Download Enemy-free space via host plant chemistry and dispersion

Oecologia (2001) 128:153–163
DOI 10.1007/s004420100679
N. Stamp
Enemy-free space via host plant chemistry and dispersion:
assessing the influence of tri-trophic interactions
Received: 24 May 2000 / Accepted: 6 February 2001 / Published online: 24 March 2001
© Springer-Verlag 2001
Abstract It has been argued that generalist natural
enemies of insect herbivores provide a major selection
pressure for restricted host plant range. This idea is a
subset of the enemy-free space (EFS) hypothesis, whereby insect herbivores escape their enemies by being
scarce in space and time and/or chemically defended via
containing plant allelochemicals. To date, there are only
two complete tests of EFS via host plant chemistry and
two via host plant dispersion, and only two of these tests
support the EFS hypothesis. However, three corollaries
to existing views on EFS are sufficiently supported by
data to warrant direct testing of the view that EFS is obtained via host plant chemistry's effects on enemies of
insect herbivores. So the issue remains. Resolution will
require a more collaborative, methodological approach to
examine the relative importance of the major multiple
factors that shape patterns of feeding specialization of
insect herbivores. Predation is certainly one of these
factors, but its role is still not clear.
Keywords Predator–prey interaction · Specialist insect
herbivores · Host plant range · Generalist predators ·
Parasitoids
Introduction
A primary focus in ecology and evolution has been to
develop an understanding of the rich diversity of species,
and one of the most species-rich groups is insect herbivores. One characteristic of this group is that most insect
herbivores are specialized feeders; 70% of insect herbivores restrict their feeding to one plant family (Bernays
and Chapman 1994), and 90% are restricted to three or
fewer families (Bernays and Graham 1988). One factor
contributing to the diversity of insect herbivores is
host plant defensive chemistry. Ehrlich and Raven (1964)
N. Stamp (✉)
Department of Biological Sciences, Binghamton University,
State University of New York, Binghamton, NY 13902-6000, USA
e-mail: [email protected]
noted the pattern of related butterfly species using plants
that were chemically related or taxonomically (and thus
presumably chemically) related, which led to the idea of
coevolution occurring between host plants and their specialist insect herbivores. A number of studies provide
evidence for such coevolution (Farrell et al. 1992; Farrell
and Mitter 1994; Becerra 1997). But other factors besides the effect of host plant defensive chemistry on herbivores may also serve as selection pressures for feeding
specialization by insect herbivores. It is not clear which
factors are most important and when.
In a past review of plant-herbivore interactions,
Bernays and Graham (1988) stated, “We argue that generalist natural enemies of herbivorous insects provide a
major selection pressure for restricted host plant range.
The significance of plant chemistry is...in terms of regulating behavior, while the chemical coevolutionary theories are...of limited value.” They further state, “...chemical coevolution between plants and herbivores has been
overemphasized, and that generalist natural enemies, especially predators of the herbivores, may be the dominant factor in the evolution of narrow host [plant] range.”
Finally, they make the statement, “Plant chemistry is but
one of many potential pressures and probably not the
predominant one, in spite of its recent popularity and
clear importance in behavior.”
A primary point of the Bernays and Graham review
was that host plant specialization by herbivores may reduce predation because the herbivores are then scarce in
space and time and/or chemically defended to some degree via plant allelochemicals. Their discussion focuses
on the effect of plant allelochemicals on herbivores and
their enemies and so much of the discussion in this paper
will do the same. Most herbivorous insects contain, at
the least, sublethal dosages of allelochemicals to an insect predator. The protective chemicals occur in the form
of plant matter in the herbivore’s gut and/or allelochemicals sequestered across the gut lining. Allelochemicals
may occur in the herbivore's tissues even when a
specialist herbivore feeds on novel host plant species
(Strohmeyer et al. 1998), and insect herbivores, especial-
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ly specialist feeders, may bioaccumulate plant allelochemicals in their tissue (Bowers 1992; Bowers and
Stamp 1997). Insect herbivores are likely to be rejected
by predators when they eat plants that yield extracts that
deter predators (Dyer 1995). Thus, this idea that predators are an important selective pressure for host plant
specialization by insect herbivores is appealing. Although host plant chemistry per se is clearly very important in shaping feeding specialization by insect herbivores, it seems likely that there is also a “top-down”
effect through predators being affected by, and so avoiding, plant allelochemicals contained in their prey.
