Plants have developed a variety of strategies to defend themselves against herbivorous animals, particularly insects. In addition to mechanical defences such as thorns and spines, plants also produce compounds known as secondary metabolites that keep insects and other herbivores at bay by acting as repellents or toxins. Some of these metabolites are produced on a continuous basis by plants, whereas others—notably compounds called green-leaf volatiles—are only produced once the plant has been attacked. Green-leaf volatiles—which are also responsible for the smell of freshly cut grass—have been observed to provide plants with both direct protection, by inhibiting or repelling herbivores, and indirect protection, by attracting predators of the herbivores themselves.

The hawkmoth Manduca sexta lays its eggs on various plants, including tobacco plants and sacred Datura plants. Once the eggs have hatched into caterpillars, they start eating the leaves of their host plant, and if present in large numbers, these caterpillars can quickly defoliate and destroy it. In an effort to defend itself, the host plant releases green-leaf volatiles to attract various species of Geocoris, and these bugs eat the eggs.

One of the green-leaf volatiles released by tobacco plants is known as (Z)-3-hexenal, but enzymes released by M. sexta caterpillars change some of these molecules into (E)-2-hexenal, which has the same chemical formula but a different structure. The resulting changes in the ‘volatile profile’ alerts Geocoris bugs to the presence of M. sexta eggs and caterpillars on the plant.

Now Allmann et al. show that adult female M. sexta moths can also detect similar changes in the volatile profile emitted by sacred Datura plants that have been damaged by M. sexta caterpillars. This alerts the moths to the fact that Geocoris bugs are likely to be attacking eggs and caterpillars on the plant, or on their way to the plant, so they lay their eggs on other plants. This reduces competition for resources and also reduces the risk of newly laid eggs being eaten by predators. Allmann et al. also identified the neural mechanism that allows moths to detect changes in the volatile profile of plants—the E- and Z- odours lead to different activation patterns in the moth brain.

Insects rely on olfaction in most aspects of life: volatile signals guide them to food sources, mating partners and oviposition hosts. Especially for herbivorous insects, plant volatiles provide important cues to locate and identify appropriate host plants for their offspring. Upon herbivory, plants respond with an increased release and de novo synthesis of several volatile compounds from their vegetative tissues (Mumm and Dicke, 2010). These so-called herbivore induced plant volatiles can provide significant information to the surrounding environment as composition and abundance reflect several biotic and abiotic factors (Takabayashi et al., 1995; De Moraes et al., 1998; Gouinguené et al., 2001; Schuman et al., 2009; Hare, 2010).

Due to the context dependent composition of plant volatile signals, the ability to detect and discriminate volatile compounds is crucial for insects to generate appropriate behavioral responses. In insects and more specifically in the hawkmoth Manduca sexta (Lepidoptera/Sphingidae), olfactory sensory neurons (OSNs) located on the antennae detect odorant molecules (Kalinová et al., 2001; Shields and Hildebrand, 2001; Fraser et al., 2003; Spaethe et al., 2013) and convey this information to the antennal lobe (AL), the first olfactory processing center. The AL of M. sexta females consists of about 70 structural and functional subunits called olfactory glomeruli (Grosse-Wilde et al., 2011). OSNs expressing the same receptor, and thus responding to the same set of odorants, converge onto the same glomerulus in the AL (Gao et al., 2000; Vosshall, 2000) as has been demonstrated for Drosophila melanogaster and indirectly also in several moth species (Hansson, 1997). Spatio-temporal patterns of neuronal activity representing sensory input to the AL can be visualized by optical imaging methods (Hansson et al., 2003; Skiri et al., 2004; Carlsson et al., 2005; Silbering and Galizia, 2007) enabling identification of compound- and blend-specific responses in the AL of M. sexta (Hansson et al., 2003; Bisch-Knaden et al., 2012; Kuebler et al., 2012).

