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Developing a Theory of Plant-Insect Herbivore Interactions: Are We There Yet?
Author(s): Nancy E. Stamp
Source: Bulletin of the Ecological Society of America, Vol. 77, No. 1 (Jan., 1996), pp. 51-61
Published by: Ecological Society of America
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lution. Macmillan,
New York, USA.
Tansley, A. G. 1947.
New
York,
tity. Pages
Frederic
Ed
Jour
1874-1945.
ward Clements,
nal of Ecology 34:194-196.
Tobey, R. 1981. Saving the prairies:
the life cycle of the founding
plant ecol
school of American
of
ogy, 1895-1955.
University
California
Press, Berkeley,
Cali
fornia,USA.
Shantz,
H.
1945.
Van Leer, D. 1991. Society
Frederic
Edward
I was
to talk
Recently,
asked
about how the field of ecology has
benefitted from study of plant-insect
To get a
herbivore
interactions.
sense of what ecologists
think this
I looked
has contributed,
discipline
at seven ecology
texts published
from 1990 through 1994. Ecology
texts are revised about every
5 years
for an intensely competitive market,
so we might expect that they would
reflect what ecologists
view as the
important contributions of plant-her
bivore interactions. On average 2.3%
of an ecology text deals with plant
herbivore interactions, but that is 9
10 pages less than for competition
(3.6%) or animal predation
(3.8%).
Only three of the seven texts devoted
a chapter to the topic of plant-herbi
vore interactions. Likewise, mutual
ism (e.g., pollination,
by animals,
seed dispersal
ants protecting
plants,
re
microbial-plant
associations)
ceives much less attention than com
petition and predation. A dominant
focus on competition
and predation
limits our understanding
of the di
of factors
versity
that shape and
maintain
communities.
and iden
in E. Elliott,
history of the
editor. Columbia
American
novel. Columbia
versity Press, New York,
Uni
New
York, USA.
sociology,
Ward, L. 1968. Dynamic
or applied social science. Two
re
The 1883 edition
volumes.
Wilson,
of natural
cal Review
communities.
28:1-240.
reflect:
vegetation
Journal of Vegeta
tionScience 2:289-290.
D.
1985. Nature's
Worster,
economy:
a history
of ecological
ideas. Second edition. Cambridge
University Press, Cambridge,
UK.
G. Barbour
Michael
Department
of Environmental
Horticulture
University
of California
CA 95616
Davis,
Poor coverage of plant-herbivore
may
1991. Does
exist?
Botani
Why less coverage?
interactions
J. B.
science
Press,
printed
by Greenwood
New York, New York, USA.
Whittaker, R. H. 1962. Classification
Clements (1874-1945). Ecology
26:317-319.
Developing a Theory
of Plant-insect Herbi
vore Interactions: Are
We There Yet?
485-509
(1) age of
the subdiscipline, (2) complexity of
(3) paucity of math
and (4) the large
models,
ogy of plants, especially production
of secondary metabolites, must be
taken into account because
this often
determines food quality for the her
the interactions,
bivore.
ematical
animal,
For an animal eating another
food quality
is largely
de
and ever-increasingvolume of litera
fined by energy gained (Stephens
ture in this field.
and Krebs
1986). For herbivores,
food quality is more complicated and
First, research on plant-insect
herbivore interactions exploded in
the late 1960s following publication
and Raven's
(1964) corre
lation of use by related butterfly spe
of Ehrlich
cies of taxonomically
and/or chemi
cally related host plants. The subdis
cipline of plant-herbivore interac
tions, then, is about 35 years old,
whereas study of competition and of
predation have been active fields of
research
for about 60 years. Our
ideas about the process and conse
and preda
quences of competition
tion have been fairly well developed
and articulated in reviews and books
for as long as 15-20 years, so it is
to authors of ecology
texts
clearer
what to present about competition
and predation.
Second, plant-herbivore interac
tionsmay be poorly covered because
of
the complexity
of factors
influ
encing these interactions, in particu
lar plant chemistry,
the interplay of
multiple trophic levels, and the inte
gration of ecological and evolution
ary time. For example,
the physiol
includes the amounts of nitrogen,
water, allelochemicals, and sub
stances
that determine
digestibility.
toughness and
All of these factors can
variable in plant material,
be highly
while
the availability
of energy is
both relatively high and less vari
able. As a consequence of such com
plexities, the field of plant-insect
herbivore interactionshas given rise
to subdisciplines, such as the nutri
tional ecology of plant-insect herbi
vore systems (Scriber and Slansky
1981,
Coley
et
al.
1985),
the
phylogenetics of plant-insect herbi
vore systems
(Farrell et al. 1992),
the
chemical ecology of plant-insect
herbivore-parasitoid systems (Dicke
et al. 1990, Vet
and Dicke
1992),
and tritrophic level interactions
(Price
et al.
Gould
1992).
1980,
The
Johnson
growth
of
and
these
subdisciplines has contributed to a
greater understandingof themecha
nisms underlying patterns of plant
insect herbivore interactions, but
without
a synthesis
January
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1996
among
these it is
51
difficult for authors of textbooks to
see how the contributions
of these
fields link together.
