Defensive Ant, Aphid and Caterpillar Mimicry in Plants?

Home , Alcea, Ant mimicry, Pieris brassicae

Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2002 77

Original Article

DEFENSIVE INSECT MIMICRY IN PLANTSS. LEV-YADUN and M. INBAR

Biological Journal of the Linnean Society, 2002, 77, 393–398. With 10 figures

Defensive ant, aphid and caterpillar mimicry in plants?

SIMCHA LEV-YADUN* and MOSHE INBAR

Department of Biology, Faculty of Science and Science Education, University of Haifa–Oranim, Tivon 36006, Israel

Received 22 January 2002; accepted for publication 21 August 2002

Here we describe three apparently novel types of visual insect mimicry in plants. In the first type, plants of Xanth- ium trumarium L. have dark spots and flecks that resemble ants (Formicidae) in size and shape in the epidermis of stems, branches and petioles, and plants of Arisarum vulgare Targ.-Tozz. have them on petioles and inflorescence stems. In the second type, the dark anthers of Paspalum paspaloides (Michaux) Scribner (= P. distichum) are the size, shape and colour of aphids (Homoptera; Aphidoidea) and they sway in the wind like swivelling aphids. Similarly, the stems of Alcea setosa (Boiss.) Alef. are covered with dark flecks that look like aphids. Finally, immature pods of three wild annual legumes (Lathyrus ochrus (L.) DC.; Pisum fulvum Sm.; Vicia peregrina L.) have conspicuous reddish spots, arranged along the pods, that appears to mimic lepidopteran caterpillars. In one of the species (V. peregrina) two different mimicking morphs were found. We propose that these morphological traits may serve as herbivore repellent cues and are part of the defence system of the plants. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 393–398.

ADDITIONAL KEYWORDS: Aposematic – herbivory – insect – repellent.

INTRODUCTION florets of Gorteria diffusa (Asteraceae) resemble aggregation of resting bee flies (Johnson & Midgley, 1997). It is widely accepted that some invertebrate and Only rarely has animal mimicry been proposed in vertebrate animals visually masquerade as parts of plants as a means of avoiding herbivore damage. Egg plants and thus gain protection from predators (Cott, mimicry in plants has been proposed to reduce egg 1940; Wickler, 1968; Edmunds, 1974). Classic exam- laying in Heliconius butterflies (Benson, Brown & ples listed in Cott (1940) include: several species of Gilbert, 1975; Gilbert, 1980; Shapiro, 1981a; Williams fish and crabs that resemble algae; geckos and moths & Gilbert, 1981). In addition, an example of possible that look like lichens; many insects, amphibians and indirect animal mimicry in plants is the supposed reptiles that masquerade as leaves; tree bark mim- resemblance of caterpillars feeding damage on the leaf icked by spiders, moths, beetles, amphibians, lizards lobes of some Moraceae (Niemelä & Tuomi, 1987). and birds; stick-insects (Phasmida) that resemble If visually searching herbivores avoid previously colo- branches; and flower masquerade by thomisid spiders nized host plants, or if such leaves attract predators and bugs. and parasitoids that prey on herbivores of these Much less attention has been paid to mimicry of ani- plants, than such mimicry would be beneficial to the mals by plants. The best-known case are orchids of the plant. genus Ophrys that mimic female bees and are thus Plants employ many physical, chemical, temporal pollinated by male bees that are attracted to them and mutualistic defence mechanisms against her- (Wiens, 1978; Dafni, 1984). The dark spots on the bivory (Crawley, 1983; Howe & Westley, 1988). The umbels of wild carrot (and several other species of Api- role of mimicry in general and of animal mimicry in aceae) consist of dark central flowers that may mimic particular in anti-herbivory has received very little insects and thus attract potential insect pollinators attention. Related issues of plant–animal communica- (Eisikowitch, 1980). Similarly, black spots on the ray tion via vegetative parts, such as aposematic coloration, which are commonplace for zoologists, are only now being recognized as important for plant biology *Corresponding author. E-mail: [email protected] (Lev-Yadun, 2001; Lev-Yadun et al., 2002).

