Available online at www.sciencedirect.com
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Olfaction in context — sources of nuance in plant–pollinator communication
1,3 2,3 2
Claire Rusch , Geoffrey T Broadhead , Robert A Raguso
1
and Jeffrey A Riffell
Floral scents act as long-distance signals to attract pollinators, choice [1,2]; thus in this review we focus on recent
but volatiles emitted from the vegetation and neighboring plant progress in understanding the behavioral and neural
community may modify this mutualistic communication underpinnings of the olfactory channel in plant–pollinator
system. What impact does the olfactory background have on communication, with an emphasis on how context and
pollination systems and their evolution? We consider recent background influence the detection and perception of
behavioral studies that address the context of when and where floral volatile signals. We begin with an overview of the
volatile backgrounds influence a pollinator’s perception of floral insect olfactory system relevant to distinguishing com-
blends. In parallel, we review neurophysiological studies that plex volatile blends from a noisy background. Here we
show the importance of blend composition and background in discuss how environmental factors influence how insect
modifying the representation of floral blends in the pollinator brains process floral scent bouquets. Next, we explore
brain, as well as experience-dependent plasticity in increasing how experience modifies olfactory processing. Finally, we
the representation of a rewarding odor. Here, we suggest that conclude with an exciting topic for future research by
the efficacy of the floral blend in different environments may be examining how signal efficacy — the interplay between
an important selective force shaping differences in pollinator signal composition and environmental background —
olfactory receptor expression and underlying neural may feedback on the speciation process in plants, through
mechanisms that mediate flower visitation and plant reproductive isolation and reinforcement.
reproductive isolation.
Addresses
1 Pollinator behavior to complex odor sources
Department of Biology, University of Washington, Seattle, WA 98195,
United States and environments
2
Department of Neurobiology and Behavior, Cornell University, Ithaca, Efficiency and accuracy of behavioral decisions in
NY 14853, United States
response to behaviorally effective odors and
environmental background odors
Corresponding authors: Raguso, Robert A ([email protected]) and
Riffell, Jeffrey A ([email protected]) Insect pollinators forage for nectar and pollen in habitats
3
Contributed equally to this paper. rife with potentially distracting sources of volatile organic
compounds (VOCs). These ‘background odorants’ in-
Current Opinion in Insect Science 2016, 15:53–60
clude the volatile signatures of organic decay and of living
This review comes from a themed issue on Behavioral ecology vegetation in a community assemblage of flowering and
Edited by Lars Chittka and Deborah Gordon fruiting plants [3], including those of competing floral
resources. Floral scent blends have long been character-
ized as species-specific [4], and there is growing experi-
mental evidence that when bouquets of neighboring
http://dx.doi.org/10.1016/j.cois.2016.03.007 plants are too similar, they suffer reduced pollinator
2214-5745/# 2016 Elsevier Inc. All rights reserved. constancy or breakdowns in reproductive isolation [5].
The challenge of distinguishing a target VOC blend —
whether innately attractive or learned [6,7] — within a
complex olfactory scene recalls the problem of signal ac-
ceptance threshold in social evolution, in which uncertainty
Introduction increases the risk of an incorrect decision [8]. From an
A challenge inherent to communication is how senders information theory standpoint, Wilson et al. [9 ] suggest that
convey reliable information to receivers within a noisy redundant VOC bouquets reduce uncertainty, which may
and unpredictable environment. Effective communica- explain why many resource-indicating odors are blends [10].
tion is fundamental to mutualistic as well as deceptive Thus, distinguishing an olfactory target from ‘background’
relationships between flowering plants and their animal might require it to be chemically, spatially or temporally
pollinators, as it mediates gene flow and reproductive distinct from other features in the same habitat [11 ].
