Gone with the wind: trembling leaves may deter herbivory

Gone with the wind: trembling leaves maydeter herbivory

KAZUO YAMAZAKI*

Osaka City Institute of Public Health and Environmental Sciences, 8-34 Tojo-cho, Tennoji, Osaka543-0026, Japan

Received 27 May 2011; revised 30 June 2011; accepted for publication 1 July 2011bij_1776 738..747

Plants employ various defensive tactics against herbivores but are rarely considered to use rapid movements toresist predation. However, the aboveground parts of plants are often forcefully moved by wind and rain. Thispassive movement has been overlooked as an anti-herbivore trait. The leaves of many plant species, such as aspens,Indian sacred fig, bamboos, and palms, tremble even in a slight breeze. Leaves that are easily moved by gentlewinds can sometimes resist strong winds and may have other benefits as well. In the present study, it is proposedthat the movement of such plant leaves physically deters arthropod herbivory and pathogen infection by repellingcolonization and oviposition by herbivorous insects. This leads to herbivores and pathogens being dislodged fromthe plants, and the ensuing death of the herbivores on the ground or at least their recolonization to other plants,as well as the interruption of feeding, intraspecific communication and the mating behaviour of herbivores, thuslowering their performance on the plant or increasing enemy attack of the herbivores. In addition, passive leafmovements may undermine herbivore camouflage and expose them to predation, and may also allow plant volatilesto diffuse efficiently to repel herbivores and attract natural enemies. Thus, the mechanistic properties of theseleaves may have anti-herbivore effects in the wind and rain. This hypothesis can also be applied to aquatic plantsthat tremble in gentle water currents. In addition, genetic manipulation of the tendency for leaf movement maybe beneficial for the management of pest insects and pathogens with reduced pesticides in forestry and agricul-ture. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 738–747.

ADDITIONAL KEYWORDS: anti-herbivore defence – biomechanics – motion camouflage – multifunctional-ity – passive plant movements – plant–herbivore interactions – plant volatiles.

MOVEMENTS IN TERRESTRIAL PLANTS

Many animal species avoid predation and parasi-tism by rapid body movements, including running,fleeing, flying, hiding, grooming, and counterattack(Valentine, 1973; Ydenberg & Dill, 1986; Cornell,Stamp & Bowers, 1987; Herberholz, Sen & Edwards,2004; Mooring, Blumstein & Stoner, 2004). At thesame time, anti-herbivore defences of plants are rela-tively static, including diverse chemical defences,spines, and herbivore satiation (Janzen, 1976;Bennett & Wallsgrove, 1994; Lev-Yadun & Halpern,2008). Defences by rapid movements are scarcelyappreciated, even though plants clearly perform

complex behaviours (Darwin, 1880; Karban, 2008;Koller, 2011) and sometimes move rapidly; forexample, carnivorous plants capture prey inverte-brates in a few seconds (Fagerberg & Allain, 1991;Braam, 2005). As an anti-herbivore defence, whendisturbed by herbivores, the sensitive plant Mimosapudica L. (Fabaceae), as well as related species,quickly folds its leaflets to hide them from herbivoresor lowers its compound leaves to expose protectivethorns (Eisner, 1981; Braam, 2005). In addition, thebitter cress Cardamine scutata Thunb. (Cruciferae)bursts its siliques in response to chewing by seed-eating caterpillars, expelling the caterpillars, or evenstrangles them with pericarps (Yano, 1997). However,these are specific cases, and the more common rapidmovements of plant organs for anti-herbivoredefences are generally overlooked.*E-mail: [email protected]

