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Herbivore-induced plant volatiles in natural and

agricultural ecosystems: open questions and future
prospects
Moshe Gish1, Consuelo M De Moraes2 and Mark C Mescher2

Herbivore-induced plant volatiles (HIPV) have been shown to Recognition of the important role of HIPV signaling in
convey ecologically relevant information to other organisms, natural communities has given rise to hope that the
including carnivorous and herbivorous arthropods and HIPV-mediated plant-arthropod interactions might be
neighboring plants. However, many questions about the managed or manipulated to facilitate the sustainable
evolutionary and ecological functions of HIPV remain management of herbivorous insect pests in agricultural
unanswered. In particular, a current lack of information about settings [7]. However, despite some notable successes
the ways in which environmental factors — including habitat (discussed below), relatively little progress has been
structure and atmospheric conditions — influence HIPV made in implementing management strategies that em-
mediated interactions in real-world settings limits our ability to ploy HIPV [8]. Such efforts would no doubt benefit
anticipate the ways in which HIPV-mediated ecological from improved understanding of the ways in which HIPV
interactions may be altered or disrupted by anthropogenic function in natural systems [7], particularly as a large
environmental change, including atmospheric pollution and proportion of previous research has focused on crop
climate change. Understanding these influences thus has species and examined highly simplified model systems,
significant implications for the sustainable management of frequently under laboratory conditions [8,9]. In the
natural and agricultural ecosystems and should be a priority for following paragraphs we highlight some significant out-
future research. standing questions about the ecological functions of
Addresses HIPV in complex real-world environments and the evo-
1
Department of Entomology, The Pennsylvania State University, lutionary forces that may have shaped volatile emission
University Park, PA, United States
2
patterns in natural plant populations. These questions
Department of Environmental Systems Science, ETH Zürich, have relevance for understanding the role of HIPV sig-
8092 Zürich, Switzerland
naling in regulating herbivore populations in natural and
Corresponding author: Mescher, Mark C (mescher@usys.ethz.ch) agricultural ecosystems, as well as for understanding the
ways in which such interactions may be impacted by
global and regional environmental change.
Current Opinion in Insect Science 2015, 9:1–6
This review comes from a themed issue on Pests and resistance
Edited by Fiona L Goggin and Keyan Zhu-Salzman
Evolution and ecology of HIPV
Induced volatile emission is a characteristic plant re-
For a complete overview see the Issue and the Editorial
sponse to tissue damage and may play a role in inhibiting
Available online 17th April 2015 microbial infection at wound sites [10]. However, HIPV
http://dx.doi.org/10.1016/j.cois.2015.04.001 blends elicited by arthropod feeding (or oviposition [11])
2214-5745/# 2015 Elsevier Inc. All rights reserved. are typically chemically distinct from blends induced by
mechanical damage alone [12], and their production is
influenced by the presence of chemical elicitors in the
oral secretions of feeding herbivores [13]. Consequently,
HIPV provide information-rich cues regarding the pres-
ence and identity of feeding herbivores that have been
Introduction implicated in a wide range of above-ground and below-
Plant odors convey ecologically relevant information to ground interactions among plants and other organisms [1–
other organisms and thereby play an important role in 4,6,14–16]. As noted above, many predatory and parasitic
mediating diverse interactions within terrestrial commu- arthropods utilize HIPV cues to locate otherwise cryptic
nities. For example, changes in plant volatile emissions herbivorous prey in complex olfactory environments
elicited by pathogen infection or insect feeding damage [1,2,4,5]; furthermore, specialist species can often recog-
can influence the behavior of foraging arthropods, with nize the characteristic odors of plants attacked by the
implications for vector-borne disease transmission and tri- particular herbivore species on which they prey [17,18].
trophic plant–herbivore–natural enemy interactions [1– Herbivores themselves also frequently utilize HIPV as
5]. Indeed, herbivore-induced plant volatiles (HIPV) are foraging cues [19,20], often exhibiting aversive responses
thought to function as an indirect form of plant defense by to the odors of damaged plants [12,21], but in some cases
recruiting natural enemies of feeding herbivores [6]. utilizing such odors as aggregation cues [22]. And HIPV