isolation for plants while driving flower choice and forag-
ing efficiency for pollinators. There have been several Beyond the distinctiveness of a floral bouquet is its
recent reviews on multimodal floral signals and pollinator compatibility with background VOCs. This might include
www.sciencedirect.com Current Opinion in Insect Science 2016, 15:53–60
54 Behavioral ecology
whether neighboring plants emit masking compounds or system that can detect and discriminate target VOC blends
repellents [3,12], reducing floral visitation or constancy. at short (<500 ms) timescales. Building on recent reviews
By swapping floral and vegetative VOCs from Datura [24–26], we focus on neural mechanisms in the peripheral
wrightii and Nicotiana attenuata, Karpati et al. [13 ] discov- (olfactory receptor neurons [ORNs] located on antennae
ered unexpected coaction between floral and vegetative and maxillary palps) and higher-level olfactory centers
volatiles, such that floral visitation by naı¨ve Manduca sexta (antennal lobe [AL] and mushroom body [MB]) by which
moths (which use these plants as larval hosts) was reduced insect pollinators distinguish a target VOC blend from a
in cross-species combinations. These findings reflect con- complex chemical background (Figure 1; Table 1). The
flicting selective pressures driving plants to enhance magnitude and temporal dynamics of ORN responses
pollinator services while mitigating herbivory [14]. In a allow rapid detection of salient VOCs from a floral source.
more extreme example of signal integration, Dufay¨ For instance, ORNs are extremely sensitive to the onset of
et al. [15] showed that the flowers of the dwarf palm odorant delivery; latency between ORN responses thus
(Chamaerops humilis) are pollinated by a specialized wee- allows the system to respond to spatially separated odor
vil attracted by the scent of leaves subtending the inflo- sources whose plumes are not entirely mixed. Szyszka and
rescence, which emit volatiles only when flowers are coworkers [27,28 ] found that bees and moths can resolve
receptive. It remains unclear whether certain community odorant fluctuations greater than 100 Hz, with response
contexts synergize floral attraction through signal contrast latencies as short as 2 ms. Thus, even when odor plumes
between neighboring species. This idea differs from the begin to blend together, the VOC filaments from the
‘magnet species’ effect, in which food deceptive plants different plumes are distinct enough to enable a pollinator
are more frequently visited when they co-bloom with to resolve the differences between the two plumes. An
other, rewarding species, often with contrasting floral additional feature for processing stimuli from background
signals [16,17]. However, their similarity resides in the is that ORNs which respond to different constituents in a
notion that some neighbors enhance pollination by alter- blend are often housed in the same sensillum [29,30],
ing the information landscape [7], an intriguing extension enabling coincident activation of ORN types for detection
of associational resistance and susceptibility [18]. of behaviorally effective blends. Finally, sensory adapta-
tion may be another process by which pollinators detect
The concept of synergy between olfactory inputs is well floral VOCs from background, but few field studies have
established in the case of insect sex pheromone signals linked adaptation with characterization of the VOC envi-
emitted in the presence of host-plant volatile cues [19]. ronment. In wind tunnel bioassays, moths adapted to
More recent work demonstrates that the enhancement or natural backgrounds were rarely able to locate the odor
inhibition of olfactory signals is dependent on the source sources; this effect was due to the combination of sensory
of background odorants as well as physical odor plume adaptation and the background ‘masking’ the floral VOCs
characteristics [20,21]. Within the context of plant–polli- because of its overlapping composition [11 ].
nator interactions, Riffell et al. [11 ] evaluated the neural
and behavioral responses of M. sexta moths tracking floral The balance of excitatory input by ORNs and inhibition
VOCs against various chemical backdrops using wind by LNs is critical both for processing floral VOCs and for
tunnel assays. These results highlight the potential for suppressing activation of PNs in response to background
co-occurring plants to alter the olfactory perception and (Figure 2). Recent studies of Spodoptera littoralis moths
behavior of pollinators. Larue et al. [22 ] further explored exemplify the importance of physiological state and AL
the influence of chemical context in a manipulative field modulation in olfactory processing. In virgin females, the
experiment. Here, plant–pollinator network links were AL glomerular representation of lilac scent is enhanced
significantly altered after the reciprocal application of relative to vegetative VOC blends, but after mating, the
floral scent extracts, in some cases due to attractants, in representation of host (cotton leaf) VOCs is enhanced and
other cases due to repellents. Nevertheless, few network other scents are suppressed [31]. Similarly, Stierle et al. [32]
interactions were lost entirely, suggesting that in the face showed that separability in AL glomerular representations
of confusing olfactory information pollinator experience of two complex VOC blends improves with increased time
or multimodal integration (e.g. with visual display) may between stimulation of the two blends in honey bees.
