Download Defense and Dynamics in Plant-Herbivore

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,
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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
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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. Langenheim, R. McGinley, P. Morrow, J. Pearse,
D. Potts, and P. Steinberg.
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