Weapon (thorn) automimicry and mimicry of aposematic colorful thorns in plants

Abstract

In order to further characterize the function of coloration in plants as defense against herbivory, two types of thorn mimicry are described: (1) A unique type of weapon (thorn) automimicry (within the same individual) that was previously known only in animals, and (2) mimicry of aposematic colorful thorns, by colorful elongated and pointed plant organs (buds, leaves and fruit) that, despite their appearance, are not sharp. Some thorny plants including dozens of species of Agave, one species of Aloe and a palm species have thorn-like imprints or colorations on their leaves, constituting thorn automimicry by giving the impression of more extensive thorns. The mimicry of aposematic colorful thorns is a typical case of Batesian mimicry, but the thorn automimicry is a special intra-organismic Batesian mimicry. I propose that both types of mimicry serve as anti-herbivore mechanisms.

Introduction

Cases of automimicry, i.e. mimicry of some parts in other parts of the same individual, have rarely been described. Weapon automimicry of horns or canines has been shown in several mammalian species (Guthrie and Petocz, 1970) and has been proposed to be of intraspecific threatening value. However, this intriguing idea has not been examined in plants. The best-known case of mimicry in plants is mimicry of animals by orchids of the genus Ophrys that mimic female bees and are thus pollinated by male bees that are attracted to them (Wickler, 1968; Wiens, 1978; Dafni, 1984). Similarly, the dark spots on the umbels of wild carrot (and several other species of Apiaceae) with dark central flowers that mimic insects are thought to attract potential insect pollinators (e.g. Eisikowitch, 1980). The same syndrome has been shown in the appearance of black spots on the ray florets of Gorteria diffusa (Asteraceae) that mimic resting bee flies, which tend to aggregate (Johnson and Midgley, 1997).

Several authors have proposed mimicry in plants as an anti-herbivore mechanism. Wiens (1978) estimated that about 5% of the land plants are mimetic, listing several types of protective plant mimicry. Egg mimicry in plants was proposed as a way to reduce egg laying by Heliconius butterflies (Benson et al., 1975; Shapiro, 1981; Williams and Gilbert, 1981). Stone (1979) proposed that reddish/brown young leaves of palms growing in Malaya mimic the color of dead leaves, thus protecting them from herbivory. Mimicry of host leaf morphology is common in mistletoes to form crypsis and thus reduce herbivory (Ehleringer et al., 1986). Mimicry of feeding damage by caterpillars on the leaf lobes of some Moraceae has also been proposed (Niemelä and Tuomi, 1987). Brown and Lawton (1991) proposed that the two non-spiny species Celmisia lyalli and C. petriei (Asteraceae) growing in New Zealand look rather like spiny members of the genus Aciphylla (Apiaceae). Three apparently novel types of visual insect mimicry have recently been described in plants (Lev-Yadun and Inbar, 2002). In the first type, plants have dark spots and flecks in the epidermis of stems, branches and petioles that resemble ants in size and shape. In the second type, dark anthers are the size, shape and color of aphids, and they sway in the wind like swivelling aphids. Finally, immature pods of several annual legumes have conspicuous reddish spots, arranged along the pods, thus they appear to mimic lepidopteran caterpillars. It has been proposed that these morphological traits may serve as herbivore repellent cues and that they are part of the defence system of the plants (Lev-Yadun and Inbar, 2002). Weeds mimic crops in both morphology and physiology, thus they can manage in agricultural ecosystems (Barrett, 1983). Launchbaugh and Provenza (1993) discussed the question of odor and taste mimicry by plants and concluded that odor is not enough to establish a good mimicry and that a combination of both is needed. From all these studies, it is clear that mimicry serves in defense against herbivory and that animals are led to behave according to the plant's interests by plant mimicry.

Because thorns provide mechanical protection against herbivory (Janzen, 1986; Grubb, 1992), it has been proposed recently that herbivores learn to identify and avoid conspicuous, harmful thorny plants (Lev-Yadun, 2001). Thorns usually differ in color from leaves, being yellow, red, black, brown and white rather than green. In addition, white spots, or white and colorful stripes, are associated with thorns in leaves and stems. Both types of aposematic coloration predominate the spine system of taxa rich with spiny species—Cacti, the genera Agave, Aloe and Euphorbia. This phenomenon has already been found in about 1300 species originating in several continents of both the Old and New World (Lev-Yadun, 2001). Agave species can have two types of thorns in their leaves: spines at the distal end or teeth along the margins (Gentry, 1982), and in many species colored stripes along the margins enhance spine and teeth visibility (Lev-Yadun, 2001). A similar leaf type with side spine morphology is common in many palm and Aloe species.

Fieldwork in an ecosystem that has a millennia-long history of large-scale grazing, such as the land of Israel, clearly and “sharply” indicates the ecological benefit of being spiny. A continuous blanket of spiny shrubs and thistles covers large tracts of the land, and other parts are just rich with dozens of such plant species that dominate the vegetation. This dominance clearly indicates the adaptive value of being spiny when grazing pressure is high. It does not just slow the rate of feeding, but gives a considerable advantage to such plants. Spiny plants, such as Echinops sp. (Asteraceae), which usually grow as individuals or in small groups, sometimes become the most common perennial plant over many acres in grazing lands.

Aposematic coloration, a well-known phenomenon in animals, has recently been shown to be common in thorny plants (Lev-Yadun, 2001). In animals, where aposematic coloration is common in unpalatable or dangerous species, there are many cases of mimicry of ants, wasps, poisonous snakes, etc., for protection from predation (Cott, 1940; Wickler, 1968; Edmunds, 1974). Usually, warning colors are red, yellow, black and white.

Here I describe two types of thorn mimicry: (1) impressions or color printing of thorns on leaves of several dozens of species belonging to three families that mimic their real thorns, and (2) colorful elongated and pointed plant organs that, despite their appearance, are not sharp at all. I propose that they serve to reduce herbivory.