apparency or defense. The diversity of exceptions to predictions of the apparency model lead to important questions about the relevance of step-wise coevolution in these systems, particularly about its utility as a general model for plant-herbivore evolutionary interactions. Apparency The concept of "apparency" involves correlations between a suite of plant properties, types of defenses and patterns of herbivore attack, as well as implying the mechanism by which these interact. Unfortunately, there are severe operational problems in defining and measuring apparency so that it is difficult to demonstrate the causal relationships predicted by this model. In addition, the observed correlations may be generated by other mechanisms, one of which is discussed in the next section. I do not have sufficient space for an extensive evaluation of the apparency concept. However, I will continue to use the terms "unapparent" and "apparent" as succinct, descriptive labels for observed sets of correlated characters, but use of these labels does not imply a particular mechanism for their evolution. ALTERNATIVE COEVOLUTIONARY MODELS I propose that the step-wise model is reasonable for "unapparent" plants and their herbivores, but for different reasons than offered by defense theory. And I also propose that very different coevolutionary processes exist in "apparent" plant communities: not step-wise ones at all. I suggest that the major differences in defenses between apparent and unapparent plants de- 859 PLANT-HERBIVORE SYSTEMS: DEFENSE, DYNAMICS TABLE 2. Two coevolutionary models of interactions between plants and herbivores. "Apparent" "Unapparenl" Herbivores Selection On plants On herbivores Coevolution Defenses Type Effective against Counteradaptation Few species Simple interactions Many species Diffuse herbivory Strong Strong Few interacting genomes Step-wise coevolution Simple selection Strong Weak Many interacting genomes Diffuse coevolution Continuous adjustment Broad array of responses Toxins Generalists Easy by specialists Digestibility-reducers All species Difficult but possible pend on differences in community structure, especially the numbers of herbivorous species involved in the interactions. Step-wise coevolutionary interactions are possible primarily in unapparent plant communities because the coevolutionary model depends on a limited number of species being involved (Table 2). In the simplest case, each plant species is eaten by only one specialized herbivore species, and strong selective pressures are exerted on each of the protagonists by the other. While this case is too simple for most natural systems, the structure of communities of unapparent plants limits the numbers of interacting herbivores for several reasons. First, by definition, the patch sizes and local densities of populations of unapparent plants are low. This "associational resistance" (Root, 1975) increases the difficulties specialists experience in locating their food—herbivores may simply lose their host plants among the miasma of confusing odors from neighboring plants. Second, unapparent plants will be used by relatively few herbivores at any one location, because they are small, structurally simple, and may be available only for a short time each year or at a site. Several studies have shown that structurally simple plants, with short life cycles have fewer herbivores than larger, more complex plants (Lawton, 1978; Strong and Levin, 1979). This pattern reflects both the structural complexity of different plants and their local persistence and predictability in space and time. With these limitations on the numbers of interactions among the components of a community, strong reciprocal evolutionary interactions may occur. There will be strong selection acting both on the herbivores to locate their hosts and overcome defenses, and on the plants to deter them. In this case, with relatively few specialized herbivores using a given local plant species population, the most likely mode of defense favored by selection would be specific in its action and would work very rapidly to cause high mortality. Toxins under simple genetic control are most likely to be selected even though herbivores may overcome them relatively easily; hence polymorphic systems that perhaps involve a few loci, provide high intraspecific variation {e.g., several types of alkaloids) and permit rapid modifications in response to changes in the herbivores, may be most effective. My argument, then, is that toxins are selected for in unapparent plants, not because they are cheap, as proposed by conventional defense theory, but rather because they are the only ones that can be successful in the circumstances—they work quickly against specific targets. In contrast, the pattern of herbivory on large and persistent plants is very different (Table 2). Each plant species population, and each individual tree, will be eaten, 860 LAUREL R. FOX even locally, by a large array of herbivores: some generalists and some specialists. Additionally, a tree has a variety of component parts—leaves, twigs, bark, for instance—that frequently are eaten by different herbivores. Population interactions between these plants and the assemblage of herbivores feeding on them is complex. Within any one community, apparent plants may be used by a large array of specialized and generalized herbivores. Evolutionary interactions between apparent plants and