Directory UMM :Data Elmu:jurnal:B:Biochemical Systematics and Ecology:Vol28.Issue7.Aug2000:
Biochemical Systematics and Ecology 28 (2000) 601}617
Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective
Marcel Dicke*
Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
Received 3 June 1999; accepted 17 August 1999
Abstract
Most herbivorous arthropods are specialists that feed on one or a few related plant species.
To understand why this is so, both mechanistic and functional studies have been carried out,
predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of
secondary plant chemicals as source of information in behavioural decisions of herbivores.
Many evolutionary studies have regarded co-evolution between plants and herbivores to
explain the diversity of secondary plant chemicals and host specialisation of herbivores.
However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of "tness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69,
886}892)] has initiated a discussion on the need of a multitrophic perspective to understand the
evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly
resulted in ecological studies on host-selection behaviour that take a multitrophic perspective.
Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies
and competitors can a!ect herbivore behaviour. These cues may constitute important information on "tness prospects, just as plant cues can do. In this paper I selectively review how
information from organisms at di!erent trophic levels varies in space and time and how
herbivores can integratively exploit this information during host selection. In doing so, research
areas are identi"ed that are likely to provide important new insights to explain several of the
questions in herbivore host selection that remain unanswered so far. These research areas are at
the interface of evolutionary ecology, behavioural ecology and chemical ecology. ( 2000
Elsevier Science Ltd. All rights reserved.
Keywords: Host-plant selection; Avoidance of competition; Predator avoidance; Herbivore; Tritrophic
interactions; Infochemical; Ecology; Optimal foraging
* Fax: #31-317-484821.
E-mail address: [email protected] (M. Dicke)
0305-1978/00/$ - see front matter ( 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 5 - 1 9 7 8 ( 9 9 ) 0 0 1 0 6 - 4
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
1. Introduction
Understanding the causes and consequences of variable traits in interactions
among individual organisms is a central theme of evolutionary ecology. Variation
among individuals may result in di!erences in reproductive success. If this variation
has a genetic basis, selection will favour those genotypes that have phenotypes with
the largest genetic contributions to the next generation. To maximise reproductive
success, individual organisms have to make many &decisions' during their life, many of
which revolve around tradeo!s. These decisions comprise e.g. how much to invest in
growth relative to defence, when to attract a mate, when and where to reproduce, how
many o!spring to allocate to a certain location, whether to search for food or to hide
from enemies etc. (Krebs and Davies, 1984; Stephens and Krebs, 1986; Ricklefs, 1990;
Price, 1997). Information on biotic and abiotic environmental conditions provides an
opportunity to make decisions that are best adapted to current and future circumstances. The information available is subject to variation in time and space. An important
challenge for organisms is to adequately interpret this variation in information so as
to maximise reproductive success.
This is where evolutionary ecology and chemical ecology meet. Information on
biotic environmental conditions is often available through chemical cues that can
consist of a mixture of a few to several tens or up to more than a hundred di!erent
compounds (e.g. Nordlund et al., 1981; Bell and CardeH , 1984; CardeH and Bell, 1995;
Dicke, 1999). The composition of infochemicals (Dicke and Sabelis, 1988) can vary e.g.
with genotype of the producer, with biotic or with abiotic conditions. Some of these
variations may represent signal, whereas other variation may represent noise to
a responding individual, which is dependent on the correlation of cue variation with
"tness prospects for the responder. Responding organisms are therefore expected to
have evolved the ability to discriminate between signal and noise in infochemical
variation. Taking such functional aspects into consideration will be important for the
development of chemical ecological approaches.
The value of an infochemical can also depend on contextual variation, e.g. on the
simultaneous presence of other cues (Robertson et al., 1995). These other cues may
represent an alternative option. For instance, the odour of an inferior host plant may
have a di!erent value to a starved herbivore in the absence or in the presence of the
odour of a superior host plant. Moreover, the contextual cues may also modulate the
intrinsic information value of the primary infochemical. For instance, the odour of
a preferred host plant may have a di!erent meaning to a herbivore in the presence or
in the absence of cues from competitors.
In this paper I will consider the role of chemical cues in host-plant selection by
herbivorous arthropods. Most herbivorous arthropods are specialist feeders that
select a limited number of plant species as a resource. For specialists, correct decision-making during host selection behaviour is crucial and chemical cues may provide
important information to do so. Host-plant selection by herbivores is a topic that has
received extensive attention over the past decades. Many excellent reviews appeared
on plant cues and their e!ect on herbivores (e.g. Denno and McClure, 1983; Visser,
1986; Rosenthal and Berenbaum, 1992; Bernays and Chapman, 1994; Hay, 1996;
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
603
Schoonhoven et al., 1998). However, considering host-plant selection by herbivores
merely as a process of selecting plants with the best quality for development and
reproduction, does not provide a complete picture. Furthermore, considering
plant}herbivore interactions in a bitrophic context cannot fully explain the evolution
of host-plant selection by herbivorous arthropods (Bernays and Graham, 1988;
Thompson, 1988b). Herbivores have evolved and function in multitrophic foodwebs
and therefore studies of host-plant selection should also consider the importance of
defence against enemies and avoidance of competition (Faeth, 1985; Bernays and
Graham, 1988; Bernays, 1998). Indeed, host plant selection by herbivores may be
a!ected by infochemicals from competitors (e.g., Wood, 1982; Birch, 1984; Prokopy
et al., 1984; Schoonhoven 1990) and natural enemies such as carnivores (Ho!meister
and Roitberg, 1997; Grostal and Dicke, 1999a), although these cues have received
much less emphasis in studies of host-plant selection by herbivores than plant cues. In
fact, the in#uence of infochemicals from natural enemies on foraging behaviour of
herbivorous arthropods in terrestrial systems is a recent discovery that may have
important consequences for future studies on host selection by terrestrial arthropods.
In this paper I will emphasise multitrophic aspects of host-plant selection by herbivores as mediated by infochemicals. In doing so, I will call attention to both the
importance of variation in infochemicals derived from di!erent trophic levels as well
as the variation resulting from the integration of di!erent combinations of infochemicals on host plant-selection by herbivores. I will restrict this paper to chemical
information representing variation in the quality of resources. It should be noted that
in addition, quantitative variation in resource availability can also be important (e.g.
Roitberg et al., 1999).
2. Variation in plant information
An overwhelmingly large number of so-called secondary plant chemicals have been
characterised in plants (Bernays and Chapman, 1994; Gershenzon, 1994; Schoonhoven et al., 1998). These secondary chemicals are thought to have a major role in
defence against attackers (Fraenkel, 1959) and for many compounds this has been
con"rmed experimentally (reviewed by Rosenthal and Berenbaum, 1992; Bernays and
Chapman, 1994; Schoonhoven et al., 1998). However, although secondary chemicals
may defend plants against generalist herbivores, many secondary chemicals are
exploited during host selection as so-called &token stimuli' by specialist herbivores that
are not negatively a!ected by the plant chemicals (StaK dler, 1986). For instance, pierid
butter#ies use glucosinolates in the plant cuticle to recognise cruciferous host plants
on which they oviposit (van Loon et al., 1992; Chew and Renwick, 1995). In addition,
plant secondary chemicals may subsequently be exploited by specialist herbivores
through sequestration, which can result in protection of the herbivores from their
enemies (e.g. Bernays and Graham, 1988; Krischik et al., 1988; Hunter and Schultz,
1993; Rowell-Rahier et al., 1995; Hartmann, 1999).