Third, developing
predictive
models of the effects of interactions
between trophic levels on population
dynamics
has long been a goal in
ing of the field. Undoubtedly,
au
thors of ecology
texts rely on re
views to help them process informa
tion and ideas. Broadly
focused re
concepts.
The same was true of the
on animal predation.
But
chapters
sections on plant-herbivore interac
tions were much less uniform in the
principles,
ideas, and terms empha
sized, and only three books provided
views providing
syn
the necessary
thesis cannot keep pace with
the
rapid expansion of this field. For in
models illustrating population dy
stance,
in the study of the effects of
resource availability
on plants and,
namics
in turn, on insects, there has been a
proliferation
of hypotheses,
all of
often
particularly
cals,
which
However,
ecology.
in
research
plant-herbivore interactions has fo
cused
on
the above
complexities,
the role of allelochemi
rather than on modeling
plant
herbivore population dynamics. Al
models
though mathematical
of the
dynamics of interacting populations
have been applied to plant-herbivore
interactions
(May 1973, Noy-Meir
1976, Crawley
1975,
Caughley
1983),
been
may
these applications
especially
be due
have
satisfactory.
to several
factors:
herbivores
kill
plants,
to predators
rarely
contrast
in
not
This
their
(1)
host
of
animal prey,
(2) the perceived asym
in the interaction (e.g., com
to
has often been shown
petition
limit plants, while
fewer studies
metry
have demonstrated
strongly limiting
of natural
on
effects
herbivory
plants do
plants,
and conversely,
have a strong effect on herbivores,
1983), (3) scarcity of data
Crawley
on plant
(e.g., impact of herbivores
growth rate, rates of consumption,
in the
herbivore population density)
are currently
viable
to some
degree, e.g., carbon:nutrient balance
(Bryant
et al. 1983),
hypothesis
growth-differentiation balance hy
pothesis (Loomis 1932, 1953, Lorio
1986, Herms
and Mattson
1992),
plant stress hypothesis
(White 1974,
1984), plant vigor hypothesis
(Price
et al. 1990, Price
fense hypothesis
Feeny
1976,
1991),
optimal
de
(McKey
1974,
Rhoades
and Cates
1976, Rhoades
1979),
and resource
of competition
predation
also make
such assump
systems are even
tions, and animal
more likely to violate
ing
and animal
assumptions
the simplify
than plants
(Caughley
1976), these versions of
have been
"predator-prey"
models
around longer and generally are ac
cepted as useful constructs in ecol
ogy texts.
Fourth, the literature of plant
herbivore interactions is increasing
exponentially, which makes it diffi
cult to assess our currentunderstand
52
illustrate
clearly
the
teractions.
The
examples
came
as "gee whiz" types or
isolated case studies. For instance,
the monarch butterfly story was of
ten presented. But usually the biol
across more
ogy of the particular
took
system
precedence
over making
clear the
generality of the example. The same
was true generally for mutualism
ex
amples
in these texts.
Furthermore,
only one of these
texts gave a historical perspective of
hypothesis development in the field
rule some out, consolidate some or all
these hypotheses,
or construct
some kind of hierarchy, is unclear. As
difficult as itmay be to develop such
of
the field of plant-herbi
syntheses,
vore interactions needs broadly fo
to develop
cused syntheses
into a
presentation ofplant-herbivore
interactions
models
did not
key concepts of plant-herbivore in
of plant-insect
herbivore
interac
tions. This is unfortunate because de
hypothesis
(Coley et al.
1987). Yet a synthesis of
how
these hypotheses
to
relate
one another, where we stand with
each of these, and whether we can
met
Although
in
1985, Coley
more mature field. Doing
so would
ensure that the general principles de
rived from the study of plant-herbi
vore interactions
will be incorpo
rated into materials we present in our
ecology courses.
1976).
and herbivores
availability
form amenable for testing the mod
els (Begon and Mortimer
1981), and
that allow for the
(4) lack of models
of herbivores
interactions
complex
with their food supply (e.g., induc
Further
tion of chemical defense).
have restrictive
more, most models
to be
that are unlikely
assumptions
(Caughley
of plants
teracting. Examples, as presented,
Some additional
These
reasons
observations
about
for the poor cover
interactions
age of plant-herbivore
are suggested by the ways that com
petition, predation, and plant-herbi
are presented
in
vore interactions
different
texts. For all of
the text
books, chapters on competitionwere
fairly uniform, emphasizing the
same principles and ideas and using
the same terms. Each text provided
models of the effects of competition
on population dynamics, and ex
amples clearly illustrated the key
velopment and testing of hypotheses
in this field is a particularly nice ex
ample of the scientific
process,
which
is all too elusive to the aver
age student.
The study of plant-insect
herbi
vore interactions
has given much
more to our current understanding of
basic ecological
issues than is appar
ent in these texts. If nothing else, it
explains much about the ecology of
50% of the macroscopic
species on
earth.