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Here we describe three novel types of a plant part DISCUSSION visually resembling an animal, which we interpret as Both authors were easily confused when trying to mimicry of an insect by the plant: dark spots and evaluate whether dark flecks and spots were ants or flecks that mimic ants, dark anthers that mimic aphids from distances larger than 1 m. The resem- aphids, and immature legume pods ornamented with blance of the dark spots and flecks to ants and the colourful spots that mimic caterpillars. dark anthers to aphids was found to be close enough to cause both authors confusion on first view of spotted OBSERVATIONS plants as if they were covered with ants or aphids. Similarly, aphid-covered stems were considered on ANT MIMICRY first view to be spotted. Likewise, the legume pods The stems, branches and some of the petioles of Xanth- described appeared to be caterpillars. We propose that ium trumarium (Asteraceae) are characterized by these colour patterns comprise three novel types of scattered conspicuous dark-coloured dots and flecks defensive insect mimicry in plants. What could be the usually 2–10 mm in size (Fig. 1). Dots predominate in benefit of these types of mimicry? We suggest that some individual plants, flacks in others. Similarly, the they may signal unpalatability to more than one group petioles and inflorescence stems of Arisarum vulgare of animals in two ways: first, insect mimicry may Targ.-Tozz. (Araceae) are covered by many dark flecks. reduce attacks by insect herbivores that refrain from Thus, to the human eye the shoots of these two species colonizing or feeding on infested plants (because of appear to be covered by a swarm of ants. Ant swarms competition and/or induced plant defences); and sec- are typically made of many moving dark flecks, each ond, where the insect mimicked is aposematic, this varying in size from several mm to over 1 cm. The could deter larger herbivores from eating the plants swaying of leaves, stems or branches in the wind in (Figs 1,5,6–9). combination with the dark spots and flecks, some of which are arranged in lines, may give the illusion that the ‘ants’ move. REDUCING COLONIZATION OF INSECTS Among other chemical and visual (shape, size and APHID MIMICRY colour) cues, insects can visually detect and assess The anthers of Paspalum paspaloides (Poaceae), a previous infestation during the process of host plant wind pollinated plant, are about 2–3 mm long, dark- selection (Vinson, 1976; Rothschild & Schoonhoven, coloured, and dangle from the green inflorescences, 1977; Rausher, 1979; Shapiro, 1981b; Bernays & gently moving with the wind (Fig. 2). The anthers Chapman, 1994). It has been proposed that egg mim- thus appear to be covered by dark aphid colonies icry by plants may reduce egg laying by butterflies (Homoptera: Aphidoidea, e.g. Aphis, Toxoptera and (Benson et al., 1975; Gilbert, 1980; Shapiro, 1981a; Macrosiphum). Similarly, the stems of Alcea setosa Williams & Gilbert, 1981). The same effect should (Boiss.) Alef. (Malvaceae) are covered with dark flecks apply to butterflies if they refrain from laying eggs on that look like aphids (Fig. 3). Many species of aphids plants that already appear to be infested, such as tend to aggregate on young stems and leaves of their the legume pods that mimic caterpillars. Interestingly, host plants (Fig. 4) (Dixon, 1998), and two common Rothschild (1974) has suggested that the stipules polyphagous species Sipha maydis Passerini and of some Passiflora are modified to look like horned Rhopalosiphum maidis (Fitch), both 2–3 mm long, are caterpillars, thus reducing female oviposition. Several found on many species of the Poaceae. studies have shown that early infestation by aphids and other homopterans has a negative impact on host plant preferences and larval performance of other CATERPILLAR MIMICRY insect herbivores. Finch & Jones (1989) reported that The immature pods of three wild legume species: large colonies of the cabbage aphid Brevicoryne brassi- Pisum fulvum (Figs 5,6), Lathyrus ochrus (Fig. 7) and cae (L.) and the peach aphid Myzus presicae (Sulz.) Vicia peregrina (Fabaceae) (Figs 8,9) have conspicuous deter ovipositioning by the root fly Delia radicum (L.). spots of several shades of red. Vicia peregrina has This seems to be a common phenomenon in aphid– two distinct morphs. Red spots characterize the first herbivore associations (studies by A. F. J. Dixon (Fig. 8), resembling those of L. ochrus and P. fulvum. and colleagues, cited in Finch & Jones (1989)). Red circles with green centres, the pods characterize Inbar Doostdar & Mayer (1999) demonstrated that the second morph (Fig. 9). All these pods mimic the homopterans (whiteflies) not only alter adult cabbage general shape, size and colour of lepidopteran cater- looper (Trichoplusia ni (Hübner) Lepidoptera: Noc- pillars ornamented with spiracles or other spots on tuidae) host selection, but also actually reduce the their sides such as a pieride moth (Pieridae) (Fig. 10). feeding efficiency of their offspring. Aphids respond to

