Israel Journal of Sciences

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Müllerian and Batesian rings of white- variegated aposematic spiny and thorny : A hypothesis

Simcha Lev-Yadun

To cite this article: Simcha Lev-Yadun (2009) Müllerian and rings of white- variegated aposematic spiny and thorny plants: A hypothesis, Israel Journal of Plant Sciences, 57:1-2, 107-116

To link to this article: http://dx.doi.org/10.1560/IJPS.57.1-2.107

Published online: 14 Mar 2013.

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Download by: [Universitaire De Lausanne] Date: 03 May 2016, At: 02:12 Israel Journal of Plant Sciences Vol. 57 2009 pp. 107–116 DOI: 10.1560/IJPS.57.1–2.107 This paper has been contributed in honor of Azaria Alon on the occasion of his 90th birthday.

Müllerian and Batesian mimicry rings of white-variegated aposematic spiny and thorny plants: A hypothesis

Simcha Lev-Yadun Department of Science Education–Biology, Faculty of Science and Science Education, University of Haifa—Oranim, Tivon 36006, Israel

(Received 4 August 2008; accepted in revised form 9 March 2009)

ABSTRACT Twenty-one wild spiny or thorny plant species growing in Israel have been found so far that are conspicuous because of white stripes and spots found on their . Twenty of these species occupy open habitats, and only one is a climber (Smilax aspera) that is found in both shady and open habitats. I propose that these spiny, thorny, or prickly conspicuous plants form a defensive Müllerian mimicry ring. The genus Launaea () includes several species that are both white variegated and spiny or thorny (a defended Müllerian mimicry ring), and four non-thorny but variegated plants (a Batesian mimicry ring). I propose that these four species that form a non-defended Batesian mimicry ring enjoy the indirect protection of both their co-generic spiny and thorny species and also of defended plants from other taxa. The long history of the considerable impact of grazing in this arid region seems to have selected for this character. Keywords: advertisement, aposematic coloration, herbivory, mimicry ring, Müllerian and Batesian mimicry, thorns, white variegation

INTRODUCTION Hinton, 1973; Harper, 1977; Wiens, 1978; Rothschild, 1980; Harborne, 1982; Knight and Siegfried, 1983; Aposematic coloration in animals is well known in Smith, 1986; Lee et al., 1987; Givnish, 1990; Tuomi insects and other invertebrates, in reptiles, fish, birds, and Augner, 1993; Archetti, 2000; Hamilton and Brown,

Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016 and mammals, and the current hypothesis about its 2001). Moreover, some of these authors, because of wide occurrence is that there is a selective advantage to their views at the moment, have rejected the operation this trait. Aposematic coloration has evolved because of the aposematic hypothesis in the specific organisms predators learn to associate the coloration (usually red, they studied (Knight and Siegfried, 1983; Smith, 1986; orange, yellow, white, black, and combinations of these) Lee et al., 1987; Archetti, 2000; Hamilton and Brown, with bad taste, danger, poison, or spines (Cott, 1940; 2001). Olfactory in poisonous plants has Gittleman and Harvey, 1980; Harvey and Paxton, 1981; also been proposed (Eisner, 1964; Rothschild, 1972, Wiklund and Järvi, 1982; Lindström et al., 1999; Mallet 1973, 1986; Levin, 1973; Atsatt and O’Dowd, 1976; and Joron, 1999; Servedio, 2000; Gamberale-Stille and Wiens, 1978; Eisner and Grant, 1981; Harborne, 1982; Guilford, 2003; Endler and Mappes, 2004; Ruxton et al., Rothschild et al., 1984; Guilford et al., 1987; Rothschild 2004; Inbar and Lev-Yadun, 2005; Marples et al., 2005; and Moore, 1987; Kaye et al., 1989; Moore et al., 1990; Speed and Ruxton, 2005). Woolfson and Rothschild, 1990; Launchbaugh and For a long time, aposematic coloration in plants re- Provenza, 1993; Provenza et al., 2000; Massei et al., ceived only marginal, scattered attention. Only a hand- 2007). Recently, several theoretical (Lev-Yadun and ful of studies have discussed it, usually very briefly and only concerning poisonous plants (Cook et al., 1971; E-mail: [email protected]