The fault for an inadequate pre
sentation of our current understand
herbivore interac
ing of plant-insect
in
tions lies with those of us working
this field. We
message
have not given
the basic
about
a clear
ideas
emerging in our discipline. We often
in detail. In
drown other ecologists
to pi
doing so, we tempt authors
geonhole our field as a host-parasite
or predator-prey
and
interaction,
to ecol
thus important contributions
ogy, particularly community ecol
ogy, are lost.
Themessages of plant-insect
herbivore interactions
Here I listwhat I perceive as 12
basic generalizations of plant-insect
SocietyofAmerica
Bulletinof theEcological
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interactions
important to
I
the field of ecology and evolution.
have organized these into six catego
ries, which
show the scope of the
generalizations,
emphasizing
both
the role of chemical
and
ecology
or tritrophic
processes,
community
herbivore
level interactions
(Table 1). With
I provide an ex
each generalization,
ample or some other justification.
This
is not an exhaustive
equate
places
or even ad
review of the field. Rather it
these generalities
in broader
ecological
Table
The plant's
support
various parts of this statement.
are characterized
ticular
are found
the
Plant
(e.g.,
in the plant
Apocyanaceae,
Asclepi
and Scrophulariaceae)
adaceae,
and Janzen 1979, Har
(Rosenthal
borne 1982). Plant genotypes vary in
their resistance to insect herbivores.
netically
interac
array of defenses.
can have a cost.
The herbivore's
ability
to exploit a plant
3. Herbivores
deal with poorer
4. Herbivores
have a dynamic
food quality
than predators.
array of countermeasures.
plays a large role in feeding
5. Plant diversity
specialization.
effects: herbivore
vs. herbivore,
among herbivores
vs. plant
plant
depends
on type of feeding and life
history traits.
7. Indirect (resource-mediatedand enemy-mediated) interactionsare
common between herbivores.
families
For example,
herbivore
8. Herbivory
lessens a plant's
distribution
and abundance
Bottom-up:
effects of plants
ability
to compete
alters
and, consequently,
of plants.
by par
allelochemicals
cardenolides
of plant-insect
itself
1. Plants have a dynamic
6. Competition
environmentalconditions.
families
to defend
ability
2. Defenses
Lateral
1. Plant species have a dynamic
array of defenses, reflecting phylog
eny, genotype, phenology and
studies
of the 12 messages
contexts.
and pedagogical
Numerous
1. Short version
tions.
on the herbivore's
9. Plant traits can affect performance
10. Parasitoids
Top-down:
are more
often specialized
effects of the herbivore's
enemies
can limit herbivores
11. Enemies
enemies
of the enemies
of herbivores.
than predators.
on plants
and improve plant productivity.
cowpeas
have three ge
to resist a
ways
different
on eating pods
specializing
on seeds: inhibition
and ovipositing
of adult feeding, inhibition of ovipo
sition, and extension of larval devel
beetle
(Cuthbert et al. 1974). The
genotypes
vary in their ex
pression of each of these resistance
traits. Environmental
conditions
al
ter the genotypic expression of host
resistance
to herbivores
plant
(Kennedy and Barbour 1992). For in
stance, high levels of fertilizer elimi
nated resistance of tomato to three
insect herbivore species (Barbour et
al. 1991). Jones (1983) gives an ex
Community
structure
12.Much biodiversity due to plant-herbivore interactions.
opment
cowpea
time. For instance, damage by herbi
vores can induce greater chemical
defense
by plants
(Tallamy
and
Raupp 1991). Such defenses can de
ter feeding by insect herbivores, kill
them, or slow their growth (Kennedy
problem
and Barbour
1992, Bernays
and
Chapman 1994), which makes them
to other sources of mor
vulnerable
bred for palatability. Furthermore,
ef
illustrating phenological
fects on potential defenses. The con
centrations of various phytochemi
tality.
For ecology students,understand
cals in bracken fern that can affect
insect performance
fluctuated over
derstanding
the growing season. Some increased,
others decreased. Thus, a dynamic
array of phytochemicals linked to
host-plant resistancewas exhibited.
All plant defenses are dynamic in
evolutionary time; chemical de
fenses are also dynamic in ecological
ducers,
ample
ing this first point
community
is critical
to un
the role of plants
structure. Plants,
the energy
provide
community
in
(e.g.,
not
for
etc.). People probably view plants as
for the most part palatable because
the grocery store carries only plant
that have been
products
selected
or
most people do not make the connec
tion that nicotine, caffeine, and co
caine are natural plant products that
help a plant defend
vores
itself from herbi
and pathogens,
the concentrations
let alone
that
vary in some
for example, with
may
the pro
systematic
for the
phylogeny, genotype, phenology,
and environmental conditions. Al
to operate,
fend that energy
for animals
themselves, cattle, gypsy moths,
but they de
and their other re
way,
though five of the ecology
texts con
sources. This now seems obvious to
ecologists, but to most people this is
veyed
news because
sented this fundamentalpoint.
from their perspective
eating plants does not seem to pose a
some
part of this message,
none of the seven texts clearly pre
January
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1996
53
2. Plant defenses
can have a cost that
affects growth and other correlates
offitness.
