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2
Recruitment of predators and parasitoids by
herbivore-injured plants
Ted C. J. Turlings
Institute of Zoology, University of Neuchatel, Switzerland
Felix W¨ackers
Netherlands Institute of Ecology, Heteren, the Netherlands
Introduction
In recent years, induced plant defenses have received widespread attention from
biologists in a variety of disciplines. The mechanisms underlying these defenses
and the interactions that mediate them appeal not only to plant physiologists, ecol-
ogists, and evolutionary biologists but also to those scientists that search for novel
strategies in plant protection. Several recent books (Karban and Baldwin, 1997;
Agrawal et al., 1999) and reviews (Baldwin, 1994; Karban et al., 1997; Agrawal
and Rutter, 1998; Agrawal and Karban, 1999; Baldwin and Preston, 1999; Dicke
et al., 2003) have been devoted entirely to the subject of induced plant defenses.
Various forces, ranging from abiotic stresses to biotic factors such as pathogens,
arthropods, or higher organisms, may trigger different plant defense responses. Yet,
the biochemical pathways that are involved appear to show considerable similari-
ties. This is also true for the so-called indirect defenses.
The term indirect defense refers to those adaptations that result in the recruitment
and sustenance of organisms that protect the plants against herbivorous attackers.
The early published examples of indirect defenses involved intimate plant–ant inter-
actions, in which myrmecophilous plants were shown to have evolved a range of
adaptations providing ants with shelter (domatia) and various food sources (Belt,
1874; Janzen, 1966). In return, these plants may obtain a range of benefits because
ants can provide nutrition (Thomson, 1981) or more commonly, protection against
herbivores, pathogens, and competing plants (e.g. Koptur, 1992; Oliveira, 1997).
The well-documented fitness benefits of ant attendance in myrmecophilous plants
(Rico-Gray and Thien, 1989; Oliveira, 1997), combined with the fact that doma-
tia and food supplements are difficult to reconcile with other functions, are con-
vincing arguments for the interpretation that these adaptations represent examples
Advances in Insect Chemical Ecology, ed. R. T. Card´e and J. G. Millar. Published by Cambridge University
Press. CCambridge University Press 2004.
21
22 T. C. J. Turlings and F. W¨
ackers
Fig. 2.1. Extrafloral nectar droplets on Ricinus communis (castor bean).
of indirect defense. The above-mentioned studies have all focussed on intimate
examples of plant–ant mutualisms. However, similar adaptations are also found
in non-myrmecophilous plants. Acarodomatia have been recorded from so-called
“mite plants.” These preexisting structures facilitate symbiotic interactions with
predatory or fungivorous mites (Bakker and Klein, 1992; Whitman, 1994).
Extrafloral nectaries (Fig. 2.1) are probably the most frequently described adap-
tations believed to serve as indirect defenses. They have been described in approx-
imately 1000 species from 93 plant families including numerous dicotyledonous
species, ferns, and such diverse monocotyledonous taxa as lilies, orchids, sedges,
and grasses (Koptur, 1992). They are found in virtually all plant types including
herbs, vines, shrubs and trees, annuals as well as perennials, and successional as
well as climax species.
Often extrafloral nectaries show prominent colorations (primarily black and red),
which set them off against the (green) background. In contrast to their floral coun-
terparts, extrafloral nectaries are generally exposed (Zimmerman, 1932), giving
insects easy access to the nectar. The nectaries are often situated on leaves or peti-
oles (Fig. 2.1), where they are ideally situated for crawling insects or flying insects
that land on the leaf surface (Fig. 2.2). In other plants, they are found on petioles or
the (leaf) stem, which is an effective placement for ants and other natural enemies
crawling up the plant.
Less evident is the primary function of plant odor emissions. Although it is clear
that plant odors are used by parasitoids (Fig. 2.3) and predators to locate potential
prey (Vinson et al., 1987; Nordlund et al., 1988; Whitman, 1988), they are likely to
have other functions as well (Harrewijn et al., 1995; Turlings and Benrey, 1998).
Predator/parasitoid recruitment by herbivore-injured plants 23
Fig. 2.2. A female of the parasitoid Cotesia glomerata feeding on extrafloral nectar
of Vicia faba.
Yet, the notion that plant volatiles may serve as signals to recruit members of the
third trophic level has been reinforced by the fact that they are inducible. So far,
evidence for plant-produced signals has been limited to interactions between plants
and arthropods, but a recent study showed that plants may also recruit nematodes
that can infect beetle larvae feeding on the roots of these plants (van Tol et al., 2001).
The accumulating evidence strongly suggests that herbivore-induced plant signals
play a very important role in the indirect protection of plants against herbivory.
The increasing number of studies on the interactions between plants and the
natural enemies of herbivores attacking these plants is revealing an astonishing
sophistication. This is most apparent in the specificity of the interactions; plants may
respond differently to different herbivores and the natural enemies are able to distin-
guish among these differences (Sabelis and van de Baan, 1983; Takabayashi et al.,
24 T. C. J. Turlings and F. W¨
ackers
Fig. 2.3. A female of the parasitoid Cotesia marginiventris attracted to the odor
emitted by a maize leaf that has been damaged by a Spodoptera exigua larva.
1995; Powell et al., 1998; De Moraes et al., 1998). There is even evidence to sug-
gest that plants selectively employ direct and indirect defenses depending on which
herbivore feeds on them (Kahl et al., 2000). An additional twist to the refinement of
the interactions is that there is now clear evidence for information transfer among
plants mediated by volatile signals (Arimura, et al., 2000a; Dolch and Tscharntke,
2000; Karban et al., 2000). These potent plant signals can be expected to affect
multiple interactions within entire food webs (Janssen et al., 1998; Sabelis et al.,
1999) and many more interchanges are likely to be discovered.
This chapter gives an overview of the developments in research on induced
indirect defenses. We discuss both the ecological aspects as well as our knowledge
of the mechanisms that are involved. This chapter differs from most other reviews
in that it includes both attraction by means of induced volatiles and the plant’s
Predator/parasitoid recruitment by herbivore-injured plants 25
strategy to keep the natural enemies of the predator on the plant by increased nectar
production in response to herbivory. We compare these two strategies, particularly
in terms of timing and specificity of induction. We argue that there is a danger of
overinterpreting results if we do not always recognize the fact that plants need to
benefit from the proposed function of the induced responses. Hence, our discussion
of how natural selection may have shaped the various interactions emphasizes
the role of the plant and to what extent its interests are in tune with those of the
third trophic level. Some recent studies provide evidence for the adaptiveness of
inducible indirect defenses, but it is concluded that field experiments, preferentially
with natural systems, are needed to establish truly if plants do benefit from these
inducible responses. Field data are also still lacking for a conclusive appreciation
of the full potential of exploiting indirect plant defenses in the protection of crop
plants.
Inducible volatile signals
The role of plant volatiles as prey and host location cues
The evolutionary “cat-and-mouse game” between entomophagous insects and their
prey has led to various refined adaptations on both sides. Potential prey may min-
imize the encounter rates with their natural enemies by being cryptic, visually as
well as chemically. Although various natural enemies make use of prey-derived
cues (for review see Tumlinson et al., 1992), others have evolved to rely primar-
ily on indirect cues that may be less efficient but are more readily available and
detectable (Vet et al., 1991; Vet and Dicke, 1992). For the many natural enemies
of herbivores, the plants on which the herbivores feed play a key role in providing
useful cues.
That predators and especially parasitoids of herbivores are attracted to plants
has long been known. In their review of this topic, Nordlund et al. (1988) suggest
that Picard and Rabaud (1914) were the first to realize the importance of plants
for foraging entomophagous insects. In numerous studies since (e.g., Taylor, 1932;
Zw¨olfer and Kraus, 1957; Salt, 1958; Harrington and Barbosa, 1978), predators and
parasitoids were found more on one plant species than another. That plant volatiles
may be responsible for such differential attractiveness was apparent from studies
by, among others, Monteith (1955), Arthur (1962), Flint et al. (1979), and Elzen
et al. (1984). These studies considered the importance of the plant only at the level
of habitat locations, as defined by Vinson (1981). It was not until papers by Price
et al. (1980), Vinson (1981), and Barbosa and Saunders (1985) that the more direct
role of plants in mediating the step of host/prey location was considered. Initial
studies suggested only that insect-derived attractants (kairomones) were affected
by the plant diet of the host or prey (e.g., Roth et al., 1978; Sauls et al., 1979;
26 T. C. J. Turlings and F. W¨
ackers
Loke et al., 1983). For instance, parasitoid females tend to respond more strongly
to feces from host larvae that have fed on their customary host plant than to feces
from larvae fed on an artificial diet (Roth et al., 1978; Sauls et al., 1979; Mohyuddin
et al., 1981; Nordlund and Sauls, 1981).
The first series of studies to provide complete behavioral as well as chemical
evidence for the ability of herbivore-injured plants actively to attract natural ene-
mies of their predators was obtained with studies on plant–mite interactions (e.g.,
Sabelis and van de Baan, 1983; Dicke and Sabelis, 1988; Dicke et al., 1990a,b).
First, it was found that plants infested with spider mites were far more attractive
to predators than were uninfested plants (Sabelis and van de Baan, 1983). Subse-
quently, Dicke and Sabelis (1988) showed the presence of several unique volatile
substances in the headspace collections of lima bean leaves infested with the spider
mite Tetranychus urticae. These volatiles were not emitted by the spider mites but
by the infested plant. Synthetic versions of some of these substances, which were
not present in the collections from uninfested plants, were attractive to the preda-
tory mite Phytoseiulus persimilis. These first studies and many since (e.g., Dicke
et al., 1990a,b; Takabayashi et al., 1991a, 1994; Scutareanu et al., 1997) show that
P. persimilis and various other predators that use phytophagous mites as prey make
effective use of a specific blend of mite-induced compounds to locate plants with
prey. This well-studied model system has proven very valuable in revealing the
intricacies and complexity of a multitude of interactions that can be affected by the
herbivore-induced plant volatiles (Janssen et al., 1998; Sabelis et al., 1999).
The majority of other studies that show conclusively that herbivory induces
plants to emit volatiles that may serve as an indirect defense involving the attrac-
tion of parasitoids (Table 2.1). In particular, studies with caterpillars on cotton
(McCall et al., 1993, 1994; Loughrin et al., 1994, 1995a; R¨ose et al., 1996),
Brassica spp. (Steinberg et al., 1992; Agelopoulos and Keller, 1994; Mattiacci
et al., 1994; Geervliet et al., 1994; Benrey et al., 1997), and maize (Turlings et al.,
1990, 1991a,b, 1995; Takabayashi et al., 1995; Potting et al., 1995; Alborn et al.,
1997) have revealed that caterpillar damage results in the release of parasitoid
attractants. In most cases, injury by caterpillars was found to cause a much stronger
reaction in terms of odor emissions than mechanical damage. Relatively new is
the finding that egg deposition by herbivores on plants can cause plants to release
volatiles that are attractive to egg parasitoids (Meiners and Hilker, 1997, 2000;
Meiners et al., 2000). The plant response to egg deposition also appears to be
systemic (Wegener et al., 2001).