Concentrations of secondary plant chemicals vary within and among individuals,
e.g. as a result of genotypic variation, variation in abiotic conditions or in response to
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
source}sink relationships (Gershenzon, 1984; Zangerl and Berenbaum, 1990; Herms
and Mattson, 1992; Rosenthal and Berenbaum, 1992; Bernays and Chapman, 1994;
Honkanen and Haukioja, 1998; Schoonhoven et al., 1998). Herbivores may use this
variation during selection of oviposition or feeding sites (Bernays and Chapman 1994;
Schoonhoven et al., 1998 and references therein).
Investments in plant defence and plant growth are often negatively correlated
and therefore variation in environmental conditions that a!ect a plant's growth
rate can also a!ect its investment in defence (Herms and Mattson, 1992; Gershenzon,
1994). Hence, the possibility for herbivores to exploit plant chemicals during
host-plant selection may be dependent on e.g. the plant's availability of light and
nutrients.
2.1. Herbivore-induced variation in plant information
Plant secondary chemicals may be induced by herbivore attack or pathogen
infestation and this may have short term (days) or long-term (up to more than a year)
e!ects (for reviews see Karban and Myers, 1989; Haukioja, 1990; Tallamy and Raupp,
1991; Karban and Baldwin, 1997; Tollrian and Harvell, 1999). For instance, herbivory
induces a drastic increase in nicotine concentration in tobacco plants within several
days and this response may vary with abiotic conditions such as nutrient availability
(Baldwin, 1999). The induction of secondary chemicals in plants may vary with the
herbivore species that damages the plant (Stout et al., 1994). Furthermore, induced
changes in chemical composition can occur locally and systemically and may lead to
intra-individual variation in addition to constitutive variation. Many of the changes
induced by herbivory lead to induced resistance, but induced susceptibility has
also been reported (Karban and Baldwin, 1997). Sometimes this induced susceptibility
can be explained by responses of specialist herbivores to increased concentrations
of &token stimuli' used in host-plant selection (e.g. Stanjek et al., 1997). However, in
other cases plant physiological responses such as source-sink relationships being
disturbed by defoliation may explain induced susceptibility (Honkanen and Haukioja,
1998).
Plants constitutively emit blends of volatiles that can attract herbivores (Visser,
1986). In addition, they can respond to feeding damage of herbivores with the
production of many novel compounds, resulting in the emission of complex volatile
blends. This response seems to be generally present in plants and has been extensively
reported with an emphasis on its e!ect on attraction of natural enemies of the
herbivores, such as predators and parasitic wasps (for reviews see Dicke, 1994;
Turlings et al., 1995; Takabayashi and Dicke, 1996; Dicke and Vet, 1999). In many
cases the volatiles are speci"c for herbivory, or even for the herbivore species that
in#icts the damage. Herbivores may also use these induced volatiles during host-plant
selection (reviewed by Dicke and Vet, 1999). Herbivores may avoid the volatiles
(Dicke, 1986; Pallini et al., 1997), but in several cases herbivores were found to be
attracted to them (Loughrin et al., 1995; Bolter et al., 1997; Pallini et al., 1997; Dicke
and Vet, 1999). Induced plant volatiles may make the plant apparent among undamaged neighbours that emit low amounts of volatiles. As a result the damaged
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
605
plant attracts more herbivores. Because many plant species emit a di!erent blend
when mechanically damaged (e.g. caused by wind-borne sand or sca"ng against other
plants) than when damaged by herbivores, speci"c information on the level of
competition is available to herbivores. Therefore, one would expect that herbivores
would bene"t from discriminating between volatiles from herbivore-infested plants
and mechanically damaged plants (see Dicke and Vet, 1999 for a discussion). However, current experimental data do not provide substantial support for this expectation (Dicke and Vet, 1999). Furthermore, if the induced plant volatiles are speci"c for
the herbivore species that damages the plant, they may enable the herbivores to
discriminate between plants infested with di!erent types of competitors. This is
supported by a study on the response of spider mites to induced plant volatiles (Pallini
et al., 1997). The response of herbivores to induced plant volatiles is a research topic
that is still in its infancy though, and future studies are expected to elucidate whether
our current view is correct and how herbivore responses can be understood from
a functional point of view. An interesting study in this respect is that on the cabbage
looper moth (Trichoplusia ni). Female moths are attracted to volatiles from cotton
plants infested with conspeci"c larvae. After arriving at the infested plants, however,
the females do not oviposit on the already infested plants, but search for nearby
uninfested plants on which they oviposit (Landolt, 1993). This indicates that volatiles
from infested plants provided a cue to locate a patch of host plants and thus made the
plants more apparent, but that competition is actively avoided during subsequent
foraging decisions.
An induced plant response may also account for a phenomenon that was long
thought to involve herbivore-produced cues. Pierid butter#ies avoid oviposition on
host plants on which other females have previously oviposited (Schoonhoven, 1990).
This was long assumed to be caused by a secretion from the accessory gland that the
female deposited during oviposition, and that was termed an oviposition-deterring or
host-marking pheromone (Schoonhoven, 1990). However, an in-depth study has
shown that a plant cue and not a herbivore product is responsible for the herbivore's
behavioural response. Blaakmeer et al. (1994) demonstrated that the plant onto which
the female oviposits, responds with the systemic production of chemicals in the leaf
cuticle that result in other butter#ies avoiding the plant as an oviposition substrate.
This represents an induced response of plants to herbivores that seems to be independent of the herbivore damaging the plant.
In conclusion, a plant's chemistry is highly variable in time and space and a plant's
biotic history may a!ect the same chemical constituents as abiotic conditions do.
However, although herbivory and abiotic conditions can lead to an increase in the
same secondary plant chemicals, a plant is likely to provide di!erent "tness prospects
to a herbivore after previous exposure to herbivory as compared to prior exposure to
certain abiotic conditions. Whether, when and how herbivores can discriminate
between cues from plants that have been exposed to herbivory or abiotic conditions
a!ecting the same secondary chemicals has remained unexplored so far. The most
likely option that herbivores have is to integrate the information from the plant with
information from herbivores that have previously fed or still feed on the plant, such as
faecal components, pheromones or other herbivore compounds.
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3. Variation in herbivore infochemicals
Products of the herbivore of course represent the most direct information on
herbivore presence. These products may comprise herbivore pheromones that are
released from glands or as components of faeces (Prokopy et al., 1984; Roessingh et al.,
1988; Hilker and Klein, 1989; Schindek and Hilker, 1996). The presence of herbivore
pheromones is usually variable in time. They are often emitted during restricted time
periods and they can have short half-lives. Adult moths emit sex pheromones during
speci"c moments of the day (CardeH and Minks, 1997). The emitted pheromone may
adsorb to the foliage and be perceived at a later moment, thus prolonging the time
window of pheromone availability (Wall et al., 1981; Noldus et al., 1991). On the other
hand, pheromones may be washed away as was shown for host-marking pheromones
applied on a host by herbivorous #ies, which shortens the time window (Averill and
Prokopy, 1987). It should be noted that in many cases, host-marking pheromones
have not been chemically identi"ed (but see Hurter et al., 1987). There is a chance,
that, as was found for Pieris brassicae, other host-marking pheromones also appear
not to be produced by the herbivore, but by the plant in response to the herbivore
(Blaakmeer et al., 1994). If the plant is the producer of the herbivore-related cue, the
information may be more variable than when the cue is a pheromone produced by the
herbivore (Vet and Dicke, 1992).