reinforce plant–pollinator interactions. Collectively, Longer time between stimulations enhances the represen-
these experiments support the importance of olfactory tation of blend constituents in the AL glomerular response
background and context and indicate that models of floral patterns [32], such that levels of inhibition and blend
constancy should account for multimodal floral displays separability are correlated with temporal offset between
rather than focusing on a single, isolated modality [23]. the competing blends. In a similar manner, M. sexta moths
require an intact AL inhibitory network for effective
How the olfactory system detects and discriminates navigation to a blend of a few key odorants. When floral
between focal odorants and environmental background VOCs are presented in a background that shares similar
The ability of pollinators to locate floral resources amidst constituents — including those from anthropogenic
a complex olfactory environment requires an olfactory sources — both the spatial AL glomerular representations
Current Opinion in Insect Science 2016, 15:53–60 www.sciencedirect.com
Olfactory basis of plant–pollinator interactions Rusch et al. 55
Figure 1
(a) (d)
Multisensory inputs
(b) (c)
Learned behavior
via lateral horn, protocerebrum, ... Innate behavior
Current Opinion in Insect Science
Peripheral and central regions of the olfactory system for the detection and processing of floral and background scents. (a) Honey bee
approaching a flower. (b) Depiction of a sensillum on the antennae. ORNs response (latencies, coincidence detectors, among others
[27,28 ,29,30]) may play a key role in processing floral scents from background. Inset: location of antennal sensillum on honeybee head. (c)
Processing of floral scents and associated background may rely on lateral inhibition. Inset: location of the AL in the honeybee brain [11 ,32]. (d)
Multisensory integration and retrieval of previously experienced sensory information in the MB may increase the accuracy of a pollinator locating a
flower [1,49]. Inset: location of the MB in the honeybee brain. ORN: olfactory receptor neurons, AL: antennal lobe, MB: mushroom body.
Source: Photo credit: Emile Pitre.
and the temporal dynamics of PN coding are lost (Figure 2) what occurs when the background synergizes responses to
[11 ]. floral scent, as discussed above for the flowers and vege-
tation of D. wrightii and the dwarf palm (C. humilis)? One
These examples highlight how a complex background explanation is that the background shares the same VOC
can alter the neural representation of floral VOCs, but ratio as the floral blend, thereby maintaining patterns of
Table 1
The ABCs of the beginning stages of the pollinator olfactory system implicated in processing focal floral blends and volatile backgrounds.
Level Cell types Effect Reference
Antenna and ORNs Activated by odorants; tuning and temporal specificity [24,27]
maxillary palps Spatial coincidence detectors [29]
Antennal lobe PNs Receive input from ORNs; show tuning and temporal specificity [32,34,36,44,47]
to floral odorants
LNs Receive input from ORNs; GABA-mediated inhibition of ORNs [11 ,24,44]
and PNs
Circuit level activity of PNs, LNs Synchronous firing to floral blend constituents [34,47]
Circuit level activity of PNs, LNs Changing the volatile blend or background can change the [11 ,33–35]
balance of excitation and inhibition in the AL
Octopaminergic neurons; circuit Octopamine release increases gain of AL responses; increases [46 ,47]
level activity of PNs, LNs PN synchrony
Mushroom Kenyon cells Kenyon cells receive input from many PNs; forms a memory [24,26]
body — calyces trace
Octopaminergic neurons; Coincident activation of PN input and octopamine increases [26,47–50]
Kenyon cells synaptic strength of Kenyon cells
www.sciencedirect.com Current Opinion in Insect Science 2016, 15:53–60
56 Behavioral ecology
Figure 2
?
