Opinion
Do Plants Eavesdrop on Floral
Scent Signals?
1, 2
Christina M. Caruso * and Amy L. Parachnowitsch
Plants emit a diverse array of volatile organic compounds that can function as Trends
cues to other plants. Plants can use volatiles emitted by neighbors to gain
Plants emit volatile organic compounds
information about their environment, and respond by adjusting their phenotype. that can function as cues to other
plants.
Less is known about whether the many different volatile signals that plants emit
are all equally likely to function as cues to other plants. We review evidence for Plants may use floral volatiles from their
neighbors to sense their mating
the function of floral volatile signals and conclude that plants are as likely to
environment.
perceive and respond to floral volatiles as to other, better-studied volatiles. We
fl
propose that eavesdropping on oral volatile cues is particularly likely to be Plants could respond by adjusting floral
traits that affect pollination and mating.
adaptive because plants can respond to these cues by adjusting traits that
directly affect pollination and mating.
Plant responses to floral volatiles cues
are particularly likely to be adaptive.
Plants Listen to the Airborne Signals of their Neighbors
Plants emit a diverse array of airborne volatile organic compounds (see Glossary) [1]. Plant
volatiles can function as signals to mutualists such as seed dispersers [2], pollinators [3], and
predators of herbivores [4]. However, these volatiles can also function as cues to other plants
[5]. Plants can perceive volatiles emitted by neighbors, and use these volatiles to gain information
about their environment, including the presence of herbivores [6] and competitors [7]. In
response to this information, plants can adjust their phenotype; for example, in response to
volatile cues emitted by herbivore-damaged neighbors, plants can increase their own herbivore
defenses [8]. While it is clear that plants can use volatiles to gain information about their
environment, less is known about whether the many different volatile signals emitted by plants
are all equally likely to function as cues to other plants.
In this opinion article we review the evidence that floral volatiles, in the same way as other
volatile signals, can function as cues to other plants. First, we describe what is known about how
plants perceive and respond to non-floral volatiles emitted by their neighbors. Second, we
discuss why plants should also be able to perceive floral volatiles emitted by their neighbors, and
use these volatiles to gain information about their mating environment. Third, we predict how
plants should respond to this information by adjusting their floral traits. Fourth, we hypothesize
the ecological conditions under which plants are likely to perceive and respond to floral volatiles
emitted by their neighbors. We conclude (i) that floral volatiles are as likely as other, better-
studied volatile signals to function as cues to other plants, and (ii) that eavesdropping on floral
1
Department of Integrative Biology,
volatile cues is particularly likely to be adaptive because plants can respond to these cues by
University of Guelph, Guelph, Ontario
adjusting traits that directly affect pollination and mating. N1G 2W1, Canada
2
Plant Ecology and Evolution,
Evolutionary Biology Centre, Uppsala
The Evidence that Non-Floral Volatiles Function as Cues to Other Plants
University, 75236 Uppsala, Sweden
The first studies on plant–plant communication were controversial, but there are now many
examples demonstrating that plants can perceive and respond to volatile cues emitted by their
*Correspondence:
neighbors [5]. Many of these studies have focused on volatiles emitted following herbivore
damage (i.e., herbivore-induced plant volatiles) [8]. Plants can use these volatiles to gain [email protected]
information about the presence of herbivores, and respond in at least two different ways. First, (C.M. Caruso).
Trends in Plant Science, January 2016, Vol. 21, No. 1 http://dx.doi.org/10.1016/j.tplants.2015.09.001 9
© 2015 Elsevier Ltd. All rights reserved.
plants can increase their defenses against herbivores. For example, wild tobacco (Nicotiana Glossary
attenuata) growing next to damaged sagebrush (Artemisia tridentata) had less leaf herbivory
Adaptive plasticity: phenotypic
fi
than wild tobacco growing next to undamaged sagebrush [9]. Second, plants can change their plasticity that increases tness (i.e.,
survival or reproduction). Plasticity is
physiology to more quickly or vigorously respond to future herbivore attack (i.e., priming) [10].
adaptive when genotypes that adjust
For example, wild tobacco plants growing next to damaged sagebrush plants upregulated the
their phenotype in response to the
expression of genes that play a role in herbivore defense [11]. environment have higher fitness than
genotypes that do not adjust their
phenotype.
