Plant Odour Plumes As Mediators of Plant–Insect Interactions

Biol. Rev. (2014), 89, pp. 68–81. 68 doi: 10.1111/brv.12043 Plant odour plumes as mediators of plant–insect interactions

Ivo Beyaert and Monika Hilker∗ Freie Universit¨at Berlin, Institut f¨ur Biologie, Haderslebener Str. 9, D-12163 Berlin, Germany

ABSTRACT

Insect olfactory orientation along odour plumes has been studied intensively with respect to pheromonal communication, whereas little knowledge is available on how plant odour plumes (POPs) affect olfactory searching by an insect for its host plants. The primary objective of this review is to examine the role of POPs in the attraction of insects. First, we consider parameters of an odour source and the environment which determine the size, shape and structure of an odour plume, and we apply that knowledge to POPs. Second, we compare characteristics of insect pheromonal plumes and POPs. We propose a ‘POP concept’ for the olfactory orientation of insects to plants. We suggest that: (i) an insect recognises a POP by means of plant volatile components that are encountered in concentrations higher than a threshold detection limit and that occur in a qualitative and quantitative blend indicating a resource; (ii) perception of the ﬁne structure of a POP enables an insect to distinguish a POP from an unspeciﬁc odorous background and other interfering plumes; and (iii) an insect can follow several POPs to their sources, and may leave the track of one POP and switch to another one if this conveys a signal with higher reliability or indicates a more suitable resource. The POP concept proposed here may be a useful tool for research in olfactory-mediated plant–insect interactions.

Key words: insect orientation, olfaction, plant–insect interactions, plant volatiles, plant odour plume.

CONTENTS I. Introduction ...... 69 II. Odour plumes in general and parameters inﬂuencing plant odour plumes (POPs) ...... 69 (1) General features of odour plumes ...... 69 (2) Parameters inﬂuencing plant odour plumes ...... 71 (a) Plant size ...... 71 (b) Plant height ...... 71 (c) Plant biosynthetic activity ...... 71 (d) Biotic and abiotic factors ...... 71 III. Comparison of insect pheromonal plumes and POPs ...... 72 (1) Source size ...... 72 (2) Quantity ...... 72 (3) Timing ...... 73 (4) Complexity ...... 73 (5) Chemical structure ...... 73 (6) Ratios of volatile compounds ...... 73 (7) Plasticity ...... 73 IV. Insect olfactory orientation to plant odours: a plant odour plume concept (POP concept) ...... 74 (1) Detecting a plume ...... 74 (2) The attractive POP: blend, threshold concentrations and ratios of volatiles ...... 74 (3) Following a plume: single plume tracking ...... 75 (4) Orientation among various plumes: hierarchical POP tracking ...... 76 V. Conclusions ...... 77 VI. Acknowledgements ...... 78 VII. References ...... 78

* Address for correspondence (E-mail: [email protected]).

I. INTRODUCTION repellent compounds or volatiles that mask the resource- indicating odour, but in some cases can also enhance the Insects can use several sensory modalities to locate a resource response to an olfactory cue released by a resource (e.g. required for nutrition and reproduction: olfaction, vision, Zhang & Schlyter, 2004; Hilker & McNeil, 2007; Schroder¨ & taste, touch, and in some insect species also audition (e.g. Hilker, 2008). Vegetation diversity and associated diversity Lehrer, 1997; Nation, 2008). When searching for distant of plant volatiles may strongly influence insect olfactory resources, many insects rely on olfactory and visual cues. orientation (Randlkofer et al., 2010, and references therein). Olfactory and visual stimuli may act in concert on the insect’s We suggest that considering olfactory orientation of insects physiology and behaviour or play different roles during the to plants as orientation to plant odour plumes (POPs) different stages of the approach to a resource (Prokopy contributes to our understanding of plant–insect interactions & Owens, 1983; Bernays & Chapman, 1994; Hansson, in complex and highly diverse odorous environments. We 1999; Raguso, 2001; Bruce, Wadhams & Woodcock, 2005; consider a POP to be a ‘plant volatile package’ or an odour Hallem, Dahanukar & Carlson, 2006; de Bruyne & Baker, entity composed of individual plant volatiles, characterised 2008; Balkenius, Bisch-Knaden & Hansson, 2009; Reeves, by the quality and quantity of the components. Like other 2011). In this review, we focus on olfactory orientation of volatiles, the plant volatiles that form an odour plume are insects to plants and the role of plant odour plumes. carried some distance by turbulent motion (Carde´ & Willis, Plant odours may be used by insects for various purposes: 2008). Although numerous studies on insect attraction by by herbivores to find food plants or sites for egg deposition pheromones have investigated the perception of pheromonal (Visser, 1986; Bruce et al., 2005; Bruce & Pickett, 2011), by plumes and behavioural orientation to such plumes (Carde´ pollinators to locate flowers (Pichersky & Gershenzon, 2002; & Willis, 2008; Baker, 2009), insect responses to plant odours Raguso, 2008; Schiestl, 2010), and also by carnivorous or have hardly ever been investigated with respect to orientation parasitic insects to find herbivorous prey and hosts (Vet & along an odour plume [but compare Hardie, Gibson & Wyatt Dicke, 1992; Vinson, 1998; Steidle & van Loon, 2003; Hilker (2001) and Bruce et al. (2005)]. & Meiners, 2006, 2010; Mumm & Dicke, 2010). Herein we first summarise knowledge about odour Volatiles emitted by plant material exhibit an immense plumes, particularly with respect to plant odour plumes. diversity. Approximately 1700 different plant volatile A comparison of insect pheromonal plumes and POPs compounds are known and produced by over 90 plant provides arguments for the consideration of plant odours as families (Dudareva et al., 2006; Laothawornkitkul et al., plumes when studying insect olfactory orientation to plants. 2009). Chemically, they belong primarily to the groups Finally, we highlight the characteristics that an attractive of terpenoids, phenylpropanoids or benzenoids, fatty acid POP should have and discuss how insects orientate to a plant derivatives, and amino acid derivatives (Dudareva et al., in environments containing many POPs. 2006), but also include highly volatile plant compounds with short carbon chains, such as acetone and methanol (Harley, Monson & Lerdau, 1999; Niinemets, 2010). The quantitative II. ODOUR PLUMES IN GENERAL AND and qualitative composition of plant odour depends not PARAMETERS INFLUENCING PLANT ODOUR only on the plant species, but also on the physiological PLUMES (POPs) state of the plant and on its environment. Biotic stresses, such as pathogen infection, herbivore damage or insect egg (1) General features of odour plumes deposition (Hilker & Meiners, 2006, 2010; Dicke & Baldwin, 2009; Dicke, van Loon & Soler, 2009; Niinemets, 2010), as Odour released from a source disperses in the air as a result well as abiotic stresses (Loreto & Schnitzler, 2010) can change of molecular diffusion and turbulent motion (Atema, 1996; the pattern of volatiles released by plants. Several reviews Zimmer & Butman, 2000). The turbulent motion carries the comprehensively cover the ecological relevance of volatile plume in so-called filaments or odour-strands, i.e. pockets of emissions by plants (Holopainen, 2004; Raguso, 2004; high odour concentrations interspaced by pockets of odour- Penuelas & Munne-Bosch, 2005). Furthermore, knowledge free medium (Mylne, Davidson & Thomson, 1996; Finelli of the olfactory capabilities of insects to sense plant volatiles et al., 1999; Murlis, Willis & Carde,´ 2000). An insect antenna has been reviewed from physiological and molecular points receives the fine structure of such a plume as repeated of view (e.g. Smith & Getz, 1994; Hildebrand & Shepherd, fluctuations between odour bursts of high concentrations 1997; Mustaparta, 2002; Keller & Vosshall, 2003; Hallem when an odour filament is encountered, and phases of low or et al., 2006; de Bruyne & Baker, 2008). zero concentration when no odour filament is encountered. In nature, resource-indicating plant volatile blends must This on/off pattern determines the intermittency of the be recognised by insects in a complex dynamic sensory plume; Murlis, Elkinton & Carde´ (1992) defined such environment, which has been described as an ‘odour intermittency ‘as the proportion of time when the signal landscape’ (Nevitt, Veit & Kareiva, 1995; Atema, 1996). is absent’ (Fig. 1). This intermittency depends on the source The odour of the habitat (= background odour) may contain size, the turbulence structure of the air flow and the distance