Biological Journal of the Linnean Society, 2011, 104, 738–747. With 1 figure

© 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 738–747738

The aboveground organs of terrestrial plants areoften forcefully moved by continuous air currents andoccasional precipitation. The drag and flexibility ofleaves vary greatly among plant species, resulting ina variety of movement patterns in the wind (Vogel,1989). For example, most plant leaves with short,stout petioles resist gentle winds and flutter errati-cally in strong winds (Vogel, 1989). Pinnately com-pound leaves and leaf clusters of several tree speciesconfigure in elongate cylinders in the turbulent wind,and the diameter of the cylinder decreases with windspeed (Vogel, 1989, 2009). Additionally, the leaves ofmany plants such as aspens and poplars Populus spp.(Salicaceae), as well as the Indian sacred fig Ficusreligiosa L. (Moraceae), tremble even in the slightestbreeze (Fig. 1A–C) (Vogel, 1989, 2007; Niklas, 1991;Gupta, 2001). The petioles of Populus spp. are long,flexible and bilaterally flattened (Fig. 1A), whichmakes their leaves tremble in modest winds (Fig. 1B)

(Vogel, 1989, 2007). The palmately lobed leaves ofcastor aralia Kalopanax pictus (Thunb.) Nakai (Ara-liaceae) have very long (10–30 cm; Fig. 1D) petiolesthat shake from side to side similar to waving handsin slight winds (K. Yamazaki, personal observations).Additionally, many bamboo and palm leaves rustle inthe breeze (K. Yamazaki, pers. observ.).

The present study focuses on leaves that are easilymoved by slight winds and their proposed adaptivesignificance. Vogel (1989) examined the drag of manyplant leaves in the wind as well as the wind speedsthat the leaves are able to resist, reporting that theleaves of the white poplar (Populus alba L.) trembleeven in a slight breeze and move violently and irregu-larly in strong winds; however, they can resistdamage even at a wind velocity of 30 m/s, whereas theleaves of other species suffer mechanical damage atthat speed. Therefore, resistance to strong winds maybe an adaptive advantage for leaves that easily

Figure 1. Leaves that tremble in a slight breeze. A, bilaterally flattened petioles of Populus carolinensis leaves. B,P. carolinensis leaves trembling in the breeze. C, Ficus religiosa leaves with long petioles and drip tips. D, Kalopanaxpictus leaves with very long petioles (underside). Scale bars: (A) and (B) 10 mm; (C) and (D) 50 mm.

PLANT PASSIVE MOVEMENTS AS DEFENCES 739


tremble. The present study explores the potentialadditional adaptive benefits to such leaves.

DEFENCE BY LEAF MOVEMENTS

Several plant traits have been revealed to have mul-tiple functions. For example, the flower bracts of thedove tree Davidia involucrata Baillon (Nyssaceae)photosynthesize, attract pollinating bees and protectpollen from degradation by rain (Sun et al., 2008).Some pigments and substances in flowers simulta-neously attract pollinators and deter floral herbi-vores (Gronquist et al., 2001; Hansen et al., 2007;Lev-Yadun, Néeman & Shanas, 2009). The volatileisoprene of tobacco plants not only protects plantsfrom temperature and oxidative stress, but alsodeters feeding by the tobacco hornworm Manducasexuta (Laothawornkitkul et al., 2008; Unsicker,Kunert & Gershenzon, 2009). Autumn leaf coloursmay not only prevent photoinhibition and the pro-duction of reactive oxygen species in leaf tissues, butalso have defensive functions against herbivores(Lev-Yadun & Gould, 2008; Archetti et al., 2009; Lev-Yadun, 2009). Thus, no reason exists to assume thatleaves that tremble even in the slightest breeze donot have other functions in addition to resistingharsh winds.