Herbivore pheromones may also be emitted in response to attack by enemies.
Alarm pheromones are well known to be induced in aphids and thrips in response to
attack by predators (Pickett et al., 1992; Teerling et al., 1993). Thus, these pheromones
not only indicate the presence of competitors, but also the presence of natural enemies.
Alarm pheromones can a!ect various herbivore behaviours, among which the abandoning of a host plant or seeking refuge (McAllister and Roitberg, 1987; Pickett et al.,
1992; Pallini et al., 1998). In addition, herbivorous arthropods may also avoid cues
related to dead conspeci"cs, which may represent another type of information on the
presence of enemies (Rollo et al., 1995; Grostal and Dicke, 1999a).
So, in addition to being indicators of competitors, herbivore cues may also
provide information on the presence of carnivorous enemies. However, the
more direct information on enemy presence would be derived from the carnivores
themselves.
4. Carnivore infochemicals and host selection by herbivores
The value of a host plant to a herbivore is dependent on whether it represents an
enemy-free or an enemy-dense resource or on whether the herbivore will have good
prospects for defence against its enemies or not (Bernays and Graham, 1988; Bernays,
1998; MuK ller and Godfray, 1999). Some plant species provide shelter or alternative
food to carnivorous arthropods, which can signi"cantly a!ect the value of the host
plant to herbivores in terms of reproductive success (Huxley and Cutler, 1991; Koptur,
1992; Grostal and O'Dowd, 1994; Yano, 1994; Walter, 1996; Agrawal and Karban,
1997). Thus, food selection and predator avoidance may represent tradeo!s that an
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
607
animal has to cope with (for reviews see e.g. Lima and Dill, 1989; Kats and Dill, 1998).
Herbivores may prefer nutritionally inferior host plants on which chances of encountering parasitoids are predictably low over nutritionally superior host plants that are
frequently visited by natural enemies (Jaenike, 1985; Ohsaki and Sato, 1994). In
addition, there are several examples of herbivores avoiding resources on which their
enemies are actually present (e.g. Bernstein, 1984; Prokopy and Duan, 1998) and the
avoidance of enemies through infochemicals has been documented for a wide range of
organisms (Kats and Dill, 1998; Tollrian and Harvell, 1999). Only recently, evidence
for the avoidance of enemies through carnivore infochemicals is becoming available
for terrestrial arthropods (Kats and Dill, 1998). For instance, host acceptance by
Rhagoletis basiola fruit #ies is negatively a!ected by cues from an egg parasitoid
(Ho!meister and Roitberg, 1997) and herbivorous spider mites avoid plant tissue
contaminated with an infochemical from phytoseiid predators that incur a large
mortality risk (Kriesch and Dicke, 1997; Grostal and Dicke, 1999a). The infochemical
responsible for this response of spider mites remained active for at least 4 days after
deposition by the predators (Kriesch and Dicke, 1997). Furthermore, the spider mites
avoided infochemicals from a wide range of carnivorous mites, including carnivores
that would not attack the spider mites such as acarine parasites of chicken or
honeybees (Grostal and Dicke, 1999b). However, the spider mites did not respond to
cues from fungivorous or pollen-feeding mites (Grostal and Dicke, 1999a,b). Moreover, the spider mites were clearly able to distinguish among potential predators: if
facultative predators were either fed on spider mites or on pollen, the spider mites had
a signi"cantly stronger avoidance of infochemicals from spider mite-fed predators
than from infochemicals of the pollen-fed predators (Grostal and Dicke, 1999b). These
data are not likely to be an exception given the widespread occurrence of predator
avoidance in aquatic systems and in terrestrial vertebrate systems (Kats and Dill,
1998). Therefore, investigating the importance of carnivore infochemicals in
host selection by terrestrial arthropod herbivores is likely to be an important
and fruitful future research area for chemical ecologists. For example, ants are well
known for marking their foraging substrate and they are abundantly available on
plants that provide the ants with shelter or alternative food (HoK lldobler and Wilson,
1990; Yano, 1994). Such plants are likely to be contaminated with ant pheromones
and herbivores would pro"t from exploiting the infochemicals to avoid running into
their predators.
Not all herbivores are expected to avoid plants on which carnivores are present.
Some herbivore species such as aphids and lycaenid caterpillars bene"t from ant
mutualists that defend them from their enemies (e.g. Pierce and Young, 1986; MuK ller
and Godfray, 1999). Such herbivores have been observed to prefer to select plants on
which ants are present over ant-free plants (Atsatt, 1981; Pierce and Elgar, 1985;
Wagner and Kurina, 1997), although it remains to be elucidated whether this is based
on visual, physical or chemical cues. In addition, host plant selection by these
herbivores can also have another in#uence on the amount of protection they will
acquire from ants. Nutritional quality of the host plant can a!ect the quality of
herbivore secretions that are provided as reward to ants and consequently the level of
ant attendance and thus protection by the ants (Baylis and Pierce, 1991).
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5. Correlation between variation in infochemicals from di4erent sources
As outlined above, chemical information from plants, herbivores and carnivores
may be available to herbivores when selecting a host plant. For an overview for
a speci"c system, see Fig. 1. The information may be produced independently by an
organism at each of the three trophic levels (e.g. Prokopy et al., 1984; Ho!meister and
Roitberg, 1997; Schoonhoven et al., 1998), or the information may be a product of an
interaction of organisms of the same or di!erent trophic levels (e.g. Pickett et al., 1992;
Dicke and Vet, 1999). In other instances, it remains unknown who produced the
infochemical used by the herbivores (e.g. Quiroz et al., 1997). Moreover, the presence
and abundance of information from these three major sources may be also correlated.
For instance, there may be a negative correlation between direct and indirect
plant defence and thus between plant secondary chemicals and carnivore cues
Fig. 1. Example of information from di!erent trophic levels that is known to a!ect host-selection behaviour
of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Arrows indicate information that
a!ects spider-mite behaviour, while accompanying numbers refer to the trophic level of the organism that
produces the information. 1: Volatiles from undamaged Lima bean plants (Phaseolus lunatus) (Dicke, 1986);
1a: spider-mite-induced volatiles emitted by Lima bean plants (Dicke, 1986) or cucumber plants (Pallini
et al., 1997); 1b: thrips (Frankliniella accidentalis)-included volatiles emitted by cucumber plants (Pallini
et al., 1997); 2: cues from spider mite eggs or adults (Grostal and Dicke, 1999a); 2a: predatory mites
(Phytoseiulus persimilis) are likely to induce an alarm pheromone in adult spider mites (Janssen et al., 1997)
that a!ects spider mite behaviour (Pallini, 1998); 3: the predatory mite P. persimilis produces a non-volatile
cue that a!ects spider mite foraging behaviour (Kriesch and Dicke, 1997; Grostal and Dicke, 1999a,b) and
a volatile cue that can a!ect alarm-pheromone emission by spider mites (Janssen et al., 1997).