Fig. 1. Simplified diagram of an odour plume. Originating from the source, the plume moves downwind and elicits a pattern of on- and off-responses in the receiver. With increasing distance from the source, the size of filaments and the space between them increase, whereas the mean concentrations of single components within filaments decrease (although filaments with high concentrations may still occur at greater distances). The absolute size of the plume defines the distance from the source where odour concentrations are above background level. The relative size describes the distance at which odour concentrations are still detectable by a specific receiver (i.e. meet threshold level). Dotted line: insect movement path; the odour plume hits the insect antennae intermittently (indicated by crossing of dotted line and odour plume). Please note that movement paths during (pheromonal) plume tracking are usually not as straight as shown in this simplified diagram; instead, cast and surge flight behaviour is often observed [compare Section IV(3)]. For real images of odour plumes see, for example, Geier, Bosch & Boeckh (1999) and Webster & Weissburg (2001). of the plume from the source [see Koehl (2006) for a review]. compounds conveyed in a filamentous plume may be The intermittency of plumes from small sources is higher, and conserved even over long distances (Vickers, 2000). However, they have a greater intensity of concentration fluctuations depending on the environmental conditions, the plant odour than those from larger sources (Murlis et al., 1992). With may change over time and distance since compounds with increasing turbulence, both the intermittency of the plumes low volatility tend to be adsorbed by substrates (Helmig et al., and the frequency of encountering the odour filament 2004) and can then be re-released (Himanen et al., 2010), increase (Finelli et al., 2000; Moore & Crimaldi, 2004). whereas compounds with a higher volatility may travel over The structure of an odour plume changes substantially longer distances. This limits the distance over which the while moving away from the source (Dekker, Geier & Carde,´ plume retains its chemical identity. 2005). The spatial sizes of filaments and the space between It is well known that moths recognise the fine structure the filaments tend to increase with increasing distance from of an odour and respond to single filaments (Fadamiro & the source (Moore & Atema, 1991; Murlis et al., 1992) (Fig. 1) Baker, 1997; Hardie et al., 2001; Bau, Justus & Carde,´ 2002; (but note that Voskamp, Den Otter & Noorman (1998) did Bau, Loudon & Carde,´ 2005; Baker, 2009). The intermittent not find increased filament sizes with increasing distance). structure of the insect pheromonal plume may be critical for The concentration of odour within single filaments decreases successful location of an upwind odour source (Vickers & with increasing distance (Voskamp et al., 1998; Murlis et al., Baker, 1992; Mafra-Neto & Carde,´ 1994; Vickers & Baker, 2000). Nevertheless, filaments with high concentrations may 1994; Justus & Carde,´ 2002; Baker, 2009; Lei et al., 2009). also occur far from the odour source, but this happens less Plume-following mechanisms known from insect navigation frequently (Murlis et al., 1992, 2000; Voskamp et al., 1998; to pheromone sources may also apply to insect orientation Webster & Weissburg, 2001). towards plant odours, as was suggested previously by Hardie The degree of mixing of plume filaments from different et al. (2001). sources depends on the distances separating the odour Herein we consider the plant odour used by an insect for sources and the distance of the filamentous plumes from their orientation as an individual odour entity that is defined by sources (Myrick et al., 2009). Even in intermingled plumes its qualitative and quantitative composition and by the fine released by spatially separated sources, pure, non-mixed structure of the plume. A plant comprises an assemblage odour strands of a particular source may reach the insect’s of odour sources which may emit the same odours (e.g. antenna (Lelito, Myrick & Baker, 2008). Interestingly, the intact leaves of the same age) or different odours (e.g. intact qualitative composition of the blend and ratios of volatile versus damaged leaves, or leaves versus flowers, roots versus