It is proposed that leaves that are easily moved bywinds and rain may deter herbivory by arthropodsand resist infection by plant pathogens. First, leavesmoving in the wind and rain evade colonizationand oviposition of herbivorous arthropods and infec-tion by plant pathogens. Herbivorous insects ingeneral select host plant species, individuals, andorgans carefully by flying around and walking on theplant parts (mainly leaves and stems) using visual,olfactory, and tactile cues (Bernays & Chapman,1994; Schoonhoven, Jermy & van Loon, 1999).However, when experiencing irregular movement ofleaves, herbivorous insects would reasonably refrainfrom performing these complex colonization and ovi-position behaviours. In addition, many plant patho-gens such as fungi and bacteria are transmitted bycontact with leaf surfaces or wounds (Huang, 1986;Knogge, 1996). Therefore, trembling leaves wouldshake off transmitting agents such as arthropods (e.g.aphids and other hemipterans), as well as directlyshake off spores and pathogenic particles from theleaves, resulting in the prevention of pathogen infec-tions. In addition, honeydew emitted by aphids andother hemipteran insects often covers leaves, causingsooty moulds that prevent photosynthesis (Tedders &Smith, 1976). By trembling in the rain, leaves mayfacilitate the washing off of the honeydew as well asother mould spores, thus preventing infection as wellas proliferation of the mould. Although rain hits

leaves perpendicularly and washes off spores andhoneydew from the upper leaf surface, breezesusually occur more frequently than rain, and trem-bling leaves in the wind and rain would shake offpathogens and honeydew from both the upper andlower leaf surfaces.

In addition, cuticular wax protects leaves frominsect herbivory and infection of pathogens by pre-vention of spore germination and shedding of insects,spores and pathogenic particles (Stork, 1980; Ried-erer & Müller, 2006). Drip tips (i.e. acuminate apicesof leaves) may also prevent pathogen infection byfacilitating water drainage (Ivey & DeSilva, 2001)(Fig. 1C). All of these leaf attributes may work inconcert with leaf trembling for the prevention ofcolonization of herbivores and pathogen infection.

Second, even if herbivorous arthropods succeed incolonizing on plants, trembling, rustling or overturn-ing leaves in the wind and rain would mechanicallyexpel or dislodge herbivorous arthropods from theplants, especially caterpillars, hemipteran nymphs,mites, and other flightless arthropods. The glabrous,smooth leaf surface with cuticular wax of manyPopulus species and F. religiosa would be effective forshaking off herbivores. Herbivores fallen from treescould die from starvation during the search for suit-able food, physical injury when they drop to theground or predation by ground-foraging predators,thus rarely returning to the original host tree(Dethier, 1987; Damman, 1991; Chau & Mackauer,1997). Perovic et al. (2008) reported that at least 15%of armyworm Helicoverpa armigera (Hübner) neo-nates drop off the host plants (herbaceous crops),many of which die on the hot ground. Thus, if the hostplants are tall trees and their leaves tremble, themortality of fallen larvae would be much higher. If theplants grow near water, the fallen herbivores maydrown, be carried away from the host plant or bepreyed upon by aquatic predators. Compared to herbleaves, tree leaves are distinctly more effective atreducing herbivore loads by dislodging via tremblingbecause returning to a tree canopy is much moredangerous and energy-consumptive than returning toherbs. Indeed, among related species, tree-dwellingcaterpillars tend to evade dropping when disturbedcompared to herb-dwelling species (Funakoshi, 1994).Naturally, many herbivores use tactics to preventdropping from host plants. For example, some herbi-vores such as stem borers, leafminers, and gallersbore into plant tissues, whereas some construct leafshelters (Loeffler, 1996) or cling to the plant organswith their claws and tarsi (Bernays, 1991; Gorb et al.,2002; Dirks, Clemente & Federle, 2010); some cater-pillars produce and climb silk threads when they dropfrom the trees to return to canopies (Brackenbury,1996; Sugiura & Yamazaki, 2006). These adaptations

740 K. YAMAZAKI


by herbivorous insects suggest the critical importanceof avoiding a fall from host plants.