Many additional studies show that herbivore-induced emissions of volatiles are
very common and are found in a wide range of plant taxa, induced by numerous
herbivorous arthropods, and affect many different natural enemies (Table 2.1). The
list in Table 2.1 is not meant to be complete but rather to illustrate how common these
Table 2.1. Examples of predators and parasitoids that use induced plant odors to locate their prey or hosts
Natural enemy Herbivore(s)aPlant(s) Evidence Selected references
Predators
Acari: Phytoseiidae
Phytoseiulus persimilis Tetranychus urticae (Acari:
Tetranychidae)
Apple, cucumber,
gerbera, lima bean
B+C Dicke et al., 1990a,b; Takabayashi et al.,
1991a,b; Shimoda et al., 1997; Krips
et al., 2001
Amblyseius andersoni Tetranychus urticae (Acari:
Tetranychidae)
Lima bean B +C Dicke et al., 1990a; Dicke and
Groeneveld, 1986
Amblyseius finlandicus Tetranychus urticae (Acari:
Tetranychidae) Panonychus
ulmi (Acari: Tetranychidae)
Apple B +C Sabelis and van de Baan 1983;
Takabayashi et al., 1991a
Coleoptera: Cleridae
Thanasimus dubius Ips pini (Coleoptera: Scolytidae) Pine B Aukema et al., 2000
Thysanoptera: Thripidae
Scolothrips takahasshi Tetranychus urticae (Acari:
Tetranychidae)
Lima bean B +C Shimoda et al., 1997
Hemiptera: Anthocoridae
Orius laevigatus Frankliniella occidentalis Cucumber B Venzon et al., 1999
Hemiptera: Miridae (Thysanoptera: Thripidae)
Tetranychus urticae (Acari:
Tetranychidae)
Cyrthorinus lividipennis Nilaparvata lugens (Homoptera:
Delphacidae)
Rice B Rapusas et al., 1996
Hemiptera: Pentatomidae
Perillus bioculatus Leptinotarsa decemlineata
(Coleoptera; Chrysomelidae)
Potato B +C van Loon et al., 2000a; Weissbecker
et al., 2000
Parasitoids
Hymenoptera: Braconidae
Apanteles (Cotesia) sp. Ectropis obliqia Tea B /C Xu and Chen, 1999
Apanteles (Cotesia)
chilonis
Chilo suppressalis Rice B Chen et al., 2002
Coeloides bostrichorum Ips typographus (Coleoptera:
Scolytidae)
Spruce B +C Pettersson et al., 2001
(cont.)
Table 2.1.(cont.)
Natural enemy Herbivore(s)aPlant(s) Evidence Selected references
Cotesia glomerata,
Cotesia rubecula
Pieris spp. Cabbage and related
subspecies
B+C Steinberg et al., 1993; Angelopoulos and
Keller, 1994; Mattiacci et al., 1994,
1995
Cotesia kariyai Pseudaletia separata
Mythimna separata
Maize, kidney bean,
Japanese radish
B+C Takabayashi et al., 1995; Fujiwara et al.,
2000
Diachasmimorpha
longicaudata
Anastrepha spp. (Diptera:
Tephritidae)
Mango, grapefruit B Eben et al., 2000
Macrocentrus grandii Ostrinia nubilalis Maize B +C Udayagiri and Jones, 1992a,b
Microplitis croceipes Helicoverpa and Heliothis spp. Cotton, cowpea,
maize
B+C McCall et al., 1993; Turlings et al.,
1993a; R¨ose et al., 1996
Microplitis demolitor Pseudoplusia includens Plant volatiles C Ramachandran and Norris, 1991
Hymenoptera: Mymaridae
Anagrus nilaparvatae Nilaparvata lugens (Homoptera:
Delphacidae)
Rice B Lou and Cheng, 1996
Hymenoptera: Aphidiidae
Aphidius ervi Acyrthosiphon pisum
(Homoptera: Aphididae)
Broad bean B +CDuet al., 1996; Powell et al., 1998
Hymenoptera: Eulophidae
Diglyphus isaea Liriomyza trifolii (Diptera:
Agromyzidae)
Bean B +C Finidori-Logli et al., 1996
Oomyzus gallerucae Xanthogaleruca luteola
(Coleoptera: Chrysomelidae)
Elm B +C Meiners and Hilker, 1997, 2000;
Wegener et al., 2001
Hymenoptera: Pteromalidae
Rhopalicus tutela Ips typographus (Coleoptera:
Scolytidae)
Pine B +C Pettersson, 2001
Hymenoptera: Scelionidae
Trissolcus basalis Nezara viridula (Hemiptera:
Pentatomidae)
Soybean B Loch and Walter, 1999
aIf not otherwise indicated the hosts or prey are lepidopteran larvae.
B, behavioral evidence; C, chemical evidence.
Predator/parasitoid recruitment by herbivore-injured plants 29
tritrophic interactions are. The evidence is not equally conclusive in all cases, but
behavioral observations and/or chemical analyses strongly indicate that induced
plant volatiles play a key role in host or prey location. Current research in this
area focusses on the mechanisms of induction and on questions concerning the
ecological significance and evolutionary history of these interactions, as well as
on the possibility of exploiting this indirect plant defense for crop protection. We
attempt to give an overview of the most significant findings of these research efforts.
Elicitors and induction mechanisms
Mere mechanical damage of leaves may result in the temporary emission of some
volatiles, but in most cases these emissions can be greatly enhanced and prolonged
by eliciting factors that come directly from a feeding insect. These factors also
elicit odor emissions when undamaged leaves take them up via the petiole, and
the response to these factors has been shown to be systemic (Dicke et al., 1990a;
Turlings et al., 1993a). After the isolation and identification of a β-glucosidase
(Mattiacci et al., 1995) and the fatty acid derivative volicitin (Alborn et al., 1997)
as elicitors from caterpillar oral secretion (regurgitant), a multitude of studies have
revealed details about the mechanisms that may mediate the formation and action
of these compounds. Notably the groups of Tumlinson (Gainesville, Florida) and
Boland (Jena, Germany) have made considerable progress in these areas, as sum-
marized below.
Beta-glucosidase
Aβ-glucosidase in the regurgitant of Pieris brassicae larvae causes a release of
volatiles in brassica plants that is similar to the release observed after feeding by
these larvae (Mattiaci et al., 1995). Beta-glucosidases are present in many organ-
isms (e.g., Robinson et al., 1967; Sano et al., 1975; Wertz and Downing, 1989;
Yu, 1989) and may function in catalyzing biochemical pathways that involve gly-
coside cleavage. The emissions by Brassicaceae are characterized by glucosinolate
breakdown products, which have not been observed in other plant families that
have been studied in this context (Agelopoulos and Keller, 1994; Mattiaci et al.,
1994; Geervliet et al., 1996). It is expected that enzymes like β-glucosidase facil-
itate this glucosinolate breakdown. This notion is reinforced by the fact that a
systemic emission after caterpillar feeding is only observed if the distant leaves are
mechanically damaged (L. Mattiaci, personal communication), suggesting that the
substrate comes in contact with enzymes only when it is released from ruptured
cells. The key enzyme involved in the hydrolysis of glucosinolates is myrosinase,
which causes the release of volatile defensive compounds such as isothiocyanates
(Bones and Rossiter, 1996). The bioactivity of enzymes in the oral secretions of
insects as inducers of volatile emissions may be limited to specific plant taxa.
30 T. C. J. Turlings and F. W¨
ackers
Volicitin
Incubation of young maize plants in the regurgitant of several lepidopteran larvae
and a grasshopper was found to induce the release of a blend of terpenoids and
indole that is typical for plants with caterpillar damage (Turlings et al., 1993a).
Similarly, Potting et al. (1995) found that stemborer regurgitant applied to mechan-
ically damaged sites caused an increase in induced odor emissions in maize plants.
In both cases, induced plants were more attractive to parasitoids than plants that
were not induced.
Volicitin (N-(17-hydroxylinolenoyl)-l-glutamine) was identified by Alborn et al.
(1997) as the active substance in the regurgitant of Spodoptera exigua larvae. Low
concentrations of this elicitor alone cause the same reaction in maize plants as pure
regurgitant and render the plants equally attractive to the parasitoids (Turlings et al.,
2000). So far, volicitin has only been shown to be active in maize (Turlings et al.,
2002) and does not induce a reaction in, for instance, lima bean (Koch et al., 1999).
Studies of the source and biosynthesis of volicitin revealed that this fatty acid
derivative is formed in the bucal cavity of the insect (Par´e et al., 1998). Linolenic
acid, the fatty acid part of volicitin, is ingested with plant material and is then
17-hydroxylated and conjugated with insect-derived glutamine (Par´eet al., 1998).
Spiteller et al. (2000) showed that bacteria isolated from caterpillar gut contents are
able to synthesize volicitin and other N-acylglutamine conjugates from externally
added precursors. Hence, it is not necessarily the plant or the insect that controls the
biosynthesis of volicitin. It remains surprising, however, that the insects “allow” the
synthesis of elicitors that trigger plant reactions with such negative consequences
for the insect. It is, therefore, expected that these metabolites play an essential
role in the insects’ physiology. Perhaps they serve as surfactants that facilitate the
transport and digestion of food, or they may neutralize the effects of plant toxins
(Alborn et al., 2000; Spiteller et al., 2000). Numerous N-acylglutamates that may
show elicitor activity (Halitschke et al., 2001) occur in the oral secretions of various
insects (Pohnert et al., 1999; Spiteller et al., 2000).
Not surprisingly, some factors in the oral secretions of caterpillars may suppress
induced plant defenses (Felton and Eichenseer, 2000). Musser et al. (2002) elegantly
showed that the enzyme glucose oxidase in the saliva of Helicoverpa zea counteracts
the induced production of nicotine. The presence of such suppressing agents would
explain the fact that the isolated active fraction containing volicitin showed more
activity than pure caterpillar regurgitant (Turlings et al., 2000).
Elicitors from plants
Plant hormones with various functions have been identified over the years and an
increasing number of studies show that they may also affect volatile emissions
Predator/parasitoid recruitment by herbivore-injured plants 31
(Farmer, 2001). Even nectar production may be effected by such hormones (Heil
et al., 2001). The gaseous hormone ethylene plays an important role in plant
development, but also in defense (Mattoo and Suttle, 1991). Upon perception of a
pathogen, plants show enhanced ethylene production, which has been shown to be
involved in the induction of defense reactions (Boller, 1991). Wild tobacco plants
engineered with an Arabidopsis sp. ethylene-insensitive gene do not show typi-
cal leaf development arrestment in the presence of leaves of other tobacco plants,
demonstrating the importance of ethylene in plant development (Knoester et al.,
1998). The ethylene-insensitive plants also showed reduced defense protein syn-
thesis and were susceptible to soil pathogens to which they were normally fully
resistant. In connection with the third trophic level, Kahl et al. (2000) found that
attack by Manduca caterpillars on wild tobacco plants causes an ethylene burst that
suppressed induced nicotine production but stimulated volatile emissions. They
argued that the plant “chooses” to employ an indirect defense (the attraction of nat-
ural enemies) rather than a direct defense to which the attacker could adapt (Kahl
et al., 2000; Winz and Baldwin, 2001). This implies that the plant is capable of
identifying its attacker. We discuss this possibility in more detail in the discussion
of specificity.
