AMER. ZOOL., 27:359-369 (1987)
Evolution of Territoriality by Herbivores in
Response to Host Plant Defenses1
THOMAS G. WHITHAM
Department of Biological Sciences, Northern Arizona University,
Flagstaff, Arizona 86011
SYNOPSIS. Plants may play an active role in the evolution of territoriality and associated
animal behaviors such as spacing and cannibalism. I hypothesize that these behaviors have
in part evolved in direct response to plant defenses that would otherwise diminish individual success. These defenses limit resource availability and concentrate herbivores at
specific sites where they then suffer from induced plant defenses, increased predation and
competition. Plant traits that enhance the negative effects of competition and increased
predation must be included in the suite of plant defenses against herbivory.
In a specific example with Pemphigus gall aphids, plant defenses result in a strong selection
pressure favoring territorial behavior. The negative effects of competition give territorial
individuals a 2.3-fold advantage over non-territorial individuals. Induced defenses (i.e.,
density dependent leaf abscission) can be just as important as competition as a selection
pressure for territorial behavior. With the addition of induced plant defenses territorial
individuals realize a 4.4-fold advantage. Furthermore, rough approximations suggest that
in the absence of territorial behavior predation would increase by 52%.
The same traits which promote territoriality also encourage cannibalism, a surprisingly
common herbivore behavior. To the extent cannibalism reduces the herbivore population,
plant traits which promote this behavior may realize a selective advantage.
Viewing plants as dynamic rather than passive in their interactions with pests may lead
to a better understanding of animal behaviors.
INTRODUCTION
It is well known that adaptive plant traits
can affect the foraging and defense behaviors of pollinators and other mutualists. For
example, swollen-thorn acacias provide ants
with food and shelter in return for their
territorial and aggressive behavior which
is directed against herbivores and competing vines (Janzen, 1966, 1967). Since plant
rewards are directly responsible for the ant
behaviors, the plant has played an active
role in the maintenance, and perhaps the
evolution, of the ants' territorial and
aggressive behavior. Similarly, it has been
suggested that plants can manipulate the
foraging and territorial behaviors of their
pollinators to promote outcrossing and
optimal pollen transfer (Price and Waser,
1979; Waser and Price, 1983). Although
plants may manipulate and promote the
territorial behavior of their mutualists, with
antagonists such as herbivores, just the
opposite may occur. With herbivores, ter-
1
From the Symposium on Territoriality: Conceptual
Advances in Field and Theoretical Studies presented at
the Annual Meeting of the American Society of Zoologists, 27-30 December 1984, at Denver, Colorado.
ritoriality may represent a counter-adaptation against the defenses of the plant.
In antagonistic relationships it has not
been appreciated that plants may have
something to gain or lose from the territorial interactions of their herbivores and
parasites. Because adaptive plant traits can
affect the behaviors of mutualists, it is reasonable to suggest that other adaptive plant
traits may have evolved to affect the territorial behaviors of plant pests. The evolution of plant defenses that manipulate
pest behaviors requires that herbivores
negatively affect their host plants. Experimental studies demonstrate that herbivores can negatively affect the survival and
reproduction of plant populations and can
alter community structure (Crawley, 1983;
Dirzo, 1984; Huffaker et al., 1984, Marquis, 1984; Whitham and Mopper, 1985).
These animal impacts place selection pressures on plants favoring defenses that not
only directly prevent herbivory but indirectly manipulate the behaviors of herbivores for the plant's benefit. Although
plants are known to employ diverse genetically-based chemical and mechanical
defenses that limit their availability and
suitability to herbivores (Day, 1974;
359
360
THOMAS G. WHITHAM
T A B L E 1.
Reproduction on leaves of the same quality as
a function of density and the probability ofpremature death
due to induced plant defenses (i.e., leaf abscission).
Galls/
leaf
Probability of
leaf abscission
and death*
1.8%
10.0
26.8
37.5
53.7
(393)
(140)
(111)
(57)
(23)
Reproductive
success on
remaining leavesb
Average
success of all
colonizers'
100.7 (215)
66.3(321)
55.2 (33)
44.3 (8)
90.6
48.5
34.5
20.5
• Data from Williams and Whitham (1986); numbers in parentheses indicate sample size.
b
Data from Whitham (1986) and unpublished data;
numbers in parentheses indicate sample size.
c
By combining the average reproductive success of
the survivors and the deaths resulting from premature leaf fall, the expected reproductive success of a
colonizer can be estimated.