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
609
(Vrieling et al., 1991; Heil et al., 1999). In an analysis of the variation in pyrrolizidine
alkaloids in Senecio jacobaea and associated herbivore numbers, Vrieling et al. (1991)
found that plants with high concentrations of pyrrolizidine alkaloids had low numbers of aphids and aphid-tending ants and vice versa. The aphid-tending ants attack
caterpillars of the specialist lepidopteran herbivore Tyria jacobaeae that is not a!ected
by di!erences in pyrrolizidine alkaloids-levels. Thus, plants with low amounts of
pyrrolizidine alkaloids may be contaminated with large amounts of carnivore infochemicals, while plants with large amounts of pyrrolizidine alkaloids may have low
amounts of carnivore cues.
Herbivore pheromones may be positively correlated with certain plant volatiles
because these plant cues induce pheromone emission by the herbivore (McNeil and
Delisle, 1989; Raina et al., 1991).
A question that has not received attention so far in the literature, is whether plants
may respond to the presence of carnivorous arthropods. Plants may constitutively
provide shelter and alternative food for carnivores (Koptur, 1992; Walter, 1996) which
can result in the presence of carnivores in the absence of herbivores. If plants can
perceive the presence of the carnivores, e.g. by perceiving the removal of alternative
food or by perceiving faeces of the carnivores, could this have an e!ect on their
induced responses to herbivores? For instance, would the investment in induced
volatiles be negatively correlated with the presence of carnivorous arthropods? This
might enable plants to reduce the exploitation of induced volatiles by herbivores. Such
an ability of plants may seem to be far-fetched at "rst. However, the extensive
information on the responses of plants to information from competing plants, herbivores and pathogens even in the absence of damage (Blaakmeer et al., 1994; Bruin
et al., 1995; Karban and Baldwin, 1997; Shulaev et al., 1997; van Loon, 1997; BallareH ,
1999) should make us careful not to underestimate the abilities of plants to respond to
biotic components in the environment.
6. Integration of information from di4erent trophic levels during host-plant selection
Infochemicals available to foraging herbivores may be induced by herbivores in
plants (e.g. induced direct defence) or by carnivores in herbivores (e.g. alarm
pheromones) and thus these cues represent an integration of information from
di!erent trophic levels (see above). Moreover, the behaviour of arthropods to infochemicals is phenotypically plastic and the response to an information source may
be dependent on e.g. physiological state, previous experiences and abiotic conditions
(for reviews see e.g. Jaenike, 1988; Papaj and Prokopy, 1989; Jaenike and Papaj, 1992;
Papaj and Lewis, 1993; Bernays, 1995; Robertson et al., 1995; Vet et al., 1995; Dicke
et al., 1998). Through associative learning herbivorous arthropods may integrate
di!erent types of information from plants, such as plant odour and plant shape
(Jaenike, 1988; Papaj and Prokopy, 1989; Szentesi and Jermy, 1990). In addition, also
information from competitors or predators might be integrated through associative
learning, although hardly any studies have been made on this to date (but see
Mallet et al., 1987; Dukas, 1998). Recent evidence on the availability of carnivore
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
infochemicals to herbivores (Ho!meister and Roitberg, 1997; Grostal and Dicke,
1999a,b) suggests that this will be a fruitful area for further investigation.
Herbivores may integrate information perceived simultaneously from di!erent
sources. For instance, the response to sex pheromones can be modulated by infochemicals from host plants present (Dickens et al., 1993; Landolt et al., 1994; Lilley
and Hardie, 1996). Furthermore, the response by herbivores to infochemicals emitted
by herbivores or by herbivore-infested plants can be dependent on the amount of
these cues relative to the amount of infochemical from uninfested plants (Dicke 1986;
Pettersson et al., 1998).
To foraging herbivores, plants represent a resource that has a value in terms of food,
competitors and natural enemies. Food selection has often been studied in a bitrophic
context, where the food quality in terms of its e!ect on herbivore "tness was
considered. Alternatively, consequences of host-plant selection for defence of herbivores against their enemies have been considered (Barbosa, 1988a; Bernays and
Graham, 1988; Pasteels et al., 1988; Rowell-Rahier and Pasteels, 1992). It will be
important to include studies on herbivore behaviour in situations with con#icting
alternatives derived from combinations of costs and bene"ts related to food, competitors and enemies. For instance, what decisions does a herbivore make when the
alternatives are an inferior host plant without carnivore cues versus a superior host
plant with abundant carnivore cues? Are the decisions di!erent for specialist and
generalist herbivores? Is the preference of specialist insects for plants containing
secondary chemicals that can be exploited in defence against carnivores di!erent in
the presence or absence of predator cues? Such research questions are an exciting part
of behavioural ecology (e.g. Krebs and Davies, 1984; Courtney, 1986; Godin and
Sproul, 1988; Anholt and Werner, 1995; Gotceitas et al., 1995; Bouskila et al., 1998)
that deserve the incorporation of a chemical ecological approach on the role of
infochemicals in host plant selection by herbivores.
7. Herbivores, information networks and food webs: conclusions
The study of foraging behaviour of carnivorous arthropods has made tremendous
progress in the past two decades by proceeding from a bitrophic perspective to
a multitrophic perspective. Considering the importance of plant information in
foraging strategies of carnivores has created a completely new view on the organisation of food webs (Price, 1981; Dicke et al., 1990; Vet and Dicke, 1992; Tumlinson
et al., 1993; Turlings et al., 1993,1995; Bruin et al., 1995; Takabayashi and Dicke, 1996;
Janssen et al., 1998; Powell et al., 1998; Dicke and Vet, 1999; Sabelis et al., 1999).
It is clear that an information web is superimposed on a food web and that the
information web creates many indirect interactions in addition to the mostly trophically based direct interactions (Vet and Dicke, 1992; Janssen et al., 1998; Dicke and
Vet, 1999).
Host-plant selection by herbivores has been considered in a bitrophic context for
a long time. A vast majority of literature exists, especially devoted to the role of plant
information. Despite this abundant knowledge on the role of plant chemicals and the
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
611
acknowledgement that plant chemistry is of signi"cant importance in host selection
by herbivorous arthropods, major questions remain unanswered (e.g. Courtney and
Kibota, 1990). Alternative approaches to the study of host-plant selection by herbivores, such as expressed in the seminal paper by Bernays and Graham (1988) have met
with mixed responses (e.g. Barbosa, 1988b; Courtney, 1988; Ehrlich and Murphy,
1988; Jermy, 1988; Schultz, 1988; Thompson, 1988a). However, if an extensive chemical information network exists with information on plant presence and nutritional
quality, on competitor abundance and identity and on chances of encountering
enemies, why would herbivores not exploit this information? At the very least, the
importance of this information network for foraging behaviour of herbivores deserves
to be investigated. This should be done both in laboratory studies and in "eld studies.
A majority of studies on host-plant selection by herbivores has been executed in the
laboratory and future laboratory studies will continue to be important to determine
the options available to herbivores. In addition, "eld studies should be carried out to
reveal to what extent the potential of decision-making that has been recorded in the
laboratory can play a role under "eld conditions where conditions are much more
variable in many respects. Taking a multitrophic approach to herbivore host-selection
behaviour will improve our knowledge and will make an important contribution to
solving several of the questions on host selection by herbivores that are still open. In
doing so, students of host selection by herbivorous arthropods will make new
contributions to evolutionary ecology, behavioural ecology and chemical ecology.
Acknowledgements
The manuscript bene"ted from constructive comments on an earlier version by
Joop van Loon, Bernie Roitberg, Louis Schoonhoven and Louise Vet. MD was
funded in part by the Uyttenboogaart-Eliasen Foundation, Amsterdam.