HIGH CONTRAST HIGH CONTRAST LOW CONTRAST INNATE RESPONSE LEARNED RESPONSE
Current Opinion in Insect Science
Impact of olfactory environment on AL processing of floral scents. (Left, top): moth navigating to, and feeding from a Datura flower that emits a
distinct scent from the local plant community. (Left, bottom): in the AL, the floral scent activates strong lateral inhibition between neighboring
glomeruli that serves to increase the neural representation of the flower scent and separate it from the background scents [11 ,31,32]. (Middle,
top): moth navigating to, and feeding from an Agave flower as a result of a learned behavior. (Middle, bottom): in the AL, the learned floral scent
impact the ratio of lateral inhibition, modifying olfactory preference [6,36,47–50]. (Right, top): moth navigating in a low contrast olfactory
environment. (Right, bottom): the plant community may emit a key volatile present also in the floral scent, thereby altering the excitation and
inhibition and thus reducing distinctiveness of its representation [11 ].
Source: Photo credit: Charles Hedgcock.
glomerular representation, excitation and inhibition in the modifies innate olfactory and behavioral discrimination by
AL. Alternately, the background may include a key volatile foraging insects. Do the volatile templates used by naı¨ve
that, when combined with the scent, elicits a new neural insects to find floral resources change when those insects
representation and increase in behavioral response [33]. learn to associate some aspect of profitability (quality,
abundance) with volatile stimuli [37,38]? Naı¨ve bumble-
How previous experience impacts locating a bees (Bombus terrestris) are innately attracted to the floral
focal odor and amidst the environmental scent of Brassica rapa, but show no behavioral preferences
background to electrophysiologically active compounds (e.g. phenyla-
Pollinator behavioral ecology and the role of learning cetaldehyde). However, experienced bees prefer pheny-
Recent studies have advanced our understanding of how lacetaldehyde, which is strongly correlated with nectar and
volatile blends are perceived, coded and tracked by insects pollen content in B. rapa flowers [39 ]. The salience of
seeking floral rewards and hostplants [34,35]. For example, learned volatiles may also reflect statistical aspects of
inhibitory interactions among antennal lobe glomeruli conditioned volatile stimuli, including their concentration
enhance the distinctiveness of specific volatile blends as and (in)variance [37]. Finally, innate preferences may be
perceived by honey bees ([36]; see Figure 2). A major overcome through the learning process, as was shown for
question complementing such studies is how experience M. sexta moths learn to associate a chemically novel scent
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Olfactory basis of plant–pollinator interactions Rusch et al. 57
with the copious nectar of Agave palmeri in the absence of As mentioned above in section IIA, a current gap lies in
D. wrightii flowers, whose scent they innately prefer ([6]; linking environmental processes in the field with con-
see Figure 2). trolled laboratory experiments examining the neural and
behavioral effects of learning on plant–pollinator inter-
Few natural environments resemble the conditions found actions. Nonetheless, controlled laboratory studies using
in laboratory olfactory associative learning experiments. various pollinator species have shown glimpses of how
For naı¨ve M. sexta, background odorants significantly olfactory learning may influence these interactions. For
affect odor-tracking ability [11 ], however wild, experi- example, after olfactory conditioning, a honeybee’s glo-
enced flower-visitors have clearly learned to navigate in merular responses are increased compared with those of
complex natural landscapes of competing olfactory sti- untrained bees; the increased responses serve to improve
muli. Despite the olfactory milieu characteristic of these the discrimination of trained stimuli [45]. Recently, Chen
natural scenes, few experiments have translated key et al. [46 ] examined how learning-mediated plasticity in
concepts of olfactory learning into more ecologically the AL modifies the representation of constituents in a
relevant contexts. For example, odor generalization, or blend. They found that training the association between a
the ability to transfer learned associations despite vari- sugar reward and an odorant, and stimulating with a blend
ability in the olfactory stimulus, is generally described as a containing that odorant, the AL neural representation is
potential mechanism for organisms to cope with the shifted toward the representation of the trained odorant
intrinsic variation characteristic of naturally occurring alone. Beyond single odorants, pollinators also readily
odor sources [40]. Yet, in odor discrimination tasks in learn natural scents and complex floral blends. As men-
which an incorrect decision risks a negative outcome, tioned above, M. sexta moths learn to associate nectar
pollinators may preferentially respond to more extreme reward with the floral scent of the century plant (Agave
versions of the original stimulus that are more detectably palmeri). During training, the AL neurons increase their
different from stimuli associated with a negative out- blend-evoked responses, thereby causing the AL repre-
come. Thus, the potential for negative outcomes can sentation to change. Similar to what was shown with
modify or narrow signal acceptance thresholds resulting honeybees, plasticity in the moth AL serves to increase
in an olfactory ‘peak-shift’ [8,41,42]. From controlled the separability between complex flower scents: during a
laboratory-based associative learning experiments (e.g. discrimination task between the scents of A. palmeri
[41,42]), it is clear that both generalization and peak- (rewarded) and the Saguaro cactus (Carnegiea gigantea;
shifted biases are strongly influenced by the conditioning unrewarded), the separability between AL representa-
paradigm, stimulus variability, and relative reward quali- tions of the two scents increased ([47]; Figure 2).