Rosenthal and Janzen, 1979; Harborne,
1982; Hedin, 1983; Vanderplank, 1984),
the more subtle effects of these defenses
on the evolution of territoriality and associated behaviors have been little studied.
Because resource distribution, quality
and abundance are widely recognized as
being crucial determinants of animal feeding and resource defense strategies (Davies,
1978; Krebs, 1978), through ecological and
evolutionary time plants can manipulate
these traits to affect animal behaviors. Plant
traits such as resource heterogeneity that
restrict plant availability and concentrate
pests at specific sites make herbivores more
susceptible to their own density dependent
mortality, induced plant defenses, the foraging of predators, and all three may act
in concert. Consequently, the evolution of
territoriality, which limits density and prevents clumping, represents a direct counteradaptation to the defenses of the host plant.
Current optimization models of territoriality approach the problem from the animal's perspective (see other chapters this
volume and general review by Davies and
Houston, 1984) and do not consider the
conflict of opposing plant and herbivore
optima.
PEMPHIGUS GALL APHIDS—A
SPECIFIC EXAMPLE
Since aphids are in general viewed as the
epitome of r-selected species in which
resources should be least limited and com-
petition least expected, it is surprising to
find territorial behavior. Several examples
of aphid territoriality are now known
(Whitham, 1979, 1986; Aoki and Makino,
1982) and this behavior has progressed
even further in other aphid species in which
soldier castes have evolved to protect the
gall and its environs from all intruders
(Aoki, 1977, 1979; Aoki et al., 1981). In
the following four sections I present specific examples of how the defenses of narrowleaf cottonwood, Populus angustifolia,
have both directly and indirectly favored
the evolution of territorial behavior by the
gall-producing aphid, Pemphigus betae.
Colonizing stem mothers are susceptible
to plant traits that affect: 1) the window in
time of plant susceptibility to successful gall
formation, 2) the restrictions of sessile living within a gall, and 3) the lack of superior
leaves for galling. These three factors make
leaf choice one of the most crucial periods
in the aphid life cycle. In early spring the
eggs hatch and first instar colonizing stem
mothers migrate en masse from the overwintering sites at the base of the tree to
newly emerging leaves. Since only immature leaf tissues are susceptible to gall formation, the colonizing stem mothers must
quickly initiate their galls before the tissues
harden and become inaccessible. Within
three days the stem mother is encapsulated
in a hollow gall where she parthenogenetically produces up to several hundred progeny (Whitham, 1978). Once settled, the
stem mother is committed to a single leaf
for the remainder of her life.
Colonizing stem mothers face a highly
heterogeneous host environment in which
failure to discriminate can greatly affect
survival and reproductive success. Host
suitability varies within an individual leaf,
between leaves, between branches of the
same tree, and between trees. For example,
in the absence of competition, survival of
stem mothers averaged 100% on the relatively rare large leaves while only 20%
survived on inferior small leaves (Whitham, 1978). Similarly, on a large-leaved
branch 72% of the colonizing stem mothers survived while on an adjacent smallleaved branch none survived (Whitham,
1983). Differences in leaf quality also affect
361
TERRITORIALITY IN RESPONSE TO PLANT DEFENSES
TABLE 2. Comparisons of aphid densities, competitive interactions, and predation on two adjacent branches of the same
tree.'
Branch #1
Aphid densities per branch (galls per 1,000 leaves)
Aphid competition (% population competing)
Predator responses to aphid clumping (% galls preyed upon)b
Vertebrates
Insects
Total
Branch #2
24 (4,630)
4.8%
478(1,333)
56.0%
7.8%
17.6%
25.4% (102)
28.2%
16.5%
44.7% (351)
* Numbers in parentheses indicate sample size.
b
Aborted galls (stem mothers died during colonization) excluded.
number and weight of progeny, and the
rate of development to maturity.
Studies that have examined temporal and
spatial variation in plant defenses within
individual plants (Whitham, 1981, 1983;
Jones, 1983; Raupp and Denno, 1983;
Schultz, 1983a, b; Whitham et al, 1984)
have concluded that the observed levels of
variation have important impacts on herbivores. Such within-plant variation may
be adaptive because it often results in
clumping which subsequently negatively
affects the herbivore population. This
clumping sets the stage for competition and
places a premium on the evolution of territorial behavior as a counter-adaptation
against the defenses of the host plant.