Although most studies have focused on volatiles emitted by herbivore-damaged neighbors,
Cue: a trait used by a receiver that is
plants can also perceive and respond to volatile cues emitted by undamaged neighbors [12].
not intentionally displayed for that
Plants can use the volatiles from undamaged neighbors to gain information about purpose. For example, if herbivores
fl fi
the presence of conspecifics and heterospecifics, and respond in at least two ways. First, use oral volatiles to nd host plants,
then floral volatiles are functioning as
plants can alter their biomass allocation and growth. For example, seedlings of the parasitic
a cue.
species five-angled dodder (Cuscuta pentagona) grew towards volatiles produced by their
Eavesdropping: using a signal
preferred host species, and away from volatiles produced by non-preferred hosts [13]. intended for other receivers to gain
information about the surrounding
Second, plants can suppress [14] or change the composition [15] of their own volatile
environment. For example, plants that
signals. For example, potato (Solanum tuberosum) plants exposed to volatiles produced
detect floral volatiles emitted to
by undamaged onion (Allium cepa) plants produced more of two terpenoid compounds [15].
attract pollinators are eavesdropping.
Potato plants that produced more of these terpenoids attracted fewer aphid herbivores Fine-grained environmental
variation: when an individual
[16] and more of the natural enemies of aphids [17]. Overall, these studies suggest that
experiences more than one
herbivore-induced plant volatiles are not the only plant volatile signals that can function as
environment within its lifetime.
cues to other plants.
Floral volatiles: low molecular
weight organic molecules emitted by
flowers. These compounds are the
Could Floral Volatiles Function as Cues to Other Plants?
constituents of floral scent, which can
Floral volatiles have been shown to function as signals to pollinators and herbivores [18,19], and
range from simple blends with few
fi fl
researchers in disparate elds have speculated that oral volatiles could function as cues to other compounds to complex bouquets of
plants (Box 1). However, only one study [20] that we are aware of has explored whether floral >50 compounds.
Herbivore-induced plant volatiles
volatiles function as cues to other plants. This study found that floral volatiles produced by
(HIPVs): low molecular weight
snapdragon (Antirrhinum majus) inhibited root growth of Arabidopsis. The response of Arabi-
organic molecules emitted by plants
fl fi
dopsis to oral volatiles was speci c: of the three primary VOCs produced by snapdragon following consumption by an animal.
flowers, only methyl benzoate affected root growth, and root growth was not affected by Green leaf volatiles are common
components of HIPVs.
Mating environment: environmental
factors that affect plant reproduction.
The mating environment of a plant
Box 1. Past Speculation that Plants Can Sense Floral Volatiles
can include conspecific plants that
With one exception [20], the hypothesis that floral volatiles function as cues to other plants has not been tested using the
act as mates, pollinators that transfer
methods described in Box 2. However, this hypothesis has been invoked by researchers in two disparate fields: chemical
gametes between conspecifics, and
ecology and reproductive biology.
heterospecific plants that compete
for or facilitate pollination.
Chemical ecologists who study communication between undamaged plants have speculated that floral volatiles could
Phenotypic plasticity: when a
function as cues to other plants for two reasons [12]. First, floral volatiles are emitted in a wide range of ecological
genotype produces a different
conditions, including in the absence of herbivore damage and abiotic stress. Consequently, floral volatiles could function
phenotype in response to different
as cues to plants growing in a wide range of ecological conditions. Second, floral volatiles and herbivore-induced plant
environmental conditions.
volatiles are chemically similar. This similarity suggests that if plants can perceive herbivore-induced plant volatiles emitted
Plant–plant communication: when
by their neighbors, then they should also be able to perceive floral volatiles emitted by their neighbors.
a plant signal is perceived by another
plant. Plant–plant communication can
Reproductive biologists who study gynodioecious species have speculated that plants could use floral volatiles emitted
occur via soil or airborne cues, and is
by their neighbors as a cue to the mating environment [45]. In gynodioecious species, plants are either female or
often used synonymously with
hermaphroditic, and females cannot produce seeds without receiving pollen from hermaphrodites. Consequently, there eavesdropping.