Biological Reviews 89 (2014) 68–81 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society Plant odour plumes 71 aboveground foliage, etc.) (Knudsen, Tollsten & Bergstrom,¨ are stored in resin ducts or glandular trichomes (Niinemets 1993; Pichersky & Gershenzon, 2002). Different insects may et al., 2004; Holopainen & Gershenzon, 2010). Biosynthesis be attracted by different plumes to different parts of a plant of volatiles is temperature and light dependent (Gershenzon, depending on the purpose of their search. A pollinator might McConkey & Croteau, 2000; Laothawornkitkul et al., 2009), follow an odour plume of a flower, whereas an herbivore but is also regulated by the plant in response to stress factors might follow a plume of a healthy leaf. Parasitoids or such as herbivory, pathogen infection, flooding or drought predators might follow the odour plumes released from a (Loreto & Schnitzler, 2010; Niinemets, 2010). Multiple leaf induced by herbivore infestation. The characteristics of stresses often occur simultaneously and can influence a POP are determined by both the plant itself and the habitat emission of volatiles in non-additive ways (Holopainen & in which the odour is released. Gershenzon, 2010). The emission of many plant volatiles can also be regulated by stomatal opening and closure (2) Parameters influencing plant odour plumes (Niinemets & Reichstein, 2003). (a) Plant size (d) Biotic and abiotic factors Plant size influences the POP in several ways. First, larger plants may emit more odour plumes that differ from each Vegetation influences POPs in physical and biological ways. other; as a consequence, plume mixing becomes more likely. Physically, wind speed and wind turbulence are affected by Second, larger plants have larger surfaces on which emitted vegetation structure, and therefore POP patterns are altered volatiles can be adsorbed (Noe et al., 2008; Himanen et al., by the vegetation in the environment of a POP-releasing 2010). However, since we suggest that not an entire single target plant (Murlis et al., 1992; Vickers, 2006; Randlkofer plant, but single plant organs should be considered as odour et al., 2010). Murlis et al. (2000) showed differences between sources, large plants do not necessarily have larger odour odour plumes in the forest and in the open field. The sources. size of odour filaments and the gaps between the filaments were both larger in forests. Voskamp et al. (1998) observed the electrophysiological response of Glossina spp. to odour (b) Plant height plumes in woodland and the open field; the antennae of the Plant height may influence the detectability and also the flies detected the plume in woodland over longer distances structure of the POP. Odours released from higher positions (up to 60 m) than in the open field (up to 20 m). They may interfere less with other plant odours if the plant height suggested that this may be due to lower wind speed in exceeds the mean vegetation height. Odour plumes emitted the woodland and resulting higher peak concentrations. from higher parts of the plant, such as flowers, are likely to be From a biological perspective, vegetation density determines sensed over longer distances than those emitted from lower the density of plant odour sources and thus the chance of plant parts. Furthermore, the higher the source of the POP, plume intermingling and eventually loss of odour identity. the less it interferes with the substrate on the ground. It has High vegetation complexity is determined by high plant been shown for aquatic systems that for odour sources close species diversity and structural heterogeneity; it increases to the substratum, the roughness of the substratum strongly the probability that unspecific odours will interfere with the influences the structure of the plume: rougher texture causes target POP (Meiners & Obermaier, 2004; Randlkofer et al., higher turbulence of the boundary layer of the plume (Moore 2010, and references therein). et al., 1994; Jimenez,´ 2004). This results in a more rapid Air flow velocity (or wind speed) is an important envi- increase in plume width and therefore a faster decrease ronmental parameter determining aerial plume structure. in mean concentration. Furthermore, the intermittency of With increasing flow speed, odour filaments become thinner the plume is reduced by substrate roughness (Jackson et al., and exhibit lower odour intrafilament concentrations (Rif- 2007). These changes in plume structure can influence the fell, Abrell & Hildebrand, 2008, and references therein). A searching pattern of organisms orientating along the plume higher flow speed also enhances the degree of turbulence in (Webster & Weissburg, 2009). The higher the POP source is the plume. Concentration fluctuations are higher in more above the ground, the less will the plume be influenced by turbulent plumes, and odour pulses are more discrete with a the substratum (Webster & Weissburg, 2001). lower mean pulse height (Moore et al., 1994). The abiotic properties of the atmosphere determine the lifespan of plant volatile compounds until degradation. Plant (c) Plant biosynthetic activity volatiles may react with hydroxyl (OH) and nitrate (NO3) The plant’s physiology determines the rate of volatile radicals as well as ozone (O3) and in the process be degraded emission and thus the quantities of compounds in the plume. within hours, minutes or even seconds after release (Fuentes The emission of volatiles from plants is determined by the et al., 2000; Atkinson & Arey, 2003; Pinto et al., 2010). Hence, plant’s biosynthetic activity, since volatiles are often released ozone and air pollution can change the identity of an odour immediately following their production (Niinemets, Loreto plume and therefore limit its range of attraction to insects & Reichstein, 2004), except for those which are glycosylated (Gate, McNeill & Ashmore, 1995; McFrederick, Kathilankal and stored as non-volatile sugar conjugates or those which & Fuentes, 2008; Blande, Holopainen & Li, 2010).