ty — suggesting the potential for extensive plasticity in
olfactory learning and recognition in more nuanced, nat- Learning-evoked changes in the pollinator olfactory sys-
ural environments. Further complicating matters, chemi- tem — often mediated by neuromodulators like octopa-
cal backgrounds and foraging contexts are not static and mine and dopamine, or GABA — can influence the
many species of flower-visiting insect are highly mobile representation of floral VOCs in the pollinator AL and
such that a given pollinator may experience a number of higher-order centers, including the MB [48]. For instance,
chemical landscapes within a single foraging event. Con- in honeybees, activation of an octopaminergic neuron,
sequently, in addition to learning phenomena (e.g. peak- VUMmx1, and stimulation with an odorant was sufficient
shifts and generalization) we must also consider the to trigger formation of an appetitive memory [48,49]. In
temporal dynamics of stimulus acquisition and extinction the AL octopamine increases responses in both PN and
in combination with species’ inherent, individual learning LNs and increases the coordinated activity of glomeruli
abilities [43] to fully understand the learning and recog- [47]. The coordinated glomerular responses ‘‘bind’’ to-
nition of rewarding floral resources in a dynamic environ- gether the representation of key VOCs from a blend —
ment. thereby creating a synergistic representation — and
increase responses of MB neurons (Kenyon cells) that
Experience related plasticity in olfactory processing and receive input from the AL (Table 1). The coordinated
focal blend-background separation input from the AL and octopamine release serves to form
Prior experience can influence pollinator olfactory proces- a ‘memory trace’ of the learned flower scent in the
sing through different mechanisms, including non-associa- Kenyon cells. The MB also provides inhibitory feedback
tive and associative processes. For example, Locatelli (via GABA release) to other brain regions, including the
et al. [44] showed in honeybees that repeated stimulation AL-PNs [50] and the Kenyon cells. This inhibitory feed-
of one floral odorant causes a shift in its AL representation back may be critical for focal blend discrimination from a
such that when it is paired with another odorant, the background; a tantalizing glimpse into this mechanism
resulting blend-evoked representation is more similar to comes from an elegant learning study in honeybees,
the second odorant. This non-associative change in neural where bees were trained to a rewarded blend but not
representation is thought to be mediated by increased its constituents, or the converse situation, in which the
inhibition from the LNs. constituents were rewarded, but not the blend (termed
www.sciencedirect.com Current Opinion in Insect Science 2016, 15:53–60
58 Behavioral ecology
IOS-1354159 (JAR), DMS-1361145 (JAR), DEB-1342792 (RAR), and the
positive and negative patterning, respectively). The
Human Frontiers in Science Program HFSP-RGP0022 (JAR).
authors showed that inhibitory feedback in the MBs is
required for accurate discrimination of the trained stimu- References and recommended reading
Papers of particular interest, published within the period of review,
lus [51 ]. This feedback is not necessary for simple
have been highlighted as:
olfactory conditioning, where the pollinator learns the
association between one odorant and the reward, but is of special interest
of outstanding interest
critical for blends or distinguishing an individual constit-
uent within a blend. Thus, inhibition and plasticity in the
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