Green leaf volatiles (GLVs) constitute a large group of herbivore-induced plant volatiles characterized by a C6-backbone. While emitted only in trace amounts from healthy, undamaged plant tissue, they are emitted instantly after cell disruption (Turlings et al., 1995; D’Auria et al., 2007). GLVs are generated from C18-fatty acids via the enzymes lipoxygenase (LOX) and hydroperoxide lyase (HPL; Allmann et al., 2010). One of the most abundant GLVs, (Z)-3-hexenal, originates from the cleavage of α-linolenic acid through the activity of HPL and it partly rearranges to (E)-2-hexenal. Both alkenals can be further metabolized by an alcohol dehydrogenase (ADH) and alcohol acyltransferase (AAT; D’Auria et al., 2007) to the corresponding alcohols and their esters (Matsui, 2006).

GLVs have been assigned various plant defense-associated functions by directly inhibiting phytopathogens (Hamilton-Kemp et al., 1992; Nakamura and Hatanaka, 2002; Prost et al., 2005) and repelling several herbivore species (De Moraes et al., 2001; Kessler and Baldwin, 2001; Vancanneyt et al., 2001; Zhang and Schlyter, 2004). Remarkably, GLVs also function as indirect plant defenses by attracting foraging predators and host-seeking parasitoids to the plant and its attacker (Kessler and Baldwin, 2001; Shiojiri et al., 2006; Halitschke et al., 2008; Schuman et al., 2012) reminiscent of the role of other herbivore induced plant volatiles.

Due to their ubiquity and instant release, GLVs are thought to act as nonspecific signals of plant damage (Hatanaka et al., 1987; Hoballah et al., 2002). We recently showed that an enzymatic component of the oral secretions (OS) of M. sexta larvae adds an herbivory-specific feature to the GLV signal. Mechanically damaged leaves of Nicotiana attenuata released large amounts of (Z)-3-GLVs and low amounts of (E)-2-GLVs. However, when the plant was attacked by M. sexta caterpillars or when puncture wounds of plant leaves were treated with M. sexta’s OS, the amount of (E)-2-GLVs released increased, while the amount of (Z)-3-GLVs decreased, resulting in a distinct change in the (Z)-3/(E)-2-ratio of GLV emissions. This herbivore-induced change in the (Z)-3/(E)-2-ratio attracted the generalist hemipteran predator Geocoris spp., which decreased the herbivore load on the plant by feeding on herbivore eggs (Allmann and Baldwin, 2010).