Table 1. Overview of differences and similarities between insect pheromone plumes and plant odour plumes and their perception by insects

Trait In pheromone plumes In plant odour plumes Similarities Size of odour source Point source Larger source When considering single plant organs as odour sources, pheromonal and plant odour sources converge with respect to size Quantity of volatiles Small quantities Mostly large quantities Insects show high response-speciﬁcity and sensitivity to both pheromonal and plant volatiles Timing of volatile Mostly release at speciﬁc Mostly diurnal pattern Both timing of pheromone and plant volatile emission times (hours) of a day of release release are dependent on the time of day, the developmental phase of the emitter, and on various environmental cues Complexity Only a few compounds in Up to several hundred Insect attraction to both a pheromone source a plume compounds in a and a plant volatile source is usually plume mediated by only a few compounds Chemical structure of Chemically homogenous Often chemically Chemical structures of plant volatiles and compounds within a blend heterogeneous pheromone components may be similar or within a blend even identical Ratios of volatile Important for insect Important for insect Ratios of constituents of both pheromonal compounds attraction attraction odour and plant odour are important for the response of insects Plasticity Plastic with respect to Plastic with respect to The actually released volatile blend depends quantities of volatiles quality and quantity on the physiological state of the organisms of volatiles and on environmental cues

III. COMPARISON OF INSECT PHEROMONAL of, e.g. a POP-releasing leaf is almost always larger than PLUMES AND POPs the point source of an insect pheromone, e.g. the minute opening of a pheromonal gland. However, source sizes may Table 1 provides a comparison of insect pheromonal plumes vary for the two types of odour. Variability of the size of POP and POPs with respect to the size of a plant odour sources will be due to the different sizes of leaves, flowers source, quantity of volatiles, timing of volatile emission, and other plant organs. Variability of the size of pheromone odour complexity, chemical structures of plume constituents, sources will be due to the size of the pheromone-releasing ratios of volatile compounds, and plume plasticity. Insect insect, its glandular openings or its pheromonal deposits on pheromone plumes and POPs show some similarities but a substrate. Moreover, source size of both POPs and insect differ particularly in the size of the source and in the pheromones may increase due to the adsorbance of volatiles heterogeneity of the chemical structures of components of by the surrounding substrate and their subsequent re-release the plume (Table 1). A larger source size of POPs may result (e.g. Perry, Wall & Clark, 1988; Karg, Suckling & Bradley, in plume structures that differ in intermittency patterns from 1994; Noe et al., 2008; Himanen et al., 2010). Furthermore, insect pheromonal plumes since intermittency depends on every puff of wind may contribute to the expansion of source size and the turbulence structure of the air flow initially small odour plumes. Thus, an initially restricted (Murlis et al., 1992). However, the wide range of similarities plume size may increase significantly. Larger odour sources between insect pheromonal plumes and POPs suggests generally release odour plumes with a reduced intermittency that knowledge of pheromone research may be useful for (Murlis et al., 1992). predictions about the mechanisms of insect attraction to plant odours. (2) Quantity The quantity of volatiles released by a single plant organ (1) Source size may be higher than the quantity of a pheromone released by The actual site of odour emission should be considered as an insect. A plant, especially when damaged by herbivory, the source, rather than the entire plant, i.e. the source of an can release volatile components in the range of nanograms odour is the individual plant organs, such as leaves, fruits, to several micrograms per hour (e.g. Turlings et al., 1991; De buds, flowers or roots. Thus, a plant may be considered Moraes, Mescher & Tumlinson, 2001; Janson & de Serves, as an assemblage of several different odour sources. These 2001; Arneth & Niinemets, 2010, and references therein). plant organs may be so far apart that they emit separate A single leaf of Pelargonium hortorum,forexample,hasapeak odour plumes of different quality and quantity (Dudareva, emission of 277 ng per 20 min (Deng et al., 2004). Most insects Pichersky & Gershenzon, 2004). Nevertheless, the surface release pheromones in quantities of less than 1 μgperhour,

