COMMENT

Potential defence from herbivory by ‘dazzle effects’ and‘trickery coloration’ of leaf variegation

SIMCHA LEV-YADUN*

Department of Biology & Environment, Faculty of Natural Sciences, University of Haifa – Oranim,Tivon 36006, Israel

Received 3 November 2013; revised 12 December 2013; accepted for publication 12 December 2013

The very conspicuous dazzle coloration invented for naval defence during World War I was used in pre-radar daysto mislead attackers of naval units about vessel size, type, speed, and direction. Among several potential types ofdefences, it is proposed that zebra-like white leaf variegation may defend leaves and other plant organs fromherbivory as a result of dazzle effects. Two different dazzle effects may be involved in defending plants fromherbivory, making it hard for herbivores (1) to decide where, in a three-dimensional space, to bite the leaves (largeherbivores) and (2) to land on them (insects). In addition, the related types of leaf coloration described in thepresent study, comprising parallels of military defensive trickery naval painting, may also deceive herbivores aboutthe actual shape, location, and identity of leaves. Some of these visual defences may operate at the same time asother visual defences, such as aposematism, or serve various physiological functions. © 2014 The Linnean Societyof London, Biological Journal of the Linnean Society, 2014, 111, 692–697.

ADDITIONAL KEYWORDS: aposematic – camouflage – deception – ecology – evolution – mimicry – visual.

INTRODUCTION

Dazzle and trickery coloration were developed todefend navies when the range of artillery and torpe-does surpassed the range of several kilometers,and when aiming by visual means ruled the navalbattlefield. Despite the huge scale of use of dazzleand trickery coloration during World Wars I andII (Wilkinson, 1969; Stanley, 1998; Williams, 2001;Forbes, 2009), and the apparent visual parallels ofthese patterns of coloration in animals and plants,very little attention was given to these potential typesof defence in biology. Defensive dazzle plant colorationreceived only a very limited attention, without dis-cussing the theoretical aspects (Lev-Yadun, 2003,2006, 2009a), even when compared with the limitedattention that it received in zoology.

Four different major types of visual deception wereinvolved in trickery naval painting (painted trickerysensu Stanley, 1998). The first type is simple: paintingthe fore and aft sectors of naval units lighter. The

second type of painted trickery involves painting falsebow waves. This can be achieved in two ways: (1)painting on the bow side, giving the impression of ahigher speed than the actual speed, or (2) paintingalso or only on the stern side, causing confusion aboutthe direction in which the vessel is heading (Stanley,1998; Williams, 2001). A similar deceptive defencetactic in animals is known as a ‘false head’ or ‘deflec-tion marks’ and these are assumed to divert predatorattacks towards less critical body parts (Cott, 1940;Wickler, 1968; Edmunds, 1974; Robbins, 1980, 1981;Ruxton, Sherratt & Speed, 2004). The third typeinvolves painting shapes of other vessels as if posi-tioned alongside the hull, creating the illusion thateither another vessel is blocking the way for artilleryshells, torpedoes, and aerial bombs to the target, orthat there is an escort vessel present that mightattack (Stanley, 1998; Williams, 2001). The fourthtype of trickery naval painting is visually and theo-retically the most complicated: dazzle painting. It wasproposed to the British Admiralty as a visual defen-sive measure during the critical German submarineattack crisis in the year 1917 by the professional*E-mail: levyadun@research.haifa.ac.il

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marine painter Norman Wilkinson, who served as anofficer in the Royal Navy during World War I andrealized, during his vessel’s patrols at sea, that, undermany types of illumination, regular naval camouflagenot only failed to conceal vessels, but also sometimeseven made them more conspicuous (Wilkinson, 1969).He proposed to the British Admiralty that, instead ofusing the non-efficient camouflaging of navy units,they should be conspicuously painted with strongcolours applied in a way that would make it hard toidentify the vessel type, as well as its distance, speed,and direction.