Studies into the effects and mechanisms of induced resistance against pathogens
and insects have revealed the role of salicylic acid (SA) and jasmonic acid (JA).
These compounds are seen as the key signals for defense gene expression (Reymond
and Farmer, 1998). It was generally thought that SA regulates resistance to fungal,
bacterial, and viral pathogens (Enyedi et al., 1992; Ryals et al., 1996), whereas
JA induces the production of various proteins via the octadecanoid pathway that
provides plants with resistance against insects (Broadway et al., 1986; Farmer
et al., 1992). However, this distinction between the two pathways is not that clear
and pathogens and arthropods may sometimes trigger both (Farmer et al., 1998;
Reymond and Farmer, 1998; Walling, 2000). SA and JA, as well as synthetic mimics,
can be applied exogenously to plants to induce the same metabolic changes that lead
to resistance as induced by pathogens and insects (Ryals et al., 1992; Kessmann
et al., 1994; G¨orlach et al., 1996; Thaler et al., 1996). The two different pathways
that the elicitors stimulate can compromise each other (Doherty et al., 1988). Thaler
(1999) demonstrated this in a field situation, where tomato plants stimulated with a
SA mimic reduced resistance to S. exigua, while JA treatment rendered plants more
vulnerable to the bacterial speck pathogen Pseudomonas syringae pv. tomato.
Treatment with SA, JA, or their mimics can also induce the release of volatiles in
plants, but the blends produced are somewhat different for the two elicitors (Hopke
et al., 1994; Dicke et al., 1993, 1999; Ozawa et al., 2000; Wegener et al., 2001;
Rodriguez-Saona et al., 2001). In a rare field experiment (see below), Thaler (1999)
showed that treatment of tomato plants with JA increased the parasitism rate of
32 T. C. J. Turlings and F. W¨
ackers
caterpillars on the plants, which was most likely the result of JA-induced increases
in odor emissions. The overall evidence clearly indicates that these inducers of
general defense reactions also play a role in volatile signaling.
Arimura et al. (2000a) found that several of the induced volatiles themselves can
serve as elicitors by triggering gene activation in neighboring leaves that leads to
further emissions. In this context, (Z)-jasmone was shown to be a potent plant-
derived volatile elicitor that triggers the release of (E)-β-ocimene in the bean
plant, Vicia faba (Birkett et al., 2000). These examples of plant odours inducing
plant defense pathways have important implications for plant–plant communication
(see below).
Pathogen-derived elicitors
Cellulysin is a fungus-derived enzyme mixture of exo- and endoglucanases that is
an extremely potent elicitor of plant volatile biosynthesis through the upregulation
of the octadecanoid pathway (Piel et al., 1997). The low-molecular-weight phyto-
toxin coronatin, which is produced by certain bacteria (Bender et al., 1996; Ichi-
hara et al., 1977), is also a strong elicitor of volatile emissions and mimics specific
compounds within the pathway (Weiler et al., 1994; Boland et al., 1995; Sch¨uler
et al., 2001). More recently, a mixture containing the ion channel-forming pep-
tide of the peptaibol class (alamethicin), isolated from the plant parasitic fun-
gus Tricoderma viride, has also been implicated in volatile induction via the
octadecanoid-signaling pathway (Engelberth et al., 2000, 2001). It should be noted
that the induced volatile blends show considerable differences for the different
elicitors. In lima bean, alamethicin only induces the production of the two com-
mon homoterpenes (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) and (3E,7E)-4,8,
12-trimethyl-1,3,7,11-tridecatetraene (TMTT), and of methyl salicilate. These com-
pounds are barely induced after treatment with JA or cellulysin, which stimulate
the production of other inducible volatiles (Engelberth et al., 2001). Coronatin and
its synthetic mimic coronalon induce the production of a complete blend of all
these compounds (Sch¨uler et al., 2001). The common elicitation of volatile syn-
thesis by pathogens is likely to affect insect induction if simultaneous infections
occur and should be considered in future studies on variability and specificity of
plant-provided signals (see below).
The genetic basis for induction
Common elicitors like JA and SA and knowledge about the biochemical pathways
that they induce are used to identify the plant genes that are involved in the induc-
tion process (Reymond et al., 2000). Various genes that are induced by JA and
related compounds have been identified (Reymond and Farmer, 1998; Stinzi et al.,
2001) and several of these genes can also be activated by some of the induced
Predator/parasitoid recruitment by herbivore-injured plants 33
volatiles themselves (Arimura et al., 2000a). However, very little is known about
the genes that code for the enzymes involved in the direct synthesis of specific
induced volatiles.
One of the main substances induced in maize by volicitin is indole, an inter-
mediate in at least two biosynthetic pathways. Frey et al. (2000) identified a new
enzyme, indole-3-glycerol phosphate lyase, which converts indole-3-glycerol phos-
phate to free indole. They found that the corresponding gene igl is selectively
activated by volicitin. This differs from previously known enzymes like BX1,
which catalyzes the conversion of indole-3-glycerol phosphate to indole to form the
secondary defense compounds DIBOA (2,4-dihydroxy-2H-1,4-benzoxazin-3(4H)-
one) and DIMBOA (2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one), or
tryptophan synthase, which produces the amino acid trytophan (Frey et al., 1997).
The selective activation of the evolutionarily similar genes igl and bx1 strongly
suggests that the plants are capable of selecting which induced defense to use
depending on the attacking species.
Volicitin has also been shown to activate a specific maize sesquiterpene cyclase
gene, stc1, which is also activated in response to caterpillar feeding or regurgitant
treatment (Shen et al., 2000). The transcription of stc1 results in the production of a
naphtalene-based sesquiterpenoid, which we have not yet detected from the many
maize lines we have studied (e.g., Gouinguen´e et al., 2001). It would be interesting
to see if this volicitin-induced substance shows attractiveness to natural enemies of
the caterpillars that induce its production.
One of the terpenoids that is almost always found in induced odor blends of
many plants species is the acyclic C11 homoterpene DMNT (Boland et al., 1992;
Dicke, 1994). Biosynthesis of DMNT proceeds via (E)-nerolidol, a sesquiterpene
alcohol (Boland and G¨abler, 1989; Donath and Boland, 1994; Degenhardt and
Gershenzon, 2000). Degenhardt and Gershenzon (2000) demonstrated the activity
ofa(E)-nerolidol synthase that converts farnesyl bisphosphate, a common precursor
of sesquiterpenes, to (3S)-(E)-nerolidol in maize leaves after the leaves had been
damaged by Spodoptera littoralis larvae. Activity of (E)-nerolidol synthase has also
been shown in lima bean and cucumber leaves in response to spider mite feeding
on these leaves (Bouwmeester et al., 1999). (E)-Nerolidol synthase appears to
be specifically committed to the formation of DMNT and could play a key role
in determining the attractiveness of herbivore-injured plants to natural enemies
(Degenhardt and Gershenzon, 2000).
The apparent selective activation of genes responsible for induced odor produc-
tion and the committed function of the resulting enzymes may allow for a precise
fine tuning between insect-derived elicitors and the responses of the plant. Thus,
plants have the potential to adapt their signals specifically to the insect that feeds
on a plant. Several studies present evidence for such specificity.
34 T. C. J. Turlings and F. W¨
ackers
Specificity
If plants respond differentially to different herbivores, producing a distinct blend
of volatiles in each case, the signals may provide the natural enemies with specific
information on the identity and perhaps even stage of the herbivores present on
a plant. Evidence for and against such specificity is accumulating. Dicke (1999)
has listed various examples that indicate specificity as well as those that suggest
a lack of specificity. For instance, Takabayashi et al. (1995) found that only the
1st through the 4th instar larvae of Pseudaletia separata (Lepidoptera: Noctuidae)
induced a significant production of volatiles in maize. In accordance, the parasitoid
Cotesia kariyi is attracted primarily to maize plants eaten by early instar larvae,
which are suitable for parasitization (Takabayashi et al., 1995). However, no such
specificity was found for the interaction between maize plants, larvae of S. littoralis
(Lepidoptera: Noctuidae), and the parasitoid Microplitis rufiventris, which also
attacks only the early stages of this preferred host (Gouinguen´e, 2000).
Other examples of specificity show that different herbivore species cause differ-
ent reactions in a plant. These differences can be in the total quantity of volatiles
released (Turlings et al., 1998) or in actual differences in the composition of the
odor blend (Turlings et al., 1993a; Du et al., 1998; De Moraes et al., 1998). A
very distinct difference occurs in the ratios among typical green leaf volatiles
released by plants damaged by either Spodoptera frugiperda or S. exigua (Turlings
et al., 1993a). Maize damaged by S. frugiperda emitted far more (E)-2-hexenal than
maize damaged by S. exigua. The parasitoid was able to learn to distinguish between
the two types of damage (Turlings et al., 1993a), but it remains unclear whether
(E)-2-hexenal played a role in this. It should be noted that the release of green
leaf volatiles in maize does not appear to be enhanced by elicitors; these volatiles
“bleed” instantanuously from damaged sites.
Learning is not required for the aphid parasitoid Aphidius ervi to recognize pea
plants that are damaged by its specific host, the pea aphid Acyrthosiphon pisum
(Du et al., 1998; Powell et al., 1998). This parasitoid is far more attracted by pea
plants infested by this host than by pea plants infested by a non-host, Aphis fabae.
Implicated in the specificity of the signal is 6-methyl-5-hepten-2-one, a substance
that was only detected in the odor profile of plants infested by A. pisum (Wadhams
et al., 1999); the pure compound was found to be highly attractive to A. ervi (Du
et al., 1998).
Behavioral and chemical evidence for signal specificity was also obtained by
De Moraes et al. (1998). They found that Cardiochiles nigriceps, a parasitoid that
specializes on Heliothis virescens, is much more attracted to plants attacked by its
host than by plants attacked by the closely related non-host H. zea. Volatile collec-
tions from maize and tobacco plants that had been subjected to feeding by these
Predator/parasitoid recruitment by herbivore-injured plants 35
noctuids showed differences in the relative ratios of some of the major compounds.
It remains to be determined whether these observed differences allow C. nigriceps
to recognize plants with hosts.
Two novel studies (Kahl et al., 2000; De Moraes et al., 2001) have reached some
spectacular conclusions concerning specific responses to insect feeding. Kahl et al.
(2000) showed that wild tobacco, Nicotiana attenuata, does not increase its pro-
duction of nicotine after it has been damaged by nicotine-tolerant Manduca sexta
caterpillars. Any other form of damage is known to result in the accumulation of
nicotine in this plant, through stimulation of the JA signal cascade. It was subse-
quently confirmed that an ethylene burst resulting from M. sexta feeding suppressed
nicotine production (Winz and Baldwin, 2001). The authors suggested that the plant
chooses not to use its direct defense against this well-adapted adversary but instead
mobilizes a strong indirect defense with the release of considerable amounts of
volatiles that were shown to attract natural enemies (Kessler and Baldwin, 2001).