In the same journal containing the Bernays and
Graham (1988) article, several people argued that the
patterns of feeding specialization generated by invertebrate herbivores were complicated by factors other than
host plant chemistry and predators, and that the interaction of the entire set of factors was important (Barbosa
1988; Courtney 1988; Ehrlich and Murphy 1988; Fox
1988; Janzen 1988; Jermy 1988; Rausher 1988; Schultz
1988; Thompson 1988). They agreed that the effect of
the third trophic level needed more attention, but they
felt that the third trophic level was unlikely to be the
dominant force proposed by Bernays and Graham.
Since then, there has been some attention on the effect of plant chemistry on predators, with a focus on the
assessment of three corollaries. If generalist predators,
via avoiding exposure to noxious plant chemicals, act as
a selective force that narrows host plant range of invertebrate herbivores, we might expect that generalist predators: (1) can learn to avoid prey containing detrimental
plant chemicals, (2) avoid specialist herbivores and more
readily attack generalist herbivores, and (3) suffer a reduction in fitness when they have a diet of prey containing detrimental plant chemicals. Evidence for these ideas
would provide circumstantial support for the Bernays
and Graham (1988) view that predation is an important
selective force for feeding specialization by insect herbivores. In this review, I focus on some of the evidence for
these corollaries.
Effect of allelochemical-containing prey
on natural enemies
Most invertebrate predators come into contact with at
least some plant allelochemicals in their herbivorous
prey, via the prey's gut, and/or sequestered in prey tissue.
For instance, predatory wasps tear prey apart and ball up
pieces of tissue that are used to provision larvae at the
nest; in this process, their faces and mouths get covered
with the prey’s body fluid. Often wasps spend much time
wiping and grooming their heads, antennae and legs after
tearing apart caterpillars containing plant allelochemicals, and sometimes the wasps reject the prey in the
process (Stamp 1992). Extra-oral feeders, such as spiders
and predatory hemipterans, inject enzymes into prey and
then suck up the partially digested fluid (Cohen 1995),
which may contain allelochemicals from prey tissue and
gut. In contrast to insectivorous birds, invertebrate predators usually capture prey about their own size and,
thus, are likely to acquire a relatively high dosage of allelochemicals.
Often, invertebrate predators are deterred by plant allelochemicals contained in their prey. Predatory wasps
preferred palatable to unpalatable prey (Rayor et al., in
press). Invertebrate predators attacked specialist herbivores less frequently than generalist feeders (Bernays
1988; Bernays and Cornelius 1989; Dyer 1995). Dyer
(1995) showed that the lower frequency of attack on
specialist herbivores was positively correlated with prey
defensive chemistry and plant defensive chemistry.
Invertebrate predators can learn to avoid prey that
contain allelochemicals (Gelperin 1968; Berenbaum and
Miliczky 1984; Brown 1984; Vasconellos-Neto and
Lewinsohn 1984; Malcolm 1986; Paradise and Stamp
1990, 1993; Traugott and Stamp 1996b; Rayor et al., in
press). For example, initially predatory wasps frequently
attacked Junonia coenia caterpillars; however, after a
few days, the wasps began rejecting this prey species
(Stamp 1992), which sequesters relatively high levels of
allelochemicals (iridoid glycosides) from its host plants
(Bowers and Collinge 1992). Experienced wasps can distinguish between palatable and unpalatable prey without
having to kill them first (Bernays 1988). These results
suggest that such predators could act as selective agents
for increased host plant specialization by insect herbivores. The negative responses by predators to specialist
herbivores also suggest that ingesting such prey is detrimental to predators.
Some results indicate that allelochemical-fed prey can
have a negative effect on predator development, growth
rate and fecundity (reviewed in Rowell-Rahier and
Pasteels 1992) and, thus, can contribute to an antagonistic relationship between some plants and invertebrate
predators. For example, predatory stinkbugs given caterpillars reared on some of the allelochemicals found in
tomato leaves took longer to develop and were smaller in
size (Stamp et al. 1991; Traugott and Stamp 1996a). Prey
fed milkweed seeds (containing cardenolides) reduced
the consumption and growth rate of praying mantids
(Paradise and Stamp 1993). When predatory wasps were
given unpalatable prey, fewer offspring were produced,
the offspring were smaller and the percent of male offspring was reduced, compared to that of wasps given
palatable prey (Stamp, in press). Clearly, unpalatable
prey can have negative effects on the fitness correlates of
invertebrate predators.