Our discovery of a (3Z):(2E)-enal isomerase in the OS of M. sexta larvae raises many questions. Why does Manduca produce an enzyme that generates volatiles which betray the insect to its enemies, and why did evolution not select against this isomerase? The enzyme might be maladaptive and therefore is, or will be, under negative selection. The occurrence of this specific isomerase activity in at least two other lepidopteran species (Allmann and Baldwin, 2010) however, suggests that it may have a beneficial function that outweighs the larva’s net costs of maintaining such an enzyme. It is well known that plants exchange information above ground by releasing volatiles into the air (Baldwin, 2010), which can be perceived by insects as well. Insects can use plant derived volatiles for communication by giving the herbivore induced volatile blend a ‘personal’ note—in our case, by converting (Z)-3-GLVs to their structural isomers and by changing the (Z)-3/(E)-2 ratio. Which message could M. sexta larvae thereby communicate? In this study we hypothesized that the altered GLV emission might serve to reduce the number of competitors on their host plant by informing conspecific ovipositing moths that this plant is already occupied and, possibly, receiving increased predation. Reduced oviposition of Manduca moths in response to feeding damage has been shown in field experiments with M. quinquemaculata (Kessler and Baldwin, 2001) as well as under laboratory conditions with M. sexta (Spaethe et al., 2013). Deviating from the previous study, we chose Datura wrightii (Solanaceae) for our experiments. Datura is a highly preferred host plant of both M. sexta and the congeneric M. quinquemaculata for both nectar feeding (Alarcón et al., 2008; Kessler, 2012) and oviposition (Spaethe et al., 2013). Its distribution covers southwestern USA (Avery, 1959; Munz, 1973) overlapping with the occurrence of both Manduca species. The perennial shrub is repeatedly described to quickly regrow leaves after herbivore damage (Bronstein et al., 2009; Reisenman et al., 2010, 2013). Laboratory experiments failed to find reduced oviposition on damaged D. wrightii (Reisenman et al., 2013; Spaethe et al., 2013) suggesting flexibility in oviposition choice of Manduca females. As the previously examined N. attenuata (Gaquerel et al., 2009), D. wrightii, respond to Manduca herbivore attack by emitting GLVs (Hare and Sun, 2011). While we investigated GLV emission during the day when focusing on the diurnal egg predator Geocoris ssp., Manduca moths oviposit at twilight and night (Madden and Chamberlin, 1945; Lingren et al., 1977). Therefore, we decided to collect volatiles during these times instead. We expected the shift to occur also during the night, as in several plant species GLV emission has been shown to occur also in the dark period (Loughrin et al., 1994; Arimura et al., 2008), and the respective shift in the (Z)-3/(E)-2-ratio is caused by M. sexta oral secretions and not by the plant itself (Allmann and Baldwin, 2010). However, volatile emissions vary with light regime (Halitschke et al., 2000; De Moraes et al., 2001; Gouinguene and Turlings, 2002; Morker and Roberts, 2011), and we therefore chose two nocturnal light conditions differing by moonlight intensity to examine whether light intensity affects GLV emission in D. wrightii. We performed functional imaging in the antennal lobe of female M. sexta moths asking whether (Z)-3- and (E)-2-structural isomers of any of the tested GLVs can be discriminated by the olfactory system. In classical host recognition experiments the Colorado potato beetle Leptinotarsa decemlineata has been shown to recognize and avoid altered ratios of (Z)-3- and (E)-2-GLVs emitted by its host plant Solanum tuberosum (Visser and Avé, 1978). Furthermore, enantioselectivity has been reported for projection neurons in the female AL of M. sexta in response to (+)- and (−)-linalool (Reisenman et al., 2004). Thus, we hypothesized that M. sexta females would be able to differentiate between (Z)-3 and (E)-2-isomers of at least one GLV. If so, ovipositing M. sexta should avoid plants with increased levels of (E)-2-GLVs as they indicate host plants with increased larval feeding competition and predation risk (Allmann and Baldwin, 2010). Here we show by combining field studies with neurophysiological imaging techniques that (i) OS-induced D. wrightii plants have altered (Z)-3/(E)-2-ratios also during the night under both laboratory and field conditions, (ii) Manduca females detect and discriminate the (Z)-3- and (E)-2-isomers and (iii) show ovipositional preference for high (Z)-3/(E)-2-GLV ratios.

Here we demonstrate that the (Z)-3/(E)-2-ratio of the GLV bouquet emitted from D. wrightii plants differs depending on the presence or absence of M. sexta larval oral secretions at sites of simulated feeding-damage. As OS-specific changes in the (Z)-3/(E)-2-ratio were detectable during one of the two nights in field experiments, this volatile signal may be encountered by ovipositing Manduca females searching for host plants. Functional imaging experiments revealed that M. sexta females detect (Z)-3- and (E)-2-hexenyl acetate with distinct OSN populations leading to discrete activation patterns in the AL. In field experiments Manduca females laid fewer eggs on plants scented with GLV mixtures with increased proportions of (E)-2-GLVs.

Our initial laboratory studies indicated that OS-induced changes in the GLV-profile of Datura wrightii plants are detectable during day and night, but they also revealed that light plays a role for the magnitude of this change in the signal. It has been shown that darkening can cause a temporary burst of GLVs in plants (Graus et al., 2004; Brilli et al., 2011). Furthermore, in Nicotiana attenuata the lipoxygenase NaLOX2, which specifically provides oxygenated fatty acids for the GLV-pathway, has its highest transcript levels during the night (Allmann and Baldwin, 2010), and, while this might explain the overall increase in GLVs with decreasing light intensities, it does not explain the specific increase in (E)-2-GLVs in w + w treated plants (Figure 3 and Table 1, night). (3Z):(2E)-enal isomerase activity has been found in crude extracts of some plants (alfalfa and soybean; Takamura and Gardner, 1996; Noordermeer et al., 1999), but not in N. attenuata (Allmann and Baldwin, 2010), and it needs to be determined whether Datura plants possess such an enzyme with a nocturnal peak activity. Circadian rhythm is also known to affect volatile emission (Goodspeed et al., 2012) and might therefore be another factor involved in the variation in GLV emission found between the light and dark period.