Biological Reviews 89 (2014) 68–81 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society Plant odour plumes 73 and sometimes just a few nanograms per hour (e.g. Roelofs & 2010; Bruce & Pickett, 2011). Thus, a similar number of Carde,´ 1977; Ando, Inomata & Yamamoto, 2004; Witzgall, compounds is used for olfactory orientation for both types of Kirsch & Cork, 2010). Although the quantities of volatiles odour plumes. released by a plant usually exceed those released from a pheromone-emitting insect, even minor amounts of volatile (5) Chemical structure constituents of a complex plant odour may be sufficient for the attraction of insects (Mumm et al., 2003; Bruce et al., Both insect pheromonal and plant odours may consist of 2005; Bruce & Pickett, 2011). High sensitivity of the olfactory a wide range of chemical structures produced by various system of insects has been demonstrated not only for insect biosynthetic pathways. Alcohols, aldehydes, carboxylic pheromones, but also for plant volatiles (Hansson, Larsson acids and their esters, isoprenoids, phenolic compounds, & Leal, 1999; Bruce & Pickett, 2011). polyketides, and other chemical classes have been identified in both insect pheromonal and plant odours (Ando et al., 2004; Dudareva et al., 2004; Francke & Dettner, 2005; (3) Timing Schiestl, 2010). Therefore, insects possess olfactory sensitivity Volatile emission is often restricted to specific times (hours) of to very different chemical structures to allow a response to a day in pheromone-releasing insects (e.g. Sower, Gaston & volatile pheromones or plant odours. Many moth species Shorey, 1971; Delisle & McNeil, 1987; Tillman et al., 1999). are known to use the same pheromonal components for In comparison, plant volatile emission often shows a diurnal communication. For example, (Z)-9-tetradecenyl acetate was pattern with higher release rates during the day and lower suggested to be involved in the intraspecific communication emission at night (Kreuzwieser et al., 2000; Dudareva et al., system of nearly 200 moth species (Byers, 2006). Similarly, 2006; Loivamaki¨ et al., 2007; Raguso, 2008). The herbivore- many plant odours consist of ubiquitous volatiles, among induced plant volatiles (HIPVs) that attract carnivores are which green leaf volatiles (C6-aldehydes, -alcohols and often released within a specific period of time after herbivore their acetates) are the most common. Compounds of insect attack (Hilker & Meiners, 2002, 2006; Schroder¨ et al., 2008). pheromonal blends are often similar in their physicochemical Furthermore, pheromones are usually released only during properties, whereas components of a POP may be quite certain developmental phases of an insect (Tillman et al., heterogenous. Water solubility, for example, may vary by 1999). The volatile blends released by a plant also generally six orders of magnitude between different plant volatiles depend on the developmental phase of the plant organ (Niinemets & Reichstein, 2003). (Pichersky, Noel & Dudareva, 2006; Raguso, 2008). Both the release of specific plant volatiles and insect pheromones may (6) Ratios of volatile compounds be induced by environmental cues. Cues such as pathogen or herbivore attack may induce plant volatile emission The quantitative composition of an odour also may (Reinecke et al., 2002; Turlings & Wackers,¨ 2004; Dicke, determine the species specificity of both insect pheromonal 2009; Dicke et al., 2009; Hilker & Meiners, 2010), while communication and plant–insect interactions. Fine-tuned release of plant volatiles can trigger pheromone release in ratios of volatile compounds may contribute to this species insects (Landolt & Phillips, 1997; Reddy & Guerrero, 2004). specificity. Attraction of mates by pheromones depends on a Hence, timing of both pheromone emission and plant volatile specific ratio of different pheromone components in several emission is determined by the time of day, developmental moth species (e.g. Linn & Roelofs, 1989; Schneider, 1992; phase of the emitter and by various environmental cues. Ando et al., 2004; Jurenka, 2004; Baker, 2008), whereas in other moths the ratio of pheromonal components varies (4) Complexity widely and is less important for pheromonal activity (Carde´ & Haynes, 2004, and references therein; Kanno et al., 2010). At a first glance, insect pheromones and plant odours differ Ratios of plant volatile compounds are also known to be in complexity. According to Byers (2006) the number of important in the olfactory foraging behaviour of insects. compounds detected in the pheromone glands of many Changes in ratios of plant volatiles may significantly affect moth species ranges between one and eight compounds, with insect behaviour (Visser, 1986; Bruce et al., 2005, 2010; a maximum of 10 compounds in Heliothis virescens. However, Beyaert et al., 2010). the number of compounds that have pheromonal significance is often lower. Plant odours are far more complex, with (7) Plasticity individual plants releasing up to several hundred compounds (e.g. Turlings et al., 1995; Dicke et al., 1998; Krips et al., Both POPs and insect pheromonal blends exhibit plasticity in 2001; Knudsen et al., 2006). Even taking different plant their composition. The quality and quantity of a plant odour organs as different odour sources, each flower or leaf may depends on many factors, such as the size and age of the emit many more than 10 compounds. However, often only plant (or plant organ), its nutritional state, water availability, a small subset of plant volatile compounds is important for neighbouring vegetation, defence status, or the cultivar (Vet insect orientation. The minimum blend of plant volatiles & Dicke, 1992; Krips et al., 2001; Holopainen & Gershenzon, that attract insects normally comprises 10 or less compounds 2010; Kegge & Pierik, 2010; Loreto & Schnitzler, 2010). The (Wei & Kang, 2006; Beyaert et al., 2010; Siderhurst & Jang, quantity of pheromones released by a female insect may also