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Figures 1–4. Fig. 1. A stem of Xantium trumarium covered with conspicuous dark-coloured dots and flecks that look as if they were covered by an ant swarm. Fig. 2. The dark-coloured anthers of Paspalum paspaloides dangle from the green inflorescences and look as if dark aphids covered them. Fig. 3. A stem of Alcea setosa covered with dark flecks that look like aphids. Fig. 4. Dark aphids feeding on a young stem.

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Figures 5–10. Fig. 5. An immature pod of Pisum fulvum ornamented with conspicuous red spots along the pods that look like a caterpillar. Fig. 6. An almost mature pod of Pisum fulvum ornamented with red conspicuous spots that looks like a caterpillar. Fig. 7. Almost mature pods of Lathyrus ochrus ornamented with red conspicuous spots that look like a caterpillar. Fig. 8. An immature pod of Vicia peregrina of the ﬁrst morph ornamented with red conspicuous spots that looks like a caterpillar. Fig. 9. An immature pod of Vicia peregrina of the second morph ornamented with red conspicuous circles that look like a caterpillar. Fig. 10. A typical lepidopteran caterpillar of a pieride moth (Pieridae) ornamented with spots on its back.

their enemies’ predators, physical shelters and chemical defences (Bowers, 1993). Unpalatable caterpillars with stinging and irritating hairs, functional osmete- ria or body-fluid toxins often advertised their presence by aposematic coloration and aggregation (Cott, 1940; Bowers, 1993). The usual warning colours are red, yel- low, black and white with stripes along the body and/ or arranged in spots, especially around the abdominal spiracles. Aposematism in caterpillars should reduce predation for several reasons, including an innate tendency of vertebrates to avoid warning colours and faster avoidance learning of bright as opposed to cryptic colours (Coppinger, 1970; Gibson, 1980; Lindström, Rowe & Guilford, 2001). Therefore we suggest that by mimicking aposematic caterpillars with red ‘spiracle spots’ wild legumes may reduce immature pod predation. It has been shown that ungulates may actively select leaves in the field by shape and colour and avoid spotted ones (e.g. Cahn & Harper, 1976) but we have failed to find data on the response of vertebrate herbivores to aposematic (or cryptic) caterpillars. However, personal information from colleagues indi- cates that in some systems caterpillars may deter herbivore feeding (A. Perevolotsky and R. Harmsen pers. comm.). The potential benefit from ant-attendance mimicry is obvious. Ants bite and sting and are aggressive and most insectivorous animals and herbivores will avoid them. Thus, ants have become models for a variety of arthropods that have evolved to mimic them (Edmunds, 1974). Plants may benefit if ants protect them from insect and mammalian herbivory (Madden crowding by enhanced dispersal (Dixon, 1998) and it & Young, 1992; Julivet, 1998). In a field experiment, is thus also probable that they may avoid previously removal of ants and aphids resulted in an increase infested or infestation-mimicked hosts. of 57% in species richness, and their abundance increased by 80% (Wimp & Whitham, 2001). Moreover, ant and aphid removal also resulted in a 76% increase DETERRENCE OF FEEDING BY LARGE HERBIVORES in the abundance of other herbivores on narrow-leaf Caterpillars employ a large array of defences that cottonwoods (Wimp & Whitham, 2001). Many plant reduce predation, such as camouflage, mimicry of species invest considerable resources in attracting

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