However, other studies show that under some conditions allelochemical-fed prey can have little or no effect
on some invertebrate predators (Malcolm 1992; Osier
et al. 1996; Stamp et al. 1996). Whether allelochemicalfed prey have a negative impact on invertebrate predators or not depends on various factors. For example,
some invertebrate predators can detoxify toxic chemicals
to some degree (Yu 1987). Consequently, some predators
may not be susceptible to plant chemical defenses ingested via prey, whereas others are (Malcolm 1992). The
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concentration of an allelochemical is also a factor. For
instance, with increasing concentration of allelochemicals in the diet of prey, the negative impact on invertebrate predators increased substantially (Stamp et al.
1991; Traugott and Stamp 1996a). Different prey species
affect the growth of predators differently (Landis 1937;
Drummond et al. 1984). For example, with prey fed
the same host plant species, predatory stinkbugs had a
higher growth rate when fed a prey species that does
not bioaccumulate iridoid glycosides (Vanessa cardui
caterpillars) versus a prey species that does (J. coenia)
(Strohmeyer et al. 1998). The effect of allelochemicals
on insects has been shown to change with age of the
insect (Schowater et al. 1977; Larsson and Tenow 1979;
Scriber and Slansky 1981; Stamp et al. 1996). The poor
growth of invertebrate enemies given prey raised on
plant allelochemicals may reflect the poor nutritional
state of the prey on an allelochemical diet and/or the
direct effects of the allelochemicals on the invertebrate
enemies (El-Heneidy et al. 1988).
Therefore, a consequence of the effects of plant
allelochemicals via prey is that invertebrate predators
can be classified as “included”, “peripheral”, or “excluded” (Malcolm 1992). “Excluded” predators are unable to
survive on prey, due to host plant chemistry encountered
via prey. “Included” predators successfully exploit prey
without detrimental effects from host plant chemistry. In
contrast, “peripheral” predators experience reduced
survivorship, smaller size and/or delayed development,
due to host plant chemistry encountered via prey and/or
the effect of host plant chemistry on the nutrition of the
prey. Most generalist predators are probably “peripheral”
in most situations. Consequently, variation in the effectiveness of peripheral predators in handling host plant
chemistry encountered via prey is likely to be the key to
understanding the ecology and evolution of interactions
between herbivorous prey and their invertebrate predators (Malcolm 1992).
What might cause variation in response to host plant
chemistry in prey by “peripheral” predators, or what
might shift an “included” predator to the category of
“peripheral”, or even to “excluded”? The two major
factors besides prey quality that have a large impact
on invertebrate predators are temperature and prey
abundance.
The effect of plant allelochemicals in the diet of prey
on the growth of invertebrate predators is a function of
temperature. For example, at a cool thermal regime
(18°C), predatory stinkbugs were not affected by increasing concentrations of rutin (a common allelochemical in plants) in the diet of their prey, but at a warm
thermal regime (28°C), they were negatively affected by
increasing concentrations of rutin (Stamp et al. 1991). In
this case, the predator would fall in the category of “included” at the cool thermal regime but in the category of
“peripheral” at the warm thermal regime. When the effect of temperature and plant allelochemicals on insects
has been examined simultaneously, often there was an
interactive effect between the two factors, and when this
occurred usually there was an increasingly negative
effect of allelochemicals at the warmer thermal regime
(Stamp and Osier 1998).
The other major factor besides prey quality and temperature that has a large impact on invertebrate predators
is prey abundance. The array of prey species in the environment affects where invertebrate predators forage.
Insect predators can exhibit a functional response to
high densities of prey (Morris 1963; Tostowaryk 1971;
Nakasuji et al. 1976). Consequently, predators may
switch from one area to another in response to prey density, or from one prey type to another (Rabb and Lawson
1957), although they may switch to new prey slowly
(Rabb and Lawson 1957; Yamasaki et al. 1978). However, frequently, invertebrate predators experience times
when prey in general are scarce or, if plentiful, most prey
are too large to be captured (Anderson 1974; Wise 1975;
Evans 1982a, b, 1983; Hurd and Eisenberg 1984; Lenski
1984; Hurd and Rathet 1986; Wiedenmann and O’Neil
1990, 1991; Legaspi and O'Neil 1994). Prey scarcity can
result in prolonged developmental time of immature predators (Legaspi and O’Neil 1994) and delayed reproduction of females (Wiedenmann and O’Neil 1990). Developmental time of immature predators may be longer
when they come from poorly fed females (Legaspi and
O’Neil 1994). When generalist insect predators experience periods of prey scarcity and when available prey
contain allelochemicals, predators might be forced to include prey containing sublethal levels of allelochemicals
in their diet. The effect of allelochemical-containing prey
on insect predators may be greater when prey are scarce.