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Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective
Marcel Dicke*
Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands
Received 3 June 1999; accepted 17 August 1999
Abstract
Most herbivorous arthropods are specialists that feed on one or a few related plant species.
To understand why this is so, both mechanistic and functional studies have been carried out,
predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of
secondary plant chemicals as source of information in behavioural decisions of herbivores.
Many evolutionary studies have regarded co-evolution between plants and herbivores to
explain the diversity of secondary plant chemicals and host specialisation of herbivores.
However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of "tness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69,
886}892)] has initiated a discussion on the need of a multitrophic perspective to understand the
evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly
resulted in ecological studies on host-selection behaviour that take a multitrophic perspective.
Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies
and competitors can a!ect herbivore behaviour. These cues may constitute important information on "tness prospects, just as plant cues can do. In this paper I selectively review how
information from organisms at di!erent trophic levels varies in space and time and how
herbivores can integratively exploit this information during host selection. In doing so, research
areas are identi"ed that are likely to provide important new insights to explain several of the
questions in herbivore host selection that remain unanswered so far. These research areas are at
the interface of evolutionary ecology, behavioural ecology and chemical ecology. ( 2000
Elsevier Science Ltd. All rights reserved.
Keywords: Host-plant selection; Avoidance of competition; Predator avoidance; Herbivore; Tritrophic
interactions; Infochemical; Ecology; Optimal foraging
* Fax: #31-317-484821.
E-mail address: [email protected] (M. Dicke)
0305-1978/00/$ - see front matter ( 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 3 0 5 - 1 9 7 8 ( 9 9 ) 0 0 1 0 6 - 4
602
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
1. Introduction
Understanding the causes and consequences of variable traits in interactions
among individual organisms is a central theme of evolutionary ecology. Variation
among individuals may result in di!erences in reproductive success. If this variation
has a genetic basis, selection will favour those genotypes that have phenotypes with
the largest genetic contributions to the next generation. To maximise reproductive
success, individual organisms have to make many &decisions' during their life, many of
which revolve around tradeo!s. These decisions comprise e.g. how much to invest in
growth relative to defence, when to attract a mate, when and where to reproduce, how
many o!spring to allocate to a certain location, whether to search for food or to hide
from enemies etc. (Krebs and Davies, 1984; Stephens and Krebs, 1986; Ricklefs, 1990;
Price, 1997). Information on biotic and abiotic environmental conditions provides an
opportunity to make decisions that are best adapted to current and future circumstances. The information available is subject to variation in time and space. An important
challenge for organisms is to adequately interpret this variation in information so as
to maximise reproductive success.
This is where evolutionary ecology and chemical ecology meet. Information on
biotic environmental conditions is often available through chemical cues that can
consist of a mixture of a few to several tens or up to more than a hundred di!erent
compounds (e.g. Nordlund et al., 1981; Bell and CardeH , 1984; CardeH and Bell, 1995;
Dicke, 1999). The composition of infochemicals (Dicke and Sabelis, 1988) can vary e.g.
with genotype of the producer, with biotic or with abiotic conditions. Some of these
variations may represent signal, whereas other variation may represent noise to
a responding individual, which is dependent on the correlation of cue variation with
"tness prospects for the responder. Responding organisms are therefore expected to
have evolved the ability to discriminate between signal and noise in infochemical
variation. Taking such functional aspects into consideration will be important for the
development of chemical ecological approaches.
The value of an infochemical can also depend on contextual variation, e.g. on the
simultaneous presence of other cues (Robertson et al., 1995). These other cues may
represent an alternative option. For instance, the odour of an inferior host plant may
have a di!erent value to a starved herbivore in the absence or in the presence of the
odour of a superior host plant. Moreover, the contextual cues may also modulate the
intrinsic information value of the primary infochemical. For instance, the odour of
a preferred host plant may have a di!erent meaning to a herbivore in the presence or
in the absence of cues from competitors.
In this paper I will consider the role of chemical cues in host-plant selection by
herbivorous arthropods. Most herbivorous arthropods are specialist feeders that
select a limited number of plant species as a resource. For specialists, correct decision-making during host selection behaviour is crucial and chemical cues may provide
important information to do so. Host-plant selection by herbivores is a topic that has
received extensive attention over the past decades. Many excellent reviews appeared
on plant cues and their e!ect on herbivores (e.g. Denno and McClure, 1983; Visser,
1986; Rosenthal and Berenbaum, 1992; Bernays and Chapman, 1994; Hay, 1996;
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
603
Schoonhoven et al., 1998). However, considering host-plant selection by herbivores
merely as a process of selecting plants with the best quality for development and
reproduction, does not provide a complete picture. Furthermore, considering
plant}herbivore interactions in a bitrophic context cannot fully explain the evolution
of host-plant selection by herbivorous arthropods (Bernays and Graham, 1988;
Thompson, 1988b). Herbivores have evolved and function in multitrophic foodwebs
and therefore studies of host-plant selection should also consider the importance of
defence against enemies and avoidance of competition (Faeth, 1985; Bernays and
Graham, 1988; Bernays, 1998). Indeed, host plant selection by herbivores may be
a!ected by infochemicals from competitors (e.g., Wood, 1982; Birch, 1984; Prokopy
et al., 1984; Schoonhoven 1990) and natural enemies such as carnivores (Ho!meister
and Roitberg, 1997; Grostal and Dicke, 1999a), although these cues have received
much less emphasis in studies of host-plant selection by herbivores than plant cues. In
fact, the in#uence of infochemicals from natural enemies on foraging behaviour of
herbivorous arthropods in terrestrial systems is a recent discovery that may have
important consequences for future studies on host selection by terrestrial arthropods.
In this paper I will emphasise multitrophic aspects of host-plant selection by herbivores as mediated by infochemicals. In doing so, I will call attention to both the
importance of variation in infochemicals derived from di!erent trophic levels as well
as the variation resulting from the integration of di!erent combinations of infochemicals on host plant-selection by herbivores. I will restrict this paper to chemical
information representing variation in the quality of resources. It should be noted that
in addition, quantitative variation in resource availability can also be important (e.g.
Roitberg et al., 1999).
2. Variation in plant information
An overwhelmingly large number of so-called secondary plant chemicals have been
characterised in plants (Bernays and Chapman, 1994; Gershenzon, 1994; Schoonhoven et al., 1998). These secondary chemicals are thought to have a major role in
defence against attackers (Fraenkel, 1959) and for many compounds this has been
con"rmed experimentally (reviewed by Rosenthal and Berenbaum, 1992; Bernays and
Chapman, 1994; Schoonhoven et al., 1998). However, although secondary chemicals
may defend plants against generalist herbivores, many secondary chemicals are
exploited during host selection as so-called &token stimuli' by specialist herbivores that
are not negatively a!ected by the plant chemicals (StaK dler, 1986). For instance, pierid
butter#ies use glucosinolates in the plant cuticle to recognise cruciferous host plants
on which they oviposit (van Loon et al., 1992; Chew and Renwick, 1995). In addition,
plant secondary chemicals may subsequently be exploited by specialist herbivores
through sequestration, which can result in protection of the herbivores from their
enemies (e.g. Bernays and Graham, 1988; Krischik et al., 1988; Hunter and Schultz,
1993; Rowell-Rahier et al., 1995; Hartmann, 1999).