Most research on herbivore induced plant volatiles has been done in laboratory studies under controlled conditions (Hunter, 2002; Kigathi et al., 2009). While these studies provide useful information about the influence of single stress factors, they often fail to include biotic and abiotic stresses that influence volatile production under natural conditions (Kigathi et al., 2009). To evaluate the importance of these stresses, we repeated our trapping experiments in the field using native populations of D. wrightii plants.

Night-GLV emissions were measured at two different dates; while (Z)-3/(E)-2-ratios were the same in w + w and w + OS treated plants during the first experimental night, shortly after a new moon, they differed significantly during the full moon, the second experimental night. Although quantitative differences in light intensities between the two experimental nights were not detectable with the instruments available on site, they were obvious to the human eye. The releases of several volatile compounds are known to exhibit diurnal photoperiodicity in their quantitative but also qualitative emission patterns (Loughrin et al., 1994; Turlings et al., 1995). In cotton, acyclic terpenes like β-farnesene and β-ocimene were emitted in a diurnal fashion, while GLVs and few terpenes did not show such a clear diurnal pattern (Loughrin et al., 1994). Diurnal-rhythm-dependent emission has also been observed in N. tabacum after feeding by larvae of Heliothis virescens, M. sexta and Helicoverpa zea, as these plants released larger amounts of (E)-2-hexenal during the night and emitted other GLVs exclusively in the dark period (De Moraes et al., 2001). Experiments with lima beans revealed that leaves damaged during the scotophase responded with an almost immediate nocturnal emission of (Z)-3-hexenyl acetate, while the main emission of β-ocimene was delayed and peaked during the photophase (Arimura et al., 2008). These studies affirm that light plays an important regulatory role in volatile emissions. Due to our sample size, it remains to be shown by further experiments whether moonlight is sufficient to regulate volatile emissions.

The herbivore-induced volatile blend comprises several groups of compounds such as GLVs, terpenoids and/or aromatics, all of which have been shown to mediate plant-insect interactions (Mumm and Dicke, 2010). GLVs, which were investigated in the present study, seem to play an important role in volatile ‘communication’ as almost every green plant releases them upon various stress conditions. Furthermore, GLVs are released instantly from plant tissue upon damage, independent of the time of day (Turlings et al., 1995; D’Auria et al., 2007), while terpenoids are released with a delay (Kant et al., 2004) and several terpenoids not at all during the night as they are linked to photosynthesis (Arimura et al., 2008). This makes GLVs an important cue for ovipositing Manduca moths as they are active during sunset and night (Theobald et al., 2010) and thus need to rely on signals that are released during the scotophase.

The use of volatile blends for host location by insects depends heavily on the ability to detect and process olfactory signals. The insect’s olfactory system is highly sophisticated and enables detection of odors at very low concentrations (Hansson et al., 1999; Tanaka et al., 2009). However, in a redolent world, insects must distinguish host odors from a high background noise. Plant volatiles are detected by OSNs and these can be tuned to highly specific (Bruce and Pickett, 2011) or to ubiquitous host plant compounds (Hansson et al., 1999; Bruce et al., 2005). We found that stimulations with hexenal- and hexenol-structural isomers led to activation of a distinct region in the AL (ROI 2, Figure 4A,B). However, calcium signals evoked by (E)-2-GLVs were significantly stronger compared with those evoked by (Z)-3-GLVs (Figure 4B). This difference in activation intensity is likely a result from different binding affinities of the structural isomers to the olfactory receptor expressed by OSNs targeting the activated glomerulus (Hallem et al., 2004; Hooper et al., 2009).