www.sciencedirect.com Current Opinion in Insect Science 2015, 9:1–6

2 Pests and resistance

have also been implicated in plant-to-plant signaling, emissions to which receiving plants and insects are
where they can mediate the priming or enhancement exposed in nature [26] or the typical and maximal dis-
of anti-herbivore defenses in neighboring plants, or in tances over which HIPV mediated signaling interactions
distant parts of the emitting plant [23,24]. occur under field conditions [40]. We can, however, cer-
tainly infer that receivers of HIPV cues that are highly
The diverse ecological roles of HIPV raise questions about mobile, including many insect species, will benefit from
the evolution of their putative signaling functions and the perception of such cues over greater distances than
about the relative significance of different HIPV-mediated more sedentary receivers such as plants (particularly where
interactions in shaping the dynamics of ecological commu- HIPV function mainly as within-plant signals). This is
nities [25,26,27]. While there are relatively clear adaptive reflected, for example, in the highly attuned olfactory
benefits for organisms that perceive and respond to HIPV organs of many parasitoid species, which can perceive
cues, including arthropods and neighboring plants and respond to minute concentrations of relevant odor
[1,9,20,28], the advantages for emitting plants are less cues [41]. In contrast, while the olfactory capabilities of
apparent [25]. It is likely that plants frequently benefit plants (i.e., their ability to perceive and respond to airborne
from enhanced recruitment of natural enemies of their chemical cues) remain almost entirely unknown, they
herbivores via HIPV, which has been documented in appear to mediate responses to HIPV cues over relatively
natural systems [29,30,31]; however, the benefits to plant limited distances [42]. It is currently unclear whether such
fitness deriving from such recruitment are difficult to factors have likewise shaped patterns of HIPV emission by
measure and remain uncertain [9]. It is possible that plants. However, the chemical composition of volatile
the role of HIPV as a cue for natural enemies arose signals clearly influences the distances over which they
secondarily (i.e., as a byproduct or exaptation) of a primary are effectively transmitted [38], suggesting that the evalu-
signaling function in plant-plant communication [24]. Here ation of plant volatile profiles might potentially reveal
again, the adaptive significance for emitting plants remains evidence of adaptation for effective communication with
somewhat uncertain, as it is not clear that plants should particular classes of receivers.
benefit by warning potential competitors of impending
herbivory; however, a number of relatively recent studies Outlook for the use of HIPV in agriculture
have documented HIPV signaling within individual plants, Open questions about the functions of HIPV in natural
which may function to overcome vascular constraints on systems are reflected in uncertainty about their potential
the internal transmission of wound signals imposed by the significance for human agriculture. As understanding of
modular nature of plant architecture [24,32]. Furthermore, the importance of plant volatile cues in mediating inter-
recent work in sagebrush [33,34] suggests that HIPV actions among plants and arthropods has grown, so have
mediated enhancement of herbivore resistance is more hopes that such knowledge might be deployed to en-
effective when signaling occurs among individuals with hance the sustainable management of pest populations in
relatively high levels of genetic relatedness, suggesting the agricultural settings [43]. However, efforts to integrate
operation of self-recognition or kin-recognition mecha- volatiles into agricultural management strategies have
nisms in plant-to-plant signaling. met with limited success to date [8,26]. A notable
exception is the ‘push-pull’ system — so called, because
Another area of uncertainty regarding the ecological and it entails surrounding agricultural plantings with trap
evolutionary functions of HIPV relates to the distances species that are chemically attractive to stem-boring
over which HIPV cues can effectively convey ecologically moths (the pull), while chemically repellent species are
relevant information to potential receivers in natural set- planted between rows of the crop (the push) — which has
tings. Once HIPV are released into the air, they begin to had transformative impacts on maize and sorghum pro-
undergo dilution as a result of diffusion and turbulent duction in some regions of Africa [44,45].
motion [35], as well as chemical breakdown by oxidizing
agents, including anthropogenic pollutants [36]. Conse- Recently, significant attention has been focused on the
quently, odor plume physical and chemical dynamics are potential for genetic modification of crop plants to help
sensitive to atmospheric conditions and may be expected restore HIPV-emission capabilities that have been lost or
to vary spatially and temporally according to habitat char- compromised during the process of domestication [46] or
acteristics such as industrialization levels, temperature, to boost existing capabilities [47]. Work in this area has
solar radiation and wind regimes (e.g., forest vs. open field) produced engineered plants that constitutively emit high
[35,37,38], Figure 1. However, we currently have only levels of HIPV [8,47,48]; however, the potential deploy-
limited understanding of how such factors influence HIPV ment of such constitutively ‘turned on’ plants in the field
signaling in specific settings, although somewhat more could be problematic. For example, costs associated with
work has explored the implications of local atmospheric the continuous emission of HIPV may have negative
conditions and habitat structure on the transmission physiological effects on germination, growth and yield
of insect pheromones [37,39]. Furthermore, we also [49]. Furthermore, constitutive emission of HIPV by
know relatively little about the concentrations of HIPV transgenic plants (or via synthetic lures) would render

Current Opinion in Insect Science 2015, 9:1–6 www.sciencedirect.com

 Herbivore-induced volatiles: questions and prospects Gish, De Moraes and Mescher 3