© 2009 Science From Israel / LPPltd., Jerusalem 108

Ne’eman, 2004; Schaefer and Schaefer, 2007; Lev- the aposematic hypothesis for poisonous plants: “The Yadun and Gould, 2007, 2008; Archetti, 2009; Archetti benefits to the plant of chemical defense against herbi- et al., 2009; Lev-Yadun, 2009) and experimental (Hill, vores would be greater if herbivores avoided such plants 2006) studies indicated that visual aposematism of altogether, rather than testing leaves for palatability, and poisonous plants is probably more common than previ- so causing some damage. A distinct color pattern ously thought. There are even fewer studies and reviews linked with chemical defense might function in this way. concerning aposematic coloration in thorny, spiny, and for leaf color should then coincide with prickly plants (Lev-Yadun, 2001, 2003a,b, 2006a, 2009; polymorphisms for chemical defense. Müllerian and Midgley et al., 2001; Lev-Yadun and Ne’eman, 2004, Batesian mimicry could result in of similar 2006; Midgley, 2004; Rubino and McCarthy, 2004; patterns of variegation, with or without associated toxic- Ruxton et al., 2004; Speed and Ruxton, 2005; Halpern ity, among other species which have herbivore species et al., 2007a,b; Lev-Yadun and Gould, 2008; Lev- in common with the model species” (Smith, 1986: 284). Yadun and Halpern, 2008; Ronel et al., 2009). These Müllerian mimicry is a phenomenon in which two or recent proposals, that spiny, thorny, and prickly plants more species with effective defenses share a similar ap- may be visually aposematic, were based on the fact pearance. Batesian mimicry is a phenomenon in which that spines, thorns, and prickles are commonly colorful members of a palatable species gain protection from or marked by various types of associated coloration, predation by resembling unpalatable or defended spe- including white markings. It has been proposed that cies (Ruxton et al., 2004). Givnish (1990) proposed that there are several types of mimics of aposematic thorny from color-blind vertebrate herbivores is plants (Lev-Yadun, 2003b, 2006a, 2009; Lev-Yadun and the major selective agent for variegated leaves in short Gould, 2008) and that plants may also use mimicry of herbs in the flora of the northeastern USA. These herbs ants, aphids, and aposematic caterpillars as defensive occupy the forest understory where sun flecks are com- coloration, which is actually a variation of aposematic mon. Givnish (1990) noted that Smith’s (1986) rejected coloration to reduce herbivory (Lev-Yadun and Inbar, hypothesis regarding the aposematic value of leaf var- 2002; Lev-Yadun and Gould, 2008; Lev-Yadun, 2006a, iegation should also be considered further, but did not 2009). elaborate on this issue. Recently, Soltau et al. (2009) White variegation is known in many plant species. It showed experimentally, by painting white variegation has been proposed that variegation has several functions on non-variegated leaves, that white variegated leaves that can compensate for the reduced photosynthetic of Caladium steudneriifolium (Araceae, from Ecuador) ability of some of the white tissues (Cahn and Harper, are less attacked by herbivorous insects than non-varie- 1976; Wiens, 1978; Shifriss, 1981; Niemelä et al., 1984; gated ones, leading them to propose that the variegation Smith, 1986; Givnish, 1990; Allen and Knill, 1991; Lev- is probably the mimicry of mining damage to deter Yadun, 2003a, 2006a,b, 2009; Lee, 2007; Campitelli et ovipositing moths. al., 2008; Soltau et al., 2009). However, in many species The leaves of the very spiny annual species of open- white variegation is the result of air spaces formed by habitats Silybum marianum, a member of the Astera- lack of adhesion between the epidermis and the photo- ceae, resemble “green zebras” with their alternating synthetic parenchyma (Hara, 1957; Scarchuk and Lent, white and dark bands. The widths of typical variegation

Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016 1965; Tsukaya et al., 2004), and so in such cases there bands correlate highly with the length of the longest is no loss of photosynthetic capacity (Konoplyova et al., spines at leaf margins and the number of spines along 2008). Cahn and Harper (1976) showed in a field experi- leaf circumference. The variegation has thus been ment with rumen-fistulated sheep (which enabled sam- proposed to be a special case of aposematic coloration pling of what was grazed) that non-variegated leaves of (Lev-Yadun, 2003a). Rothschild and Moore (1987) Trifolium repens were clearly preferred to variegated proposed that S. marianum uses olfactory aposematism ones. Wiens (1978) proposed that leaf variegation might via pyrazine. It is likely that both types of aposematism be aposematic and that it should be examined for apose- operate simultaneously in the Silybum case, possibly matic effects and for possible mimicry by non-protected towards different herbivores. The Silybum stripes were associated plants. Smith (1986) hypothesized that leaf proposed by Lev-Yadun (2003a) to have additional de- variegation may theoretically be aposematic, but con- fensive functions: (1) mimicking the damage of tunnel- cluded that for the vine species Byttneria aculeata that ing insects, making it look as if it were already infested he studied, the variegation was related to another type to prevent insects from attacking; (2) reducing insect of defense from herbivory, mimicking leaf mining dam- landing on the leaves in general, as was proposed for age. Although Smith (1986) rejected the aposematic the evolution of zebra stripes as defense against tsetse hypothesis, he gave a clear and detailed formulation of flies (Waage, 1981; Brady and Shereni, 1988; Doku and

Israel Journal of Plant Sciences 57 2009 109

Brady, 1989; Gibson, 1992; Ruxton, 2002); or (3) serv- several centimeters in length). All three species display ing as defensive dazzle coloration of the type used by annual rosettes that have a white network of stripes many navies in World Wars I and II as defense from eye- (several to dozens of centimeters long, and several mil- targeted torpedoes, bombs, and artillery shells as they limeters wide) on the upper surface of their spiny leaves, were aimed before the age of electronics (Lev-Yadun, which gives them a zebra-like appearance (Lev-Yadun, 2003a, 2006a, 2009). 2003a). White spots (ca. 3–20 mm in size) are found Here, I show that twenty-one spiny, thorny, and prick- in the rosette and cauline leaves of the spiny annual ly wild plant species belonging to several plant families Carduus argentatus L. (Fig. 1c), which has moderately (of which twenty typically grow in open habitats in long (2–10 mm) spines. Launaea spinosa (Forssk.) O. Israel and one occupies both open and shady habitats) Kuntze, a small thorny desert shrub, has leaves with are variegated with white stripes or spots associated white-tipped lobes. Two perennial herbs of the same with their sharp defensive structures. This variegation genus, L. nudicaulis (L.) Hook. and L. capitata (Spreng.) represents a general phenomenon of conspicuousness. I Dandy (= L. glomerata (Cass.) Hooker fil.), also have propose that these are not cases of camouflage, but rath- leaves with small spines along their white margins (Fein- er constitute an advertisement system that serves as an brun-Dothan, 1978). Helminthotheca echioides (L.) aposematic coloration for communication from plants Holub, a thorny annual, has short spines (2–5 mm long) to herbivores about being defended. I propose that these and white spots (ca. 1–4 mm in size) on the rosette and plants thus form a Müllerian mimicry defensive guild in cauline leaves. Eight annual species of the Boraginaceae which well-defended plants mimic one another. Several are characterized by white spots (1–3 mm in size) found other non-spiny plant species belonging to the genus around the base of the short and somewhat soft spines Launaea (which includes several thorny or spiny and (ca. 1–4 mm long) that characterize leaves of Nonea white-variegated species) seem to mimic the aposematic obtusifolia (Willd.) DC. (Fig. 1d), N. ventricosa (Sm.) ones, thus forming a Batesian mimicry defensive ring. Griseb., Echium judaeum Lacaita, E. rauwolfii Delile, Anchusa aegyptiaca (L.) DC., A. strigosa Banks et So- lander, A. undulata L., and Cerinthe palaestina Eig et MATERIALS AND METHODS Samuelsson. Two annuals of the Brassicaceae also have As part of a broader effort to understand aposematic white spots on their bristle-covered leaves: Raphanus coloration in spiny plants (Lev-Yadun, 2001, 2003a,b, aucheri Boiss. has conspicuous white spots on its spiny 2006a, 2009; Lev-Yadun and Ne’eman, 2004, 2006; rosette leaves (Fig. 1e), and some of the plants of Bras- Halpern et al., 2007a,b; Lev-Yadun and Gould, 2008; sica tournefortii Gouan also have white spots on their Lev-Yadun and Halpern, 2008; Ronel et al., 2009), somewhat spiny leaves, but they are much less conspicu- a field survey of wild plant species with white- varie ous than those of R. aucheri. Two tree species of the Cu- gation growing in Israel was conducted in the years pressaceae have white stripes along their spiny leaves: 1994–2007. In addition, descriptions of many species both Juniperus drupacea Labill. and J. oxycedrus L. that were not found in the field were checked in Flora have needle-like adult leaves 1.2–2.0 cm long with white Palaestina (Zohary, 1966, 1972; Feinbrun-Dothan, longitudinal stripes along the adaxial side of the spiny 1978, 1986), in Analytical Flora of Israel (Feinbrun- leaves. In the Liliaceae, many individuals of Smilax

Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016 Dothan and Danin, 1991), in a pictorial encyclopedia of aspera L., a poisonous climber, have white variegated nature in Israel (Livneh and Heller, 1982, 1983), and in leaves (Fig. 1f) (variegation several to 40 millimeters local pictorial floras (Plitmann et al., 1983; Shmida and in size), and very sharp prickles (several millimeters to Darom, 1985, 1986, 1992). 1 cm long) on their branches and spines on some of their To examine the possibility that the 21 variegated leaves. These prickles and spines are also colorful (yel- plant species form mimicry rings, their overlapping dis- low, brown, red, and black). tribution was tabulated (Table 1) from the maps given In addition to the 21 thorny species with white var- by Danin (2004). iegation or mottling, four non-spiny Launaea species (Asteraceae) have white variegation on their leaves. Launaea resedifolia (L.) O. Kuntze, a perennial herb, RESULTS has dentate leaves that are white-calloused at the tip. Eight spiny species of the Asteraceae were found to have Launaea tenuiloba (Boiss.) O. Kuntze, a perennial white variegation. The first three—Silybum marianum herb, has dentate leaves with white-tipped lobes. Lau- (L.) Gaertner (Fig. 1a), syriaca (L.) Cass. naea mucronata (Forssk.) Muschler, a perennial herb, (Fig. 1b), and Scolymus maculatus L.—are the spiniest has dentate leaves with white-callous tipped lobes. of the eight (spines ranging from several millimeters to Launaea angustifolia (Desf.) O. Kuntze is an annual

Lev-Yadun / Mimicry rings of aposematic plants 110

, – – – – – – – – – – – – – – – – – – – – – – – – + + + + + + La , (Ln) Smilax – – – – – – – – – – – – – – – – – – – + + + + + + + + + + + Lm aegyptiaca angustifolia

. spinosa , (Sa) – – – – – – – – – – – – – – – – – – – – – – + + + + + + + + Lt

L – – – – – – – – – – – – – – – – – – – – – – + + + + + + + + Lr Anchusa , (La) Launaea oxycedrus . – – – – – – – – – – – – – – + + + + + + + + + + + + + + + + Sa J , (Aa) , (Ls) – – – – – – – – – – – – – – – – – – – – – – – – – – – – – + Jo mucronata , (Jo) . L rauwolfii – – – – – – – – – – – – – – – – – – – – – – – – – – – – – + Jd . E argentatus