Of all tested compounds, only the (Z)-3- and (E)-2-isomers of hexenyl acetate activated two different discrete regions in the AL of M. sexta females (Figures 4B,C and 5A,B) strongly suggesting different isomer-specific OSN populations on the insect antenna. This leads to the proposition that for M. sexta females, changes in the volatile emission of (Z)-3- and (E)-2-GLVs might primarily be detected via hexenyl acetate. Given that all other tested GLVs activated only ROI 2, the investment in isomer-specific receptors and consequently glomeruli to detect and process ubiquitous GLV compounds such as (Z)-3- and (E)-2-hexenyl acetate indicates the importance of the information content transferred by these compounds and their respective ratios. Specific responses to different types of green leaf volatiles have been reported both at physiological (Hansson et al., 1999; Røstelien et al., 2005) and behavioral levels (Reinecke et al., 2005).

For hexenyl acetate, AL activation patterns elicited by stimulations with mixtures of both structural isomers were purely additive suggesting no mixture interaction at the OSN and AL input levels, which is consistent with other studies (Deisig et al., 2006; Carlsson et al., 2007; Silbering and Galizia, 2007; Kuebler et al., 2012). When comparing the ratio of ROI activation, we did not find any difference between the mixtures (Figure 6A). This result is not surprising when taking the different response characteristics of ROI 3 and 4 into account. Calcium activity of ROI 4 in response to mixtures with increasing percentages of the (E)-2-isomer were dose-dependent, whereas the activation of ROI 3 to the same mixtures resembled more an ‘on–off’ mechanism and was thus solely dependent on the presence of the (Z)-3-isomer, leading to a constant bias towards (Z)-3-hexenyl acetate (Figures 5B and 6B). We can, however, not neglect the possibility that the logarithmic, dose-dependent phase in the neural dynamics of the neurons innervating ROI 3 lies at a concentration range below what was tested here.

The different response characteristics of ROI 3 and 4 might mirror the relevance of the odors for M. sexta females. (Z)-3-hexenyl acetate is a rather ubiquitously occurring plant volatile, which is released in large amounts after damage irrespective of its origin (Arimura et al., 2008; Mumm and Dicke, 2010). Electrophysiological experiments revealed that this compound elicited many responses in OSNs on the female M. sexta antenna: 60% of the tested sensilla (Spaethe et al., 2013) as well as 21 of 34 cells in the female AL (Kuebler et al., 2011) responded to this compound. (E)-2-hexenyl acetate, in contrast, has rarely been reported in insect-plant interactions (Whitman and Eller, 1990; Quiroz and Niemeyer, 1998; Williams et al., 2010), aside from its release among other GLVs after larval feeding of M. sexta on N. attenuata (Allmann and Baldwin, 2010) as an indication of actual larval damage. Thus, the presence of each structural isomer contains specific information but at different levels of resolution and in different contexts. In the case of (Z)-3-hexenyl acetate, the detected signal might also be relevant in long-range host location and host choice. Information about (E)-2-hexenyl acetate gained by ROI 4 in a dose-dependent fashion should, on the other hand, be most valuable at a short distance to the plant, possibly to locate the best spot for oviposition depending on the actual amounts emitted by different plant sites or to choose among neighboring plants with different levels of (conspecific) herbivory.