Figure 1

(g)
(d)

(a)

(a)

(c)

(e)

(b) (b)
(f)

(h)

Current Opinion in Insect Science

Herbivore-induced plant volatiles (HIPV) can convey ecologically relevant information to carnivorous and herbivorous arthropods (a), as well as
neighboring plants (b), and can also function as wound signals within individual plants (c). A wide range of environmental factors may influence
such HIPV-mediated interactions (e.g., by limiting the distances over which HIPV cues can be reliably perceived). These include factors that vary
naturally across habitats (e.g., open fields and forests), such as differences in the intensity of solar radiation (d) or airflow dynamics
(e,f). Anthropogenic environmental changes may also impact HIPV signaling. For example, some atmospheric pollutants (g) may interact with and
degrade HIPV blends; and changing climate patterns could alter the frequency and intensity of drought stress (h), which can influence HIPV
emissions by inducing stomatal closure or via other physiological effects.

HIPV-cues unreliable as indicators of plant-damage sta- crops will typically be drawn from surrounding environ-
tus. Consequently, natural enemies might waste foraging ments capable of sustaining a more diverse ecological
time in prey-free environments and thereby fail to make community. As a consequence, management strategies
appropriate learning associations between HIPV cues and involving HIPV-mediated natural enemy attraction may
the presence of prey — an important factor in successful be ineffective at controlling pests in the main-central
foraging by entomophagous arthropods [50–52]. On the parts of large agricultural fields. For example, Kaplan
other hand, such emissions may enhance the apparency and Lewis [8] evaluated field-scale implementation
and attractiveness of plants to some herbivore species of HIPV for pest control using a predator–prey population
[19,20]. A potentially more sustainable alternative that model and consequently expressed skepticism regarding
might overcome many of these drawbacks entails the large-scale deployment of HIPV in agriculture.
development of transgenic plants with modified HIPV
genes that have inducible promoters, more closely mim- The plant-to-plant signaling functions of HIPV may well
icking the production of HIPV cues in nature [47]. also have implications for agriculture. Sugimoto et al.
However, even if enhanced natural enemy attraction to [54] recently reported that some HIPV compounds
HIPV-augmented crops can be maintained at meaningful can be chemically transformed into effective herbivore
levels, it remains unclear whether increased attraction deterrents in the leaves of receiving plants. In other
would translate to higher rates of predation or parasitism systems, HIPV-mediated defense enhancement has been
[8,53]. shown to entail the priming of induced defenses regulat-
ed by jasmonic acid [55,56]. Such mechanisms suggest a
Another challenge to the effective implementation of significant role for HIPV in strengthening anti-herbivore
HIPV in agriculture relates to the highly simplified com- defenses in plants exposed to incipient or expanding
munity structure of large-scale agricultural plantings and herbivore outbreaks that would seem highly relevant
the fact that natural enemies recruited into agricultural for plant-protection in agricultural settings. However,

www.sciencedirect.com Current Opinion in Insect Science 2015, 9:1–6

4 Pests and resistance

prospects for the exploitation of plant-plant signaling in changing environmental factors) [71]. The ecological
agriculture are limited at present by our near-complete outcomes of such factors are likely to depend on the
lack of knowledge about the mechanisms by which plants extent to which volatile-mediated signaling interactions
perceive and respond to olfactory cues. are resilient to such changes in community composition
(e.g., the responsiveness of natural enemies to HIPV
HIPV-mediated interactions in changing cues from novel plant or herbivore species or the re-
environments sponse of plants to novel herbivores) [71]. It is currently
The roles of HIPV in mediating the diverse ecological difficult to project the impacts of anthropogenic envi-
interactions described above in natural and agricultural ronmental changes on volatile-mediated ecological
ecosystems are likely to be influence both directly and interactions among plants and insects, not least because
indirectly by anthropogenic environmental changes. As of our limited understanding of the normal functioning
noted above, the transmission of HIPV cues can be of HIPV in natural communities. Improved understand-
significantly impacted by atmospheric conditions, includ- ing of such interactions would greatly enhance our
ing the presence of oanthropogenic pollutants. These ability to predict and manage such impacts, as well as
include oxidizing agents such as ozone (O3), nitrogen our ability to effectively conserve and manage HIPV
oxides (NOx), and hydroxyl radicals (OH) that readily signaling in agriculture.
react with HIPV compounds. Ground-level ozone, in
particular, is a widespread pollutant — readily trans- Acknowledgement
ported by wind from urban and industrialized areas to We thank Nick Sloff for assistance in creating Figure 1.
neighboring natural habitats [57] — known to have sub-
stantial adverse effects on ecosystem health and agricul- References and recommended reading
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