Induced plant defenses and the
evolution of territorial behavior
Leaves occupied by gall aphids are selectively dropped by their host trees, P. angustifolia and P. fremontii, and less than 1 % of
the aphids within the galls survive (Williams and Whitham, 1986). Although most
trees drop 25% of their parasite load (average from 100 P. angustifolia), some trees
abscised as much as 53% of the aphid population. Since aphids occupying abscised
leaves realize nearly zero reproductive success, selection should favor aphid behaviors that circumvent this plant defense.
Premature leaf fall as an induced defense
against gall aphids is highly density dependent. Table 1 shows that the probability of
a leaf being dropped by the host tree is
dependent upon the number of galls occupying the leaf. For example, if the leaf does
not support a gall the probability the leaf
will abscise is only 1.8%. As densities rise
from one to four galls per leaf the proba-
bility of abscission increases from 10.0 to
53.7%. Thus stem mothers that share leaves
with three other stem mothers are 5.4 times
more likely to be dropped from the host
plant than those occupying leaves singly.
Because stem mothers that share leaves
are much more likely to trigger the induced
defenses of the host plant, induced defenses should be most effective when combined with high variation in leaf quality
which further concentrates pests. For
example, variation in leaf quality concentrates colonizing stem mothers on superior
leaves and branches, which in turn increases
the probability that induced plant defenses
will be effective. To avoid triggering
induced host defenses territoriality may
represent an important counter-adaptation to maintain densities at reduced levels.
Competition and the evolution of
territoriality
To the extent that competition among
herbivores reduces their population, then
competition should be included among the
suite of plant defenses against herbivory.
For example, Table 1 shows the reproductive success of stem mothers that survived the induced plant defenses. As the
number of stem mothers increased from 1
to 4 per leaf, average reproductive success
dropped from 100.7 to 44.3 progeny. If
colonizing stem mothers were able to avoid
such competitive interactions, the resulting populations on individual trees would
have been much greater.
As one might expect in a system where
the host plant benefits from the negative
interactions of its pests, these aphids suffer
the negative effects of competition at low
population densities. Table 2 shows that
362
THOMAS G. WHITHAM
CC
UJ
6.0
O
DISTAL STEM MOTHER
BASAL STEM MOTHER
LEAF BASE
5.0
UJ
5
4.0
_
UJ
CO
2 <
O m
3.0
DC
U- LL
UJ LU
o
lt- oI-J-
2.0
co
Q
1.0
1400
1600
1800
1000
1200
1400
1600
1800
800
1000
TIME
FIG. 1. The positions of two competing stem mothers on a single leaf blade are plotted as a function of time.
Position on the leaf blade was measured as the distance from the stem mother to the base of the leaf blade.
During the first 24 hr of observation both competing stem mothers spent most of their time at a common
boundary engaged in kicking-shoving contests. When the distal stem mother was removed, the basal stem
mother crossed the boundary that had previously separated their territories and incorporated the territory
of the other stem mother into a new enlarged territory (adapted from Whitham, 1986). Stem mothers released
from competitive interactions show both behavioral and reproductive release (see text).
even when population densities are as low
as 24 galls per 1,000 leaves, 5% of the aphid
population was doubled-up on the same
leaves and suffered reduced success. At
higher population densities of 478 galls per
1,000 leaves, 56% of the aphid population
was engaged in competitive interactions.
The decline in reproductive success with
increased competitor densities is due in part
to the negative effects of competition on
the gall-forming behavior of colonizers.
Figure 1 shows the probing behaviors of
two stem mothers competing for a leaf during the early stages of gall formation. These
stem mothers spend little time engaged in
probing the leaf tissues to induce gall formation; most of their time is spent at a
common boundary engaged in kickingshoving contests that may last two days and
often result in the death of one or both
competitors (Whitham, 1979,1986). If one
of the colonizers loses in a competitive
interaction or is experimentally removed,
the remaining stem mother shows behav-
ioral release. In the example shown in Figure 1, when the distal competitor was
removed the basal stem mother soon incorporated the vacated territory into a new
enlarged territory and began continuously
probing the leaf tissues. The amplitude of
the probing behavior (shown in Figure 1
as the back and forth movements of the
stem mother along the midrib of the leaf
blade) is important because it is correlated
with the size of the mature gall and the
number of progeny. The sizes of the mature
galls formed by competing stem mothers
and the number of progeny they produce
are reduced in comparison to solitary stem
mothers.