Herbivores, which are usually not well defendedagainst fierce carnivores at close range, operate undervarious fears (Rothschild, 1984; Brown, 1999; Sheriff,Krebs & Boonstra, 2009; Janzen, Hallwachs & Burns,2010). Thus, part of the attention of herbivorousanimals is always drawn away from their prey (i.e.the plants) and this helps the defending plantsthat have evolved characters adding various visualdifficulties to prolong the time needed for decisionmaking, thus exploiting for defence the herbivore’slimited attention (Jones, Krebs & Whittingham,2006).

The present study describes the theoretical basisof the dazzle issue and the related types of trickeryleaf coloration as potential visual defences of plantsfrom herbivory. These issues were never discussed indepth by botanists or zoologists with respect to plant–herbivore interactions.

DAZZLE COLORATION IN ANIMALS

Because coloration has been ignored as a significantdefensive mechanism in plants for a long time, thestate of art in zoology (although also very far frombeing sufficient) can be used as a standard in manycases, whereas dazzle coloration has received, untilrecently, only limited attention even in animals and,for many years, it remained untested and the defini-tions were also partly misleading because of thecommon confusion with disruptive coloration (Forbes,2009). In both the military and nature, the bordersbetween these two types of defensive coloration arenot always clear, especially because certain colourpatterns may serve as camouflage when distant andfor dazzling or trickery at close range. Dazzle colora-tion consists of high contrast patterns that make theprey conspicuous, although it results in difficultiesin estimating the speed and trajectory of prey andin identifying its specific limbs. The best commonlyknown suggestion for the operation of dazzle asan anti-predator defence is for the zebra’s stripes(Kruuk, 1972; Kingdon, 1984; Morris, 1990), althoughthis hypothesis, which was not supported by carefullyexamined predation statistics, was basically rejected

(Ruxton, 2002). The recent detailed experimentalstudy (Egri et al., 2012) of the role of zebra stripes inhorsefly (tabanids) repellence appears to give verystrong indications that such patterns indeed functionat least in insect repellence, even if the mechanismis unknown. After decades of some theoretical dis-cussions (Stevens, 2007; Stevens & Merilaita, 2009),only recently was some experimentation of the poten-tial for defensive dazzle effects by animals conducted,although still with human subjects as hunters ofimages on computer screens rather than in nature(Stevens, Yule & Ruxton, 2008; Scott-Samuel et al.,2011; Stevens et al., 2011; von Helversen, Schooler& Czienskowski, 2013). A study of the neuronalresponse in locusts indicated that dazzle effectsby high-contrast patterns indeed weaken move-ment detection (Santer, 2013). The results of allthese experiments illuminate both the possibilitiesand limitations of the defensive potential of dazzlecoloration.

ACTUAL AND RELATIVE PLANTMOVEMENT AND ITS POSSIBLE ROLE

IN DAZZLE EFFECTS

As discussed above, the operation of naval dazzlepainting is related to giving the wrong impression ofidentity, size, speed, and direction. When this type ofvisual defensive tactic is discussed with respect toplants, it immediately raises the question of themovement component in such a defence. The role ofplant movement as defence against herbivory hasbeen almost overlooked. The classic examples includethe escape from herbivory by folding of Mimosapudica leaves (Jensen, Dill & Cahill, 2011) or theexposure of thorns by leaflet folding (Eisner, 1981).Lev-Yadun & Inbar (2002) proposed that the blackanthers of Paspalum, which move with a light wind,may look like swivelling aphids. Later, Lev-Yadun(2009a) proposed that the swaying of leaves, stems orbranches in the wind may help in ant mimicry byplants by giving the illusion that the pigmentationpatterns proposed to mimic ‘ants’ (Lev-Yadun & Inbar,2002) are moving. Yamazaki (2011), in the first broad,innovative and intriguing theoretical treatment ofdefensive plant movement, advocated the hypothesisof considering the possible roles of passive leaf move-ment as a common anti-herbivory defence, althoughnot in the connotation of dazzle effects.