For example, allelochemical-fed prey had no adverse effect on growth of an insect predator when prey were
plentiful, whereas when prey were scarce, allelochemical-fed prey increased the negative effects of prey scarcity on predator growth (Bozer et al. 1996; Weiser and
Stamp 1998). The ability to handle plant chemical defenses may reflect the availability of nutrients (Duffey
1980; Slansky and Wheeler 1992). With prey scarcity,
nutrients that may facilitate dealing with plant defenses
may be limiting. Such an effect of prey scarcity may be
fairly common among invertebrate predators primarily
feeding on insect herbivores.
In sum, data on invertebrate predators support the
three corollaries, which suggests that invertebrate predators may provide a strong selective pressure for feeding
specialization by insect herbivores. But the data also indicate that invertebrate predators should not be thought
of as static entities, i.e., a particular predator species may
exert selective pressure under some conditions but not
under others.
Evidence for the corollaries also occurs in studies
about the response of birds and parasitoids to plant
allelochemicals. It is clear that birds have served as a
selection pressure on herbivorous insects (Heinrich 1979,
1993; Heinrich and Collins 1983), that some bird species
have more physiological susceptibility to particular
allelochemicals than others (Fink and Brower 1981;
Brower 1984), and that plant allelochemicals can
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adversely affect weight gain and feather development
of nestlings (L. Pezzolesi and A. Clark, SUNY-Binghamton, unpublished data). Although many parasitoids may
feed on and within tissue likely to be free of allelochemicals (reviewed by Gauld et al. 1992), many others are
likely to be exposed to plant allelochemicals contained
within their hosts. Even when the concentrations in host
tissue are relatively low, plant allelochemicals can have
detrimental effects on fitness correlates of endoparasitic
koinobionts, parasitoids that are fairly specialized in
the use of habitat and host (Thurston and Fox 1972;
Campbell and Duffey 1979; Barbosa et al. 1986, 1991;
El-Heneidy et al. 1988). So parasitoids may provide
a selection pressure on herbivores that reflects the
parasitoids’ response to plant allelochemicals.
Ascertaining enemy-free space
Overall, these results infer that generalist predators or
parasitoids could provide selection pressure for a restricted host plant range for insect herbivores. They also
suggest that specialist parasitoids could provide selection pressure for a broader host plant range for insect
herbivores. So the issue of the role of predators and
parasitoids in shaping the pattern of feeding specialization by invertebrate herbivores remains equivocal.
The idea that insect herbivores may escape generalist enemies by narrowing host plant range and specialist
enemies by broadening host plant range is a subset of
the enemy-free space hypothesis. The definition of enemy-free space is “ways of living that reduce or eliminate a species' vulnerability to one or more species of
natural enemies” (Jeffries and Lawton 1984). Some of
the “habits” that can generate enemy-free space (EFS)
are adaptations in morphology and size, position, interspecific interaction, visibility, and chemistry (Berdegue
et al. 1996). So host plant chemistry and host plant rarity, via their effects on enemies, are just two of several
potential habits that could confer EFS to invertebrate
herbivores.
To examine the idea of EFS via host plant chemistry’s
effect on natural enemies, a good place to start is with
the general EFS criteria established by Berdegue et al.
(1996). They proposed three working hypotheses that
must be tested and accepted to conclude that EFS exists
and the enemies have had a significant role in shaping
the EFS. Firstly, their hypothesis (H1A1) is that the fitness of the prey in the presence of enemies is less than
that in the absence of enemies. Such a finding establishes
the importance of the enemies on the prey’s fitness. Secondly, their hypothesis (H2A1) is that the fitness of the
prey in the alternative (potential EFS) habit with enemies
is greater than that in the original habit with enemies.
Such a finding establishes that the alternative habit provides enemy-free space. But it does not indicate the role
of predation in shaping enemy-free space. Thirdly, their
hypothesis (H3A1) is that the fitness of the prey in an
alternative habit without enemies is less than in the origi-
nal habit without enemies. Such a finding establishes
that there is a cost to this EFS when predators are absent
and, consequently, we can be sure that predation is the
major factor generating this EFS habit. This shows the
relative importance of predation compared with other
unidentified factors, such as resource limitations (e.g.,
via food quality and competition), that can shape a pattern of feeding specialization by an insect herbivore.
Hypotheses 1 and 2 support the idea that enemies are
a factor in shaping the feeding niche of an insect herbivore. But all three of these one-tailed, alternative hypotheses must be supported to conclude that predation is a
dominant force in generating enemy-free space for the
species under consideration (Berdegue et al. 1996). With
these criteria in mind, we can examine the studies on invertebrate herbivores in which all three hypotheses have
been tested, or for which there are data to examine the
hypotheses.