Concentrations of secondary plant chemicals vary within and among individuals,
e.g. as a result of genotypic variation, variation in abiotic conditions or in response to
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
source}sink relationships (Gershenzon, 1984; Zangerl and Berenbaum, 1990; Herms
and Mattson, 1992; Rosenthal and Berenbaum, 1992; Bernays and Chapman, 1994;
Honkanen and Haukioja, 1998; Schoonhoven et al., 1998). Herbivores may use this
variation during selection of oviposition or feeding sites (Bernays and Chapman 1994;
Schoonhoven et al., 1998 and references therein).
Investments in plant defence and plant growth are often negatively correlated
and therefore variation in environmental conditions that a!ect a plant's growth
rate can also a!ect its investment in defence (Herms and Mattson, 1992; Gershenzon,
1994). Hence, the possibility for herbivores to exploit plant chemicals during
host-plant selection may be dependent on e.g. the plant's availability of light and
nutrients.
2.1. Herbivore-induced variation in plant information
Plant secondary chemicals may be induced by herbivore attack or pathogen
infestation and this may have short term (days) or long-term (up to more than a year)
e!ects (for reviews see Karban and Myers, 1989; Haukioja, 1990; Tallamy and Raupp,
1991; Karban and Baldwin, 1997; Tollrian and Harvell, 1999). For instance, herbivory
induces a drastic increase in nicotine concentration in tobacco plants within several
days and this response may vary with abiotic conditions such as nutrient availability
(Baldwin, 1999). The induction of secondary chemicals in plants may vary with the
herbivore species that damages the plant (Stout et al., 1994). Furthermore, induced
changes in chemical composition can occur locally and systemically and may lead to
intra-individual variation in addition to constitutive variation. Many of the changes
induced by herbivory lead to induced resistance, but induced susceptibility has
also been reported (Karban and Baldwin, 1997). Sometimes this induced susceptibility
can be explained by responses of specialist herbivores to increased concentrations
of &token stimuli' used in host-plant selection (e.g. Stanjek et al., 1997). However, in
other cases plant physiological responses such as source-sink relationships being
disturbed by defoliation may explain induced susceptibility (Honkanen and Haukioja,
1998).
Plants constitutively emit blends of volatiles that can attract herbivores (Visser,
1986). In addition, they can respond to feeding damage of herbivores with the
production of many novel compounds, resulting in the emission of complex volatile
blends. This response seems to be generally present in plants and has been extensively
reported with an emphasis on its e!ect on attraction of natural enemies of the
herbivores, such as predators and parasitic wasps (for reviews see Dicke, 1994;
Turlings et al., 1995; Takabayashi and Dicke, 1996; Dicke and Vet, 1999). In many
cases the volatiles are speci"c for herbivory, or even for the herbivore species that
in#icts the damage. Herbivores may also use these induced volatiles during host-plant
selection (reviewed by Dicke and Vet, 1999). Herbivores may avoid the volatiles
(Dicke, 1986; Pallini et al., 1997), but in several cases herbivores were found to be
attracted to them (Loughrin et al., 1995; Bolter et al., 1997; Pallini et al., 1997; Dicke
and Vet, 1999). Induced plant volatiles may make the plant apparent among undamaged neighbours that emit low amounts of volatiles. As a result the damaged
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
605
plant attracts more herbivores. Because many plant species emit a di!erent blend
when mechanically damaged (e.g. caused by wind-borne sand or sca"ng against other
plants) than when damaged by herbivores, speci"c information on the level of
competition is available to herbivores. Therefore, one would expect that herbivores
would bene"t from discriminating between volatiles from herbivore-infested plants
and mechanically damaged plants (see Dicke and Vet, 1999 for a discussion). However, current experimental data do not provide substantial support for this expectation (Dicke and Vet, 1999). Furthermore, if the induced plant volatiles are speci"c for
the herbivore species that damages the plant, they may enable the herbivores to
discriminate between plants infested with di!erent types of competitors. This is
supported by a study on the response of spider mites to induced plant volatiles (Pallini
et al., 1997). The response of herbivores to induced plant volatiles is a research topic
that is still in its infancy though, and future studies are expected to elucidate whether
our current view is correct and how herbivore responses can be understood from
a functional point of view. An interesting study in this respect is that on the cabbage
looper moth (Trichoplusia ni). Female moths are attracted to volatiles from cotton
plants infested with conspeci"c larvae. After arriving at the infested plants, however,
the females do not oviposit on the already infested plants, but search for nearby
uninfested plants on which they oviposit (Landolt, 1993). This indicates that volatiles
from infested plants provided a cue to locate a patch of host plants and thus made the
plants more apparent, but that competition is actively avoided during subsequent
foraging decisions.
An induced plant response may also account for a phenomenon that was long
thought to involve herbivore-produced cues. Pierid butter#ies avoid oviposition on
host plants on which other females have previously oviposited (Schoonhoven, 1990).
This was long assumed to be caused by a secretion from the accessory gland that the
female deposited during oviposition, and that was termed an oviposition-deterring or
host-marking pheromone (Schoonhoven, 1990). However, an in-depth study has
shown that a plant cue and not a herbivore product is responsible for the herbivore's
behavioural response. Blaakmeer et al. (1994) demonstrated that the plant onto which
the female oviposits, responds with the systemic production of chemicals in the leaf
cuticle that result in other butter#ies avoiding the plant as an oviposition substrate.
This represents an induced response of plants to herbivores that seems to be independent of the herbivore damaging the plant.
In conclusion, a plant's chemistry is highly variable in time and space and a plant's
biotic history may a!ect the same chemical constituents as abiotic conditions do.
However, although herbivory and abiotic conditions can lead to an increase in the
same secondary plant chemicals, a plant is likely to provide di!erent "tness prospects
to a herbivore after previous exposure to herbivory as compared to prior exposure to
certain abiotic conditions. Whether, when and how herbivores can discriminate
between cues from plants that have been exposed to herbivory or abiotic conditions
a!ecting the same secondary chemicals has remained unexplored so far. The most
likely option that herbivores have is to integrate the information from the plant with
information from herbivores that have previously fed or still feed on the plant, such as
faecal components, pheromones or other herbivore compounds.
606
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
3. Variation in herbivore infochemicals
Products of the herbivore of course represent the most direct information on
herbivore presence. These products may comprise herbivore pheromones that are
released from glands or as components of faeces (Prokopy et al., 1984; Roessingh et al.,
1988; Hilker and Klein, 1989; Schindek and Hilker, 1996). The presence of herbivore
pheromones is usually variable in time. They are often emitted during restricted time
periods and they can have short half-lives. Adult moths emit sex pheromones during
speci"c moments of the day (CardeH and Minks, 1997). The emitted pheromone may
adsorb to the foliage and be perceived at a later moment, thus prolonging the time
window of pheromone availability (Wall et al., 1981; Noldus et al., 1991). On the other
hand, pheromones may be washed away as was shown for host-marking pheromones
applied on a host by herbivorous #ies, which shortens the time window (Averill and
Prokopy, 1987). It should be noted that in many cases, host-marking pheromones
have not been chemically identi"ed (but see Hurter et al., 1987). There is a chance,
that, as was found for Pieris brassicae, other host-marking pheromones also appear
not to be produced by the herbivore, but by the plant in response to the herbivore
(Blaakmeer et al., 1994). If the plant is the producer of the herbivore-related cue, the
information may be more variable than when the cue is a pheromone produced by the
herbivore (Vet and Dicke, 1992).