should be selection on females to perceive the frequency of hermaphroditic neighbors and respond by adjusting their
Priming: a physiological response
floral traits. Consistent with this hypothesis, females in the gynodioecious species great blue lobelia (Lobelia siphilitica)
that prepares a plant to more quickly
adjust their rate of flower opening in response to the frequency of hermaphroditic neighbors; females open more flowers
or vigorously respond to a stressful
per unit time when they are rare relative to hermaphrodites than when they are common relative to hermaphrodites.
biotic or abiotic environment in the
Female great blue lobelia plants adjust their rate of flower opening even when hand-pollinated and grown in individual
future. For example, plants exposed
pots, suggesting that they do not use pollen receipt or soil chemicals as cues to the frequency of hermaphroditic
to herbivore-induced plant volatiles
neighbors. However, in some gynodioecious species, female and hermaphroditic flowers emit different volatile com-
can upregulate the expression of
pounds [46], suggesting that female plants could use floral volatiles as a cue to hermaphroditic neighbors.
herbivore defense genes.
10 Trends in Plant Science, January 2016, Vol. 21, No. 1
snapdragon leaf volatiles. Although this study [20] establishes that floral volatiles can function as Signal: a trait displayed by an
individual with the specific intent of
cues to other plants in a laboratory environment, it does not ascertain whether floral volatiles also
communicating with and changing
function as cues to other plants in more complex field environments (Box 2). Below we describe
the behavior of a receiver. For
fl fi
the evidence that oral volatiles can be perceived by other plants growing in the eld, and that example, floral volatiles can signal the
plants can use these volatiles to gain information about the mating environment. presence of nectar rewards to a
pollinator. A signal can be transmitted
through the air or the soil.
Floral Volatiles Are Likely To Be Perceived by Other Plants
Volatile organic compounds
fl
Volatiles are emitted by all plant organs, including leaves, stems, fruits, and owers. The (VOCs): low molecular weight
likelihood that these volatiles will be perceived by other plants depends on two factors: first, compounds with a low vapor
pressure at moderate temperatures.
the concentration of the volatiles in the atmosphere; and, second, the amount of time that a plant
Plants can emit VOCs from all their
is exposed to the volatiles [21]. Consequently, volatile compounds that are emitted at a low rate
organs, including leaves, stems,
or for a short duration are less likely to function as a cue to other plants than compounds that are flowers, and fruits.
emitted at a high rate or for a long duration.
Floral volatile compounds are likely to be emitted at a sufficiently high rate and/or long duration to
be perceived by other plants. Floral volatiles represent a significant proportion of the total flux of
VOCs emitted by plants [22], and are emitted at a higher rate than leaf volatiles [23]. Given that
leaf volatiles can be perceived by other plants, it is likely that floral volatiles are emitted at a
sufficiently high rate to also be perceived by other plants.
Plants Can Use Floral Volatiles To Gain Information about the Mating Environment
Floral volatiles are likely to convey reliable, ecologically-relevant information about the mating
environment for three reasons. First, many of the volatile compounds emitted by flowers are not
emitted by other plant organs [3], and floral volatile emission can vary across the phases of floral
development; for example, unopened buds emit different volatiles than open flowers [24,25].
Consequently, plants could use floral volatile cues to sense whether their neighbors are in flower.
Second, relative to leaves and stems, flowers emit a greater diversity of volatile compounds [26];
over 1700 compounds have been identified from angiosperm flowers [26], and the identity,
amount, and ratio of volatile compounds in the floral scent bouquet varies among species [3].
Consequently, plants could use floral volatile cues to sense the identity of their flowering
neighbors, such as whether they are conspecifics that could act as mates, or heterospecifics
that could compete for or facilitate pollination. Third, pollinated flowers can emit different volatiles
than unpollinated flowers [27]. Plants could use the unique volatiles produced by pollinated
flowers to sense the presence of pollinators, in the same way as they use herbivore-induced
plant volatiles to sense the presence of herbivores.
How Could Plants Respond to Information from Floral Volatile Cues?
We can make two general predictions about how plants should adjust their phenotype in
response to floral volatile cues. First, because floral volatiles convey information about the mating
environment, plants should respond by adjusting their floral traits. Second, because long lag-
times place a limit on the evolution of adaptive plasticity (Box 3), plants should adjust floral
traits for which there is a short lag-time between when the volatile cue is perceived and when the
new phenotype is produced. If the time between perceiving a floral volatile cue and producing a
new floral phenotype is long relative to temporal variation in the mating environment, then
eavesdropping on floral volatiles will not be adaptive.