They also point out that ingested nicotine probably has not much effect on M. sexta
but may negatively affect its natural enemies. Equally interesting is the finding by
De Moraes et al. (2001) that in Nicotiana tabacum the odor emitted after caterpillar
feeding is different during the night than during the day. The day-time volatiles
are known to attract parasitoids (De Moraes et al., 1998), whereas the night time
volatiles repelled female H. viresens moths and kept them from laying eggs on the
emitting plants (De Moraes et al., 2001). Again the plant appears to choose what
and when to emit.
These examples suggest great sophistication in how the plants “choose” to
respond to herbivore attack. However, the ability of natural enemies to take advan-
tage of this specificity may be hampered by the great variability that can be observed
among different genotypes of a plant species in the release of the major volatile
compounds. Possibly, subtle differences in some of the minor compounds play an
important role in determining signal specificity. Below we discuss this genotypic
variation and its implication for the reliability and specificity of herbivore-induced
signals.
Variability
It seems that plant-provided signals are limited in the specific information that they
can provide because of the high variability that is found among plant genotypes
(Takabayashi et al., 1991b; Loughrin et al., 1995a; Gouinguen´e et al., 2001, Krips
et al., 2001). Variation can also be found between plant parts (Turlings et al., 1993b)
and between different growth stages of a plant (Gouinguen´e, 2000). Moreover, many
parasitoids and predators, whether they are generalists or not, can find their hosts or
36 T. C. J. Turlings and F. W¨
ackers
prey on a variety of plant species and each of these has its own characteristic basic
odor blend. Therefore, natural enemies that use plant odors to locate their prey will
need to determine which odors are most reliably associated with a certain prey at a
certain time.
The variation in odor emissions that can be found among plant species is illus-
trated in Fig. 2.4. The chromatograms depict the volatile blends released by four
crop plant species (maize, cotton, cowpea, and alfalfa) at different times after an
attack by the common lepidopteran pest S. littoralis. For this experiment, 2- to 4-
week-old plants that had been grown in pots in a climate chamber were transplanted
into a glass vessel (a cylinder 10 cm in diameter and 45 cm high) the day before
odor collections started. Pure humidified air was pumped into each vessel just above
soil level, while close to the open top of the vessel most of the air was pulled out
through a collection trap. With this technique, which is similar to the one described
by Turlings et al. (1998), the volatiles emitted by each plant were collected for
periods of 3 h. The volatiles were extracted from the traps, two internal standards
were added, and each sample was analyzed on a gas chromatograph coupled to a
mass spectrometer. The top chromatograms in Fig. 2.4 show the odor emissions
before caterpillar attack. Most plants are virtually odorless when undamaged, but
some, like the maize line used here, constitutively release a few substances (e.g.,
linalool and (E,E)-α-farnesene).
After the first 3 h collection, 20 starved 3-day-old S. littoralis larvae were placed
on each plant. A new 3 h collection was started immediately after. As can be seen
in the second chromatogram for each plant, there was considerable variation in
the types of substance that were released by each plant, but all of them released
the highly volatile green leaf odors (e.g., (E)-2-hexenal, (Z)-3-hexenol, and (Z)-3-
hexenyl acetate). These volatiles are characteristic for fresh damage and may play
a common role in the initial attraction of nave natural enemies to damaged plants
(Fritzsche Hoballah et al., 2002) as well as in the location of recently damaged
sites on a plant. Of the plants tested, cotton was the only one that showed an
immediate release of significant amounts of several of terpenoids (e.g., α-pinene,
β-pinene, and caryophyllene). These terpenoids are stored in glands located near the
surface of cotton leaves and are released when the glands are ruptured (Elzen et al.,
1985; Loughrin et al., 1994). In maize, only small amounts of induced terpenoids
were collected during the first hours of attack. We had previously shown (Turlings
et al., 1998) that these are compounds induced after caterpillar damage and that the
reaction in this plant can be observed within hours.
That maize is faster in the production of induced substances than the other plants
is clear from the remaining chromatograms. On the second day of the experiment,
the maize plants showed a full release of all induced substances, while for the other
plants the release takes more time. After 2 days, cotton plants also released induced
Fig. 2.4. Chromatographic profiles of volatiles emitted by four plant species at different time periods after an attack by Spodoptera
littoralis larvae. The labeled peaks are: 1,(Z)-3-hexenal; 2,(E)-2-hexenal; 3,(Z)-3-hexenol; 4,(Z)-3-hexenyl acetate; 5, linalool;
6,(E)-4,8-dimethyl-1,3,7-nonatriene; 7, indole; 8,(E)-β-caryophyllene; 9,(E)-α-bergamotene; 10,(E)-β-farnesene; 11,(E,E)-
α-farnesene; 12, nerolidol; 13,(E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene; 14,α-pinene; 15,β-pinene; 16,β-myrcene; 17,
d-limonene; 18,(E)-β-ocimene; 19,β-sesquiphellandrene; 20, germacrene D. Two internal standards, n-octane and nonyl acetate,
are labeled with IS1 and IS2, respectively.
38 T. C. J. Turlings and F. W¨
ackers
terpenoids (e.g., (E)-β-ocimene, DMNT, (E)-β-farnesene) alongside the ones that
are released constitutively from the glands (see also McCall et al., 1993; Loughrin
et al., 1994; R¨ose et al., 1996). The late reaction in this plant may be a strategy
in which it first relies on its stored defenses and then, when an attack continues,
switches to an induced defense.
The cowpea and especially alfalfa plants released relatively few substances and
in lesser amounts. Parasitoids and predators that can find their victims on all of
these plants will have to deal with all this variability and are likely to show dif-
ferences in their preferences for these odors based on their interactions with cer-
tain plant species over evolutionary time. One behavioral characteristic that has
been frequently shown for parasitoids, and which may help them to deal with this
tremendous variation, is the ability to learn by association. This ability allows par-
asitoid females to change their responses in accordance with the odor cues that
they experience to be most reliably associated with the presence of hosts (Turlings
et al., 1993b; Vet et al., 1995). This associative learning is expected to be impor-
tant for generalist parasitoids, which are unlikely to rely on innate preferences for
specific cues but rather need to establish what cues are most reliably associated
with the presences of suitable hosts at a given time. This may be different for
highly specialized parasitoids such as C. nigriceps, which only attacks H. virescens
(De Moraes et al., 1998). It too relies on plant volatiles for host location but appar-
ently has adapted to respond to subtle differences in the plants’ responses to damage
by different insects. It still has to be determined what these differences are. Studies
on the host-locating behavior of the aphid parasitoid A. ervi suggest that it distin-
guishes between plants that carry host and non-host aphids with the use of a single
compound, 6-methyl-5-hepten-2-one. So far, this compound has only been found
in the odor blend emitted by host-infested plants (Du et al., 1998; Powell et al.,
1998). Further studies with additional plant genotypes and plant species will reveal
if such specific indicators are indeed provided by the plants.
Benefits
Among others, Faeth (1994), van der Meijden and Klinkhamer (2000), and Hare
(2002) have stressed the need for ecological evidence that plants benefit from
recruiting natural enemies of herbivores. Van der Meijden and Klinkhamer (2000),
who focus on parasitoids, criticized the studies that imply mutualistic interactions
between the first and third trophic level. They cite several papers on parasitoids that
may not reduce herbivory in their hosts. Indeed, there are examples where plants
do not benefit from the action of parasitoids (e.g. Coleman et al., 1999), but the
authors overlooked most of the papers that found such a reduction in herbivory
after parasitization (see Beckage, 1985). In fact, van Loon et al. (2000b) pointed
out that all studied solitary parasitoids cause their hosts to feed less, whereas for
Predator/parasitoid recruitment by herbivore-injured plants 39
gregarious parasitoids this can vary. However, a reduction of herbivory does not
necessarily imply a fitness gain for the plant. That plant fitness can indeed increase
as a result of parasitization was convincingly demonstrated by G´omez and Zamora
(1994). They studied the effects of chalcid parasitoids that attack a seed weevil
(Ceutorhynchus sp.) on the fitness of a woody crucifer, Hormathophylla spinosa.
With exclusion experiments in the field, they were able to show that, in the presence
of the parasitoids, plants that were attacked by the weevil produced more seeds
per fruit than weevil-infested plants without parasitoids. The parasitoids reduced
weevil-inflicted seed damage to such an extent that the plants produced almost three
times as much seed (G´omez and Zamora, 1994).
For leaf-feeding insects, which have been most studied in the context of induced
odors that are attractive to parasitoids, such evidence was missing until recently. In
a first study, van Loon et al. (2000b) showed that Arabidopsis thaliana plants
attacked by larvae of Pieris rapae (Lepidoptera: Pieridae) produced consider-
ably more seed when the larvae were parasitized by the solitary endoparasitoid
Cotesia rubecula. We obtained similar results with the maize–Spodoptera system
and found that plants infested with larvae parasitized by Cotesia marginiventris
yielded more seed than those attacked by healthy Spodoptera larvae (Fritzsche
Hoballah and Turlings, 2001). This evidence clearly shows the potential of plant
signals indirectly to reduce herbivory and enhance plant fitness, but it remains to be
seen what the consequences of these interactions are for wild plants in their natural
environment.
Other ecological consequences of induced odor emissions
Attraction or repellence of herbivores by induced plant odors
A limited number of studies have looked at how induced plant volatiles affect the
attractiveness of herbivores. It was found that different herbivores are affected
differently. Landolt (1993) showed that adult females of the cabbage looper,
Trichoplusia ni (Lepidoptera: Noctuidae), may be more attracted to cotton plants
that have already been damaged by its larvae, but they prefer to oviposit on healthy
plants rather than damaged plants. In the case of cabbage plants, cabbage looper
females avoided previously damaged plants altogether (Landolt, 1993). Repellence
of plants that emit herbivore-induced volatiles was also observed for the corn-leaf
aphid Rhopalosiphum maidis. This was demonstrated under laboratory as well as
field conditions (Bernasconi et al., 1998).
Interestingly, Lepidoptera and aphids seem to avoid already infested plants,
whereas Coleoptera are in general attracted to volatiles emitted by plants that are
under attack by conspecifics. This has been shown for scarabaeid (Domek and
Johnson, 1988; Harari et al., 1994; Loughrin et al., 1995b) and chrysomelid beetles
(Peng and Weiss, 1992; Bolter et al., 1997; Kalberer et al., 2001). The Colorado
40 T. C. J. Turlings and F. W¨
ackers
potato beetle, a chrysomelid, is more attracted not only to potato plants damaged
by conspecifics rather than undamaged plants (Bolter et al., 1997; Landolt et al.,
1999) but also to plants treated with insect regurgitant or the synthetic elicitors of
odor emissions volicitin and methyl jasmonate (Landolt et al., 1999), as well as
to plants exposed to damaging ozone levels (Schutz et al., 1995). These beetles
specialize on specific host plants and are well adapted to, and may even exploit,
their hosts’ chemical defenses. Increases in these defensive chemicals in response
to damage or elicitors may not be harmful to these insects. Moreover, beetles
may be less vulnerable to natural enemies, especially if they rely on plant-derived
chemicals for their defense. They may, therefore, be under less or no pressure to
avoid plants that emit attractants for natural enemies. It has been proposed that the
beetles visiting already attacked plants increase their chances of finding a suitable
mate (Loughrin et al., 1995b; Kalberer et al., 2001) and a mass attack may weaken
the plants’ chemical defense potential.