Third, even if herbivores do not drop from hostplants, moving leaves could disturb or interrupt thefeeding, communication and mating behaviours ofherbivores. When immature herbivorous insects aresubjected to conditions of reduced nutritional qualityof their host plants, their development is prolongedand they are exposed to more natural enemies andadverse climatic conditions, thus increasing theirmortality (Benrey & Denno, 1997; Fordyce & Shapiro,2003). Therefore, when perpetual leaf movementhampers the feeding of herbivorous insects, theirgrowth could slow and their mortality increase.Moving leaves may also reduce leaf consumption bylarger herbivores such as leaf-feeding mammalsbecause leaf movement is likely to extend the han-dling time of plant leaves. Such an effect is demon-strated by several plant structures that can affect theefficiency of food intake for large mammals (Wilm-shurst, Fryxell & Colucci, 1999; Drescher et al., 2006).In addition, many herbivorous arthropods communi-cate and mate on their host plants. For example,some lepidopteran caterpillars and many hemipter-ans communicate with other conspecific individualsusing leaves and stems as vibrational substrates(Yack, Smith & Weatherhead, 2001; Virant-Doberlet& Cokl, 2004; Cocroft & Rodríguez, 2005; Scott et al.,2010). Given that wind-induced noise is known tointerrupt vibrational communications among herbivo-rous insects (McNett, Luan & Cocroft, 2010), rustlingleaves in the wind reasonably disrupt such commu-nication. Finally, many specialist herbivorous insectsperform courtship and mating behaviours on andaround their host plants (Headrick & Goeden, 1990;Aiello, 2004; Arbuthnott & Crespi, 2009). Therefore,moving leaves could lower the efficiency of thesebehaviours, ultimately resulting in reduced damageto the plants.

Less evidence is available for the final two mecha-nisms of the deterrence of herbivores and pathogeninfection by leaf movements; however, these visualand chemical pathways should be considered to betterunderstand the interactions between plants withpassive leaf movements and their herbivores in anatural setting. Fourth, trembling leaves may under-mine herbivore camouflage. When a slight windoccurs, most leaves that are prone to move flap uni-formly. However, leaves bearing relatively largeinsects such as caterpillars, grasshoppers, and scara-baeid beetles may move less or tremble with a differ-ent motion. Most predators detect their prey from thebackground. This slight change in leaf movement mayexpose herbivorous insects to predators, resulting inhigher herbivore mortality and reduced damage onplants. Lev-Yadun et al. (2004) argued that unusual

plant colour (e.g. red, yellow, white) may undermineherbivorous insect camouflage, resulting in exposureto predators and subsequent predation becausemost insects are plainly coloured (green, brown). Thishypothesis is similar to the hypothesis presented inthe present study (i.e. moving in sequence with thebackground is a type of motion camouflage for theprey) (Srinivasan & Davey, 1995; Justh & Krish-naprasad, 2006). Indeed, some leaf-mimicking leafinsects (Phyllidae) and orthopterans move similarlyto trembling leaves, thus using the motion to camou-flage themselves (Imamori, 2004; K. Yamazaki, pers.observ.). Therefore, the restricted or differing move-ment of leaves carrying large insects could reasonablyattract a predator’s attention. Moreover, leaf move-ment may expose herbivorous insects or other inver-tebrates hidden on the underside of leaves.