Below we describe three traits that plants are particularly likely to adjust in response to floral
volatile cues: the rate of flower opening, floral nectar rewards, and floral volatile signals. All these
traits affect pollination and mating, change rapidly in response to environmental cues, and can
reduce fitness if mismatched to the mating environment. For each trait, we describe how plants
could adjust their phenotype in response to information about heterospecific competitors for
pollination, as an example of how eavesdropping on floral volatiles could be adaptive.
Trends in Plant Science, January 2016, Vol. 21, No. 1 11
Box 2. Methods for Testing Whether Volatiles Function as Cues
To test whether plants perceive and respond to floral volatile cues, we need to compare plants that have been
experimentally exposed to floral volatiles versus unexposed control plants. However, there are multiple methods for
experimentally manipulating the volatile signal that a plant is exposed to (Figure IA), and the choice of method affects how
the results are interpreted. We describe these methods and their interpretation below.
Three methods can be used to experimentally expose a plant to floral volatiles (Figure IB): (i) expose a plant to a co-
flowering plant; (ii) expose a plant to floral volatile emissions from a co-flowering plant; and (iii) expose a plant to a synthetic
floral volatile compound or compounds. The first method can establish that a plant responds to the presence of a
co-flowering plant, but does not isolate floral volatiles as the cue. The second method can establish that a response to
a co-flowering plant is elicited by an airborne floral volatile cue. The third method can identify the specific floral volatile
compound or compounds that elicit a response.
Plants that have been experimentally exposed to floral volatiles can be compared to negative and/or positive controls. In a
negative control, a plant is exposed to ambient air to establish plant behavior in the absence of the floral volatile cue. In a
positive control, a plant is exposed to volatiles emitted by other portions of the shoot organ system such as leaves; if
a plant does not respond to leaf volatiles, but does respond to floral volatiles, then we can conclude that plants can
distinguish between different types of volatile cues and respond appropriately.
The methods described above can be used to test whether plants respond to floral volatile cues in both laboratory and
field environments. Although laboratory experiments are necessary to determine whether plants can respond to floral
volatile cues, they are not sufficient to determine whether plants do respond to these cues in the field. In the field, plants
are exposed to a wide array of volatiles, as well as weather conditions and pollution that can degrade volatile signals [47].
Consequently, some floral volatiles may function as cues to other plants in the lab but not in the field. Field experiments
are thus necessary to determine whether eavesdropping on floral volatile cues is common enough to affect the ecology
and evolution of plant populations.
(A)
Manipula on Control
Flowering plant Lab (–) Blank or or Floral vola les and/or Field or (+) Plant vola les Synthe c compounds
(B)
(i) (ii) (iii)
Figure I. Methods for Testing Whether Plants Respond to Floral Volatile Cues. (A) An overview of the
experimental design described in Box 2, including potential experimental floral volatile treatments and control groups.
(B) Three methods for experimentally manipulating the floral volatiles that a plant is exposed to. (i) Exposing a plant to a co-
flowering plant. (ii) Exposing a plant to floral volatile emissions from a co-flowering plant. (iii) Exposing a plant to synthetic
floral volatile compound(s).
12 Trends in Plant Science, January 2016, Vol. 21, No. 1
Box 3. Plasticity in Response to Temporal Environmental Variation
Many organisms live in environments that vary temporally within a single generation (i.e., fine-grained environmental
variation). In response to this environmental variation, individuals can adjust their phenotype (phenotypic plasticity). If
individuals that adjust their phenotype have higher fitness than non-plastic individuals, then adaptive plasticity can evolve
[48].