Berdegue et al. (1996) reviewed the literature for nonagricultural terrestrial and freshwater arthropod systems
to evaluate the state of the EFS hypothesis, and found 41
studies that examined the idea. Of those, 17, or 41%,
were on terrestrial systems. Using Berdegue et al.’s criteria, only one that had host plant chemistry as the mechanism for EFS was a complete test, and it did not meet all
three of Berdegue et al.’s criteria for supporting the EFS
argument. A search of the literature for more recent
studies revealed only one in which host plant chemistry
affecting the natural enemies of herbivores was the likely
mechanism. Using Berdegue et al.’s criteria, that study
did support the EFS argument. It is worth reviewing
these two studies to ascertain why there are so few tests
of EFS via host plant chemistry influencing natural enemies.
EFS via host plant chemistry test no. 1:
willows, herbivorous beetles and carnivorous beetles
The first study was conducted by Denno et al. (1990).
Their system was two leaf beetle species that specialized
on willows. One of these beetle species (Phratora
vitellinae) defended itself with secretions made from
host plant allelochemicals (salicylates and other phenolic
glycosides). The other (Galerucella lineola) lacked this
ability. Performance on three species of willow was
evaluated. Two willow species were rich in salicylates
(Salix fragilis and S. dasyclados) and one was poor
(S. viminalis). The chemical-secreting beetle specializes
in salicylate-rich willows, and so may obtain EFS by a
narrower host plant range than the non-secreting beetle
that uses a wider range of willows (Fig. 1A). The predators were coccinellid beetles (Adalia bipunctata).
Hypothesis 1
The insect predators caused a high level of mortality.
This result fits the EFS criteria of Berdegue et al. (1996).
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Fig. 1A, B A specialist insect herbivore (Phratora vitellinae) prefers a willow species (Salix fragilis) that has high concentrations
of salicylates, which it sequesters. A Relative to generalist predators, the potential EFS via host plant chemistry for P. vitellinae is
the salicylate-rich willow species. B In the absence of predators,
P. vitellinae’s performance on S. fragilis is similar to that on
S. viminalis, which does not meet the EFS criteria. Data for the
herbivore (Galerucella lineola), which does not sequester salicylates, are shown also. Modified from Denno et al. (1990)
Hypothesis 2
The fitness (i.e., survival) of the “specialist” herbivores
(P. vitellina) on a salicylate-rich or proposed EFS host
plant (S. fragilis) with the predators was greater than
their fitness on a salicylate-poor host plant (S. viminalis)
with the predators. This result fits the EFS criteria.
Hypothesis 3
The fitness (i.e., survival) of the “specialist” herbivores
(P. vitellina) on a salicylate-poor host plant without the
predators was less than their fitness on a salicylate-rich,
or proposed EFS, host plant without the predators
(Fig. 1B). This result does not fit the EFS criteria.
There are two explanations for this last result. First, it
may be that some other factor, by itself or in conjunction
with predation, plays a role in the use of the salicylaterich host plant by P. vitellina beetles. For example, nutritional quality of the host plants may be different and influence the herbivores (Denno et al. 1990; Berdegue et al.
1996). Therefore, other potential factors would need to be
evaluated. Niches of insect herbivores are shaped by a
variety of factors, including host plant defensive chemistry, host plant nutritional quality, host plant abundance,
competition, pathogens, predators, and parasitoids.
The second explanation illustrates a fundamental problem with examining EFS related to plant chemistry. From
an evolutionary perspective, it is difficult to evaluate where
EFS has played a role. The hypothesis that there should be
a cost in terms of fitness to the herbivore for use of a salicylate-rich host plant when enemies are absent, is logical,
but it ignores the possibility of selection against the cost,
which over time could reduce the cost to the point of making it undetectable. Just as there are mechanisms that may
reduce the cost of defense to host plants in their interaction
with herbivores (Simms 1992; Gershenzon 1994), we
should expect in insect herbivores selection against the cost
of utilization of host plants. Therefore, predation may be
an important factor, and perhaps even the most important
factor, in shaping an EFS habit, even though data used to
test Berdegue et al.’s hypothesis 3 may not support the EFS
criteria. So due to evolutionary issues, a “clean” test (i.e.,
as described by Berdegue et al. 1996) may be quite difficult to obtain. But we can examine how EFS might come
about; that is, we can investigate the potential mechanisms.