Herbivore pheromones may also be emitted in response to attack by enemies.
Alarm pheromones are well known to be induced in aphids and thrips in response to
attack by predators (Pickett et al., 1992; Teerling et al., 1993). Thus, these pheromones
not only indicate the presence of competitors, but also the presence of natural enemies.
Alarm pheromones can a!ect various herbivore behaviours, among which the abandoning of a host plant or seeking refuge (McAllister and Roitberg, 1987; Pickett et al.,
1992; Pallini et al., 1998). In addition, herbivorous arthropods may also avoid cues
related to dead conspeci"cs, which may represent another type of information on the
presence of enemies (Rollo et al., 1995; Grostal and Dicke, 1999a).
So, in addition to being indicators of competitors, herbivore cues may also
provide information on the presence of carnivorous enemies. However, the
more direct information on enemy presence would be derived from the carnivores
themselves.
4. Carnivore infochemicals and host selection by herbivores
The value of a host plant to a herbivore is dependent on whether it represents an
enemy-free or an enemy-dense resource or on whether the herbivore will have good
prospects for defence against its enemies or not (Bernays and Graham, 1988; Bernays,
1998; MuK ller and Godfray, 1999). Some plant species provide shelter or alternative
food to carnivorous arthropods, which can signi"cantly a!ect the value of the host
plant to herbivores in terms of reproductive success (Huxley and Cutler, 1991; Koptur,
1992; Grostal and O'Dowd, 1994; Yano, 1994; Walter, 1996; Agrawal and Karban,
1997). Thus, food selection and predator avoidance may represent tradeo!s that an
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
607
animal has to cope with (for reviews see e.g. Lima and Dill, 1989; Kats and Dill, 1998).
Herbivores may prefer nutritionally inferior host plants on which chances of encountering parasitoids are predictably low over nutritionally superior host plants that are
frequently visited by natural enemies (Jaenike, 1985; Ohsaki and Sato, 1994). In
addition, there are several examples of herbivores avoiding resources on which their
enemies are actually present (e.g. Bernstein, 1984; Prokopy and Duan, 1998) and the
avoidance of enemies through infochemicals has been documented for a wide range of
organisms (Kats and Dill, 1998; Tollrian and Harvell, 1999). Only recently, evidence
for the avoidance of enemies through carnivore infochemicals is becoming available
for terrestrial arthropods (Kats and Dill, 1998). For instance, host acceptance by
Rhagoletis basiola fruit #ies is negatively a!ected by cues from an egg parasitoid
(Ho!meister and Roitberg, 1997) and herbivorous spider mites avoid plant tissue
contaminated with an infochemical from phytoseiid predators that incur a large
mortality risk (Kriesch and Dicke, 1997; Grostal and Dicke, 1999a). The infochemical
responsible for this response of spider mites remained active for at least 4 days after
deposition by the predators (Kriesch and Dicke, 1997). Furthermore, the spider mites
avoided infochemicals from a wide range of carnivorous mites, including carnivores
that would not attack the spider mites such as acarine parasites of chicken or
honeybees (Grostal and Dicke, 1999b). However, the spider mites did not respond to
cues from fungivorous or pollen-feeding mites (Grostal and Dicke, 1999a,b). Moreover, the spider mites were clearly able to distinguish among potential predators: if
facultative predators were either fed on spider mites or on pollen, the spider mites had
a signi"cantly stronger avoidance of infochemicals from spider mite-fed predators
than from infochemicals of the pollen-fed predators (Grostal and Dicke, 1999b). These
data are not likely to be an exception given the widespread occurrence of predator
avoidance in aquatic systems and in terrestrial vertebrate systems (Kats and Dill,
1998). Therefore, investigating the importance of carnivore infochemicals in
host selection by terrestrial arthropod herbivores is likely to be an important
and fruitful future research area for chemical ecologists. For example, ants are well
known for marking their foraging substrate and they are abundantly available on
plants that provide the ants with shelter or alternative food (HoK lldobler and Wilson,
1990; Yano, 1994). Such plants are likely to be contaminated with ant pheromones
and herbivores would pro"t from exploiting the infochemicals to avoid running into
their predators.
Not all herbivores are expected to avoid plants on which carnivores are present.
Some herbivore species such as aphids and lycaenid caterpillars bene"t from ant
mutualists that defend them from their enemies (e.g. Pierce and Young, 1986; MuK ller
and Godfray, 1999). Such herbivores have been observed to prefer to select plants on
which ants are present over ant-free plants (Atsatt, 1981; Pierce and Elgar, 1985;
Wagner and Kurina, 1997), although it remains to be elucidated whether this is based
on visual, physical or chemical cues. In addition, host plant selection by these
herbivores can also have another in#uence on the amount of protection they will
acquire from ants. Nutritional quality of the host plant can a!ect the quality of
herbivore secretions that are provided as reward to ants and consequently the level of
ant attendance and thus protection by the ants (Baylis and Pierce, 1991).
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
5. Correlation between variation in infochemicals from di4erent sources
As outlined above, chemical information from plants, herbivores and carnivores
may be available to herbivores when selecting a host plant. For an overview for
a speci"c system, see Fig. 1. The information may be produced independently by an
organism at each of the three trophic levels (e.g. Prokopy et al., 1984; Ho!meister and
Roitberg, 1997; Schoonhoven et al., 1998), or the information may be a product of an
interaction of organisms of the same or di!erent trophic levels (e.g. Pickett et al., 1992;
Dicke and Vet, 1999). In other instances, it remains unknown who produced the
infochemical used by the herbivores (e.g. Quiroz et al., 1997). Moreover, the presence
and abundance of information from these three major sources may be also correlated.
For instance, there may be a negative correlation between direct and indirect
plant defence and thus between plant secondary chemicals and carnivore cues
Fig. 1. Example of information from di!erent trophic levels that is known to a!ect host-selection behaviour
of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Arrows indicate information that
a!ects spider-mite behaviour, while accompanying numbers refer to the trophic level of the organism that
produces the information. 1: Volatiles from undamaged Lima bean plants (Phaseolus lunatus) (Dicke, 1986);
1a: spider-mite-induced volatiles emitted by Lima bean plants (Dicke, 1986) or cucumber plants (Pallini
et al., 1997); 1b: thrips (Frankliniella accidentalis)-included volatiles emitted by cucumber plants (Pallini
et al., 1997); 2: cues from spider mite eggs or adults (Grostal and Dicke, 1999a); 2a: predatory mites
(Phytoseiulus persimilis) are likely to induce an alarm pheromone in adult spider mites (Janssen et al., 1997)
that a!ects spider mite behaviour (Pallini, 1998); 3: the predatory mite P. persimilis produces a non-volatile
cue that a!ects spider mite foraging behaviour (Kriesch and Dicke, 1997; Grostal and Dicke, 1999a,b) and
a volatile cue that can a!ect alarm-pheromone emission by spider mites (Janssen et al., 1997).
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
609
(Vrieling et al., 1991; Heil et al., 1999). In an analysis of the variation in pyrrolizidine
alkaloids in Senecio jacobaea and associated herbivore numbers, Vrieling et al. (1991)
found that plants with high concentrations of pyrrolizidine alkaloids had low numbers of aphids and aphid-tending ants and vice versa. The aphid-tending ants attack
caterpillars of the specialist lepidopteran herbivore Tyria jacobaeae that is not a!ected
by di!erences in pyrrolizidine alkaloids-levels. Thus, plants with low amounts of
pyrrolizidine alkaloids may be contaminated with large amounts of carnivore infochemicals, while plants with large amounts of pyrrolizidine alkaloids may have low
amounts of carnivore cues.