Finally, trembling leaves may facilitate the diffu-sion of plant volatiles and negatively affect herbivoreperformance. Plants emit complex volatiles whendamaged by herbivorous arthropods (Kessler &Baldwin, 2001; Karban, 2008; Unsicker et al., 2009).These herbivore-induced plant volatiles are known todirectly deter herbivores (Bernasconi et al., 1998; DeMoraes, Mescher & Tumlinson, 2001; Laothawornkit-kul et al., 2008; Unsicker et al., 2009) and indirectlykill herbivores by attracting their natural enemies(Sabelis & van de Baan, 1983; Turlings & Tumlinson,1992; Takabayashi et al., 1995; Unsicker et al., 2009).In addition, even without herbivore damage, plantsemit olfactory aposematic cues to herbivores to cir-cumvent herbivory (Eisner & Grant, 1981; Launch-baugh & Provenza, 1993; Massei et al., 2007;Holopainen, 2008; Lev-Yadun et al., 2009). Therefore,trembling leaves may reduce leeward stagnancy oftheir anti-herbivore volatiles and efficiently transportthem longer distances, resulting in reduced herbivoredamage. Furthermore, plants communicate withother parts of the same plants, other conspecificplants and even other plant species via airbornesignals (Farmer & Ryan, 1990; Karban, 2008;Himanen et al., 2010; Karban, Shiojiri & Ishizaki,2010). For example, when plants receive herbivore-induced plant volatiles from other organs or plants,the receiver plants emit volatiles that attract naturalenemies (Choh et al., 2004) or adsorb and re-releasethe volatiles to defend themselves from herbivores(Himanen et al., 2010), increase defensive substancesagainst herbivores (Farmer & Ryan, 1990; Arimuraet al., 2000; Karban et al., 2006, 2010) or increaseextrafloral nectar secretion, which attract ants andother natural enemies (Heil & Silva Bueno, 2007).Thus, plants ‘talk’ with each other using volatileemission, thereby possibly defending themselves atthe community level (associational resistance)(Karban, 2007; Himanen et al., 2010). If trembling



leaves can more efficiently transport their volatiles toambient plants, surrounding plants would reinforceanti-herbivore mechanisms and enjoy a fitness gainvia reduced herbivory. As such, herbivorous insectsfallen from plants to the ground by moving leaveswould try to search for other suitable food plants,although ambient plants may be prepared for thearrival of the herbivore beforehand.

COST OF PASSIVE LEAF MOVEMENTS

As discussed above, leaves that are prone to move-ment by wind may possess many advantages for thedeterrence of herbivory. However, the wind-inducedleaf-moving tendencies among plant species varygreatly (Vogel, 1989, 2007, 2009; Niklas, 1991). Thissuggests that the costs of allowing leaf movement arenot always negligible and that the cost/benefitbalance for leaf passive movement differs amongplant species and habitats.

Several potential costs and disadvantages to leavesthat are easily moved in the wind and rain areoutlined below. First, because leaves moving in thewind are severely bent and twisted, they mustpossess flexible leaf lamina and petioles (Niklas,1996, 1999; Read & Stokes, 2006). Thin, flexibleleaves may be vulnerable to desiccation, increaseddamage by ultraviolet radiation and herbivory as aresult of thin cuticles and soft vascular bundles (Read& Stokes, 2006). Second, leaves generally align at anoptimal angle to the sun for efficient photosynthesis(Niinemets & Fleck, 2002); however, moving leavescannot maintain this optimal horizontal alignment inthe sun and thus may experience reduced photosyn-thetic efficiency, although moving leaves may experi-ence increased opportunities to capture sun flecksin the understorey. Third, although moving leavespotentially ward off herbivores and pathogens, theymay also deter beneficial partners including preda-tors, parasitoids, pollinators, and seed dispersalagents. Moving leaves would hinder these organismsfrom feeding, colonizing, ovipositing and communicat-ing on the plants. However, because many predatorshave adaptations to dislodgement (Federle, Baum-gartner & Hölldobler, 2004) and exhibit greatermobility and flight ability than immature herbivorousinsects, any disturbance by leaf movement for thesenatural enemies is likely to be lower than that forimmature herbivores.

Ground predators would not be negatively affectedby leaf movements, although they would enjoy anincreased availability of fallen prey by wind. Addi-tionally, for plants whose flowers and fruits are borneon stable, stout parts, this negative effect would notapply to pollinators and seed dispersers. Fourth, theefficient diffusion of plant volatiles by trembling