An experimentby Baldwin, Sims,
and Kean
(1990) on the effect of leaf
damage
on wild
such costs.
tobacco
Seed production
in plants
duced
illustrates
was
that increased
re
alka
loid production in response to dam
in damaged
age, but not
which
in
plants
alkaloid production was
blocked with
there was
auxin. Thus,
a trade-off between
alkaloid
produc
tion and seed production.
Cost, the trade-off between de
fense and correlates of fitness such
as growth
and seed set, is most
com
monly demonstrated at vulnerable
or when
stages
For
resources
a variety
of
are poor.
reasons,
it has
proven extremely difficult to esti
mate
these
costs
(Gulmon
and
Mooney
in
1986). For example,
in a defensive trait (such as an
3.Although food quantity is espe
cially criticalfor secondary consum
ers (carnivores/predators),it is food
quality (toughness,digestibility,
spines, toxins,and nutrientsof
plants)
that is of major
importance
for most insectherbivores.
Nitrogen, a limiting nutrient, is
content
(Scriber
course,
and
in plant
1981). Of
eating plant material
is fur
ther complicated
chemicals
material
Slansky
present,
by the allelo
which
can con
straingrowth (Slansky 1992).
Numerous studies and reviews
provide evidence for the message
nogenetic genotypes of fall canker
in a
(Mole
eral, resistance
plant because
tively
rapid
Earth
is now
of a
are the founda
plants
With
climate
the rela
that
change
experiencing,
plants
and
be increasingly
stressed,
to her
thus the cost of resistance
may
bivory may
increase
sumes
(Ayres
the general
Increasingly,
that we
1993).
public
can (or soon will
able to) genetically
engineer
as
be
our way
out of trouble with
insect pests. But
plants
to resist
engineered
insect
pests may be less fit than the original
plant stock because
ally mean
an added
added genes usu
cost of synthe
sizing plant chemicals (Tiedje et al.
1989). Thus, an understandingof the
potential cost of plant resistance to
herbivory is critical to determining
how tomaintain (or increase) pro
ductivity in natural and managed
ecosystems.
54
physiological mechanisms.
Defensive countermeasures em
ployed by insect herbivores include
clipping trichomes (hairlike growths
on plants
that may
chemicals),
cutting
contain defensive
leaf veins to pre
vent transport of defensive chemi
cals, aversion learning, inducing
detoxification systems, altering gut
Ph, maintaining gut redox conditions
and gut surfactants
(detergents
that
herbivores
for the economy
tion of communities.
have a dynamic
The
to herbivory
Ecology studentsneed to develop
an appreciation
4. Insect herbivores
transfer, a
1992).
it is
that, in gen
ness costs to a plant (Simms
of energy
ferences in timing of leaf flush of in
dividual host plants (maple and oak).
1994). However,
to conclude
cal inefficiency
has fit
they do not sum to 100% of the or
reasonable
on insect
solubilize phenolic-protein com
plexes), altering rate of excretion,
having reduced sensitivity
to
allelochemicals, and sequestering
plant
toxins (Slansky
1992,
Dussourd 1993). Determining that
decrease in reproduction if together
ganism
of food quality
array of countermeasures
that
facilitate exploitation of plants,
which include behavioral and
1% of biomass)
not result
constraint
herbivores helps explain the ecologi
and Scriber 1985), so herbivores deal
with poorer food quality than preda
tors. Much of the variation
in rela
tive growth rate of insect herbivores
can be explained
by nitrogen
and
water
to un
on in
sect herbivorenumbers,which in turn
limits secondary consumers, or
predators. This message about the
central principle of ecology.
allelochemical comprising less than
may
sects to extract is fundamental
derstanding a major limitation
in plant ma
much less concentrated
terial than in animal tissue (Slansky
that food quality is more of a prob
lem for most insect herbivores
than
food quantity. For instance, parthe
crease
make that nitrogen difficult for in
worm
differ in both adult emergence
time and egg hatching
time (Mitter
et al. 1979). These times parallel dif
cankerworms
grow best on
young leaves, which have higher ni
trogen and water content. Individual
trees tend to be relatively constant in
timing of leaf flush, e.g., early year
after year, and cankerworm
clones
tend to use the same trees year after
year. Consequently, via genotype
and low dispersal, the herbivores are
able to track the narrow window
of
availability of new leaves, the high
est quality food. It is the work on in
sect herbivores, a very diverse group
of herbivores in terms of plant tissue
that makes
used and feeding method,
it clear that obtaining
high-quality
food is a basic problem for herbivore
species in general. Yet only half of
the ecology
texts addressed
this
point, and even then the message
was diffusely presented. It is a point
that seems obvious to us, but one
that students can easily miss.
Understanding that animalsmust
extract nitrogen in order to grow and
thatplants contain little nitrogen and
can
counter
plant
de
fenses increases our understanding
of the mechanisms
structuring food
webs and provides
insight into the
success of insect pests.
5. Plants are a major force driving
the evolution offeeding
specializa
tion by insect herbivores that
frequently leads to narrow host plant
ranges.