Numerous studies suggest that the ratio of plant volatiles is an important component of the olfactory signal (Visser and Avé, 1978; Bruce et al., 2009; Cha et al., 2011). Visser and Avé (1978) found several GLVs playing important roles in host recognition of Leptinotarsa decemlineata. Augmenting the volatile emission of a potato host plant with the single GLV components (Z)-3- or (E)-2-hexenol, (E)-2-hexanal or 1-hexanol resulted in a disruption of the orientation of L. decemlineata to the potato plant. Further studies found neurons specifically responding to these GLVs both at the periphery and in the AL of L. decemlineata (De Jong and Visser, 1988a, 1988b). In the case of the oriental fruit moth, Grapholita molesta, the ratio of a minor compound to the remaining components of a plant-derived synthetic mixture determined behavioral acceptance of this mixture, which could be associated with the response of two glomeruli in the female AL (Piñero et al., 2008; Najar-Rodriguez et al., 2010). We found that ovipositing Manduca moths distinguished between different (Z)-3/(E)-2-ratios and that they used these volatile cues to choose oviposition sites associated with less feeding competition and predation. However, independent of whether the mixtures tested were rather complex in their composition (9:1 vs 1:1 ratios), or less complex (only (Z)-3-GLVs vs only (E)-2-GLVs), or consisted of only a single compound ((Z)-3-hexenyl acetate vs (E)-2-hexenyl acetate) ovipositing Manduca moths continuously made a choice and always preferred the side of the plant that smelled more of (Z)-3-GLVs, or less of (E)-2-GLVs (Figure 7B). From our results we cannot conclude whether a complex GLV bouquet of different ratios provides more reliable information than do single compounds, but our results demonstrate that by adding a single component to the volatile bouquet of native D. wrightii plants one can alter the choice of ovipositing Manduca moths.

How did this behavior evolve? It has been shown that M. sexta moths learn to feed from flowers of non-hosts due to olfactory conditioning (Riffell et al., 2008, 2013). Experience could as well shape female oviposition choice as it has been shown in other moth species (Rietdorf and Steidle, 2002; Olsson et al., 2006). During oviposition M. sexta females might encounter the herbivory-specific signal, but can never experience the reward of oviposition success associated with it. A M. sexta larva feeding on plants, however, is continuously surrounded by GLVs emitted from wounded plants and more importantly encounters almost continuously a low (Z)-3/(E)-2-ratio caused by its own oral secretions. The retention of odor memory learned at the larval stage onto the adult stage has been shown to occur in M. sexta (Blackiston et al., 2008). However, in such a case you would rather expect a preference for OS-elicited bouquets, as the larva grew up in these. More experiments are needed to solve whether experience and learning are involved in the avoidance of herbivory-specific (Z)-3/(E)-2-ratios.

Almost every green plant releases volatiles in highly variable amounts and compositions. This makes it a challenge for host searching insects to simultaneously extract useful information while flying through the odor plumes from multiple sources. Our results show that the AL, the first odor processing center of the insect brain, has the capacity to resolve the composition of GLV blends as emitted by highly relevant host plants. Correspondingly, gravid females make an informed choice. They prefer oviposition sites with reduced predation and competition risks for their offspring, as indicated by the plant volatile bouquet. Future work will reveal whether increasing amounts of (E)-2-GLVs or rather changes in the (Z)-3/(E)-2-ratio at the background of other host odors provide crucial information for female Manduca moths.

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Author details

1. Silke Allmann

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Present address

   Department of Plant Physiology, Swammerdam Institute for Life Sciences, Amsterdam, Netherlands

   Contribution

   SA, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Contributed equally with

   Anna Späthe

   Competing interests

   No competing interests declared.

2. Anna Späthe

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   AS, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Contributed equally with

   Silke Allmann

   Competing interests

   No competing interests declared.

3. Sonja Bisch-Knaden

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   SB-K, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

4. Mario Kallenbach

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   MK, Conception and design, Acquisition of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

5. Andreas Reinecke

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Present address

   Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany

   Contribution

   AR, Conception and design, Drafting or revising the article

   Competing interests

   No competing interests declared.

6. Silke Sachse

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   SS, Conception and design, Drafting or revising the article

   Competing interests

   No competing interests declared.

7. Ian T Baldwin

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   ITB, Conception and design, Acquisition of data, Drafting or revising the article

   For correspondence

   baldwin@ice.mpg.de

   Competing interests

   ITB: Senior editor, eLife.

8. Bill S Hansson

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   BSH, Conception and design, Drafting or revising the article

   For correspondence

   hansson@ice.mpg.de

   Competing interests

   No competing interests declared.

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