Given that the mating environment can vary within a flowering season [49,50], and plants can adjust their floral traits [29],
adaptive plasticity in floral traits could evolve. However, not all phenotypic plasticity is adaptive [51,52], and there have
been no direct tests of whether plants that adjust their floral traits in response to fine-grained variation in the mating
environment have higher fitness than non-plastic individuals. To test whether plasticity in floral traits is adaptive, individual
plants need to be sequentially exposed to different mating environments – for example, scarce versus abundant
pollinators. Plasticity would be estimated as the floral trait value when the plant was in the scarce pollinator treatment
minus the floral trait value when the plant was in the abundant pollinator treatment. Fitness for each plant would be
estimated at the end of the experiment, after exposure to both pollinator treatments. If individual plants with more plastic
floral traits have higher fitness across both mating environments, then we can conclude that plasticity is adaptive. For an
example of this experimental design applied to different types of environments and traits, see [53].
The evolution of adaptive plasticity in response to fine-grained environmental variation can be limited by an organism's
ability to produce a phenotype that matches its environment [54,55]; an organism that produces a phenotype that
matches its environment will have higher fitness than an organism that produces a mismatched phenotype. An organism
may produce a mismatched phenotype for two reasons. First, an organism may unable to sense its environment: either
the cues to the environment are not reliable or the environment changes too rapidly (i.e., information reliability limit [54]).
Second, an organism may produce a mismatched phenotype because too much time elapses between sensing and
responding to an environmental cue (i.e., lag-time limit [54]). These limits on the evolution of plasticity suggest that plant
responses to floral volatile cues are most likely to be adaptive when volatiles convey reliable information about the mating
environment, and when plants can quickly respond by developing a new floral phenotype.
The Rate of Flower Opening
The rate at which a plant sequentially opens its flowers can affect pollination and mating by
determining the number of flowers that are simultaneously displayed [28,29]. Plants can open
flowers within minutes of perceiving temperature and light cues [30], suggesting that they have the
physiological ability to rapidly adjust their rate of flower opening. In response to floral volatile cues to
the presence a competitor for pollination, a plant could increase its rate of flower opening and thus
produce a larger floral display. Large floral displays can increase pollinator visitation in the presence
of a competitor [31], suggesting that adjusting the rate of flower opening could be adaptive.
Floral Nectar Rewards
Floral nectar rewards can affect pollination and mating by manipulating pollinator behavior and
by extension the movement of pollen [32,33]. The quantity, quality, and/or chemical composition
of floral nectar can change, for example, within minutes of visits by nectar robbers [34] and within
hours of simulated visits by pollinators [35], suggesting that plants have the physiological ability
to rapidly adjust their nectar rewards. Because pollinators can alter their preference for nectar
rewards depending on the availability of alternative resources [36], a plant could respond to floral
volatile cues to the presence of a competitor for pollination by producing more nectar. In the
presence of a competitor, producing more floral nectar can increase pollinator visitation and
fitness [32,37].
Floral Volatile Signals
Floral scent bouquets can affect pollination and mating by simultaneously attracting some
pollinator taxa while repelling others [38]. The degree of attraction and repellence can be
determined by the dosage of particular compounds (e.g. [39]), suggesting that both the identity
of the compounds that are emitted and the rate of emission can affect pollination and mating.
The chemical composition and emission rate of floral scent bouquets can change within minutes
in response to environmental cues such as increased temperature [40], suggesting that plants
could rapidly alter their own floral volatile production in response to floral volatile cues from their
neighbors. For example, in response to cues to the presence of a competitor for pollination, a
Trends in Plant Science, January 2016, Vol. 21, No. 1 13
plant could produce more floral volatiles. This increase in floral volatile emission could attract Outstanding Questions
fl
more pollinators, which could increase plant fitness [41]. Could oral volatiles function as cues to
other plants? Are common or unique
floral volatile compounds more likely to
Which Ecological Conditions Favor Eavesdropping on Floral Volatiles?
be perceived by other plants? Are
fl fl
Even if oral volatiles commonly function as cues to other plants, not all oral volatile signals will complex bouquets of volatile com-
be equally vulnerable to eavesdropping. Instead, the likelihood that a plant will perceive and pounds or individual compounds emit-
ted by flowers more likely to convey
respond to floral volatiles should vary predictably depending on ecological conditions. Because
information about the mating environ-
cue reliability places a limit on the evolution of adaptive plasticity (Box 3), we predict that plants
ment? How do plants distinguish
fl
should be more likely to perceive and respond to oral volatiles in ecological conditions where between their own floral volatiles and
those produced by their neighbors?