This point is nicely illustrated in
and Mitter's
(1994) study of
Farrell
milkweeds
(Asclepias)
of beetles
and a group
on them. Phy
specializing
logenies of the host plants and herbi
vores are closely matched. While
the
process
that generates
patterns of
feeding
specialization
is unclear,
host-plant chemistry would often
have had a role, perhaps directly as
feeding deterrent or stimulant, re
ducing or enhancing insect growth or
survivorship, or perhaps simply by
favoring "specialization" through
simplification of decision-making
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texts gave
borers, seed and fruit feeders, but
less for exposed leaf chewers (Denno
et al. 1995). In contrast to other data
an example of feeding specialization
and mentioned
by insect herbivores
the roles of secondary metabolites,
this
how common
none indicated
sets (e.g., Connell
1983, Schoener
1983), the data set for insect herbi
to compare
is large enough
vores
feeding guilds and life history traits
pattern was.
and
and aggregation),
(e.g., mobility
thus to test hypotheses. For example,
competition was detected more fre
and Chapman
processes
(Bernays
1994). Al
1994, Bernays and Wcislo
though half of the ecology
people may think that her
like grasshop
bivores are generally
have a very
pers, some of which
Most
wide
more
host plant range. But in fact,
than 90% of insect herbivores
to plants in three or
are restricted
fewer plant families
(Bernays and
Graham
1988), and 70% of insect
are even more special
herbivores
their feeding to plant
restricting
ized,
species in one family (Bernays and
So the study of
Chapman
1994).
interactions, with an
plant-herbivore
emphasis on the role of phytochem
istry, has contributed
to
significantly
of host plant
our understanding
by insect herbivores
specificity
of
a striking
pattern
yielding
biodiversity.
This is an important
since plants and insect her
message,
bivores
together account for about
50% of macroscopic
species (Strong
et al. 1984).
6. The importance of direct competi
tion forfood among insect herb
ivores instructuringcommunities
depends on typeoffeeding and life
history traits.
Half
tioned
of
the ecology
texts men
Smith
Hairston,
and
that
Slobodkin's
(1960) observation
is green,"
from which
"the world
these authors deduced that predators,
rather than food, limited population
size of herbivores.
for a
Although
different reason (number of species
present on a host plant being limited
by
pool
Strong,
of
gregated
feeders
species,
(Denno
and forb and grass
et al. 1995).
Since
insect herbivores account for 26% of
the macroscopic
species (Strong et
al. 1984), these patterns of competi
insect herbivores give
tion between
us insight into the conditions under
can be more or
which competition
less important than other factors in
structuringcommunities.
7. Indirect,or resource-mediated
and enemy-mediated,interactions
among
insect herbivores
as well as negative
ent, yet both are important
in orga
nizing community structure. Large
vertebrate herbivores are often eco
systemmodifiers (e.g., beaver, prai
rie dogs, moose, Thomson's gazelle,
and elephants alter nutrient cycling
of
and abundance
and distribution
and thus have a large impact
plants)
on other herbivores (McDowell and
et al.
1986, McNaughton
Pastor et al. 1988, Whicker
and Detling
1988). In comparison,
on a
herbivores
operate
insect
Naiman
1988,
yet can have just as pro
on their associates.
found an effect
herbivores
associa
ability
can reduce nitrogen
avail
in
and induce plant defenses
tions.
Resource-mediated interactions
foliage, resulting in reduced growth
rate, survival, fecundity and density
refers to feeding by
of herbivores
one
causing
herbivore
species
changes in the plant that in turn in
fluence the plant's quality as food
of other herbivore species (Denno et
the scale of ef
al. 1995). Likewise,
fects of enemy-mediated interactions
differs for invertebratevs. vertebrate
herbivores, yet both contribute sig
nificantly to community structure.
for other species
1993).
(Damman
For example, damage on cotton by a
herbivorous mite induced resistance
These
indirect
interactions
to armyworms
than ecological
subtleties;
and another mite
spe
and Carey
1984,
(Karban
Karban
1988). In enemy-mediated
interactions, herbivores interact indi
the foraging be
rectly by affecting
havior and population
dynamics of
cies
natural enemies. For instance, leaf
miners near colonies
of ant-tended
treehoppers suffered lower levels of
predation by nabid bugs than those
colonists),
farther
from
the ant-treehopper
groups,
because
the ants chased
bugs away
leaf miners
insect herbivores as it is for other
kinds of organisms. However, a re
cent review of 193 species interac
tions suggests that exploitative and
interference competition are impor
tant for insect herbivores, particu
larly for sap feeders,wood and stem
the interactions of predators and of
predators and leaf miners. Enemy
mediated interactionsbetween insect
herbivores are as common as direct
competitive interactions, and re
source-mediated interactions be
tween insect herbivores are more
ence of
(Fritz 1983). Thus, the
benefitted
by the pres
treehoppers,
which
are more
they are
importantin explaining the distribu
of insect herbi
tion and abundance
vores.