EFS via host plant chemistry test no. 2:
plant family Asteraceae, a leafminer and parasitoids
The second study was conducted by Gratton and Welter
(1999), and it illustrates the point about investigating
potential mechanisms. Their system was leafminer larvae
of a fly that specializes on the sunflower Helianthus
annuus. The novel host plants were also in the family Asteraceae: H. maximilianii, Ambrosia artemisiifolia, Taraxa-
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Fig. 2A, B A specialist insect
herbivore (L. helianthi) oviposits on one species (Helianthus annuus) in the Asteraceae.
A Relative to generalist
parasitoids, the potential EFS
via host plant chemistry is that
plant species (H. annuus).
Relative to specialist parasitoids, the potential EFS via host
plant chemistry is other species
of Asteraceae, i.e., novel host
plant species that the herbivore
can use. B Response by three
categories of parasitoids.
Endoparasitoids dominated in
1994 and 1996 but less so in
1995 (H Helianthus annuus,
C Centaurea solstitialis,
A Ambrosia artemisiifolia,
M Helianthus maximilianii,
T Taraxacum officinale). Modified from Gratton and Welter
(1999)
cum officinale, and Centaurea solstitialis. The larvae were
manually transferred to novel host plants by inserting the
larvae into pinholes in the leaf epidermis. The plants were
exposed to enemies under field conditions. By using leafminers, the set of enemies was limited to parasitoids.
The working hypothesis was that specialist parasitoids act as selective agents for host plant shifts that result
in an increase in diet breadth of the host insects (Lawton
1986; Bernays and Graham 1988; Weseloh 1993;
Fig. 2A). Since most parasitoids are more specialized
than insect predators in habitat and/or host use, their host
insects, at least the exposed feeders, are more likely to
escape their parasitoids by broadening their range of
host plant use than by narrowing it.
Hypothesis 1
There was not a direct test, but observational data indicate enemies caused significant mortality. This result fits
the EFS criteria of Berdegue et al. (1996).
Hypothesis 2
When endoparasitoids, which are more specialized by
habit, dominated the parasitoid assemblage, parasitoidcaused mortality of the leafminers in the novel, or proposed EFS, plants averaged 17% less than in the normal
host. This result fits the EFS criteria. Presumably host
plant chemistry contributed to this result. For example,
perhaps the novel host plants provided fewer recognizable volatile cues for the specialist parasitoids.
Hypothesis 3
Feeding trials indicated that larval survivorship was
greater on the original host plant; i.e., the original host
plant provided better food, and so there was a cost of the
shift to novel host plants. This result fits the EFS criteria.
However, in 1 of the 3 years, generalist ectoparasitoids dominated the parasitoid assemblage, and then mortality among the original and novel host plants was simi-
159
lar (Fig. 2B; 1995). This result does not support the EFS
view of the effect of generalist enemies. The EFS view is
that generalist enemies select for a narrowing of host
plant range (Bernays and Graham 1988). So we would
expect that mortality caused by generalist parasitoids
would be less on the original host plant, presumably the
evolved EFS for these specialist leafminers, relative to
generalist enemies (Fig. 2A). Perhaps that result would
have occurred if the miners were only exposed to the
generalist ectoparasitoids rather than to a parasitoid assemblage made up of both endoparasitoids and ectoparasitoids. So another important message from this study
is that as environmental conditions changed, the advantage to the herbivores of a host plant shifted or, in this
case, increasing diet breadth, changed.
But where does this study leave us in terms of understanding the role of host plant chemistry in influencing
the herbivore’s parasitoids? The underlying feature of
the parasitoid-leafminer interaction is the response by
the parasitoids to the host plant. However, we do not
know whether the specialist parasitoids had greater difficulty finding the novel host plants and/or were repelled
by the novel host plants. Furthermore, tests were not
conducted to ascertain the effect of host plant chemistry
on survivorship of the parasitoids (because the leafminers were dissected to determine parasitism). So the study
suggests how host plant chemistry may play a role, but it
does not actually examine that issue.
(Sato and Ohsaki 1987). The third pierid (P. melete) encapsulated the parasitoid eggs, so it has a physiological
defense whereby it kills the parasites.
P. rapae: hypothesis 1
Parasitoids caused a high level of mortality, as required
by the EFS criteria of Berdegue et al. (1996).
Hypothesis 2
P. rapae was successful in new sites until parasitoid
numbers increased, as required by the EFS criteria.
Hypothesis 3
P. rapae was successful in new sites without parasitoids,
which does not support the EFS criteria. The spatial-temporal availability of the host plants, rather than parasitoids, contributes to the herbivores moving to new sites.