Herbivore pheromones may be positively correlated with certain plant volatiles
because these plant cues induce pheromone emission by the herbivore (McNeil and
Delisle, 1989; Raina et al., 1991).
A question that has not received attention so far in the literature, is whether plants
may respond to the presence of carnivorous arthropods. Plants may constitutively
provide shelter and alternative food for carnivores (Koptur, 1992; Walter, 1996) which
can result in the presence of carnivores in the absence of herbivores. If plants can
perceive the presence of the carnivores, e.g. by perceiving the removal of alternative
food or by perceiving faeces of the carnivores, could this have an e!ect on their
induced responses to herbivores? For instance, would the investment in induced
volatiles be negatively correlated with the presence of carnivorous arthropods? This
might enable plants to reduce the exploitation of induced volatiles by herbivores. Such
an ability of plants may seem to be far-fetched at "rst. However, the extensive
information on the responses of plants to information from competing plants, herbivores and pathogens even in the absence of damage (Blaakmeer et al., 1994; Bruin
et al., 1995; Karban and Baldwin, 1997; Shulaev et al., 1997; van Loon, 1997; BallareH ,
1999) should make us careful not to underestimate the abilities of plants to respond to
biotic components in the environment.
6. Integration of information from di4erent trophic levels during host-plant selection
Infochemicals available to foraging herbivores may be induced by herbivores in
plants (e.g. induced direct defence) or by carnivores in herbivores (e.g. alarm
pheromones) and thus these cues represent an integration of information from
di!erent trophic levels (see above). Moreover, the behaviour of arthropods to infochemicals is phenotypically plastic and the response to an information source may
be dependent on e.g. physiological state, previous experiences and abiotic conditions
(for reviews see e.g. Jaenike, 1988; Papaj and Prokopy, 1989; Jaenike and Papaj, 1992;
Papaj and Lewis, 1993; Bernays, 1995; Robertson et al., 1995; Vet et al., 1995; Dicke
et al., 1998). Through associative learning herbivorous arthropods may integrate
di!erent types of information from plants, such as plant odour and plant shape
(Jaenike, 1988; Papaj and Prokopy, 1989; Szentesi and Jermy, 1990). In addition, also
information from competitors or predators might be integrated through associative
learning, although hardly any studies have been made on this to date (but see
Mallet et al., 1987; Dukas, 1998). Recent evidence on the availability of carnivore
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M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
infochemicals to herbivores (Ho!meister and Roitberg, 1997; Grostal and Dicke,
1999a,b) suggests that this will be a fruitful area for further investigation.
Herbivores may integrate information perceived simultaneously from di!erent
sources. For instance, the response to sex pheromones can be modulated by infochemicals from host plants present (Dickens et al., 1993; Landolt et al., 1994; Lilley
and Hardie, 1996). Furthermore, the response by herbivores to infochemicals emitted
by herbivores or by herbivore-infested plants can be dependent on the amount of
these cues relative to the amount of infochemical from uninfested plants (Dicke 1986;
Pettersson et al., 1998).
To foraging herbivores, plants represent a resource that has a value in terms of food,
competitors and natural enemies. Food selection has often been studied in a bitrophic
context, where the food quality in terms of its e!ect on herbivore "tness was
considered. Alternatively, consequences of host-plant selection for defence of herbivores against their enemies have been considered (Barbosa, 1988a; Bernays and
Graham, 1988; Pasteels et al., 1988; Rowell-Rahier and Pasteels, 1992). It will be
important to include studies on herbivore behaviour in situations with con#icting
alternatives derived from combinations of costs and bene"ts related to food, competitors and enemies. For instance, what decisions does a herbivore make when the
alternatives are an inferior host plant without carnivore cues versus a superior host
plant with abundant carnivore cues? Are the decisions di!erent for specialist and
generalist herbivores? Is the preference of specialist insects for plants containing
secondary chemicals that can be exploited in defence against carnivores di!erent in
the presence or absence of predator cues? Such research questions are an exciting part
of behavioural ecology (e.g. Krebs and Davies, 1984; Courtney, 1986; Godin and
Sproul, 1988; Anholt and Werner, 1995; Gotceitas et al., 1995; Bouskila et al., 1998)
that deserve the incorporation of a chemical ecological approach on the role of
infochemicals in host plant selection by herbivores.
7. Herbivores, information networks and food webs: conclusions
The study of foraging behaviour of carnivorous arthropods has made tremendous
progress in the past two decades by proceeding from a bitrophic perspective to
a multitrophic perspective. Considering the importance of plant information in
foraging strategies of carnivores has created a completely new view on the organisation of food webs (Price, 1981; Dicke et al., 1990; Vet and Dicke, 1992; Tumlinson
et al., 1993; Turlings et al., 1993,1995; Bruin et al., 1995; Takabayashi and Dicke, 1996;
Janssen et al., 1998; Powell et al., 1998; Dicke and Vet, 1999; Sabelis et al., 1999).
It is clear that an information web is superimposed on a food web and that the
information web creates many indirect interactions in addition to the mostly trophically based direct interactions (Vet and Dicke, 1992; Janssen et al., 1998; Dicke and
Vet, 1999).
Host-plant selection by herbivores has been considered in a bitrophic context for
a long time. A vast majority of literature exists, especially devoted to the role of plant
information. Despite this abundant knowledge on the role of plant chemicals and the
M. Dicke / Biochemical Systematics and Ecology 28 (2000) 601}617
611
acknowledgement that plant chemistry is of signi"cant importance in host selection
by herbivorous arthropods, major questions remain unanswered (e.g. Courtney and
Kibota, 1990). Alternative approaches to the study of host-plant selection by herbivores, such as expressed in the seminal paper by Bernays and Graham (1988) have met
with mixed responses (e.g. Barbosa, 1988b; Courtney, 1988; Ehrlich and Murphy,
1988; Jermy, 1988; Schultz, 1988; Thompson, 1988a). However, if an extensive chemical information network exists with information on plant presence and nutritional
quality, on competitor abundance and identity and on chances of encountering
enemies, why would herbivores not exploit this information? At the very least, the
importance of this information network for foraging behaviour of herbivores deserves
to be investigated. This should be done both in laboratory studies and in "eld studies.
A majority of studies on host-plant selection by herbivores has been executed in the
laboratory and future laboratory studies will continue to be important to determine
the options available to herbivores. In addition, "eld studies should be carried out to
reveal to what extent the potential of decision-making that has been recorded in the
laboratory can play a role under "eld conditions where conditions are much more
variable in many respects. Taking a multitrophic approach to herbivore host-selection
behaviour will improve our knowledge and will make an important contribution to
solving several of the questions on host selection by herbivores that are still open. In
doing so, students of host selection by herbivorous arthropods will make new
contributions to evolutionary ecology, behavioural ecology and chemical ecology.
Acknowledgements
The manuscript bene"ted from constructive comments on an earlier version by
Joop van Loon, Bernie Roitberg, Louis Schoonhoven and Louise Vet. MD was
funded in part by the Uyttenboogaart-Eliasen Foundation, Amsterdam.
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