For some herbivores, the responses to herbivore-induced plant odors differ under
different circumstances. For instance, the spider mite T. urticae is more attracted
to healthy lima bean leaves than leaves that emit volatiles induced by spider mite
infestation (Dicke, 1986; Dicke and Dijkman, 1992). However, Pallini et al. (1997)
found that the same mite is attracted to cucumber plants that are already infested
by conspecifics. In contrast, T. urticae avoids the odor of cucumber plants under
attack by the western flower thrips, Frankliniella occidentalis, which is a herbivore
but also feeds on spider mites. Bark beetles can cause strong reactions in their host
trees, resulting in the emission of a blend of volatile terpenoids that, in combination
with aggregation pheromenes, is used in mass attacks. These same substances may
attract predators (Byers, 1989) and parasitoids (Sullivan et al., 2000; Pettersson,
2001; Pettersson et al., 2001) to infested trees.
As yet, there is no specific pattern in how induced volatiles affect the attractive-
ness of plants to herbivores. Obviously, the responses will be correlated with fitness
consequences. Insects vulnerable to natural enemies and induced plant toxins are,
therefore, expected to avoid induced plants, whereas those that are adapted to plant
defenses and/or benefit from aggregating are likely to be attracted. Comparative
studies could test such hypotheses.
Plant–plant “communication”
Evidence for interactions among plants mediated by airborne chemicals was first
obtained some twenty years ago (Baldwin and Schultz, 1983; Haukioja et al., 1985;
Rhoades, 1983, 1985), but skepticism and criticism of methodology and statistical
procedures (Fowler and Lawton, 1985) initially prevented general acceptance by
biologists. Evidence obtained since then has changed this. Ethylene was shown to
activate defense genes (Ecker and Davis, 1987) and, in the seminal paper by Farmer
Predator/parasitoid recruitment by herbivore-injured plants 41
and Ryan (1990), it was shown that methyl jasmonate induced the synthesis of
proteinase inhibitors in tomato plants.
In the spider mite–lima bean system, it has now been shown that mite infestation
activates defense genes in the plants and, in addition, several of these genes can
also be activated when a lima bean plant is exposed to some of the induced volatiles
of neighboring conspecifics (Arimura et al., 2000a,b). Clearly, the genetic basis for
plant–plant communication is in place. That it can actually take place in the field
has now also been confirmed.
Dolch and Tscharntke (2000) studied the effects of artificial defoliation of alder
trees on subsequent herbivory by alder leaf beetle (Agelastica alni). After defoli-
ation, herbivory by A. alni was significantly lower in the defoliated trees and its
neighbors compared with trees distant from the manipulated trees. Laboratory stud-
ies confirmed that resistance was induced not only in defoliated alders but also in
their undamaged neighbors (Dolch and Tscharntke, 2000). Follow-up work showed
that alder leaves respond to herbivory by A. alni with the release of ethylene and of
a blend of volatile mono-, sesqui-, and homoterpenes. This herbivory also increased
the activity of oxidative enzymes and proteinase inhibitors (Tscharntke et al., 2001).
Additional convincing evidence for odor-mediated interactions between plants
comes from a field study by Karban et al. (2000). They showed, over several years,
that clipping sagebrush caused neighboring wild tobacco plants to become more
resistant to herbivores. Preventing root contact between the plants did not change
this effect, but preventing the exchange of volatiles between the plants by enclosing
the clipped shoots in plastic bags did mitigate the effect. The explanation is that the
release of methyl jasmonate by the damaged sagebrush caused an increase in phenol
oxidase in the tobacco plants, rendering them more toxic to herbivores (Karban
et al., 2000). The relevance of such interactions in natural interactions remains to
be elucidated for odor emissions resulting from natural herbivory.
In the context of tritrophic interactions, plant–plant communication has been
subject to only few studies (Bruin et al., 1995). In one such study, Bruin et al. (1992)
demonstrated that healthy cotton plants that were exposed to spider mite-induced
volatiles from conspecific plants increased in their attractiveness to predatory mites.
This increased attraction was probably not simply the result of adsorbence and
re-release of these volatiles from the healthy plants, because there is now clear
evidence that volatiles from spider mite-infested plants can induce odor releases in
neighboring plants (Arimura et al., 2000a).
Inducible nutrition
Although insect predators and parasitoids are carnivorous by definition, they often
also feed on plant-derived foods. This vegetarian side to their diet includes various
42 T. C. J. Turlings and F. W¨
ackers
plant substrates, such as nectar, food bodies, and pollen. In addition, they often
utilize foods indirectly derived from plants (e.g. honeydew, or pycnial fluid of
fungi). In some cases, predators may also feed on plant productive tissue, in which
case they have to be classified as potential herbivores. The level in which predators
or parasitoids depend on primary consumption varies.
Nutritional requirements of natural enemies
Ants display a broad variation in lifestyles, which is reflected in an equally broad
dietary diversity, ranging from species that are primarily predators to species that
rely almost entirely on honeydew and extrafloral nectar. Although it has long been
held that the majority of ant species are predominantly carnivorous (H¨olldobler
and Wilson, 1990; Sudd and Franks, 1987), Tobin (1994) argued that the dominant
species are largely primary consumers, for which the bulk of their diet consists
of plant-derived carbohydrates. An important dichotomy might occur between the
nutrition of immature and mature stages. Ants tend to feed protein-rich food prefer-
entially to their larvae, whereas the adults survive mostly on a diet of plant-derived
carbohydrates (Haskins and Haskins, 1950; Vinson, 1968). Further differentiation
takes place among the adult castes, as it is believed that certain activities such as
foraging, killing, and dismemebering of prey, as well as the transporting of food
items or building material, require most energy (Beattie, 1985). Foraging workers
retain the majority of sugar-rich foods, while passing the bulk of protein-rich food
to castes remaining in the nest (Markin, 1970; Schneider, 1972). The important
role of carbohydrates to ant nutrition was also demonstrated by Porter (1989). He
showed that fire ant colonies kept on insect prey only had a retarded growth and
reproduction rate in comparison with colonies fed both prey and sugar water. It
has been argued that displacement of the native fire ant Solenopsis geminata by
the imported fire ant Solenopsis invicta is partly based on the latter species’ higher
efficacy in collecting liquids such as nectar (Tennant and Porter, 1991). The main
carbohydrate sources exploited by ants are extrafloral nectar (Fisher et al., 1990)
and honeydew, the sugar-rich excretions from sap-feeding insects (Retana et al.,
1987). Interestingly, the use of floral nectar appears to be relatively uncommon
(Tobin, 1994).
While sugar solutions can be a significant item in the diet of ants, parasitoids
are often entirely dependent on carbohydrates as an adult food source (Jervis
et al., 1993). The parasitoids’ longevity and fecundity are usually subject to ener-
getic constraints (Leatemia et al., 1995; Stapel et al. 1997; W¨ackers et al., 2001),
whereas the parasitoids’ behavior can also be strongly affected by their nutritional
state (Takasu and Lewis, 1995; W¨ackers, 1994). There is strong evidence that the
availability of suitable sugar sources can play a key role in parasitoid host dynamics
(Krivan and Sirot, 1997; F. L. W¨ackers unpublished data).
Predator/parasitoid recruitment by herbivore-injured plants 43
Plant-provided nutrition and its functions
Plants employ nutritional supplements in a range of mutualistic interactions. Best
known are the floral rewards targeted at pollinators (Faegri and van der Pijl, 1971),
and the fleshy fruit tissue promoting seed dispersal by vertebrates. Ants as well can
play an important role in the dissemination of seeds. Their tendency to harvest seeds
and to transport them to their (underground) nests makes ants efficient seed dis-
persers (Horvitz and Schemske, 1986; Jolivet, 1998). Some plant species stimulate
this interaction by producing protein- and lipid-rich seed appendages, the so-called
elaiosomes (Milewski and Bond, 1982). Ants collect these seeds preferentially,
consume the nutrient-rich elaiosomes and may subsequently discard the hard seeds
in underground waste dumps. The scarring of the seeds, the moist and nutrient-
rich surroundings, as well as the clustering of seeds, might be factors benefiting
germination and seedling growth (Beattie, 1985).
Defense is a further category in which plants employ food rewards to acquire
protection by arthropod mutualists. The provision of food sources allows plants to
recruit or sustain predators or parasitoids, which, in turn, can provide protection
against herbivory. The plant-derived food structures involved in indirect defen-
sive interaction can be divided in two main groups: food bodies and extrafloral
nectaries.
Food bodies are protein- and/or lipid-rich epidermal structures, including Beltian
bodies, M¨ullerian bodies and pearl bodies (Rickson, 1980). Food bodies can be
harvested by ants for consumption by either larvae or adults. However, in some of
the examples that have been described as “food bodies,” actual collecting by ants
has not yet be observed (Beattie, 1985). Unlike extrafloral nectar, food bodies can
serve as an alternative to insect protein. However, it incurs the risk that ants become
protein satiated, which may hamper carnivory. This facilitates intimate interactions
with ants, as it allows ants to remain on the plant (nesting) during times in which the
availability of insect protein is low. Some ant species rely entirely on food bodies of
their particular host plant for their protein supply (Carroll and Janzen, 1973). Even
though food bodies are collected by some non-mutualists (Letourneau, 1990), the
range of potential consumers is not as broad as in the case of the easily accessible
and digestible extrafloral nectar (Whitman, 1994). This makes food bodies less
vulnerable to consumption by unintended consumers.
Extrafloral nectaries include a wide range of nectar-excreting structures, which
are distinguished from their floral counterparts by the fact that they are not involved
in pollination. Extrafloral nectar is typically dominated by sucrose and its hexose
components glucose and fructose. The fact that these common sugars are acceptable
to the majority of insects, combined with the exposed nature of extrafloral nectaries,
makes them suitable food sources for a broad range of insects. Compared with floral
nectar, extrafloral nectar often has increased fructose and glucose levels (Tanowitz
44 T. C. J. Turlings and F. W¨
ackers
and Koehler, 1986; Koptur, 1994), as well as a higher overall sugar concentration
(Koptur, 1994; W¨ackers et al., 2001). These characteristics can be explained by
the exposed nature of most extrafloral nectaries, which result in faster microbial
breakdown of sucrose and increased evaporation. The high sugar concentration
may also serve an ecological function, as high sugar concentrations reduce intake
by visiting ants and increase durations of ant visits (Josens et al., 1998). A further
benefit of highly concentrated extrafloral nectar may lie in the fact that it prevents
nectar use by a range of non-intended visitors (W¨ackers et al., 2001). This applies
especially to Lepidoptera, whose mouthpart morphologies restrict them to feeding
on nectar with relatively low sugar concentrations.
In addition to carbohydrates, extrafloral nectar may contain variable amounts
of proteins, amino acids, and lipids (Baker et al., 1978; Smith et al., 1990). The
particular amino acid composition can increase the attractiveness of extrafloral
nectar as a food source (Lanza, 1988). Nevertheless, extrafloral nectar by itself falls
short from providing a well-balanced diet. Low amino acid levels or the absence of
certain essential amino acids forces nectar consumers to seek out supplementary
protein sources, thereby stimulating predation.
