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Müllerian and Batesian Mimicry Rings of White- Variegated Aposematic Spiny and Thorny Plants: a Hypothesis

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Müllerian and Batesian Mimicry Rings of White- Variegated Aposematic Spiny and Thorny Plants: a Hypothesis Israel Journal of Plant Sciences ISSN: 0792-9978 (Print) 2223-8980 (Online) Journal homepage: http://www.tandfonline.com/loi/tips20 Müllerian and Batesian mimicry rings of white- variegated aposematic spiny and thorny plants: A hypothesis Simcha Lev-Yadun To cite this article: Simcha Lev-Yadun (2009) Müllerian and Batesian mimicry 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. Submit your article to this journal Article views: 41 View related articles Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tips20 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 leaves. 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 (Asteraceae) 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 aposematism 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 leaf 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 Polymorphism 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 evolution 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 camouflage 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
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