P. napi: hypothesis 1
Mortality due to parasitoids was high in one of the areas.
Data were not gathered to test EFS but seem to support
the EFS criteria.
EFS via host plant dispersion test no. 1
The other way that use of host plant species by herbivores may convey EFS is through herbivore specialization (narrowing of host plant range), resulting in greater
spatial dispersion of the herbivores, and so the herbivores are less likely to be found by enemies. There are
only two complete tests of EFS for insect herbivores via
spatial-temporal patterns. The study by Ohsaki and Sato
(1990) provides an example of EFS in an agricultural situation. In Japan, cultivated and wild crucifers are used
by three species of pierid butterfly larvae. A braconid
parasitoid, Apanteles glomeratus, causes considerable
mortality of Pieris rapae. The other two pierid species,
Pieris melete and Pieris napi, are infrequently parasitized. The question was: what accounted for this difference? More specifically, what EFS mechanisms might be
involved here? The pierid (P. rapae) that was heavily
utilized by the parasitoid appeared to escape parasitism
by continually colonizing newly available sites before
the parasitoid did. In the study area, the second pierid
(P. napi) was a specialist on rock cresses, even though
the plants were poor quality for larval growth. The rock
cresses in the study area grew under other weeds and,
consequently, the P. napi larvae were less apparent to the
parasitoids. So the EFS mechanism was low host plant
apparency. In another area of Japan, P. napi uses a different host plant species, one which is more apparent, and
correspondingly, it suffers a high parasitism rate there
Hypothesis 2
Pieris napi was more successful in the other site. Data
were not gathered to test EFS but seem to support the
EFS criteria.
Hypothesis 3
P. napi had poor larval growth on rock cresses in the area
where the host plants were unapparent. That is, there was
a cost to EFS. This fits the EFS criteria.
The current status of EFS
Overall, there are only two “complete” tests of EFS, via
plant chemistry affecting natural enemies, and only two
“complete” tests of EFS, via spatial-temporal patterns
affecting natural enemies. Why are there so few studies
of the EFS phenomena, via host plant chemistry and dispersion?
Firstly, perhaps the EFS hypothesis has been already
accepted or rejected by the scientific community. Consequently, perhaps it is not perceived as an interesting idea
to test, or as an idea that is fundable. The Berdegue et al.
(1996) review clearly makes the point that there are few
160
“complete” tests of the EFS hypothesis, and a close look
reveals the paucity of “complete” tests examining the
idea that EFS for insect herbivores can be created by increasing or decreasing host plant range. This would suggest that it is premature to accept or reject the hypothesis, at least as it applies to plant-insect herbivore interactions.
Secondly, perhaps the problem is that any test will
have to be system specific. So the question then is: how
many tests do we need to make a generalization about
the EFS hypothesis? It took hundreds of studies (as of
1983, over 500; Connell 1983) on the role of competition
in structuring communities and a lot of debate to arrive
at a generalization (e.g., Schoener 1982; Simberloff
1984). Furthermore, usually when we test hypotheses in
ecology and evolution, we choose systems to maximize
the likelihood of rejecting the null hypotheses and accepting the alternative (our “working”) hypotheses. This
is the “if it occurs, it will occur here” approach. But that
will not give us an accurate picture of how important
EFS is or when it is important. The key for EFS research
on plant-insect systems would be a very methodical and
coordinated approach by a group of researchers to ensure
that an appropriate range of systems was investigated
and comparable approaches taken. By doing that, it
might take only five studies to ascertain the basic pattern. Although this strategy is seldom utilized in ecological studies, it can be a very powerful one.
Thirdly, perhaps the problem is that multiple causes
are at work in shaping niches. Therefore, often univariate tests about the role of EFS, competition, etc. do not
provide satisfactory explanations. For example, the parasitoid patterns found for tropical versus extra-tropical
regions (Gauld and Gaston 1994) suggest that the direct
effects of host plant chemistry and dispersion on insect
herbivores are probably more important than parasitoid
pressure in shaping feeding specialization by insect
herbivores in the tropics. Therefore, multiple factors
should be examined to assess the relative effects. The
relative effects of multiple factors can be assessed with
path analysis (Ullman 1996). For instance, levels of a
resource, such as light, can be manipulated, which will
alter the carbon:nutrient balance in plants and so alter the
concentrations of allelochemicals (Bryant et al. 1983).
The effect of different concentrations of allelochemicals
on insect herbivores can be measured in the presence and
absence of predators (Fig. 3). The effect on predators can
also be measured.