The visual aspect of plant movement as a way ofcommunication with (and deception of) animals hasalready been studied in two cases of pollinator attrac-tion. In the first, some orchid species belonging to thegenus Oncidium induce attacks by territorial maleCentris bees when the inflorescences move in thewind because the male bees mistake them for rival

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male bees. During the attacks of the pseudo rivals,the male bees transfer the pollen (Dodson & Frymire,1961; Wiens, 1978). In the other case, Warren &James (2008) showed that movements (‘waving’) ofthe inflorescences of Silene maritima increase polli-nation success. Thus, following such functional exam-ples from pollination biology, there is no theoreticalreason to dismiss the possibility that actual and rela-tive plant movements take part in visual defence fromherbivory (Lev-Yadun & Ne’eman, 2012).

There are two ubiquitous possibilities for plantmovement. The first is the actual swaying ofleaves, stems, branches or flower parts in thewind (Lev-Yadun & Inbar, 2002; Lev-Yadun, 2009a;Yamazaki, 2011). When the plants move, their mor-phological and colour patterns move with them. Aftermaking many attempts myself to photograph varioustypes of defensive coloration under windy conditionsin the field, it became apparent that the movement,especially of leaves, may be significant. The othertype of movement is relative: the outcome of themovement of the head of large herbivores as theyapproach plants, or that of the whole body of insectsthat fly towards the plants. This is not true forcaterpillars, aphids or other small herbivores thatalready inhabit leaves or walk slowly on them. There-fore, although plants are commonly considered to bemotionless targets for foraging herbivores, this is notthe case in many instances.

POTENTIAL DEFENCE BY DAZZLEEFFECTS AND OTHER TRICKY TYPES OFLEAF VARIEGATION AND COLORATION

Two types of leaf variegation and coloration indicatethe possibility that variegated plants indeed use var-iegation and coloration as a visual defence to trick thesensory system of the herbivores with repect to leafsize and location, such as with naval trick coloration.It is suggested that this is not aposematism and,instead, a simultaneous aposematic function mayoperate in certain cases when the variegated leavesare spiny or toxic. The variegation types are classifiedin accordance with the naval terminology: trickeryand dazzle coloration. The basic principle of suchdefence is its bearing on the trade-off between speedof decision/operation and accuracy when biting theplant. A similar trade-off appears to operate in imper-fect mimicry based defence systems (Chittka &Osorio, 2007; Janzen et al., 2010). The longer ittakes a herbivore to decide where to bite or land, thehigher are the risks of attacks by predators (Lima &Dill, 1990; Brown, 1999; Ripple & Beschta, 2004;Nersesian, Banks & McArthur, 2011), along with thedecrease in feeding efficiency.

Certain plant species have white or colourful zoneson their leaves formed parallel to their contours,which create a visual illusion of several leaf layersinstead of one. This pattern is typical of several wildtaxa common in Israel: Amaranthus sp., Lamiummoschatum, and Cyclamen persicum, all with whitemarkings; Polygonum lapathifolium, with dark mark-ings; and Trifolium spp. and Medicago spp., witheither white or various similar colourful markings.The genus Cyclamen is especially characterized bysuch white variegated leaves (Grey-Wilson, 1988). Ina much more limited search of the flora of Switzer-land, the same phenomenon was found in Lamiumgaleobdolon, Trifolium repens and Trifolium pratense(with white markings), as well as Medicago arabicaand Polygonum lapathifolium (with dark markings).Except for Cyclamen species that occupy both openand forested habitats, all other taxa occupy open andwell illuminated habitats.

It is proposed that, in certain plant leaves, colora-tion patterns formed parallel to their contours (Fig. 1)may cause the visual illusion of a fake leaf shape,size, distance, and perspective, blurring actual leafshapes, sizes, and distances, making it difficult forherbivores to estimate the distance to the leaf andaim their bites or landing. When there are severalsuch parallel markings, the leaf may look as if it ismade of several leaf layers that occupy differentplanes. Leaves of such taxa use the vegetal parallel tothe third type of defensive naval painting (i.e. paint-ing shapes of smaller vessels as if positioned along-side the hull) (Stanley, 1998; Williams, 2001). As withseveral other types of defensive plant coloration, addi-tional physiological or defensive functions of suchcoloration should also be considered specifically foreach species and ecology.