their herbivores are not necessarily reciprocal. While most longlived plants accumulate a complex assemblage of herbivores, the herbivores themselves show different degrees of dietary restriction. I refer to damage imposed by the complex assemblage on persistent plants as "diffuse herbivory," a term roughly analogous to diffuse competition. This implies that there are many herbivorous species feeding on and among the plants in these communities; each plant responds continually to the many species in this array in both ecological and evolutionary time. For instance, diffuse herbivory is typical of Eucalyptus communities that are dominated by related species of plants: many herbivorous insects feed on several Eucalyptus species, even in a local community, while each eucalypt tree typically is eaten by many herbivores (Morrow, 1977; Fox, unpublished data). Diffuse herbivory also describes the pattern of lepidopterans feeding on an array of unrelated plants in a mixed deciduous forest in upstate New York (Futuyma and Gould, 1979): plants in this community were eaten mainly by generalists, though on any one plant species there was a complex of generalists and specialists. The chances for simple step-wise evolution in communities of apparent plants, are very low. The web of interactions on persistent plants involves many interacting genomes, because each plant species responds to numerous and probably different selective pressures exerted by an array of herbivore species. Thus, even if the combined herbivore load on a plant is high, selective pressures exerted by any one species are likely to be relatively weak. In addition, the array of herbivores on any plant may even be exerting conflicting defensive demands. The chances for simple step-wise coevolution in communities of apparent plants are very low. In this situation, selection should favor defenses with i generalized actions, that are difficult to detoxify and that can affect a diverse array of consumers at the same time. Most importantly, these types of defenses should not impose very strong selective pressures that might easily select for counteradaptations. This is critical for plants with generation times so much greater than those of their herbivores. The digestibility-reducing defenses of persistent plants fit these criteria very well. These DRs are very generalized in their action; they affect very basic animal functions, as appropriate for use against an array of herbivores; and they do not impose strong selection on each consumer because they do not impose heavy mortality. They reduce herbivore viability and vigor, affecting fitness in a very general sense: slowing down growth and development, and reducing reproduction. The whole array of herbivores may exert strong selective pressures on the plants. But the selection imposed on each herbivore is generalized, and very weak compared with the high mortality caused by toxins. Frequently, this array of defenses is effective, as for herbivorous insects feeding on summer oak leaves (Feeny, 1970). But in other systems, such as beetles feeding on Eucalyptus and some grasshoppers feeding on an array of woody plants, the herbivores have been able to adapt successfully (Fox and Macauley, 1977; Bernays et al, 1980). Rather than reciprocal step-wise alterations, this system results in continuous minor adjustments in the plants, involving not only defensive chemistry, but also changes in phenology, increases in structural defenses (e.g., toughness) and reductions in the nutritional quality to enhance overall resistance to herbivores. There is a broad array of potential responses by the plants, and to be overcome, they would require a broad array of responses by the herbivores trying to cope with this poor PLANT-HERBIVORE SYSTEMS: DEFENSE, DYNAMICS # + ™ 861 diet. Both the plants' defenses and the her- tion results in continuous minor changes bivores' counteradaptations will probably in plant defenses in response to the assembe under complex polygenic control. Each blage of herbivores using them. The deline of defense and especially the entire fenses are not the result of simple stepsuite of plant resistance would be difficult, wise coevolutionary interactions, and the though possible, to overcome. In addition, presence of DRs is not related to easily afintraspecific variation in these defenses fordable costs as suggested by the appar(e.g., several types of tannins) makes it ency model. Instead, they form the best even more unlikely that they will be over- mode of action to employ against a large come completely. However, because suc- number of species of herbivores. cessful herbivores may counteradapt in DISCUSSION AND SUMMARY different ways to all or part of the plants' resistance, new modes of defense would Several major assumptions of defense evolve very slowly. theory need to be modified to accommoSimilar arguments may also be applied date recent data and a different commuto parts of plants with different life expec- nity perspective. First, there are good reatancies. Although defense theory draws sons to question the assumption of major analogies between ephemeral plants and differences in costs of different modes of young leaves in terms of costs of produc- defense. Some data suggest that defenses tion and availability to herbivores (Feeny, have a cost, but assumed differences in 1976; Rhoades and Cates, 1976; Rhoades, costs between toxins and DRs shrink