Biological Reviews 89 (2014) 68–81 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society 74 Ivo Beyaert and Monika Hilker be highly variable, depending on (i) exogenous factors, such et al., 2005). Hence, the impact of habitat odour complex- as time of day (e.g. Hunt & Haynes, 1990; Lacey & Sanders, ity on olfactory orientation is limited by the perceptional 1992), temperature (Delisle & McNeil, 1987), presence of capabilities of the insect. plant volatiles that stimulate pheromone release (Reddy & However, if background volatiles are received, continuous Guerrero, 2004) and (ii) endogenous factors, such as feeding exposure to them while moving through an odorous status (Foster, 2009; Foster & Johnson, 2011) and hormonal landscape may change the responsiveness to those volatiles. control (Cusson & McNeil, 1989). Continuous exposure may sensitise the receptors and thus, enhance the response to those volatiles, but may also cause olfactory adaptation and habituation, and thus reduce the physiological response (e.g. Kaissling, 1986; Masson & IV. INSECT OLFACTORY ORIENTATION TO Mustaparta, 1990; Smith & Getz, 1994; Schroder¨ & Hilker, PLANT ODOURS: A PLANT ODOUR PLUME 2008). Continuous exposure to one volatile compound CONCEPT (POP CONCEPT) may also change the response to another volatile (Kelling, Ialenti & Den Otter, 2002). Both cross-adaptation and (1) Detecting a plume cross-sensitisation may occur, that is, if a background Insects may find resources by random movements, by volatile compound induces adaptation or sensitisation to auditory, visual, gustatory or tactile cues, and/or by a resource-indicating odorant (Schroder¨ & Hilker, 2008, and orientation along odour plumes. Since an odour plume is references therein). With respect to orientation to a resource- carried by the wind, wind is the most important parameter indicating odour plume, adaptation and habituation may affecting the use of resource-indicating odour plumes. Wind lead to background suppression and help filter the plume determines the shape of a plume as well as the dynamics of interest from irrelevant background odours. Furthermore, of plume dispersal; furthermore, wind speed and direction sensitisation to resource-indicating plume volatiles as well as will influence the energetic costs of insect movements along cross-sensitisation to them by background volatiles might facilitate recognition of resource-indicating plumes. By an odour plume (Carde,´ Carde´ & Girling, 2012). In a contrast, (cross-)adaptation to a resource-indicating volatile theoretical model, Dusenbery (1989) analysed how optimum compound impedes the insect’s response to a plume released searching behaviour should be adjusted to the form of the from a resource. Thus, the time period during which an odour plume. According to the model, when searching for a plume is received may significantly affect the olfactory response. with roughly the same diameter in any direction (spherical In addition to time periods of odour reception, the spatial plume), the optimal movement direction is upwind. When distance between odour sources adds a further dimension to perceiving plumes with a greater dispersion in wind direction the features determining plume detection and discrimination than in the crosswind direction (long plumes), a course nearly of host plant odour against background odours, which may across the flow seems to be optimal. The relative advantage contain some of the same volatiles as the target plant. of upwind (versus downwind) searching is higher for searches Volatiles released from spatially separated odour sources of short total path length (Sabelis & Schippers, 1984). Thus, will encounter the insect antenna at different times. Several the upwind searching strategy is more important when studies showed that an insect’s behavioural response to two targets are expected to occur at high density, and when the confluent plumes released from spatially separated sources likely path is of similar length to the range at which the plume is different from the response to a single-source plume that can be detected (Finch & Skinner, 1982). Upwind, downwind consists of the same volatiles (e.g. Witzgall & Priesner, 1991; (Gibson et al., 1991) and crosswind (Zanen et al., 1994) search Liu & Haynes, 1992). Baker, Fadamiro & Cosse´ (1998) strategies are known for different insect species. The optimal showed that a moth is able to discriminate between plumes strategy depends on the interactions between wind condi- separated by only 1 mm in space and 0.001 s in time. When tions, plume shape and plume dispersal within the habitat, intermingling odour strands released by different sources do target traits, and the insect’s energetic resources (Carde´ et al., not arrive simultaneously at the antenna, insects are able 2012). Some insects are able to change their search strategy to decipher this complex information and follow the strand in response to wind conditions (Zanen et al., 1994). of interest (e.g. Lelito et al., 2008; Szyszka et al., 2012). In a complex environment, insects are expected to The ability to decode such ‘high-resolution spatio-temporal encounter continuously various plant odour plumes. Detec- information’ (Bruce et al., 2005) obtained from two odour tion of a resource-indicating plume requires sensing and sources allows an insect to discriminate a resource-indicating discrimination against an unspecific odorous background. plume as a defined ‘odour-object’ from other plumes (see Background odour that does not convey resource-specific Szyszka et al., 2012, and references therein). information may simply not be received by the foraging insect because the antenna could lack receptors for those specific volatiles or the compounds do not reach thresh- (2) The attractive POP: blend, threshold concentrations and ratios of volatiles old concentrations. Receptors for plant volatiles were long considered to be generalist, but today many specific insect When encountering the strands of an odour plume, an insect receptors for plant volatile components are known (e.g. Lars- has to decide whether the plume is of interest and whether son, Leal & Hansson, 2001; Bichao et al., 2005; Roestelien to respond behaviourally. Odour plume characteristics, such