Figure 1. Coloration patterns formed parallel to leafcontour in Cyclamen persicum giving the visual impres-sion of several leaf layers when only one exists.

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Theoretically, coloration that produces an illusion ofa different leaf shape may also cause identificationproblems for insects that search for specific leaf typesor leaf developmental stages (Prokopy & Owens,1983; Brown, Lawton & Grubb, 1991; Reeves, 2011).Moreover, because some of the plants with leavesvariegated in white (or with other colours) (e.g. Cycla-men spp. and certain Trifolium spp. and Medicagospp.) may be poisonous in that there are cyano-genic types in Trifolium spp. and Medicago spp.(Crawford-Sidebotham, 1972; Dirzo & Harper, 1982)and Cyclamen species known to be rich with alkaloidsand saponins (Hornell, 1941; Reznicek et al., 1989),the visual illusion may thus not be the sole visualdefensive mode and these patterns may also serveas aposematic coloration. Müllerian and Batesianmimicry rings are expected to exist in such cases.

To date, zebra-like white leaf variegation has beenvery briefly proposed to serve as defensive dazzlecoloration (sensu Wilkinson, 1969) only for the threespecies of open, well-illuminated Mediterranean habi-tats Silybum marianum, Notobasis syriaca, andScolymus maculatus (Lev-Yadun, 2003, 2006, 2009a,b) (Fig. 2). It is proposed that this hypothesis can beextended to various species belonging to the generaHaworthia, Gasteria, and Sansevieria, which alsohave zebra-like white leaf variegation, as well as toany other plant taxa with such coloration. Interest-ingly, all these three genera are common in openhabitats in arid and semi-arid districts of SouthAfrica, habitats resembling those occupied by thethree Mediterranean species listed above. This coin-cidence may indicate a similar function(s) and similarevolutionary pressures. Such plants actually haveclassic dazzle coloration very similar to that appliedto naval vessels [compare photographs of the French

cruiser Gloire in Williams (2001) or on the Internet,and other photographs in Wilkinson (1969), andStanley (1998), with those in Lev-Yadun (2003)]. Theswaying of the leaves in the wind, and the relativemovements of plants with respect to flying insects orthe head movements of large herbivores approachingthe plants, increase the potential to form the desireddazzle effects on the visual nerve systems of theherbivores, making it difficult for them to land on orbite the leaf because of problems in locating its actualposition in space.

The putative dazzle effects of such variegation areprobably not the sole visual defensive function insome of these plants. It has been proposed that theconspicuous zebra-like leaf variegation of the veryspiny species S. marianum, N. syriaca, and S.maculatus serves mainly as visual aposematism(Lev-Yadun, 2003, 2006, 2009a, b). Lev-Yadun (2003)proposed that mimicking of tunnelling by flies belong-ing to the Agromyzidae to deter female Agromyzidaeflies from laying eggs, and that such conspicuousstripes reduce insect landing on the leaves in general,as was proposed for the evolution of zebra stripesshould also not be ruled out.

In conclusion, in accordance with the data obtainedfrom recent experiments indicating that dazzle effectsmay defend animals from predation (Stevens et al.,2008, 2011; Scott-Samuel et al., 2011; von Helversenet al., 2013) and from the morphological descriptionsof potential dazzle patterns in leaves of various taxa(Lev-Yadun, 2003, 2009b) and those described in thepresent study, defence from herbivory by dazzle andtrickery coloration should be considered as a workinghypothesis with respect to the hundreds, if not thou-sands, of plant species that express such types of leafcoloration.

ACKNOWLEDGEMENTS

I thank Professor John A. Allen and two anonymousreviewers for their important suggestions.

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