, (Lm) drupacea – – – – – – – – – – – – – – – + + + + + + + + + + + + + + +

Bt , (Er) – – – – – – – – – – – – – – – – – – – + + + + + + + + + + + Carduus Ra tenuiloba . Juniperus judaeum L – – – – – – – – – – – – – – – – – + + + + + + + + + + + + +

Cp , (Ca) , (Jd) – – – – – – – – – – – – , (Lt) + + + + + + + + + + + + + + + + + + Au Echium – – – + + + + + + + + + + + + + + + + + + + + + + + + + + + maculatus As

, (Ej) resedifolia tournefortii

– – –

+ + + + + + + + + + + + + + + + + + + + + + + + + + + Aa Scolymus – – – – – – – – – – – – – – – – – – – – – – – + + + + + + + Er ventricosa . Launaea Brassica N – – + + + + + + + + + + + + + + + + + + + + + + + + + + + + Ej , (Scm) , (Bt) , (Nv) – – – – – – – – – – – – – – – – – – – – – + + + + + + + + + Nv Table 1 Table syriaca

aucheri – – – – – – – – – – – – – – – + + + + + + + + + + + + + + +

No obtusifolia

– – – – – – – – – – – – – – + + + + + + + + + + + + + + + + He Notobasis Raphanus Nonea – – – – – – – – – – – – – – – – – – – – – – – – + + + + + + Lc , (Ns) – – – – – – – – – – – – – – – – – + + + + + + + + + + + + + , (Ra) , (No) Ln – – – – – – – – – – – – – – – – – – – – – – – – – – + + + + Ls marianum

echioides

palaestina

– – – + + + + + + + + + + + + + + + + + + + + + + + + + + + Ca Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016 Silybum – – – – + + + + + + + + + + + + + + + + + + + + + + + + + + Scm Cerinthe – – + + + + + + + + + + + + + + + + + + + + + + + + + + + + Ns species that have white variegation on their leaves: (Lr) Helminthotheca , (Cp) – – – – + + + + + + + + + + + + + + + + + + + + + + + + + + Sm , (He) Launaea undulata . A capitata

L. , (Au) , (Lc) strigosa . . The four non-spiny A nudicaulis . Coastal Galilee Acco Plain Carmel Coast Sharon Plain Philistean Plain Upper Galilee Lower Galilee Mt. Carmel Esdraelon Plain Samaria Shefela Judean Mountain Northern Negev Negev Western Negev Highlands Southern Negev Hula Plain Valley Kinrot Valley Beit Shean Mt. Gilboa Samarian Desert Judean Desert Valley Lower Jordan Valley Dead Sea Valley Arava Golan & Mt. Hermon Gilead Ammon Moav Edom Overlapping and non-overlapping distribution of white variegated spiny plant 2004). species The 21 in spiny variegated Israel species: (Sm) according to the 30 territories of L Israel and Jordan (compiled from Danin, (As) aspera

Israel Journal of Plant Sciences 57 2009 111 Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016

Fig. 1. (a) A zebra-like rosette leaf of the very thorny annual Silybum marianum (Asteraceae). (b) A zebra-like rosette leaf of the very thorny annual Notobasis syriaca (Asteraceae). (c) White spots on a rosette leaf of the very thorny annual Carduus ar- gentatus (Asteraceae). (d) White spots associated with short and somewhat soft thorns on a leaf of the annual Nonea obtusifolia (Boraginaceae). (e) White spots associated with short and somewhat soft thorns on a rosette leaf of the annual Raphanus aucheri (Brassicaceae). (f) Variegated leaves of the poisonous and thorny climber Smilax aspera (Liliaceae).