these volatiles provide reliable information about the mating environment. If floral volatile cues
provide unreliable information about the mating environment, then eavesdropping on floral
How could plants respond to informa-
volatiles will not be adaptive.
tion from floral volatile cues? How
quickly can plants respond to informa-
tion from floral volatile cues? Are plants
Three ecological conditions should increase the likelihood that a plant receives a reliable floral
more likely to respond to information
volatile cue: high plant densities, high temperatures, and the presence of plants that produce
from floral volatile cues by adjusting
chemically-unique floral scent bouquets. High plant densities will decrease the distance between
floral traits that function as signals or
a plant and its neighbors, which should increase the reliability of floral volatile cues by decreasing as rewards?
the likelihood that the signal will degrade before it can be perceived by other plants. High
Are plant responses to floral volatile
temperatures can increase the rate of floral volatile emission [40], and this should increase the
cues likely to be adaptive? Is plasticity
fl
reliability of oral volatile cues by increasing the amount of signal that is available to be perceived in response to floral volatile cues more
fi
by other plants. Plants that produce unique floral scent bouquets should be more likely to likely to affect male or female tness in
hermaphroditic plant species? What
provide reliable floral volatile cues because they can produce signals that encode very specific
limits the evolution of plasticity in
information about the mating environment [3]. For example, floral volatiles used in private
response to floral volatile cues (e.g.,
communication between plants and their pollinators [42] should be more likely to provide information reliability vs lag-time limits;
reliable cues to the presence of flowering heterospecific plants, whereas floral volatiles produced Box 3)?
after pollination [27] should be more likely to provide reliable cues to the presence of pollinators.
Which ecological conditions favor
eavesdropping on floral volatiles? Do
Concluding Remarks plants respond differently to floral vola-
tile cues from competitors for pollina-
We conclude that floral volatiles are equally likely as other volatiles to function as cues to other
tion versus species that facilitate
plants. Moreover, eavesdropping on floral volatiles cues is more likely to increase fitness than
pollination? Does eavesdropping only
eavesdropping on other volatile signals because floral volatiles are the only volatile signals
occur between plants that share polli-
emitted by plants that have the potential to convey information about the mating environment. nators or antagonists?
Consequently, plants should respond to floral volatile cues by adjusting floral traits, and floral
traits are unique among plant traits in directly affecting pollination, mating, and thus fitness [43].
However, the possibility that plants eavesdrop on floral volatiles has generally been ignored both
by researchers studying floral scent signals [44] and by researchers studying plant–plant
communication [5]. Therefore, most questions about the nature and extent of eavesdropping
on floral volatiles remain unanswered (see Outstanding Questions). Answering these questions
will be important because if floral volatiles commonly function as cues to other plants, then we
have underestimated the ability of plants to perceive and respond to their environment.
Acknowledgments
We thank R. Rivkin for discussion and two anonymous reviewers for comments on an earlier version of the manuscript.
During the writing of this manuscript C.M.C. was supported by a Discovery Grant from the Natural Science and Engineering
Research Council of Canada.
References