8. Herbivory
lessens a plant's ability
to compete with its neighbors and
thus affects plant density.
of
Here
are a few examples
increasing levels of de
many. With
foliation, defoliated plants were
the
reached a similar conclusion:
is not as important a
competition
force in structuring communities
of
(1984)
of resource
scale of effects
For example, throughfeeding, insect
common,frequently resulting in
positive
The
mediated interactionsbetween inver
tebrateherbivores vs. those between
vertebrate herbivores is quite differ
microscale,
are
and Southwood
potential
Lawton,
quently between sessile species, ag
common than direct competitive in
teractions (Damman 1993). Also, in
contrast to competitive interactions,
not all indirect interactionsbetween
herbivoreshave a negative outcome.
altered
in terms of height
smaller
and produced
damaged
fewer
plants
and mass,
than un
and Bazzaz
seeds
(Lee
1980). In another study, insectherbi
vores feeding on flowers and fruits
dramatically reduced seedling re
cruitment to the plant population
(Louda 1982). Thus, herbivory less
ens a plant's ability to competewith
its neighbors and influences popula
tion size of plants.
January
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1996
55
Although
this message
seems ob
vious to us, the implications
for a
plant are not so obvious to students,
most of whom have had little or no
experience
ture. The
gardens or agricul
fundamental
ecological
constraints on plants are that plants
have
limited
resources,
some of
which
with
they must
neighbors
use
to battle with
and herbivores.
plant-insect
What
the
herbivore literature
shows is that even small herbivores,
such as insects, can reduce the abil
ity of a plant to compete with
its
neighbors for light, water, and nutri
ents and consequently
influence dis
tribution and abundance of plant spe
cies (Louda et al. 1990).
9. Plant chemistryandmorphology
can influence
the abilities
of
parasitoids and insectpredators to
locate insectherbivores.
Examples of how plant chemistry
and morphology
hinder the herbi
enemies
vores'
are the numerous
studies on the effects of trichomes on
herbivores and their invertebrate en
emies. Some trichomes have glands
at the tips that break open to release
chemicals, and the exudate from the
trichomes can hinder insect preda
tors. For instance, four cultivars of
tomato differing in their susceptibil
ity to an insect herbivore that was a
specialist on Solanaceae were tested
(Barbour et al. 1993). Egg predators
were placed
on leaves, with
tri
chomes unmanipulated
or exudate
removed from the trichomes. When
the exudate was present,
egg con
sumption declined in the more resis
tant cultivars. Predator mortality was
higher
when
was
the exudate
is an example
of
present.
This
chemical
resistance
interfering with
of the host plant
the effectiveness
of
can also
Trichomes
emies (Vet and
mans are visually
relatively
poor
students do not
Dicke
1992). Hu
oriented and have a
sense of smell, so
easily relate to the
fact that detecting odor plays a huge
role
in a parasitoid
or insect
predator's ability to locate hosts or
prey. Most vertebrate predators de
pend greatly
on visual
prey
(Heinrich
Collins
1993),
on plant
pend
cues to locate
1993,
Seigel
and
and they do not de
chemistry
for cues.
Plant-insect herbivore-insect enemy
interactions
pattern
show a very different
from that of plant-vertebrate
herbivore-enemy
interactions: a
plants (i.e., use of plant morphology
and chemistry as cues, and tolerance
or detoxification
of plant allelo
vore-enemy
biodiversity.
chemicals
interactions
on
plants.
None
of the ecology
texts con
the
veyed
point that plants can en
hance or hinder the activity and thus
effectiveness
of the herbivores'
en
11. Parasitoids
and insect predators
can reduce herbivore populations
enough to improveplant productivity
emies. This is an important message
for understanding
tritrophic level in
teractions in natural systems and the
limits of biological
control in agri
and otherfitness
correlates.
For example,
the mango
shoot
was accidentally
caterpillar
intro
duced to Guam, where
one of the
major
crops is mango.
In 1986, a
culture and managed
parasitoid
forests.
How
can enemies
be selected
upon by their prey or hosts? De
fenses, concealment,
and
phenology,
numbers of insect herbivores
limit
was introduced to control
the caterpillar
pest. With
the in
crease in parasitism, caterpillar num
bers declined
(Nafus 1991). What
were
the consequences
for the
plants? After
1986, the number of
flowers and fruits increased.
Extra-floral
nectaries
on plants
promote this kind of relationship be
tween plants and insects attacking
the evolutionary
herbivores
10. Insect herbivores act as selective
agents on their enemies, with the
result that parasitoids
tend to be
more host specific than predators.
vores'
options of the herbi
enemies
(Price
1994).
Allelochemicals
herbivores
ingested by insect
can interfere with devel
than predators and their generation
timemust be synchronized to thatof
their host. Such characteristicsallow
parasitoids to use microhabitats that
would not support a predator and to
evolve as fast as theirhost (Weseloh
1993).
the Ecological
sitoids and insect herbivores
than
predators
(ratio of 0.9:1:0.1),
i.e.,
there are seven times as many parasi
toid as predator species (Price 1980).
The rich biodiversity of the inver
tebrate portion of the third trophic
level reflects an intimate link with
of the third trophic level (=
carnivores) are intimately linked with
portion
On the other hand, parasitoids
and insect predatorsuse plant chem
istry as a cue to locate theirhosts or
prey (Vinson 1976, Obrycki 1986).