Biological Reviews 89 (2014) 68–81 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society Plant odour plumes 75 as the blend, threshold doses and ratios, can aid in this decision. Furthermore, prior experience with the odour and its association with successful resource location may significantly affect the behavioural response to a plume (Vet & Papaj, 1992). As the blend of compounds in an odour plume released from a single source initially is carried in stable filaments, the compounds will arrive simultaneously at the antennae. The co-location of receptors in sensilla allows the detection of simultaneously arriving odorants present in a blend. Insects are able to distinguish between a blend of volatiles (e.g. compounds A+B) released from a single source and the same volatile compounds A and B each released from different sources since in the latter case the antennae encounter the strands from different sources consecutively, and the compounds are received asynchronously (Nikonov & Leal, 2002; Bruce et al., 2005, and references therein). Fig. 2. Influence of the qualitative and quantitative composition Odour filaments with a specific composition and information of a volatile mixture in an odour plume on successful olfactory may be distinguished from non-informative filaments with resource location. Filaments of four different odour plumes the ‘wrong’ composition. While pheromone perception is I–IV released by four different sources are shown. Filaments of normally processed by so-called ‘labelled lines’ leading plume III are illustrated at different distances from the source directly from highly specific receptors to the central nervous (IIIa, b, c). All odours consist of combinations of three volatile system, plant odours are often coded by across-fibre patterns compounds A, B and C. An insect can distinguish filaments of plume III [the resource-indicating plant odour plume (POP) in (e.g. Hildebrand, 1995). In across-fibre coding, several this example] from filaments of plumes I and II (background receptors respond to an odorant, and thus several stimulus- odour plume) by the occurrence of all three compounds instead responsive neurons are involved in the odour code (e.g. of only two of them. It can also distinguish the filaments of Hildebrand, 1995; Sandoz et al., 2007). An insect that plume IV (background odour plume) from those of plume III by measures the quantitative and qualitative composition of detecting the ratios of the three compounds. Suboptimal ratios odour conveyed by an odour filament is able to discriminate may occur in a resource-indicating POP (IIIc) with increasing a specific plume from other plumes present at the same time distance from the source. Insects that rely on a distinct ratio in the surroundings (Fig. 2). may risk missing such a plume. Insects that are less specific with In addition to the qualitative composition of a POP, regard to ratios could risk responding incorrectly to plume IV, which exhibits the right blend but in the wrong ratios. concentrations of components within a plume are also important in rendering a POP attractive. The relevant components have to be present in a filament at concen- a host odour, but a higher risk of responding to the wrong trations reaching at least the threshold concentrations that signal (plume IV in Fig. 2). Wiley (2006) states that reducing can be detected by the receptors (Almaas & Mustaparta, the probability of missing the right signal will always increase 1990). In insect pheromone research, the active space of the probability of responding to the wrong signal and vice a pheromone is defined as ‘the volume of air inside which versa. Hence, the degree of specificity towards quantitative the odor concentration is above threshold, i.e., the level plume traits always implies a trade-off between accuracy in sufficient to produce a behavioral reaction in the receiving resource encountering and risk of missing the resource. organism’ (Elkinton & Carde,´ 1984, p. 73). Keeping track Numerous studies have shown that an insect’s prior of a POP may not only depend on the concentration of experience with a plant odour and the association of this a single major component, but also on the upper and odour with successful resource location can significantly lower concentration thresholds for the blend in a manner affect behavioural responses to this odour (Visser & Thiery, similar to the active space of a pheromone proposed by 1986; Papaj & Prokopy, 1989; Vet & Dicke, 1992; Riffell, Linn, Campbell & Roelofs (1986). 2011). It has been shown for some insects that such Insect olfactory orientation by means of the ratios of associative learning of plant odours not only depends on the components of a POP may help insects to obtain specific qualitative composition of the blend of volatiles or threshold resource information even in cases involving ubiquitous concentrations, but also on the ratio of components within volatiles. An insect that recognises a host plant by odour a blend (Wright & Thomson, 2005, and references therein; may specifically respond to the ratios of host plant volatiles, Beyaert et al., 2010). but in the process risk ignoring a host odour plume if the ratios in this plume are suboptimal (i.e. if ratios do not (3) Following a plume: single plume tracking perfectly match the ratios of the volatile blend of the host plant) (plume IIIc in Fig. 2). An insect that is less specific The process of following an odour plume to its source is with respect to ratios of volatiles faces a lower risk of missing called plume tracking. The best understood system of plume

Biological Reviews 89 (2014) 68–81 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society 76 Ivo Beyaert and Monika Hilker tracking by using wind and odour is that of orientation of 1992). Plume switching due to higher quality may occur, for male moths to female pheromones. example, when an herbivorous insect encounters first a POP Male moths follow a plume of pheromone by means of a host plant of low preference followed by a POP of a of surge and cast flight behaviour. Encounter with a highly preferred host plant. Plume switching due to reliability single pheromone filament of the right plume induces an may occur in parasitoids switching from an odour released upwind surge. A surge is performed by steering upwind by the host to POPs released by the host-induced plant, or and increasing airspeed (while groundspeed may remain vice versa. For example, the egg parasitoid Closterocerus ruforum unchanged) (Mafra-Neto & Carde,´ 1994, 1996; Vickers & is attracted by pheromones of its diprionid pine sawfly hosts, Baker, 1994, 1996; Quero, Fadamiro & Baker, 2001). The but also by the odour emitted by Scots pine in response surge lasts for a defined period of time. If another odour to egg deposition by the host sawflies (Hilker et al., 2000, filament is encountered during the surge, another surge 2002). It has been postulated that the parasitoid uses the host is initiated, resulting in a prolonged surge. If at the end pheromone as a long-range cue and the egg-induced plant of the surge no filament has been encountered, casting volatiles over short distances (Hilker et al., 2002; Hilker & is initiated (Mafra-Neto & Carde,´ 1996). Casting involves Meiners, 2011). For an egg parasitoid, the egg-induced pine flying crosswind with repeated turns and lateral excursions odour may be more reliable than the host pheromone since but without substantial progress upwind (Kennedy, Ludlow the egg-induced POP leads directly to the eggs, whereas the & Sanders, 1981). Odour quality influences this behaviour. host pheromone only leads to the location of the pheromone- Addition of an antagonistic compound to a sex pheromone emitting female sawfly, which may or may not lay host eggs blend elicits suboptimal casting/surging responses in moths at the calling site later on. (e.g. Vickers & Baker, 1997). Whether repellent or masking A theoretical pattern of plume switching by an insect plant volatile components have similar effects on cast-and- foraging for a resource by odour is shown in Fig. 3. In surge movements towards attractive host-plant odour has this case the foraging insects successively encounter three not been studied to date. different plumes, which are all of interest to them, but of Behaviour similar to that described for male moths moving different ranks. For example, a parasitoid searching for its towards a pheromone source has been shown for other insects herbivorous host insect by using herbivore-induced plant orienting towards plant odours (e.g. Carde´ & Willis, 2008, volatiles. Plume A is emitted by a plant in response to and references therein). Upwind counterturning similar to herbivory by the preferred and optimal host of the parasitoid. casting in moths has been observed in several insect taxa, Thus, it has a high reliability and indicates high quality, and such as flies (e.g. Voskamp et al., 1998; Budick & Dickinson, therefore is most preferable (high rank). Plume B is emitted 2006), parasitic wasps (Whitman & Eller, 1990; Kaiser, Willis by a plant in response to herbivory by a suboptimal host &Carde,´ 1994), and ants (Wolf & Wehner, 2000). Casting insect. It has a high reliability but indicates an intermediate behaviour is not limited to insects or other arthropods; it has quality (suboptimal host) (intermediate rank). Plume C is also been found in fishes and birds (DeBose & Nevitt, 2008). emitted by a plant which may serve as food plant for the parasitoid’s host, but no host insect is feeding upon the (4) Orientation among various plumes: hierarchical plant. Thus, a plume from this plant offers low reliability POP tracking (not induced) and indicates low quality since a host did Considering the response of an insect to a single odour plume not yet infest this plant; this plume is least preferable (low is an oversimplification, which does not reflect the situation rank). Figure 3 presents an odour plume ‘grid’ in which that normally occurs in the field. In nature, an insect is likely three sources of each rank are present, and each plume is to encounter several different plumes simultaneously. POPs crossed by the other plumes. The figure shows the outcomes may act together with odour plumes emitted from other for an insect following the encountered POPs according to insects, insect faeces, etc. to guide an insect to a resource. their ranks, i.e. in a hierarchical order. For example, insect For example, parasitoids of herbivorous insects are known 1, which initially follows the plume of the least preferable to use host cues as kairomones as well as feeding-induced or source C, switches to the plume of source B of intermediate oviposition-induced plant odours to find insect hosts (Hilker rank. Insects 2–6 reach source A with the highest rank & McNeil, 2007; Fatouros et al., 2008). by tracking plumes according to their hierarchical order. We suggest here that insect olfactory navigation through Although these examples represent theoretical situations various different odour plumes might follow a pattern of since all plumes unrealistically cross each other at right ‘plume switching’ in a hierarchical order. If odour strands of angles, they show how plume switching might contribute a second plume are encountered during navigation along a in an optimal foraging behaviour context (Charnov, 1976; plume, the first plume might be left in favour of the second. Scheirs & de Bruyn, 2002) to guide insects to an optimal This could happen if the insect considers the latter to be of source in a complex odour environment. higher interest, or essentially of higher rank. Several plumes In nature, plumes from sources of different rank (and could be followed successively in this manner. attractiveness) will not cross in a regular pattern (unlike The rank of an odour plume should depend on both the Fig. 3) due to air movement or vegetation structure. quality of the resource indicated by the odour, and on the Nevertheless, the theoretical ideas outlined in Fig. 3 may reliability of the odour in indicating a resource (Vet & Dicke, be transferred to a more natural situation. For example,