1. Dudareva, N. et al. (2013) Biosynthesis, function and metabolic 3. Raguso, R.A. (2008) Wake up and smell the roses: The ecology
engineering of plant volatile organic compounds. New Phytol. 198, and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39,
16–32 549–569
2. Rodríguez, A. et al. (2013) Fruit aromas in mature fleshy fruits as 4. Heil, M. (2014) Herbivore-induced plant volatiles: targets,
signals of readiness for predation and seed dispersal. New Phytol. perception and unanswered questions. New Phytol. 204,
197, 36–48 297–306
14 Trends in Plant Science, January 2016, Vol. 21, No. 1
5. Karban, R. (2015) Plant Sensing and Communication, University of 31. Brown, B.J. et al. (2002) Competition for pollination between an
Chicago Press invasive species (purple loosestrife) and a native congener. Ecol-
ogy 83, 2328–2336
6. Heil, M. and Karban, R. (2010) Explaining evolution of plant com-
munication by airborne signals. Trends Ecol. Evol. 25, 137–144 32. Hodges, S.A. (1995) The influence of nectar production on hawk-
moth behavior, self pollination, and seed production in Mirabilis
7. Kegge, W. and Pierik, R. (2010) Biogenic volatile organic com-
multiflora (Nyctaginaceae). Am. J. Bot. 82, 197
pounds and plant competition. Trends Plant Sci. 15, 126–132
33. Kessler, D. et al. (2012) Unpredictability of nectar nicotine promotes
8. Karban, R. et al. (2014) Volatile communication between plants
outcrossing by hummingbirds in Nicotiana attenuata: variability in
that affects herbivory: a meta-analysis. Ecol. Lett. 17, 44–52
nectar nicotine promotes outcrossing. Plant J. 71, 529–538
9. Karban, R. et al. (2000) Communication between plants: induced
34. Kaczorowski, R.L. et al. (2014) Immediate effects of nectar robbing
resistance in wild tobacco plants following clipping of neighboring
by Palestine sunbirds (Nectarinia osea) on nectar alkaloid concen-
sagebrush. Oecologia 125, 66–71
trations in tree tobacco (Nicotiana glauca). J. Chem. Ecol. 40,
10. Morrell, K. and Kessler, A. (2014) The scent of danger – volatile-
325–330
mediated information transfer and defence priming in plants. Bio-
35. Castellanos, M.C. et al. (2002) Dynamic nectar replenishment in
chemist 36, 26–31
flowers of Penstemon (Scrophulariaceae). Am. J. Bot. 89, 111–118
11. Kessler, A. et al. (2006) Priming of plant defense responses in
36. Gegear, R.J. et al. (2007) Ecological context influences pollinator
nature by airborne signaling between Artemisia tridentata and
deterrence by alkaloids in floral nectar. Ecol. Lett. 10, 375–382
Nicotiana attenuata. Oecologia 148, 280–292
37. Brandenburg, A. et al. (2012) Hawkmoth pollinators decrease
12. Glinwood, R. et al. (2011) Chemical interaction between undam-
seed set of a low-nectar Petunia axillaris line through reduced
aged plants – effects on herbivores and natural enemies. Phyto-
probing time. Curr. Biol. 22, 1635–1639
chemistry 72, 1683–1689
38. Junker, R.R. et al. (2010) Responses to olfactory signals reflect
13. Runyon, J.B. et al. (2006) Volatile chemical cues guide host location
network structure of flower–visitor interactions. J. Anim. Ecol. 79,
and host selection by parasitic plants. Science 313, 1964–1967
818–823
14. Kigathi, R.N. et al. (2013) Plants suppress their emission of volatiles
39. Galen, C. et al. (2011) Dosage-dependent impacts of a floral
when growing with conspecifics. J. Chem. Ecol. 39, 537–545
volatile compound on pollinators, larcenists, and the potential
15. Ninkovic, V. et al. (2013) Volatile exchange between undamaged
for floral evolution in the alpine skypilot Polemonium viscosum.
plants – a new mechanism affecting insect orientation in intercrop-
Am. Nat. 177, 258–272
ping. PLoS ONE 8, e69431
40. Farré-Armengol, G. et al. (2014) Changes in floral bouquets from
16. Vucetic, A. et al. (2014) Volatile interaction between undamaged
compound-specific responses to increasing temperatures. Glob.