For instance, chemical changes in
plant tissue induced by herbivores
have been shown to attract insect en
of
which are much less spe
in diet (Price 1980). For in
in the British
insect fauna,
there are many more species of para
cialized
stance,
None
ingested).
of the
texts
ecology
put this together in a
way that permits students to see the
of plant-insect
consequences
herbi
of parasi
opment and survivorship
toids and insect predators (Barbosa
et al. 1991, Malcolm
1992). But
parasitoids are usually much smaller
Bulletin
predators,
greater interdependency
with plants
that, in turn, has shaped a very differ
ent sensory perception of the world.
About 25% of the macroscopic
spe
cies are parasitoids and insect preda
tors (Price 1980). Thus, a large pro
egg predators.
search
physically hinder parasitoids
ing for their hosts (Hulspas-Jordan
and van Lentren 1978).
56
The result of such interactions is
that parasitoids are relatively special
ized in use of host species and are
much more
speciose
than insect
Society
1978, Koptur
(Bentley
1977,
Tilman
and thus are an
of this top
product
1992),
evolutionary
down effect of the herbivores'
en
emies on plants. Although
extra-flo
ral nectaries are usually discussed
in
in
ecology
texts, they are presented
the context of a special
type of mutu
alism rather than as at one end of a
continuum of interactions among
plants, insect herbivores and insects
attacking herbivores. That may be a
consequence of thinking that plants
and predators do not interact,but as
discussed in points 9 and 10 above,
of America
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parasitoids and insect predators
clearly respond to plant traits and
plants can provide signals to insects,
This is an
though nonspecifically.
example of how we can help students
see the broader patterns, as opposed
to just seeing the details of a particu
lar case study.
That parasitoids and invertebrate
predators can reduce herbivore
popu
lations enough to improve plant pro
in
ductivity has been demonstrated
thus
natural and managed
systems,
ter the introduction
of the parasi
toids, species diversity increased dra
matically, and thus the parasitoid spe
acted as a keystone
species
(sensu Paine 1966) by suppressing
the dominant herbivore. Although not
a natural system, this example illus
cies
trates natural
(and repre
common phe
sents an increasingly
as species
are moved
nomenon
around the world by humans). Al
though many
biodiversity
processes
know there is a
few have a con
people
crisis,
for what main
control a viable
biological
alternative
to pesticides
commercial
in at least some situations
(Jutsum
ceptual
1988, Waage
and Greathead
1988).
Even though most of the ecology
texts provided
an example of bio
logical control, only half of these
on
system
(1966,1974)
rocky intertidal system
help students see the link between in
texts
logical
scale and biodiversity
pression
on an ecological
making
plants
clearly
made
the point
that
benefit
by the presence
and predators.
of
parasitoids
12. The problems
framework
tains a community
of diverse
of organisms
teractions
on an eco
(an ex
scale of
But to see
processes).
picture, such examples
evolutionary
the broader
need to be integrated
that must be
organ
such as the mango
Guam
and Paine' s
isms. Examples
into a hierarchy
overcome
before insects can feed on
plants have led to host plant special
ization and proliferation of species.
which we can now
of generalities,
provide, for instance, via an overview
of the messages of plant-insect herbi
Plant effects on herbivores carry
vore-insect
over to the third trophic level,
(Table 1).
Lastly, although there is much to
admire in these ecology
texts, I felt
that none of these 12 messages were
conveyed clearly in these texts, that
especially toparasitoids, resulting
in another very speciose group.
The number of macroscopic
spe
cies is estimated as between 5 and 30
million
1988). Although
insect species are
distributed among only 8 of 29 insect
orders, they account for 26% of the
and
macroscopic
species
(Weis
Berenbaum
the her
1989). Thus,
most
(Wilson
herbivorous
bivorous insect orders are very spe
cies rich. Insects, their host plants
and their parasitoids and invertebrate
predators together account for an es
timated 75% of species. Thus, study
of plant-insect
herbivore
interac
tions, as evident by these messages
(Table 1), has taken us a long way
toward understanding a large portion
of this planet's
The mango
biodiversity.
system on Guam
is, not
interactions
enemy
in any way
that a student
could
and
recognize and assimilate,
there were not even hints of many of
them. This handicaps students in un
as the
issues
such
of
crisis, management
of rapid global
pests, consequences
warming, etc. As a starting place for
a more detailed overview
of plant
I suggest
herbivore
interactions,
Abrahamson's
(1989) edited volume
on plant-animal
interactions.
derstanding
biodiversity
Some general
comments
about
thesepoints
microcosm reflecting the sum effects
of these 12 points for community
ecology. Prior to the introductionof
parasitoids to control the dominant
insect herbivore on mango, diversity
of insect herbivores on mango was
low (SchreinerandNafus 1992). Af
herbivore
interactions,
herbivores
mon
available,
but it is also
worth noting some importantdiffer
ences between invertebrateand ver
tebrate terrestrialherbivores. In gen
eral, 10 of these points apply to
plant-vertebrate as well as plant-in
vertebrate herbivore systems. The
exceptions are points 9 and 12. Re
are not a com
feature of plant-vertebrate
her
bivore systems.