Lev-Yadun / Mimicry rings of aposematic plants 112

that has incised-dentate leaves ending in a hard white be considered a mimicry ring (sensu Mallet and Gilbert, mucro. 1995). The only partial exception is Smilax aspera, The geographical distribution of the 21 variegated which grows in both well-illuminated habitats and in and spiny plant species (Table 1) showed that in most the shady understory. Smilax aspera might enjoy the regions of Israel and Jordan at least 10 such species benefits of camouflage under the shade of trees (e.g., are found together or in close proximity. The smallest Givnish, 1990) and the benefits of aposematic color- number of such species growing in a single zone (south- ation in the well-illuminated habitats. The defensive ern Negev) was six, and the highest number (Samaria) role (although the mechanism of operation remains was 15 (Table 1). Similarly, the non-spiny variegated unexplained) of white variegation has been shown in Launaea species grew among several white variegated the experiment with sheep grazing (Cahn and Harper, spiny species (Table 1). 1976), which clearly indicated that Trifolium repens in- dividuals with white variegation on leaves are not eaten as much as the plain green ones. Similarly, the variegat- DISCUSSION ed morph of Byttneria aculeata suffered less herbivory In spite of the numerous studies dealing with the than the non-variegated one when they were found at evolution of aposematic coloration in animals (e.g., the same frequency (Smith, 1986), as did the variegated Cott, 1940; Ruxton et al., 2004; and see references in morph of Caladium steudneriifolium (Araceae) from Komárek, 1998), the generality of the phenomenon in Ecuador (Soltau et al., 2009) and that of Hydrophyllum spiny plants and its possible ecological significance has virginianum (Campitelli et al., 2008). While a defensive only recently begun to receive the attention it deserves role of white variegation in leaves seems likely, addi- (Lev-Yadun, 2001, 2003a,b, 2006a, 2009; Midgley et tional physiological roles of such coloration cannot be al., 2001; Midgley, 2004; Lev-Yadun and Ne’eman, ruled out (e.g., Lev-Yadun 2006a). 2004, 2006; Rubino and McCarthy, 2004; Ruxton et It is probable that in addition to the 20 wild thorny, al., 2004; Speed and Ruxton, 2005; Halpern et al., spiny, and prickly plant species growing in Israel that 2007a,b; Lev-Yadun and Gould, 2008; Lev-Yadun and are conspicuous because of their white stripes and spots Halpern, 2008; Ronel et al., 2009). In cacti, Agave, described above, there are other similarly variegated Aloe sp., and thorny members of the Euphorbiaceae, spiny species in the flora of Israel expressing the same white variegation or marking associated with thorns or phenomenon. However, a major obstacle to studying spines seems to represent a widespread phenomenon defensive plant coloration in general and aposematic (Lev-Yadun, 2001). Similarly, white thorns are com- coloration in particular is the fragmentary and inconsis- mon in African acacias (Midgley et al., 2001; Midgley, tent descriptions of plant coloration, especially of veg- 2004). The white marking is conspicuous, especially etative organs. Taxonomists usually refer only to where the marks are large and patterned like zebras, colors, and even this character is not always described i.e., in three common Mediterranean spiny annual ro- in full. Thorn, spine, and prickle color, leaf colors, and settes of the Asteraceae (Silybum marianum, Notobasis color changes in all plant organs have usually not been syriaca, and Scolymus maculatus) (Lev-Yadun, 2003a). systematically described. Harper (1977) commented in This conclusion seems at first glance to oppose that of his seminal book on plant demography about the pos-