plants affects tritrophic interactions through changed plant volatile
Change Biol. 20, 3660–3669
emission. Plant Signal. Behav. 9, e29517
41. Majetic, C.J. et al. (2009) The sweet smell of success: floral scent
17. Dahlin, I. et al. (2014) Changed host plant volatile emissions
affects pollinator attraction and seed fitness in Hesperis matrona-
induced by chemical interaction between unattacked plants
lis. Funct. Ecol. 23, 480–487
reduce aphid plant acceptance with intermorph variation. J. Pest
42. Schäffler, I. et al. (2015) Diacetin, a reliable cue and private com-
Sci. 88, 249–257
munication channel in a specialized pollination system. Sci. Rep. 5,
18. Raguso, R.A. (2009) Floral scent in a whole-plant context: moving
12779
beyond pollinator attraction. Funct. Ecol. 23, 837–840
43. Harder, L.D. and Johnson, S.D. (2009) Darwin's beautiful con-
19. Schiestl, F.P. and Johnson, S.D. (2013) Pollinator-mediated evo-
trivances: evolutionary and functional evidence for floral adapta-
lution of floral signals. Trends Ecol. Evol. 28, 307–315
tion. New Phytol. 183, 530–545
20. Horiuchi, J. et al. (2007) The floral volatile, methyl benzoate, from
44. Parachnowitsch, A.L. and Manson, J.S. (2015) The chemical
snapdragon (Antirrhinum majus) triggers phytotoxic effects in
ecology of plant–pollinator interactions: recent advances and
Arabidopsis thaliana. Planta 226, 1–10
future directions. Curr. Opin. Insect Sci. 8, 41–46
21. Girón-Calva, P.S. et al. (2012) Volatile dose and exposure time
45. Rivkin, L.R. et al. (2015) Frequency-dependent fitness in gyno-
impact perception in neighboring plants. J. Chem. Ecol. 38,
dioecious Lobelia siphilitica. Evolution 69, 1232–1243
226–228
46. Ashman, T-L. et al. (2005) The scent of a male: the role of floral
22. Baghi, R. et al. (2012) Contribution of flowering trees to urban
volatiles in pollination of a gender dimorphic plant. Ecology 86,
atmospheric biogenic volatile organic compound emissions. Bio-
2099–2105
geosciences 9, 3777–3785
47. Wilson, J.K. et al. (2015) Noisy communication via airborne info-
23. Ibrahim, M.A. et al. (2010) Diversity of volatile organic compound
chemicals. Bioscience 65, 667–677
emissions from flowering and vegetative branches of Yeheb, Cor-
48. Pigliucci, M. (2001) Phenotypic Plasticity: Beyond Nature and
deauxia edulis (Caesalpiniaceae), a threatened evergreen desert
Nurture, Johns Hopkins University Press
shrub. Flavour Fragr. J. 25, 83–92
49. Brookes, R.H. and Jesson, L.K. (2010) Do pollen and ovule
24. Steenhuisen, S-L. et al. (2010) Variation in scent emission among
number match the mating environment? An examination of tem-
floral parts and inflorescence developmental stages in beetle-polli-
poral change in a population of Stylidium armeria. Int. J. Plant Sci.
nated Protea species (Proteaceae). South Afr. J. Bot. 76, 779–787
171, 818–827
25. Burdon, R.C.F. et al. (2015) Spatiotemporal floral scent variation of
50. Price, M.V. et al. (2005) Temporal and spatial variation in polli-
Penstemon digitalis. J. Chem. Ecol. 41, 641–650
nation of a montane herb: a seven-year study. Ecology 86,
26. Knudsen, J.T. et al. (2006) Diversity and distribution of floral scent.
2106–2116
Bot. Rev. 72, 1–120
51. Palacio-López, K. et al. (2015) The ubiquity of phenotypic plasticity
27. Schiestl, F.P. and Ayasse, M. (2001) Post-pollination emission of a
in plants: a synthesis. Ecol. Evol. 5, 3389–3400
repellent compound in a sexually deceptive orchid: a new mech-
52. Winn (1999) Is seasonal variation in leaf traits adaptive for the
anism for maximising reproductive success? Oecologia 126,
–
531–534 annual plant Dicerandra linearifolia? J. Evol. Biol. 12, 306 313
53. Van Kleunen, M. et al. (2007) Selection on phenotypic plasticity of
28. Harder, L.D. and Prusinkiewicz, P. (2012) The interplay between
morphological traits in response to flooding and competition in
inflorescence development and function as the crucible of archi-
the clonal shore plant Ranunculus reptans. J. Evol. Biol. 20,
tectural diversity. Ann. Bot. 112, 1477–1493
2126–2137
29. Harder, L.D. and Johnson, S.D. (2005) Adaptive plasticity of floral
54. DeWitt, T.J. et al. (1998) Costs and limits of phenotypic plasticity.
display size in animal-pollinated plants. Proc. R. Soc. Lond. B: Biol.
Trends Ecol. Evol. 13, 77–81
Sci. 272, 2651–2657
55. Scheiner, S.M. (2013) The genetics of phenotypic plasticity. XII.
30. van Doorn, W.G. and van Meeteren, U. (2003) Flower opening and
Temporal and spatial heterogeneity. Ecol. Evol. 3, 4596–4609
closure: a review. J. Exp. Bot. 54, 1801–1812
Trends in Plant Science, January 2016, Vol. 21, No. 1 15