Extrafloral nectar can make a significant contribution to the diet of ant species
visiting these food sources. Fisher et al. (1990) reported that the six ant species
investigated in their study derive between 11 and 48% of their diet from extrafloral
nectar. Retana et al. (1987) found (extrafloral) nectar to be the main food source
for Camponotus foreli. Extrafloral nectar can also be extensively used by other
predators (Bakker and Klein, 1992; Ruhren and Handel, 1999), as well as parasitoids
(Bugg et al., 1989). In some instances, these carnivores, rather than ants, might
represent the primary force protecting the plant (Ruhren and Handel, 1999; V. Rico
Gray, personal communication).
Constitutive versus induced extrafloral nectar
Constitutive nectar production
Most plants excrete some extrafloral nectar irrespective of whether herbivores are
present. Such constitutive nectar production may be synchronized with the most
susceptible stages of plant growth (Bentley, 1977) or with the times during which
damaging herbivores are usually active (Tilman, 1978). Furthermore, nectar produc-
tion may coincide with the daily activity pattern of ants (Pascal and Belin-Depoux,
1991). Further synchronization is achieved through the ability of the plants to
increase nectar secretion in response to herbivore presence (Koptur, 1989; W¨ackers
and Wunderlin, 1999; Heil et al., 2001).
In general, constitutive nectar production may provide a degree of prophylactic
protection, because it allows plants to accommodate some natural enemies before
Predator/parasitoid recruitment by herbivore-injured plants 45
herbivores arrive (W¨ackers et al., 2001). Prophylactic protection by natural enemies
may include, for example, the prevention of herbivore oviposition or removal of
herbivore eggs. Maintaining some baseline nectar production in undamaged plants
is also likely to assure some level of ant visitation, which expedites the defense
response to herbivore attack.
Induction of food provision
In addition to the constitutive production of food supplements, some plants
can actively adjust their food provision in response to their biotic environment
(Table 2.2). Unlike other defense mechanisms, this induction can be elicited by two
distinct mechanisms. Food provision can be raised both by food removal (Risch
and Rickson, 1981; Koptur, 1992; Heil et al., 2000) and by tissue damage (Koptur,
1989; W¨ackers and Wunderlin, 1999; W¨ackers et al., 2001; Heil et al., 2001).
These mechanisms represent active responses by the plants to both ant attendance
and herbivore feeding. This receptiveness toward the presence of both the second
and the third trophic level represents a unique and highly dynamic type of plant
response.
In the case of food bodies, the primary mechanism of induction might be food
body removal. Risch and Rickson (1981) showed that the production of unicellular
food bodies by Piper cenocladum is stimulated by the presence of the mutualist ant
Pheidole bicornis. When ants are present, the plant produces 30 times as many food
bodies as control plants. Similar effects had previously been reported for other types
of food body (Carroll and Janzen, 1973). In P. cenocladum, a clerid beetle exploits
this relationship. Their larvae are also able to stimulate food body production in
the absence of the ants (Letourneau, 1990).
Extrafloral nectar production can be raised in response to both nectar removal
(Koptur, 1992; Heil et al., 2000) and tissue damage. Stephenson (1982), using
Catalpa speciosa, was the first to investigate the latter mechanism. He diluted the
nectar of individual nectaries with water and demonstrated that the diluted nectar
collected from sphingid-damaged leaves was richer in solutes compared with nectar
collected from undamaged leaves. Smith et al. (1990) point out that this does not
resolve whether C. speciosa actually increased its nectar volume or whether it
produced the same volume with an increased solute concentration.
Koptur (1989) reported that mechanical damage of Vicia sativa leaves increased
the volume of extrafloral nectar production by a factor of 2.5. Heil et al. (2001)
reported a two- to five-fold increase in volume of nectar secretion in Macaranga
tanarius following leaf damage. In Ricinus communis and Gossypium herbaceum,
the increase in extrafloral nectar production following S. littoralis herbivory was
three-fold and ten-fold, respectively (W¨ackers et al., 2001). Through parallel high
pressure liquid chromatographic analysis of sugars in the collected nectar, the
Table 2.2. The effect of leaf damage on extrafloral nectar production
Quantitative changes Qualitative changes
Plant species Damage type Nectar volume Carbohydrates Amino acids Carbohydrates Amino acids Reference
Catalpa speciosa Herbivory ? Increase in
solutes
Increase in
solutes
? ? Stephenson,
1982
Ipomoea carnea Mechanical No ? ? ? ? Koptur, 1989
Inga spp. Mechanical No ? ? ? ? Koptur, 1989
Vicia sativa Mechanical 2.5-fold
increasea
? ? ? ? Koptur, 1989
Impatiens sultani Mechanical No No 5.6-fold increase No No Smith et al.,
1990
Passiflora spp. Mechanical Yes ? ? ? ? Swift and
Lanza, 1993
Gossypium
herbaceum
Herbivory
(caterpillar)
and
mechanical
10-fold
increase
No ? No ? W¨ackers and
Wunderlin,
1999;
W¨ackers
et al., 2001
Macaranga
tanarius
Herbivory and
mechanical
Yes ? ? ? ? Heil et al., 2000,
2001
Ricinus
communis
Herbivory
(caterpillar)
2.5-fold
increase
No ? No ? W¨ackers et al.,
2001
Vicia faba Herbivory
(aphids)
No No ? No ? Engel et al.,
2001
aIn one of the four defoliation levels tested.
Predator/parasitoid recruitment by herbivore-injured plants 47
latter study was the first to demonstrate that the increased nectar secretion actually
represents a proportionate increase in carbohydrate secretion.
All these examples focus on the temporal aspect of nectar induction. In addition,
extrafloral nectaries are also especially suited for the study of spatial dynamics
following induction. This aspect can be easily assessed because of the discrete
distribution of nectaries, the possibility of non-destructive sampling, as well as the
ease of nectar collection. With respect to the spatial pattern of induction, W¨ackers
et al. (2001) showed that the impact of herbivory on extrafloral nectar induction
is primarily localized (i.e., restricted to the damaged leaf). This local increase in
nectar production can help in actively guiding ants to the site of attack. In addition,
a weaker systemic response was found. This systemic induction was restricted to
the younger leaves.
These examples show that several plants possess the ability to raise extrafloral
nectar production in response to herbivory, but this induction is not necessarily uni-
versal and might vary depending on both plant and herbivore species (Table 2.2).
Koptur (1989) could not demonstrate an effect of mechanical defoliation on extraflo-
ral nectar production in Ipomoea carnea, Inga brenesii and Inga punctata.In
V. faba, aphid feeding had no effect on the quantity of extrafloral nectar secretion
(Engel et al., 2001). A similar lack of induction was found following feeding by
S. littoralis larvae (F. L. W ¨ackers, unpublished data).
Specificity of induction: elicitors and mechanisms
The few studies that have addressed the induction of extrafloral nectar produc-
tion have examined either actual herbivory or mechanical damage. The fact that
mechanical damage failed to elicited nectar induction in several plant systems
(Koptur, 1989) could be interpreted as indicating that the method of mechanical
damage is not a suitable mimic of herbivory.
Induction of nectar secretion could require a herbivory-specific elicitor, similar to
the induction of plant volatiles. To investigate this W¨ackers and Wunderlin (1999)
conducted a set of experiments analogous to those conducted by Turlings et al.
(1990), in which cotton plants were subjected either to herbivory or to mechanical
damage with and without caterpillar regurgitant. In contrast to the mechanism of
herbivore-induced volatile emission, the induction of extrafloral nectar secretion
was found to be elicited by tissue damage, irrespective of whether this damage
was mechanical or caused by actual herbivory. The addition of S. littoralis regur-
gitant had no significant effect on the level, the timing, or the distribution of nectar
secretion. These findings indicate that the induction of extrafloral nectar secretion
constitutes a general response by the plant to tissue damage, rather than representing
a herbivory-specific mechanism.
48 T. C. J. Turlings and F. W¨
ackers
This rather unspecific induction of nectar secretion in cotton was surprising in
light of the fact that the induction of volatile emission by this plant had been demon-
strated to be specific. Herbivore-damaged plants show a higher rate of volatile
emission compared with mechanically damaged plants (McCall et al., 1994),
and herbivore feeding induced de novo synthesis of various terpenoids (Par´e and
Tumlinson, 1997), which resulted in a quantitative as well as a qualitative response
to herbivory. The specificity of the plant response is not restricted to the differenti-
ation between mechanical damage and herbivory. The composition of the induced
volatile blend also varies between (even closely related) herbivore species (De
Moraes et al., 1998).
The difference in induction specificity between the two categories of indirect
defense indicates that the induction pathways involved are not entirely identical. It
may also reflect differences in the costs and benefits of such specificity (W¨ackers
and Wunderlin, 1999). The use of volatiles as a signal to recruit natural enemies is
dependent on induction, as this communication between plants and the third trophic
level breaks down when the volatile signal is not reliably associated with herbivore
presence. Extrafloral nectar, by comparison, constitutes a reward in itself rather than
serving as a signal to indicate the location of a reward. The response by the third
trophic level, as a result, is not dependent on the degree in which nectar secretion
correlates with herbivore presence. Therefore, an increase in nectar production
following mechanical damage entails the additional cost of nectar production but
has no negative implications for the efficacy of this indirect defense mechanism.
Working with M. tanarius, Heil et al. (2001) also reported that mechanical dam-
age is sufficient to induce nectar secretion. They were also able to achieve a similar
response through exogenous application of JA to undamaged plants. This fact, com-
bined with the finding that the response in damaged plants could be suppressed by
phenidone, an inhibitor of JA synthesis, indicates that the induction of extrafloral
nectar production is elicited via the octadecanoid signal cascade (Heil et al., 2001),
which is also involved in the production of various inducible plant volatiles (see
above).
Costs and benefits
The benefit of extrafloral nectar production to plant fitness has been well established
(Bentley, 1977; Inouye and Taylor, 1979; O’Dowd, 1979; Wagner, 1997; Koptur
et al., 1998). Whether induction further enhances plant fitness over constitutive
nectar production remains an open issue. The fact that both inducible and consti-
tutive nectar production occurs (Table 2.2) indicates that the costs and benefits of
nectar induction vary among plants.
It is often believed that the primary benefit of induction is economical, as it
restricts defensive investments to those periods in which plants are actually under
Predator/parasitoid recruitment by herbivore-injured plants 49
attack (Rhoades, 1979; Zangerl and Rutledge, 1996). In addition to these economic
benefits, induction of extrafloral nectar production may also enhance the effective-
ness of natural enemy recruitment, because it results in an accumulation of natural
enemies on the site of attack (F. L. W¨ackers and F. Frei, unpublished data). How-
ever, these benefits of induction come at the price of increased vulnerability during
the plant’s non-induced state. To understand the pattern in which extrafloral nectar
is produced, we need to identify and quantify the particular costs involved in the
use of this indirect defense.
Costs of extrafloral nectar production
Pyke (1991) demonstrated a trade-off between floral nectar secretion and seed
production in hand-pollinated Brandfordia nobilis. Comparable studies on fitness
consequences of extrafloral nectar production have yet to be conducted. However,
strong indirect evidence for the high cost of extrafloral nectar production is provided
by the finding that some plant species have lost extrafloral nectaries in ecosystems
void of mutualist ant species. Rickson (1977) was able to track the gradual regres-
sion of Cecropia peltata extrafloral nectaries from Azteca ant-inhabited mainland
Central America over a range of Caribbean islands lacking the mutualist ant species.