Because losing a competitive interaction
or having to share a leaf with a competitor
negatively affects survival and reproduction, selection should favor territorial individuals that exclude competitors. Whitham
(1979, 1986) showed that the outcomes of
competitive interactions are largely determined by body size. The best gall sites on
TERRITORIALITY IN RESPONSE TO PLANT DEFENSES
363
an individual leaf and the best leaves are where the density of aphids was much
occupied by the largest stem mothers. In higher (478 galls/1,000 leaves), these same
comparisons of competing first instar stem predators destroyed 28.2% of the galls (x2 =
mothers that had just settled, the body sizes 18.163, P < 0.001).
of those occupying superior gall sites were
In contrast to the selective foraging of
significantly larger than those occupying vertebrate predators, insect predators (two
inferior gall sites. Additionally, stem moth- dipteran larvae, Syrphus sp., Leucopis sp.,
ers that did not share their leaves with a and adults and nymphs of the hemipteran,
competitor had the largest body sizes of Anthocoris sp.) did not discriminate between
all. Aoki and Makino (1982) report similar different prey densities (x2 = 0.071, P >
body size relationships for the colonizing 0.7).
stem mothers of the territorial gall-formThe combined impact of both predator
ing aphid, Epipemphigus niisimae.
groups on aphid survival is yet another
The importance of large body size in ter- selective pressure for the evolution of territorial conflicts may be so great that it has ritorial behavior. By combining both seleccontributed to evolution of a characteristic tive and non-selective predation, aphid
trait of the Eriosomatidae or gall-forming mortality on the high density branch was
aphids. Each stem mother is the sole prog- 45% compared to only 25% on the adjaeny of a female sexuale {i.e., each stem cent low density branch (x2 = 12.149, P <
mother is the largest possible size) (Whit- 0.001).
ham, 1979). Because the largest stem
mothers can completely exclude others Cumulative effects of induced plant defenses,
from their leaves and avoid both the neg- competition, and selective predator
ative effects of competition and the induced foraging on the evolution of
defenses of the plant, it would appear that territoriality
plant traits may have contributed to the
From the data presented in the above
evolution of energy allocation patterns of sections we can estimate the cumulative
the egg as well as the territorial behavior reproductive advantage a territorial aphid
of the first instar stem mother.
realizes over non-territorial or subdominant aphids (Table 1).
Selective foraging of predators and the
The negative effects of competitor denevolution of territoriality
sity alone give a territorial stem mother a
From the plant's perspective host het- 2.3-fold reproductive advantage over stem
erogeneity is directly responsible for P. betae mothers that share their leaves. When leaf
clumping on the best leaves and branches quality is held constant, increasing density
where they then suffer from the selective results in a decline of reproductive success
foraging of predators. From this point of from 100.7 progeny when one stem mother
view, plants may manipulate the foraging occupies a leaf to only 44.3 progeny per
behavior of aphid predators to reduce par- stem mother when four stem mothers share
the same leaf (Table 1).
asite loads.
The plant's induced defenses {i.e., preVertebrate predators such as the least
chipmunk, Eutamias minimus, black-capped mature leaf abscission) are at least as
chickadee, Parus atricapillus, and probably important as the negative effects of commany other species capable of slicing open petition as a contributing selective presthe galls of P. betae (see also Speich and sure in the evolution of territorial behavior
Radke [1975] for another example) selec- (Table 1). Although stem mothers that
tively foraged four times more intensively occupy leaves singly run a 10% risk of trigwhere gall densities were highest (Table gering this generalized plant defense, stem
2). For example, on branch #1 where the mothers that share leaves with three other
density of aphids was low (24 galls/1,000 stem mothers run a 53.7% risk. Thus, when
leaves) vertebrate predators destroyed the negative effects of competitor density
7.8% of the galls, whereas, on branch #2 are added to the increased probability of
364
THOMAS G. WHITHAM
death due to induced plant defenses, territorial individuals realize a 4.4-fold
increase in reproductive success (90.6
progeny with one stem mother per leaf versus 20.5 progeny per stem mother with 4
competitors per leaf).
The above estimates should be very conservative because they do not include the
fate of colonizers that are competitively
displaced from superior leaves and subsequently forced to settle on inferior leaves.
When survival rates were compared, 72%
of the "winners" survived to establish galls,
whereas only 24% of the "losers" survived
(Whitham, 1979).