leaves may be exploited by herbivores. Some herbi-vores use plant volatiles to locate hosts (Bernays &Chapman, 1994; Schoonhoven et al., 1999; Halitschkeet al., 2008; Unsicker et al., 2009). Larvae of the noc-turnal herbivore Mythimna separata use plant vola-tiles to regulate their circadian rhythms to facilitateescape from diurnal parasitoids (Shiojiri, Ozawa &Takabayashi, 2006). Although this type of exploitationof plant volatiles by herbivores appears to be rare,future studies may reveal additional patterns of vola-tile use by herbivores. Thus, herbivorous insects maytake advantage of the efficient diffusion of plant vola-tiles facilitated by leaf movement to locate host plantsand avoid enemies. Finally, the possibility exists thatleaf trembling may cause volatiles to be too diffused,thereby reducing their concentration and thus theefficiency of repelling natural enemies, which maynecessitate the plants to invest additional resourcestoward increasing volatile production. In addition,leaf trembling may positively or negatively affectallelopathy and interplant competition among plants.

The above-mentioned factors may limit the numberof plant species that have moving leaves in slightwinds and may thus maintain various leaf typeson land. In addition, many other biotic and abioticfactors affect leaf size and shape (Givnish & Vermeij,1976; Gutschick, 1999; Niklas, 1999; Read & Stokes,2006; Vogel, 2009), and developmental and phyloge-netic constraints limit leaf morphology (Tsukaya,2006; Sanders & Wyatt, 2009).

EVALUATION OF THE HYPOTHESIS

Despite the above noted limitations, the anti-herbivore hypothesis of passive leaf movementdeserves testing as a result of its potential applica-bility to a wide variety of terrestrial plants and theirenemies. Although little direct evidence exists tosupport this hypothesis, especially for underminingherbivore camouflage and efficient diffusion of defen-sive volatiles, there are many examples of dislodge-ment from host plants inflicting considerablemortality on herbivorous insects (Dethier, 1987;Damman, 1991; Chau & MacKauer, 1997; Perovicet al., 2008), and wind-induced noise interrupts vibra-tional communication among herbivorous insects(McNett et al., 2010). In addition, Populus trees (Sali-caceae) that have moving leaves in slight breezesharbour less herbivorous arthropod species than Salixplants (Salicaceae) that have normal leaves. InEngland, 189 species of herbivorous insects attackPopulus trees (four species), whereas 450 speciesattack Salix (five species) (Kennedy & Southwood,1984). In Germany, 470 phytophagous arthropodspecies attack Populus, whereas 728 species attack

742 K. YAMAZAKI


Salix (Brändle & Brandl, 2001). This pattern is con-sistent with the present hypothesis.

To rigorously test the hypothesis in the laboratory,both leaves that tend to move and those that moveless should be exposed to winds with differingstrengths and speeds using wind tunnels thatharbour herbivores. If the moving leaves experiencesignificantly reduced herbivory in comparison towindless conditions as well as to the motionlessleaves, the hypothesis will be supported. In the field,damage by herbivores on plant species with movingleaves in the wind should be monitored in windy andwindless habitats. In addition, herbivore damage canbe compared among plant species or phenotypes withdifferent leaf movements in areas having high andlow wind loads. In the field, fans could be used togenerate winds, or windbreaks could be used toprevent winds. However, the results obtained wouldrequire careful interpretation because the wind maynot only move the leaves, but also may directly blowoff or interrupt herbivorous insects. Experimentalmanipulation by fixing leaves to twigs that do tremblein the wind may be useful to separate these effects inthe field. The hypothesis would be supported if fixedleaves suffer relatively more herbivory than unfixedmoving leaves. To indirectly test this hypothesis, thetendencies of leaf movements in wind can be com-pared among habitats with different wind and herbi-vore loads. Habitats with continuous winds andhigher herbivore loads would be predicted to harbourmore plant species or phenotypes that have movingleaves in the breeze, whereas windless and herbivore-poor habitats may exhibit more plant species withmotionless leaves.