Bentley (1977) described a decline in sepal nectaries of Bixa orellana from ant-rich
lowlands to higher altitudes where ant populations are scarce.
Direct costs
To the plant, the direct cost of producing extrafloral nectar can be relatively low.
O’Dowd (1979) estimated that the energy invested in the lifetime petiolar nectar
production of an individual Ochroma pyramidale leaf constitutes about 1% of the
leaf’s energy content. However, since leaf tissue makes up only part of the total
plant mass, this figure does not reveal which fraction of the total assimilated energy
is diverted to extrafloral nectar. A more accurate way to estimate allocational costs
is to express the quantity of excreted sugars as a fraction of the daily production
of assimilates. W¨ackers et al. (2001) calculated that castor (Ricinus communis)
diverts 0.9% of its daily assimilates to the production of extrafloral nectar. Even
though this cost may seem unsubstantial, its cumulative nature could lead to rapid
cost increments over the total period of plant growth. In addition to the loss of
carbohydrates, nectar secretion also entails a loss of other compounds, in particular
amino acids and water. Depending on the growth conditions of the plant, loss of
these compounds may represent considerable additional cost factors.
Direct costs also include the costs involved in active nectar sequestration, as well
as the cost involved in producing the nectary. This latter cost is probably low, as
nectaries are often simple and small, showing little differentiation. In other types of
defense, costs relating to biosynthesis, transport, and storage (i.e., autotoxicity) can
50 T. C. J. Turlings and F. W¨
ackers
be considerable (Karban and Baldwin, 1997). However, these costs do not apply
in the case of extrafloral nectar as nectaries are usually vascularized and obtain
non-toxic primary metabolites directly from the phloem or xylem (Frey-Wyssling,
1955; Beattie, 1985).
Ecological costs
In addition to the direct costs, the production of extrafloral nectar can also entail sub-
stantial indirect (ecological) costs. In insect-pollinated plants, extrafloral nectaries
can have adverse effects on pollination efficacy. Interference with the pollination
process can occur when extrafloral nectaries distract the pollinators away from the
floral nectar (Koptur, 1989) or when nectary-attending ants attack flower visitors
(F. L. W¨ackers personal observation). Considerable ecological costs may arise when
extrafloral nectaries are exploited by herbivores. Adult herbivores such as moths are
often entirely or partly dependent on sugar solutions as an energy source. Nectar
feeding frequently increases herbivore longevity as well as the number and size
of matured eggs (Leahy and Andow, 1994; Binder and Robbins, 1996; Romeis
and W¨ackers, 2000, 2002). When herbivores are attracted or retained by extrafloral
nectaries, this can severely increase herbivory levels on nectar-producing plants
(Adjei-Maafo and Wilson, 1983; Rogers, 1985; McEwen and Liber, 1995). To
reduce these ecological costs, plants may have adapted the extrafloral nectar com-
position to exclude unintended visitors and to cater selectively to those insects from
which they benefit (W¨ackers et al., 2001).
How heavily these direct and indirect cost factors weigh on plant fitness depends
on the plant species and its growing conditions. Induction of extrafloral nectar
production, however, allows plants to minimize almost all of these cost factors
simultaneously. In the absence of herbivory, nectar production and its associated
costs may be all but eliminated, with the full costs only being assumed during
periods of herbivory.
The cost-saving benefit of inducible defense is counterbalanced by the loss of
preventative protection (Zangerl and Bazzaz, 1992). Any damage inflicted during
the lag period between herbivore attack and the onset of the induced defense should
be included in the costs of induction. It is our experience that the induced produc-
tion of nectar takes about 24 h (W¨ackers et al., 2001). In the economic terms of the
optimal defense theory, inducible defenses have a selective advantage over consti-
tutive defenses when the savings in defensive costs during herbivore-free periods
outweigh the loss in preventative protection during the lag time of induction. In
comparison with direct defenses, lag time of indirect defense is extended because
of the inherent delay in natural enemy response. In the case of ants responding
to extrafloral nectaries, this delay includes the time for ant scouts to encounter
the nectary, as well as the time required for nestmate recruitment (W¨ackers et al.,
Predator/parasitoid recruitment by herbivore-injured plants 51
2001). This additional lag time likely reduces the economic benefits of induction
of indirect defenses relative to those of direct defense. Plants may have developed
various strategies to minimize the lag time of indirect defense induction. Maintain-
ing some baseline nectar production in undamaged plants could be such a strategy.
By accommodating at least a few natural enemies, the indirect defense can begin
to operate quickly once the plant is attacked.
The need for more field data
To demonstrate that a plant trait has a defensive function, it is necessary to show
that it has a negative effect on plant antagonists, reduces the damage done to the
plants, and increases plant fitness under natural conditions (Hare, 2002). Attraction
of natural enemies to herbivore-induced volatiles has mainly been demonstrated
in laboratory studies, and the role of these volatiles for interactions in the field is
still poorly understood (Sabelis et al., 1999). Initial evidence comes from studies
in which caged plants out in a field were found to attract more parasitoids or
predators when damaged by herbivores than when undamaged. Drukker et al. (1995)
showed that psyllid-infested pear trees attracted more predatory anthocorid bugs
than trees without psyllids. In the laboratory, Scutareanu et al. (1997) demonstrated
that infested trees release more and different volatiles than uninfested pear trees, and
that the production of these volatiles was positively correlated with the density of the
psyllids on the trees. Similar results were obtained by Shimoda et al. (1997), who
found in a field experiment that the predator Scolothrips takahashii was attracted
to cages that contained a lima bean plant infested with spider mites. Spider mite
infestation is known to cause lima bean to emit a blend of specific terpenoids and
methyl salicylate (Dicke and Sabelis, 1988; Dicke et al., 1990a,b). However, as
for the study with the psyllid-infested pear trees, it could not be excluded that the
predators were directly attracted by the herbivores on the plants rather than the
induced plant odor.
Conclusive field evidence has been obtained with the manipulation of odor emis-
sions of free-standing plants. Thaler (1999), for example, observed an increase in
parasitism of S. exigua larvae on tomato after the plants had been treated with
JA. This treatment induces the octadecanoid pathway, which results in the pro-
duction of various defense compounds, including volatiles. In an earlier study in a
tobacco field, De Moraes et al. (1998) had already found that the specialist parasitoid
C. nigriceps could distinguish between the odor of plants that have been damaged
by its specific host H. virescens and the odor of plants damaged by a closely related
non-host. In a natural, non-agricultural environment, Kessler and Baldwin (2001)
supplemented the odor of wild tobacco plants with synthetic volatiles and found
that (Z)-3-hexenol, linalool and (Z)-α-bergamotene all increased the predation rate
52 T. C. J. Turlings and F. W¨
ackers
of M. sexta eggs and neonate larvae by a generalist predator. Similar increases of
predation were obtained by treating wild tobacco plants with methyl jasmonate
(Kessler and Baldwin, 2001). In one of our own studies, we trapped considerably
more parasitoids on sticky traps downwind from maize plants treated with caterpil-
lar regurgitant than upwind from these plants or near untreated plants (Bernasconi
Ockroy et al., 2001). These studies provide good evidence for a role of induced
plant volatiles in host and prey location. What is still missing, however, is field evi-
dence from unmanipulated studies showing that plants actually benefit from these
interactions.
The sophisticated equipment required for volatile identification has long confined
the topic of herbivore-induced volatiles to the laboratory, but extrafloral nectaries
have traditionally been studied in the field. Moreover, the work on extrafloral nec-
taries has mainly addressed wild plant species within their natural habitat, whereas
the study of plant volatiles has long focussed on agricultural crops. As a result,
we have a relative wealth of field evidence for the defensive function of extrafloral
nectaries.
It has been well established that extrafloral nectaries are visited by a range of
predators and parasitoids (Janzen, 1966; Bugg et al., 1989; Koptur, 1992). Ants
are by far the most common visitors to extrafloral nectaries. The facts that ants
are social, show recruitment behavior, and have a strong tendency to defend lucra-
tive sugar sources against competitors make them especially suitable as defen-
sive agents. Nevertheless, not all ants are equally effective. Their aggressiveness
ranges from species that attack large mammals (Bennett and Breed, 1985) to species
that are passive or even tend to drop from the nectary when disturbed (O’Dowd,
1979).
In a number of cases, it has been demonstrated that increased levels of nectar
production translates to higher levels of ant attendance (Passera et al., 1994). The
fact that the most aggressive ants monopolize the most productive nectar sources
(Del-Claro and Oliveira, 1993) constitutes a further benefit to high levels of nectar
production.
Using exclusion experiments, several studies were able to demonstrate that
ants effectively protect the plant against herbivory (O’Dowd and Catchpole, 1983;
Wagner, 1997; but see O’Dowd and Catchpole, 1983; Rico-Gray and Thien, 1989).
In the same way, reduction of herbivory has recently been demonstrated in mutu-
alisms between extrafloral nectaries and spiders (Ruhren and Handel, 1999), as well
as predatory wasps (V. Rico-Gray, personal communication).
A number of studies have provided the ultimate proof for the defensive function
of extrafloral nectaries by demonstrating that herbivory reduction by ants actually
translates to an increased reproductive fitness of nectar-providing plants (Koptur,
1979; Rico-Gray and Thien, 1989; Oliveira, 1997; Wagner, 1997). In the most
Predator/parasitoid recruitment by herbivore-injured plants 53
extreme cases, unattended plants die as result of herbivory in the absence of ants
(Janzen, 1966).
In addition to these empirical studies, there is indirect ecological evidence for the
defensive function of extrafloral nectaries. Several studies have reported correla-
tions between the abundance of plants with extrafloral nectaries and ant abundance
(Pemberton, 1998; Rico-Gray et al., 1998). Bentley (1977) and Rickson (1977)
showed that plants may lose extrafloral nectaries in ecosystems void of mutualist
ant species.
Even though this evidence supports the defensive function of extrafloral nec-
taries, the evidence is largely based on myrmecophilous plants. In other plant
species, the benefit of ant attendance is not always as clear (O’Dowd and Catchpole,
1983; Koptur and Lawton, 1988). In these species, the provision of extrafloral nec-
tar may serve to enhance the effectiveness of other plant–predator (Ruhren and
Handel, 1999) or plant–parasitoid interactions (Lingren and Lukefahr, 1977; Bugg
et al., 1989; Koptur, 1994), or serve other (non-defensive) functions.
Future directions
Although much is known about various intricacies of the active role of plants in
tritrophic interactions, it is evident from the above review that numerous questions
remain and several areas are virtually unexplored. We identify three areas that
appear to us as particularly interesting and they can be expected to receive special
attention in future research programs.
Cross-effects
Almost all studies on induced indirect defenses have looked at the effects of an
attack by a single herbivore or pathogen species. In a natural situation, however,
plants often suffer from simultaneous attacks by multiple adversaries. Many plants
carry several herbivores and they can be infested by pathogens at the same time
that they are eaten by herbivores. This should again contribute to the variability of
reactions that plants exhibit. Plant infestations by multiple species and their cross-
effects have been studied for direct defenses (Hatcher, 1995; Agrawal et al., 1999;
Rost`as et al., 2003), but not yet in the context of indirect defenses.