Territorial stem mothers that prevent
others from settling on their leaves may
also reduce their risk of being preyed upon.
Table 2 showed that predators selectively
foraged on a high aphid density branch at
nearly twice the level as on an adjacent low
aphid density branch.
Rough approximations suggest that in
the absence of territorial behavior, predation would increase by about 52%. To
address the importance of territoriality in
reducing predation, one must first determine how much territoriality reduces the
aphid population of a branch. Using
removal experiments I showed that when
the residents were removed, floaters
quickly moved onto the vacated leaves
(Whitham, 1979). If the increased number
of colonizers on removal branches is indicative of population densities in the absence
of territorial interactions, then in the
absence of territoriality the density of colonizing stem mothers would have been 69%
higher. Thus on branch #2 in Table 2, gall
densities in the absence of territorial
behavior would have been an estimated
808 galls per 1,000 leaves rather than
the observed 478 galls per 1,000 leaves.
Assuming that the relationship between
predation and aphid density is linear in
Table 2, the predicted increase in aphid
density in the absence of territoriality would
have resulted in the selective predation by
vertebrates increasing from 28.2% to
43.0% at the higher aphid density (a 52%
increase).
Although it is difficult to combine the
impacts of induced plant defenses and com-
petition (which act within individual leaves)
with the selective foraging of predators
(which discriminate between branches but
not at lower levels), all act in concert to
favor territorial behavior.
GENERALITY OF BEHAVIORAL
COUNTER-ADAPTATIONS TO
PLANT DEFENSES
Greater understanding of the complex
interactions and feedbacks of different
trophic levels (Price et al, 1980; Boucher
et al, 1982; Thompson, 1982; Addicott,
1984; Jones, 1984) may reveal that plantinfluenced animal behaviors are common.
In this section, I briefly examine how
induced plant defenses and plant-mediated
predation and competition may have
affected territoriality and associated animal behaviors in other systems.
Territoriality and induced defenses
Defensive responses to fungi, insect and
mammal attack are thought to be widespread in diverse plant groups (McFarland
and Ryan, 1974; Kuc, 1976; Haukioja and
Niemela, 1979; Bryant, 1980, 1981; Carroll and Hoffman, 1980; Cruickshank,
1980; Faeth et al, 1981; Ryan, 1983).
Because induced plant defenses appear to
be widespread and affect all herbivore
groups, it seems likely that many behavioral counter-adaptations to these plant
defenses will have evolved.
If greater herbivore densities trigger
even greater defensive responses in their
host plants {i.e., defense is density dependent), then herbivores should avoid densities that would trigger these defenses. For
example, the probability of a stem mother
and her progeny being killed by induced
leaf abscission increased from 10.0 to
53.7% as the densities of stem mothers
increased from 1 to 4 per leaf (Table 1 and
Williams and Whitham, 1986). Similarly,
Haukioja (1980) argued that the defensive
responses of the birch, Betula pubescens, to
the feeding of the moth, Oporinia autumnata, were also density dependent. In systems where plant defenses are triggered by
higher herbivore densities, territorial and/
or associated behaviors that limit density
should be favored.
TERRITORIALITY IN RESPONSE TO PLANT DEFENSES
In a mammalian example, snowshoe hare
overgrazing on willow, birch and aspen
induces the production of new shoots that
contain much higher concentrations of resins and other secondary compounds on
which hares cannot survive. Thus the population cycle of snowshoe hares may be
caused by induced plant defenses that are
triggered by increased grazing pressures at
high population densities (Bryant, 1980,
1981; Bryant and Kuropat, 1980).
Edwards and Wratten (1983) argue that
induced defenses represent a powerful
selective pressure for the spacing of feeding. In support of their argument, they
observed over-dispersion of invertebrate
grazers on the leaves of many herbaceous
and deciduous woody plants. In systems
where territories become smaller with
increasing densities and/or collapse altogether, the subsequent concentration of
herbivores may trigger even greater
plant defenses. Consequently, the spacing
behaviors of many animals may have
evolved in part to limit animal densities
below levels that would trigger the induced
defenses of their food plants. For example,
Carroll and Hoffman (1980) showed that
leaves of squash, Cucurbita moschata, rapidly mobilized feeding deterrents within
20-40 min of being damaged. Associated
with these induced defenses, coccinellid
beetle larvae were never observed feeding
within 2 m of a fresh feeding scar.