Fourthly, perhaps the problem is that predators and
parasitoids are not static entities. The effect of host plant
chemistry on natural enemies varies with other conditions with which the natural enemies must contend, such
as temperature and prey abundance. So the presence of
natural enemies, or susceptibility of herbivores to natural
enemies, does not indicate constant selective pressure.
One way to deal with this is to conduct experiments long
enough to see how the pattern of interaction changes
with different environmental conditions (e.g., tests over
multiple years, as in Gratton and Welter 1999). Also, one
Fig. 3 Example of a design for a path analysis of multiple factors
in a system of plants used by insect herbivores attacked by insect
predators. For a path analysis to ascertain the relative effects of
various factors on response by, and performance of the herbivores,
different levels of a factor can be tested. The factors of interest
are: resources for plants, plant availability, and presence of predators. In the category of resources for plants, light and soil nutrients
are two important resources that will affect: (1) concentration of
plant nutrients, (2) allocation to mass and reproduction, and (3)
defenses. An experiment could manipulate a resource for plants;
e.g., soil nitrate could be set at low and high levels. For plant
availability, an experiment could manipulate plant species and/or
dispersion. In addition, the predator factor can be tested via absence versus presence of predators. The arrows show the interactions of interest, and point to an effect on one factor by another
predator species is unlikely to provide a strong enough
selection pressure to generate an EFS pattern. Examining
a guild, as Gratton and Welter (1999) did, provides a
better picture.
A path to resolving the future status of EFS
Resolution about the relative role of the third trophic
level in shaping the patterns of feeding specialization of
insect herbivores would be useful because it would help
us understand the pattern of species diversity in plants,
invertebrate herbivores, and invertebrate enemies. The
advantage of the EFS framework is that it provides an
explicit way to evaluate the role of host plant chemistry
and dispersion on the herbivores’ enemies. However, because there very likely would be selection against the
costs of dealing with plant allelochemicals, of locating
dispersed host plants and of EFS habits, it is difficult
to ascertain the relative effects of host plant chemistry,
host plant dispersion, and enemies on shaping feeding
patterns of herbivores. Accordingly, the case studies discussed here suggest that we cannot determine where
EFS, via the effects on enemies of host plant chemistry
and dispersion, has occurred, but we can examine the
process by which it may evolve. This latter research
strategy is a kind of reductionism. The utility of reductionism is “to find points of entry into otherwise impenetrably complex systems” (Wilson 1998).
Specifically, descriptive study of natural systems is
unlikely to enlighten us much because whenever there
are data supporting the Berdegue et al. hypotheses 1 and
2 (so suggestive of EFS), it is also probable that data will
not support hypothesis 3 due to selection against the cost
of the EFS habit. In contrast, experiments that manipulate a system for the purpose of examining the effects of
161
expansion of host plant range (e.g., Gratton and Welter
1999) can be informative. But such studies should determine why survivorship is higher on novel plants and, in
particular, the role of allelochemicals. For example, in
the leafminer-Asteraceae system, we would like to
know to what extent the parasitoids: (1) found the novel
host plants, (2) found the novel plants but could not
handle the external environment of the plant (e.g., due to
trichomes), and (3) oviposited in the leafminers, but with
low survivorship of offspring due to poor host nutrition
and/or plant allelochemicals. Once again, path analysis
would be useful in resolving these issues.
Furthermore, the effects of plant dispersion could be
examined by conducting experiments that vary the relative density of the original and novel host plants. Spatial and temporal scales should also be incorporated.
But while the effect of spatial-temporal scale on the
herbivore’s avoidance of enemies can be investigated,
the effect of spatial-temporal scale on the range of host
plant species used by the herbivore cannot be evaluated
because manipulation of the herbivore requires placing
it on the novel host plants (i.e., oviposition may not occur there). Experiments that manipulate a system for
the purpose of examining the effects of narrowing host
plant range could also be done. In this case, predation
(or parasitism) could be increased to determine if it
would cause a reduction in number of host plant species
used, and if a reduction corresponds to the negative
effect of plant allelochemicals on the predators. By
using an introduced predator that causes significant
mortality or an introduced herbivore, the problem of
previous selection against cost of using EFS could be
avoided, i.e., there has not been time for selection
against such a cost.
The message here is that a rigorous test of the hypothesis of EFS will require broadening the scope of
measurements in the context of an experimental design
such as path analysis, which allows assignment of relative effects of the major factors.
Acknowledgements I thank Russell Monson for his insightful
comments. This work was supported by NSF grant DEB 9726222
and USDA grant NRI 98-35302-6878.
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