Downloaded by [Universitaire De Lausanne] at 02:12 03 May 2016 Givnish (1990), i.e., that white variegation serves as sibility of the operation of defensive plant coloration: camouflage, but since Givnish studied understory spe- “botanists were reluctant to accept things that are com- cies growing in a habitat characterized by sun flecks, monplace for zoologists”. Lev-Yadun and Gould (2008) and here species of open areas are discussed, there is emphasized that in spite of all current difficulties to ac- no contradiction. Thus, white mottling can act as cam- cept, understand, and prove defensive plant coloration, ouflage in undergrowth in the forest and as a conspicu- there is no reason to continue with the long tradition ous aposematic coloration in open, well-illuminated of plant scientists of neglecting the study of defensive areas. A white signal has an advantage over a colorful plant coloration, including aposematism. one, because color-blind animals can see it (Givnish, In order to form mimicry rings, the relevant species 1990) and it is still visible even under low light condi- must have an overlapping distribution. The compiled tions (Midgley et al., 2001; Lev-Yadun, 2003a, 2006a, data of the geographical distribution of the 21 variegat- 2009). ed and spiny plant species (Table 1) clearly show such I propose that the 20 wild thorny, spiny, and prickly overlap. Moreover, the same is true for the geographical plant species growing in open habitats in Israel that are distribution of the non-spiny variegated Launaea spe- conspicuous because of their white stripes and spots cies with the variegated spiny species (Table 1). There- form a Müllerian mimicry defended guild, or else may fore, there is no distribution limitation on the possibility

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that these two plant species groups form Müllerian and more common in the Near East than non-spiny white- Batesian mimicry rings, respectively. variegated plants, e.g., the very common Silybum mari- I therefore propose that there are also Batesian mim- anum, Notobasis syriaca, and Scolymus maculatus. ics of the white variegation. Many species of the genus In conclusion, the proposal presented here that white Launaea are very thorny or spiny (Bremer, 1994), and leaf variegation may be aposematic (along with other some of these well-defended species are shown here to functions) and that Batesian mimics for this character have white markings. However, four non-spiny annual or should also exist (see Wiens, 1978) seems to be sup- perennial Launaea species growing in Israel (L. resedi- ported by the data presented here. It seems that both folia, L. tenuiloba, L. mucronata, L. angustifolia) also Müllerian mimicry defense guilds and Batesian mim- have leaves with white-tipped lobes (Feinbrun-Dothan, icry defense guilds exist in white variegated wild plants 1978). I propose that these four species form a non-de- in Israel. This group of thorny, spiny, and prickly white fended Batesian mimicry ring that enjoys the protection variegated species and their mimics is an additional of their co-generic thorny or spiny species and probably demonstration of the phenomenon of aposematic col- also of other thorny or spiny variegated taxa. oration in plants. The long history of the considerable An important issue is the possibility of testing the impact of grazing in this arid region seems to have hypothesis. Intuitively it seems simple, but in reality it is selected for these characters. It has recently been shown very complicated and there are contradicting theoretical that increasing the number of Müllerian mimics helps considerations. (1) If white variegation has an apose- to reduce the cost of learning by herbivores even if matic role, then it should deter herbivores with previous the various species differ in their strength of defense foraging experience, but not naïve ones. The problem (Rowland et al., 2007; Sherratt, 2007), and the common is that since aposematism is a very old and common existence of well-defended white variegated plants in phenomenon, there are no genetically naïve animals. the Near East seems to support their conclusions. The Moreover, at least in Silybum marianum, which was possibility that a parallel phenomenon of chemically proposed to use visual aposematic markings by white defended plants with white variegated leaves exists in stripes (Lev-Yadun, 2003a), Rothschild and Moore our flora has not escaped my attention and this subject (1987) proposed that it uses olfactory aposematism via is under investigation. pyrazine. It is likely that both types of aposematism operate simultaneously, not only in the Silybum case, ACKNOWLEDGMENT but also in other species. The possibility that thorny, spiny, and prickly plants simultaneously use visual and I thank three anonymous reviewers for their illuminat- olfactory aposematism was never studied systematically ing comments. (see Lev-Yadun, 2009) and this complicates the analy- sis of whatever results one gets. Moreover, as already REFERENCES pointed out (Lev-Yadun, 2003a, 2006a, 2009), white variegation may have several simultaneous defensive Allen, J.A., Knill, R. 1991. Do grazers leave mottled leaves in and physiological functions that may further complicate the shade? Trends Ecol. Evol. 6: 109–110. Archetti, M. 2000. The origin of autumn colours by coevolu- the analysis of experimental results. (2) If white varie- tion. J. Theor. Biol. 205: 625–630.

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