Studies on the cross-effects of herbivore and pathogen infestation on direct
defenses have yielded results that can be quite different for different systems
(Karban and Kuc, 1999; Stout and Bostock, 1999; Rost`as et al., 2003). The cucum-
ber plant has been studied in detail with several pathogens and herbivores (Apriyanto
and Potter, 1990; Ajlan and Potter, 1991; Moran, 1998). In most cases, infection
with one pathogen caused a systemic resistance to other pathogens but had no
54 T. C. J. Turlings and F. W¨
ackers
systemic effect on insect herbivores, except for a positive effect on the striped
cucumber beetle (Apriyanto and Potter, 1990). Moran (1998) reported that locally,
at the site of pathogen infestation, both positive and negative effects on insects
may occur. The most extensively studied system is that of Rumex spp. attacked
by the leaf beetle Gastrophysa viridula and the biotrophic rust fungus Uromyces
rumicis. Hatcher and co-workers (Hatcher et al., 1994a,b, 1995; Hatcher and Paul,
2000) found that fungus infection made Rumex plants less preferred for oviposition
and consumption by the beetle and, vice versa, that plants subjected to leaf beetle
damage were less prone to rust infection. The studies reviewed by Rost`as et al.
(2003) showed a general tendency of adverse effects of plant antagonists on each
other. Very little information is available on how such cross-effects affect tritrophic
interactions.
How does pathogen infestation affect odor emissions and does it interfere with
emissions induced by insect herbivores? So far, only one study has specifically
looked at this cross-effect (Cardoza et al., 2002). It showed that insect feed-
ing (beet armyworm, S. exigua) and fungus infection (white mold, Sclerotium
rolfsii) resulted in distinctly different odor blends in peanut plants, whereas plants
that were simultaneously infested by these two antagonists released a mix of both
blends.
Shiojiri et al. (2001, 2002) revealed a fascinating cross-effect resulting from
simultaneous feeding by larvae of two lepidopteran species. They showed that
Plutella xylostella and P. rapae caused cabbage plants to release different odor
blends that could be distinguished by Cotesia plutella.Costesia glomerata females
were only attracted by plants damaged by P. xylostella and not by those damaged by
P. rapae, which it cannot parasitize. Interestingly, the parasitoid is also less attracted
to plants infested by both herbivores. This could explain why adult P. xylostella
females show a preference to oviposit on plants that have already been infested by
P. rapae (Shiojiri et al., 2002),
How can multiple infestations affect each other? JA has typically been assumed
to be involved in induced responses to herbivory and SA was assumed to be involved
in most responses to pathogen infection. The interactions are not as straightforward
and various insects and pathogens differ in the defense genes they activate (Walling,
2000). Ozawa et al. (2000) compared the induction of volatiles in lima bean leaves
by caterpillars and spider mites with induction with JA and methyl salicylate. Their
results suggest that response to caterpillar feeding involves the JA-related signaling
pathway and that spider mite feeding triggers both the SA- and JA-related signaling
pathways. Dicke et al. (1999) had already shown that JA-triggered emissions in
lima bean showed some differences from mite-induced emissions and concluded
that the induction involves more than just JA. This might indicate that the reaction
to spider mite feeding is more similar to the reaction triggered by sucking insects
Predator/parasitoid recruitment by herbivore-injured plants 55
such as whiteflies and aphids (Walling, 2000). A crucial issue in these types of
study is how elicitors are applied (Schmelz et al., 2001); ideally, the treatment
should reflect natural conditions. The involvement of various pathways that can
be triggered differently by different plant antagonists implies that infestation by
multiple organisms will add to the variability in plant responses. In light of the
likelihood that plants are subject to attack by more than one adversary, it seems
pertinent to study further this so-called cross-talk and its ecological implications.
Exploitation of induced defenses for biological control
The above examples illustrate how plant attributes may contribute to successful
prey location by natural enemies and it has been suggested that these attributes may
be exploitable in pest control (Bottrell et al., 1998; Lewis et al., 1998; Cortesero
et al., 2000). It has been long recognized that efficacy of adult natural enemies as
biological agents against insect pests may be increased by supplying them with food
sources. Reviews on how plant-provided nutrition may aid in biological control are
presented by Hagen (1986), Whitman (1994), Jervis and Kidd (1996), and Cortesero
et al. (2000). Several examples show that predation and parasitism are higher on
plants with extrafloral nectar than on plants without extrafloral nectar (Treacy, et al.,
1986; Pemberton and Lee, 1996). Clearly, there is the potential that the production
of extrafloral nectar could be optimized to increase the efficiency of biological
control agents. Such selection or manipulation programs should also account for
the risk that the nectar can be exploited by phytophagous insects (Rogers, 1985;
Schuster and Calderon, 1986).
After it was recognized that plant volatiles play an essential role in host location
by various parasitoids, it has been suggested that emission of these cues could be
manipulated to facilitate prey finding and thus improve biological control (e.g.,
Nordlund et al., 1988; Dicke et al., 1990a; Turlings and Benrey, 1998; Cortesero
et al., 2000). The potential of such an approach remains unexplored, but two of the
above mentioned field studies suggest that it is feasible. Thaler’s (1999) treatment of
tomato plants with JA increased parasitism of an important pest. Equally promising
is the increased predation of M. sexta eggs and neonate larvae that Kessler and
Baldwin (2001) observed after supplementing the odor of wild tobacco plants with
synthetic volatiles or by treating wild tobacco plants with methyl jasmonate. The
possibilities offered by biotechnology will certainly make it possible to tailor the
odor production of crop plants. The challenge will be to determine which odor
blends are most effective in attracting the right control agents and again to avoid
attracting herbivores at the same time.
Genetic transformation of plants for the purpose of enhancing biological control
will still be some time away. These traits, however, could be well suited for the
56 T. C. J. Turlings and F. W¨
ackers
development of methods for the evaluation of other transgenic crops, as discussed
in the next section.
Evaluation of transgenic crops
Current controversy over the use of transgenic crops places much emphasis on their
potential effects on non-target insects. Various direct and indirect effects on natural
enemies that are important in pest control are possible (Sch¨uler et al., 1999a) and a
number of studies have addressed these potential effects. Most of these studies have
involved Bt maize (maize plants producing a Bacillus thuringiensis toxin) and have
shown little or no negative effect of Bt maize (e.g., Orr and Landis, 1997; Pilcher
et al., 1997). A notable exception is the reduced development and increased mortal-
ity of the predatory lacewing Chrysoperla carnae when it consumes Bt maize-fed
prey (Hilbeck et al., 1998).
We are aware of only one study that has looked at the attractiveness of trans-
genic plants to natural enemies. Sch¨uler et al. (1999b) studied the attractiveness of
Bt oilseed rape to the parasitoid Cotesia plutellae, which attacks the diamondback
moth (P. xylostella), an important pest. As expected, feeding by the susceptible
P. xylostella larvae was much reduced, resulting in fewer odors being emitted and
a reduced attractiveness to the parasitoids. However, the outcome of this study
was favorable in the sense that caterpillar-induced emissions of attractive volatiles
was highest when Bt-resistant P. xylostella larvae were feeding on the plants. The
authors argue that this could reduce the development of resistance to transgenic
plants in field situations (Sch¨uler et al., 1999b).
For the evaluation of possible pleiotropic effects (side-effects resulting from
genes effecting more than one phenotypic trait) in transgenic crops, the analyses
of plant-produced odors and exudates (such as extrafloral nectar) may be ideal.
Significant changes in biochemical pathways would likely result in alterations in the
production of these secondary plant metabolites. Careful analyses of a large range
of conventional varieties of a particular crop would also reveal the existing natural
variation and would allow for a more realistic comparison than is commonly made.
The significance in any observed changes for the interactions between the crop
and beneficial insects could then be tested in appropriate bioassays. In such assays,
conventional crops that exhibit clear differences in the trait under investigation (e.g.,
attractiveness to parasitoids or nutritional value of extrafloral nectar) could serve as
realistic controls. For maize, we already have ample information on the considerable
variation among genotypes in the emissions of volatiles (Gouinguen´e et al., 2001
and unpublished data). In most cases, it is not to be expected that transgenesis
has a major effect on the composition of odor blends or extrafloral nectar, as the
production of, for instance, Bt involves entirely different biochemical pathways.
Herbicide resistance in maize, however, does involve the shikimate pathway (Shah
et al., 1986; Padgette et al., 1994), which is responsible for the production of
Predator/parasitoid recruitment by herbivore-injured plants 57
several aromatic volatiles that are induced after insect attack (Par´e and Tumlinson,
1999). It would be interesting to investigate if transgenic plants with herbicide
resistance produce more or less of these substances and if this has any consequences
for the attraction of parasitoids and predators. It would be equally interesting to
study potential changes in the carbohydrate and amino acid composition of plant
nectar and honeydew resulting from transgenesis. In all cases, it will be pertinent to
compare such changes with the full spectrum of existing variability and to determine
the ecological relevance of the changes.
Conclusions
Extrafloral nectar and plant odors play essential roles in the protection of plants
from herbivores by natural enemies. Both these traits can be inducible, but plants
without insect damage may have nectaries that produce significant amounts of nec-
tar, whereas most undamaged plants are virtually odorless compared with damaged
plants. The induction of plant odor emissions is relatively specific for insect feed-
ing, and in some cases plants respond differentially to different herbivores. So far,
studies into specificity have not addressed the considerable variation in signals emit-
ted by different plant genotypes. There appears to be a danger of overinterpreting
results from experiments conducted with just one insect–plant combination. Not
only can different plant genotypes differ considerably in their induced responses
(e.g., Gouinguen´e et al., 2001; Krips et al., 2001), but, in addition, the arthropods
that make use of plant signals and food may show variation and rapid genetic
changes in their responses (Margolies et al., 1997; Maeda et al., 1999; Dicke et al.,
2000). This variation needs to be considered and included in studies on specificity.
Both indirect defenses have now been shown to function in field situations, but
further field studies are needed to confirm that plants do indeed benefit from emitting
induced odors in natural settings. Moreover, nothing is yet known about the cross-
effects of multiple infestations on plant indirect defenses. Also still lacking are
appropriate field tests for the evaluation of plant-odor manipulation to enhance the
effectiveness of biological control agents. However, various studies have indicated
the potential of such approaches. Current biotechnology techniques offer ample
opportunities for the manipulation of indirect plant defenses, which should largely
facilitate the design of experiments that can help to answer the remaining questions
on their function and exploitability.
Acknowledgments
We are grateful to Hans Alborn, G¨oran Birgersson, Cristina Faria, Monika Frey,
Jonathan Gershenzon, Bernd H¨agele, Yonggen Lou, Michael Rost`as, Goede Sch ¨uler
and Cristina Tam`o for advice and information on specific topics that are discussed
58 T. C. J. Turlings and F. W¨
ackers
in this chapter. Cristina Tam `o also provide editorial assistance. This work is in part
supported by funds from the Swiss National Science Foundation (grants 31-46237-
95 and 31-58865-99) and the Swiss Center of Competence in Research on “Plant
Survival.”
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