Abstract
Müllerian mimicry is common in aposematic animals but till recently, like other aspects of plant aposematism was almost unknown. Many thorny, spiny and prickly plants are considered aposematic because their sharp defensive structures are colorful and conspicuous. Many of these spiny plant species (e.g., cacti and Agave in North American deserts; Aloe, Euphorbia and acacias with white thorns in Africa; spiny plants in Ohio; and spiny members of the Asteraceae in the Mediterranean basin) have overlapping territories, and also similar patterns of conspicuous coloration, and suffer from the evolutionary pressure of grazing by the same large herbivores. I propose that many of these species form Müllerian mimicry rings.
Key words: aposematic coloration, defense, evolution, herbivory, müllerian mimicry, spines, thorns
Aposematic (warning) coloration is a biological phenomenon in which poisonous, dangerous or otherwise unpalatable organisms visually advertise these qualities to other animals. The evolution of aposematic coloration is based on the ability of target enemies to associate the visual signal with the risk, damage or non-profitable handling, and later to avoid such organisms as prey. Typical colors of aposematic animals are yellow, orange, red, purple, black, white or brown and combinations of these.1–5 Many thorny, spiny and prickly plant species were proposed to be aposematic because their sharp defensive structures are usually colorful (yellow, orange, red, brown, black, white) and/or associated with similar conspicuous coloration.5–22 Animal spines also have similar conspicuous coloration and were proposed to be aposematic.1,5,17,23
Several authors have proposed that mimicry of various types helps in plant defense, e.g.,9,24–34 More specifically, Müllerian mimicry was already proposed to exist in several defensive plant signaling systems. The first was for several spiny species with white-variegated leaves.8,10 The second was for some tree species with red or yellow poisonous autumn leaves.35 The third cases are of a mixture of Müllerian and Batesian mimicry, of thorn auto-mimicry found in many Agave species.8
Here I propose that many species of visually aposematic spiny plants of the following taxa: (1) Cactaceae, (2) the genus Agave, (3) the genus Aloe, (4) African thorny members of the genus Euphorbia, (5) African acacias with white thorns, (6) spiny vascular plants of southeastern Ohio, (7) spiny Near Eastern plants with white variegation on their leaves, (8) Near Eastern members of the Asteraceae with yellow spines, form Müllerian mimicry rings of spiny plants.
To consider the existence of Müllerian mimicry rings in aposematic organisms, two factors are needed: (1) a similar signal, and (2) an overlapping distribution in respect to the territory of predators in animals, or herbivores in plants. I will show below that for the plant taxa proposed here to form Müllerian mimicry rings, both criteria operate.
The accumulating data about the common association of plant defenses by spines with visual conspicuousness, along with the fact that many such species overlap in their habitat, raises the possibility of the broad phenomenon of existence of Müllerian mimicry rings in plants. Even from the limited number of publications proposing visual aposematism in spiny plants, the operation of vegetal Müllerian mimicry rings seems to be obvious. The phenomenon can now be traced to both the Old World (Asia, Africa and Europe) and the New World (North America). The best-studied cases include Cactaceae and the genera Agave, Aloe and Euphorbia,6 African acacias with white thorns,12,15 Near Eastern spiny plants with white variegation on their leaves,7,11 aposematic spiny vascular plants of southeastern Ohio,16 and many spiny Mediterranean species of the Asteraceae with yellow spines.22
In the four spiny taxa (Cactaceae and the genera Agave, Aloe and Euphorbia) that were the first to be proposed as visually aposematic6 there is a very strong morphological similarity. In cacti, there are two types of conspicuousness of spines that are typical of many plant species: (1) colorful spines, and (2) white spots, or white or colorful stripes, associated with spines on the stems. These two types of aposematic coloration also dominate the spine system of Agave, Aloe and Euphorbia. The fact that many species of three of these four spiny taxa (Agave, Aloe and Euphorbia) are also poisonous36–38 further indicates their potential to form Müllerian mimicry rings.
I propose that each of these groups for itself and some of these groups (e.g., Cactaceae and the genus Agave in North America; Aloe, Euphorbia and acacias in east and south Africa) that have overlapping distribution and share at least some of the herbivores, form Müllerian mimicry rings.
The first Müllerian mimicry ring is of cacti and Agave that have an overlapping distribution over large areas in North America.37,39 The large herbivores in North America disappeared not so long ago in evolutionary time scales and seem to have shaped the spiny defense of these plant taxa.40
The second Müllerian mimicry ring is of the spiny and thorny members of the African genera Aloe, Euphorbia and certain acacias with very conspicuous white thorns, which partly overlap in distribution and share various large mammalian herbivores.12,15,36,41
The third Müllerian mimicry ring is the outcome of the common presence of aposematic coloration in spiny vascular plants of southeastern Ohio,16 with color patterns in thorns and spines similar to those of Cactaceae and the genera Agave, Aloe and Euphorbia described in Lev-Yadun.6
The next case of potential operation of Müllerian mimicry ring of spiny plants with overlapping territories that suffer from the same large herbivores, but on a much smaller geographical scale, has recently been proposed for several spiny species with white-variegated leaves,7 and later for more than 20 spiny species in the flora of Israel that have white markings associated with their spines.11
The last case of a probable Müllerian mimicry ring was described by Ronel et al.22 who while studying the spine system of Near Eastern spiny members of the Asteraceae, found 29 spiny species with yellow spines, and additional such species are expected to occur. Since some of these species and others with yellow spines also grow in southern Europe, it is clear that the same phenomenon is also common there.
I conclude that Müllerian mimicry rings seem to be very common in plants, and that it is probable that many other spiny plants that form Müllerian mimicry rings are waiting to be studied. Such defensive rings are probably also formed by poisonous plants that share similar colors or odors.
Footnotes
Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/8848
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