with 1980; Cates, 1980), the selective pressures increasing chemical information about deimposed on them are very different and fenses. In any case, the explanation I prothey might be expected to be protected pose for the presence of toxins and DRs differently (McKey, 1979). Young leaves suggests that within very broad limits conof persistent plants are ephemeral, but are siderations of costs may even be largely irprobably grazed by a greater diversity of relevant. herbivores than are unapparent plants, Second, the basic distinctions between with higher chances of being found by de- qualitative and quantitative compounds scendants of herbivores that successfully also are not supported. Some major comused the plant the previous season. Fur- pounds fit into both groups: some "qualither, cost arguments about toxins vs. DRs tative" defenses may elicit dose-dependent are probably irrelevant, not only for rea- responses in partially adapted herbivores, sons discussed earlier, but also because ex- while clearly, it is possible for herbivores panding leaves on a persistent plant may to completely overcome some "quantitause previously stored nutrient or energy tive" defenses, such as tannins. However, reserves for defense. Therefore, while tox- the terms that describe the mode of action ic defense compounds are likely to be of different defenses remain very useful found in young leaves as predicted from and biologically appropriate: toxins and defense theory, arguments invoking the digestibility-reducing compounds describe herbivore community suggest that DRs both the actions and their effects. should also be present. Recent data show Finally, I have argued that differences that young leaves and even buds of many in the complexities of the herbivore assempersistent plants contain both DRs, such as blages cause differences in types of defentannins and terpenes, and toxins. These ses that have evolved in apparent and unplants include eucalypts, madrones, everapparent plants. In addition, the scenario green oaks, and rainforest trees (Belserof step-wise coevolution is much more ene, 1980; Crankshaw and Langenheim, plausible in diverse communities of 1981; Fox and Macauley, 1977; Langenshort-lived plants than among persistent heim et ai, 1980; McKey, 1979). plants. The spatial and temporal patterns These arguments provide an alternative in each community have led to major difexplanation for the observed defenses of ferences in the complexities of the assemapparent plants (Table 2). Diffuse selec- blages of herbivores using these types of 862 LAUREL R. FOX plants. Among apparent plants both herbivory and coevolution are diffuse, involving gradual and continuous adjustments rather than step changes in a simple system. This model of two coevolutionary processes affecting plant-herbivore interactions explains the same observations as the original defense theory, but for very different reasons, with very different mechanisms and with very different assumptions. This model also explains more recent data that are not compatible with conventional defense theory. Many additional factors modify simple step-wise coevolution even in unapparent plant communities. First, herbivores' diets may be restricted locally by the numbers of potential hosts or other features of a particular community (Fox and Morrow, 1981). Second, other environmental stresses on herbivores or plants may greatly reduce population densities, creating evolutionary bottlenecks. The selective effects of both of these factors may be unrelated to variation in plant defenses: bottlenecks, in particular, may result in selection for factors independent of any consistent previous history (Wiens, 1977). Finally, my arguments, and defense theory in general, share the implicit assumption that both plants and their herbivores are the main selective pressures influencing defenses and patterns of host use. This is not necessarily so. Dynamics of these species are linked in very complex ways, and are affected by other ecological pressures. Defensive compounds or structures affect mortality caused by the herbivores' predators and parasites (Lawton and McNeill, 1979; Vinson and Iwantsch, 1978; Price et al., 1980), while these same compounds affect allelopathic interactions among plants (Whittaker and Feeny, 1971). The latter may be particularly important in very complex communities of unapparent plants. Ultimately, explanations of defenses and counteradaptations will have to account for effects of the herbivores' own competitors and natural enemies, and of competing plants. The patterns of interactions in many communities are rarely simple enough to fit the step-wise evolutionary model very easily. They are, rather, much more diffuse, showing a broad array of small responses appropriate when there are many interacting genomes. Simple step-wise coevolution is most likely to occur when the number of interacting species is small: diffuse coevolution will become increasingly important as the number of species increases. It is important to emphasize, however, that complex interacting assemblages have special properties that cannot be derived just by summing up all of the simple interactions that occur. ACKNOWLEDGMENTS I am grateful to several people who provided critical interactions at all stages in the development of the ideas presented in this paper, especially J. Estes, J. 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