Fig. 3. Model of hierarchical plant odour plume (POP) tracking. This example shows optimal parasitoid insect host-searching behaviour arising from switching among POPs according to their rank. Highest rank A: resource of high quality (preferred host feeding on plant) and POP of high reliability (released in response to herbivory); intermediate rank B: resource of intermediate quality (suboptimal host feeding on the same plant) and POP of high reliability (released in response to herbivory); lowest rank C: resource of low quality (no host present yet on plant) and POP of low reliability (released by plant without host present). A POP grid illustrates the crossing of POPs of different ranks. Six insects are released at the distal end of a POP. The dashed arrows indicate how an insect follows encountered POPs according to their ranks. In this model, the insect only switches from one plume to another if the newly encountered plume is of a higher rank. Encountered plume strands of lower or equal rank than that being followed are ignored. POP tracking in this way guides five of the six insects to the most preferred and optimal source A, whereas a single insect reaches source B, and no insect lands on source C. imagine a foraging insect first encounters a plume of low orients to and reaches the high-rank source, the first odour rank, but as it flies upwind, it comes closer to a source of plume has been left. A third source could be tested in a high rank and thus meets the meandering high-rank plume similar way. In order to test whether plume tracking indeed during cast-and-surge-flight. follows the hierarchy of the odour source, a further test run This concept of hierarchy-guided plume-switching should investigate whether the insect remains in the high- behaviour could be tested in bioassays investigating if a rank plume if this is offered first and the low-rank plume is plume of low rank is abandoned by an insect when it meets offered later. The experimental set-up suggested here may a plume of high rank. Such behaviour of an insect for which allow to test whether insects can discriminate intermingling at least two attractive plant odours of different hierarchy are plant odour plumes of different ranks; this discriminative known could be tested in a wind tunnel. The bioassay should ability may be similar to the well-known ability of insects to take into account information obtained using behavioural discriminate between intermingling conspecific (high interest) and electrophysiological assays testing the insect’s response to and heterospecific (no interest) pheromonal plume strands intermingling odour plumes (e.g. Witzgall & Priesner, 1991; that share the same major components, but differ in minor Liu & Haynes, 1992; Baker et al., 1998; Myrick et al., 2009). ones (e.g. Lelito et al., 2008). Knowledge of the chemistry of the test plant odours would allow appropriate ratios and concentrations of the odour chemicals to be used. A suggested protocol is as follows. Two or more test odour sources should be located V. CONCLUSIONS separately (several distances should be tested) in the wind tunnel. The location of the odour sources, the aeration of the (1) This review introduces a plant odour plume (POP) concept system and the length of the wind tunnel should be designed as a tool for understanding the odour orientation of insects such that the test source plumes meet or intermingle within to plant volatiles in complex and heterogenous odorous the tunnel. For the bioassay, initially only the low-rank odour environments. is offered to the insect. When oriented flight towards that (2) A comparison of several traits of POPs and insect odour is initiated, the high-rank odour source is offered by pheromonal plumes revealed that these types of plumes uncovering the source or opening a valve. If the insect now show some similarities in how they are recognised by insects.

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(Received 12 December 2011; revised 19 April 2013; accepted 25 April 2013; published online 28 May 2013)