In addition to spacing and territorial
behavior representing counter-adaptations to circumvent induced defenses, other
effective behavioral strategies have also
evolved. For example, Carroll and Hoffman (1980) showed that another beetle,
Epilachna tredecimnotata, cut the vascular
tissues of the leaves of squash, thereby preventing translocation of the feeding deterrents. Having aborted the induced defenses of the plant, afterwards the beetle may
feed at leisure. Thus, a suite of behavioral
strategies may be employed against the
defenses of plants (see Rhoades [19836] for
other examples).
The scale of the induced plant defense
relative to the mobility of the herbivore
may be important in the evolution of
appropriate counter-adaptations by ani-
365
mals. For example, induced defenses can
be restricted to the plant cells directly
affected (Seigler, 1977), as widespread as
the whole plant (Green and Ryan, 1972),
or may even spread to other non-attacked
plants (Baldwin and Schultz, 1983;
Rhoades, 1983a). The lower the ability of
the animal to escape the zone of induced
defenses {i.e., herbivores restricted to a single plant or plant part for the duration of
their life cycle), then the greater the need
to completely avoid triggering the plant's
defenses.
Since leaf abscission is commonly observed in diverse plant groups in response
to wounding (Addicott, 1982), sessile
species such as galling insects face this plant
defense. With such species territoriality
may be very important in preventing
clumping and subsequent leaf abscission.
It is interesting to note that the aphids
known to exhibit territorial behavior (Aoki,
1977, 1979; Whitham, 1979, 1986; Aoki
et al., 1981; Aoki and Makino, 1982) all
form galls even though gall formers represent only 9% of the aphid species (Whitham, 1978).
Predation and territoriality
Price et al. (1980) state that predators of
herbivores must be considered as part of a
plant's battery of defenses against its pests.
Predators often predictably forage where
herbivore densities are greatest (Hassell,
1966; Murdie and Hassell, 1973; Cheke,
1974; Tullock, 1971; Solomon and McNaughton, 1979). Consequently, any host
plant trait {e.g., temporal and spatial variability in resource quality) that tends to
concentrate herbivores in time and/or
space should facilitate predation. In
response to the selective foraging of predators where herbivores are most concentrated, herbivores that hyperdisperse or are
territorial could circumvent the plant's
predator defenses.
Tullock (1971) found that the coal tit
selectively foraged on pine trees where prey
densities were greatest. At the beginning
of the season, approximately seven-fold
differences in the densities of the eucosmid moth, Ernarmonia
conicolana, were
observed. At the end of the season, how-
366
THOMAS G. WHITHAM
ever, the selective foraging of these birds
on high prey density trees had so diminished the moth larvae that only two-fold
differences in densities were observed.
Although there may have been compensating factors for the moths, it would appear
that larvae that were dispersed before the
onset of predation lived to disproportionately contribute to the next generation.
The importance of territorial behavior
in limiting herbivore densities should also
increase as the variation in prey densities
increases. For example, Whitham (1983)
observed 42-fold differences in prey densities between adjacent branches of the
same tree. The higher the differences in
prey densities, the easier it becomes for
predators to discriminate between patches
and selectively forage where the return is
greatest. This may be particularly important for some predators that can only profitably forage where prey are very concentrated. When prey are dispersed the food
item may not be included in the diet and
the plant loses a beneficial predator.
Schultz (1983a, b) argued that host heterogeneity increased herbivore exposure
to predators because herbivores were then
forced to continually move about the plant
to find suitable feeding sites. Induced plant
defenses would have the same effect in
which after feeding, a herbivore would be
forced to move on to avoid the defenses
that had just been triggered.
H O S T PLANT DEFENSES AND THE
EVOLUTION OF CANNIBALISM
White (1978) suggested that plants of
poor nutritional quality may have evolved
in response to the selective foraging of herbivores in which resistant or poor quality
plants realized an ecological or evolutionary advantage. It is generally recognized
that plants constitute low quality resources
because they are low in important nutrients,
such as nitrogen, essential to animal development and reproduction (White, 1978;
Mattson, 1980; Scriber and Slansky, 1981).
Mattson (1980) suggested that these nutritional constraints have selected for a wide
array of animal solutions to the shortage
of nitrogen.