If differences in herbivore damage or in leaf traitswere observed using the above-mentioned observa-tions and experiments, the next step would be toclarify the mechanisms. The degree of leaf movementby which herbivorous arthropods cannot successfullycolonize plants, are shaken off the plants or cannotcommunicate or hide on plants, should be quantita-tively measured in the laboratory and comparedunder field conditions. The hypothesis would befavoured if typical outdoor winds prevent such herbi-vore behaviours via leaf movements, although volatilediffusion may also be involved. To test the hypothesisthat trembling leaves undermine herbivore motioncamouflage, whether predators efficiently locate her-bivorous insects on motionless or atypically movingleaves from the background, uniformly moving foliageshould be examined in the laboratory. Whetherleaf movement increases volatile diffusion could bestudied in wind tunnels. In addition, because moststudies examining the effects of plant volatiles onherbivores have been conducted under laboratory con-ditions (Unsicker et al., 2009), volatile emission and

its diffusion patterns should be intensively studied inthe field with different wind conditions and leaf move-ments. How winds and leaf movements affect plantcommunication via volatiles and the consequent resis-tance against herbivores should be studied under fieldconditions. In addition, the costs and constraints oftrembling leaves in the wind and rain should beevaluated. If the distribution of trembling species ishighly phylogenetically determined, potential supportof this anti-herbivore hypothesis would be reduced.

FUTURE DIRECTIONS

Despite its great impacts on plant populations, com-munities and ecosystems, the biotic effects of windhave not been well studied. Plant responses to windshave been examined mainly from the viewpoint ofmechanical resistance and physiology (van Gardingen& Grace, 1991; Ennos, 1997). By contrast, althoughthe effects of leaf morphology and structures onherbivory have been extensively investigated (Brown& Lawton, 1991; Peeters, 2002), the defensive effectsof passive leaf movements by wind and rain onherbivores have been overlooked. Leaf morphologyand anatomy that enable leaves to tremble in thebreeze should be studied as an important trait ofanti-herbivore defence.

The present hypothesis can be extended to aquaticenvironments. The variations in movements inresponse to water currents are great for aquatic mac-rophytes such as macroalgae, seaweeds, and sea-grasses of the sea and inland waters (Denny &Gaylord, 2002; Koehl et al., 2008). Aquatic plants thatare easily moved by gentle water currents may deteraquatic herbivores such as algivorous fish, snails, andsea urchins in similar ways as suggested above forterrestrial plant leaves. Aquatic macrophytes mustresist continuous water currents (Denny & Gaylord,2002) and are subject to various herbivore pressures(Hatcher & Larkum, 1983; Sheldon, 1987; Lodge,1991). Thus, their passive movements in the watercurrent may have a two-fold advantage: physicalresistance to strong water currents and anti-herbivore defences.

It is proposed that this hypothesis presents a con-ceptual framework for a new direction to pest man-agement technologies. To reduce insecticide andfungicide applications, various cultivating systemshave been devised and performed, including organicfarming and enemy release, as well as the use ofresistant cultivars, transgenic plants, and enemyattractants. Therefore, if plant phenotypes withleaves that move in the breeze are selectively culti-vated, chemical use could possibly be reduced. Ifeffective management techniques such as organicfarming enhance the presence of ground-dwelling



predators, herbivorous insects that drop off the plantsas a result of leaf movements would be effectivelypreyed upon. In more artificial systems such as glass-houses, if floors are covered with sticky pads or pansof water with detergents and fans are turned on, pestinsects may fall from the plants and die in the traps.Given that the evolutionary developmental biologyof leaf morphogenesis has recently been elucidated(Tsukaya, 2006; Sanders & Wyatt, 2009), plantphenotypes and genotypes with appropriate leafmorphologies might be artificially selected for orgenetically engineered. Thus, the passive move-ment of leaves may be a useful plant trait for pestmanagement.

ACKNOWLEDGEMENTS

I thank Professor John Allen, Simcha Lev-Yadun andfour anonymous reviewers for many useful commentson this manuscript.

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Gone with the wind: trembling leaves may deter herbivory