Exception
to point 12 requires
more explanation. Relatively
less di
versity of vertebrate herbivores com
pared to invertebrate herbivores may
largely
reflect
the constraints
of
size and of endothermy
for
Due to these
birds and mammals.
constraints and thus a need for large
amounts of food, vertebrate herbi
body
vores
are usually generalist
feeders
to
though they limit their feeding
particular
types of plants or plant
and Georgiadis
parts (McNaughton
1986, Lindroth
1989).
Furthermore, parasites and preda
tors of vertebrate herbivores are not
as speciose as those of invertebrate
herbivores, reflecting the differences
in the direct
and indirect
on vertebrate vs.
parasites and predators.
plants
effects
of
invertebrate
the relationship of
Consequently,
these points, especially the effects of
plant chemistry,
competition
and
predation,
for vertebrate herbivore
vs.
invertebrate
herbivore
systems
systems, differs. The high degree of
exhibited by
feeding specialization
most insect herbivores
is largely at
tributed
to two selective
pressures,
host plant chemistry and the herbi
vores' enemies
(Bernays and Gra
ham 1988), although
competition
may play an important role for many
et al.
insect herbivores
(Denno
1995). Thus, plant chemistry, preda
tors being deterred by prey contain
ing plant toxins, and parasites'
spe
cialization shaped by plant chemistry
seem much more
than
important
in structuring
inverte
competition
brate
herbivore
communities
they do in vertebrate
The focus here is on plant-insect
is a
garding point 9, the effects of plants
on the herbivores'
predators, other
than through changes in numbers of
herbivore
In contrast,
munities.
ter-specific
competition
than
com
intra- and in
may
have
a
larger role in shapingvertebrateher
bivore communities (Lindroth1989).
Even though 10 of themessages
apply to both invertebrateand verte
brate terrestrialherbivores, some of
these points need furtherexplanation
relative to vertebrates. Regarding
January
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All use subject to JSTOR Terms and Conditions
1996
57
point 3, due to body size and to en
dothermy of birds and mammals,
ob
taining sufficient food quantity, e.g.,
during unfavorable
seasons, may of
ten constrain vertebrate herbivores
more
dom
than food quality. That is sel
the case for insect herbivores,
but only
active
in part because
they are in
unfavorable
seasons.
1 and 2, adapta
points
during
Regarding
tions to herbivory
cotyledonous
by most
plants,
mono
such as struc
meristems, high root-to-shoot ratio,
seem to re
and grazing
tolerance,
flect an association with orthopteran
and
large
mammals
in ecology
texts and to
facilitate
the presentation of the mes
sages of plant-herbivore
interactions
to ecology
students (via communi
cating to those teaching ecology and
writing ecology texts). However,
for
some other groups, I would suggest
on a subset
focusing
sages. For example,
seven
introductory
of
these mes
I also examined
texts
biology
in 1990-1995
for their
published
tural reinforcement
through accumu
lation of silica, intercalary sheathed
insects
represented
coverage of plant-herbivore
interac
tions. On average,
two pages,
or
0.2% of the text, dealt with plant
herbivore
interactions.
Conse
quently, given the page restriction,
these texts could not begin to cover
et al. 1985). In con
(McNaughton
trast, adaptations
to herbivory
by
the 12 messages
that I have listed.
Four of the texts addressed some part
of point 1, three addressed some part
other
terrestrial plants (e.g., elabo
rate secondary chemistry) largely re
flect an association
with other in
of points
sects. Thus, for the former group of
the cost of evading and suf
in terms
is mainly
fering herbivory
interactions entirely. My rec
ommendation
for an introductory bi
text is solid presentation
ology
of
points 1, 4, 5, 1 1, and 12. We might
also want to emphasize
these five
to the public.
messages
plants,
of
tolerance mechanisms,
whereas
for the latter group, cost is more
likely to include physical and chemi
4, 5 and 11, but none ad
dressed points 6-10 or point 12. One
text ignored plant-her
introductory
bivore
degree
to which
these
12
messages would apply to marine sys
tems is unclear. Marine plant-herbi
vore systems differ fundamentally
from terrestrial systems (Hay 1991).
For example, in general the intensity
of grazing is greater in marine sys
tems, the dispersal stages (planktonic
larvae) have very limited ability to
choose microhabitats,
and specialist
herbivores
are rare. Probably
the
messages
apply in general, but with
a qualifier for point 11 in particular.
Marine mesograzers
(such as amphi
pods and polychaetes),
probably the
to terrestrial
equivalents
insects, are subject to intense preda
as well as car
tion by herbivorous
fish (Hay and Fenical
nivorous
ecological
Conclusions
our colleagues,
and the
Acknowledgments
I thank Robert Fritz, Patrice Mor
row, John Titus, Rich Wilkens,
and
ErnestWilliams for their insightful
comments
on the manuscript,
and
May Berenbaum
for the suggestion
to look at introductory biology texts.
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