Plant adaptations which reduce nutri-
tional quality may have contributed to the
evolution of cannibalistic behavior of herbivores (Mattson, 1980). Cannibalism and
territoriality are closely associated. Both
limit density, involve aggression and result
in a greater accumulation of food resources
for dominant individuals. Several authors
have noted that cannibalism may be widespread among herbivores. Fox (1975, p.
88) notes that "surprisingly, a large proportion of observations of cannibalism
among terrestrial animals is for species that
are usually 'herbivores'. . . ." In her review
of the literature, cannibalism was found to
be common and fully half of the known
examples of cannibalism were terrestrial
herbivores. Additionally, Kirkpatrick
(1957, p. 194) noted that although cannibalism is rare among terrestrial predatory
insects, ". . . some plant-feeding insects are
inveterate cannibals, even in the pesence
of an abundance of food."
With herbivores killing other herbivores
the question must be asked, Who really
benefits from cannibalism? Clearly the cannibal that obtains a high quality meal benefits relative to the unfortunate individual
that became the meal, and to other herbivores that were forced to rely solely upon
poor quality plant resources. In addition
to the successful cannibal benefiting from
the behavior, the plant has also benefited,
perhaps even more so. Of direct importance to the plant, a successful cannibal
reduces the herbivore population. For
example, Barber (1936) reported that the
corn earworm, Heliothis tea, is cannibalistic
and only one larva per ear survives even
though resources are sufficient to support
several. Stinner etal. (1977) states that cannibal-caused mortality commonly exceeds
75%, making it the major source of corn
earworm mortality. In such instances, the
host plant may be the biggest winner.
Plants may benefit most from the cannibalism that occurs early in the life cycle
of a herbivore. For example, the first larvae of Monarch and Queen Butterfly to
hatch often cannibalize nearby eggs, even
when population densities are low (Brower,
1961). Such egg cannibalism is common
(Fox, 1975) and causes the density of herbivores to be reduced before any damage
TERRITORIALITY IN RESPONSE TO PLANT DEFENSES
has been inflicted upon the host plant. Fox
also points out that even though a small
portion of the total diet may be derived
from cannibalism (in large part because
eggs are small and thus a small portion of
the total diet), the net impact on mortality
and population age structure can be highly
significant.
Since temporal and spatial variability in
plant defenses concentrate herbivores and
intensify negative behavioral interactions
such as cannibalism, through evolutionary
time those plants that increase the likelihood that herbivores will destroy themselves should realize a selective advantage.
In her review, Fox (1975) notes that cannibalism is often intensified by crowding
and poor nutrition. The commonly observed plant trait of high variation in suitability within individual plants, both temporal and spatial (Whitham et al., 1984),
tends to concentrate pests where they are
subsequently more likely to exhibit cannibalistic behavior. For example, Southwood (1978) found that temporal variation
in broom, Sarothamnus scoparius, concentrated four species of mirid (insect) herbivores in which the larger larvae preyed
upon the smaller ones.
CONCLUSIONS
Plants may play an active role in the evolution of aggressive animal behaviors. In
mutualistic relationships (e.g., ant defense
of plant tissues) territoriality is a positive
response to plant rewards and both parties
benefit. In antagonistic relationships with
plant pests, however, aggressive behaviors
by herbivores may evolve as a negative
response or counter-adaptation against the
defenses of the host plant.
Territoriality, spacing behavior and cannibalism may represent counter-adaptations by pests to limit density and subsequently avoid induced and other plant
defenses. Because predation and competition can negatively affect herbivores, these
plant influenced factors should be considered plant defenses against herbivory.
Although aggressive behavior clearly benefits dominant individuals by enabling them
to sequester superior resources and avoid
plant defenses, they may ultimately reduce
367
pest populations and benefit the host plant
(e.g., cannibalism).
Because plant derived selective pressures
favoring territorial behavior are high (e.g.,
at least a 4.4-fold advantage with P. betae
gall aphids), the potential is great for plants
to manipulate aggressive animal behaviors
for their own benefit. The viewpoint
expressed throughout this paper requires
that plants be more dynamic than generally
supposed. New approaches in plant ecology should permit the validity of this viewpoint to be critically ascertained.
ACKNOWLEDGMENTS
I thank P. R. Atsatt, F. L. Carpenter, D.
D. Hart, N. Moran, J. N. Thompson and
K. Whitham for their constructive comments on the manuscript. I gratefully
acknowledge the support of N.S.F.
BSR8303051 and U.S.D.A. 84-CRCR-l1443.
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