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Does bee or wasp mimicry by orchid flowers also deter herbivores?

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Abstract

General visual bee mimicry and specific chemical mimicry by flowers to solitary female bees or wasps are well known in several orchid genera, for example, the Mediterranean genus Ophrys, the Australian genera Cryptostylis and Chiloglottis, and the South-African Disa. This mimicry has been shown to attract solitary male bees or wasps, which are their species-specific pollinators. The visual and chemical signals are considered to be a type of deceptive pollination mechanism based on mimicry for the exploitation of perceptual biases of animals. We propose that in addition to this unique pollination mechanism, these plants exhibit another, rarely mentioned and practically forgotten, non-exclusive function of bee or wasp mimicry (Batesian mimicry). This mimicry may deter large mammalian herbivores, and possibly also insects from the plants and especially from their flowers by a type of visual and olfactory deceptive aposematism. While visiting the flowers, bees and wasps may add a Müllerian effect to this defense. We extend this hypothesis to many other rewarding flowers that are bee or wasp pollinated and propose that abundance of pollinating bees or wasps may deter herbivorous mammals and insects from the plants during their peak flowering season.

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References

  • Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006

    PubMed  CAS  Google Scholar 

  • Bain RS, Rashed A, Cowper VJ, Gilbert FS, Sherratt TN (2007) The key mimetic features of hoverflies through avian eyes. Proc R Soc B 274:1949–1954

    Article  PubMed  Google Scholar 

  • Benson WW, Brown KS, Gilbert LE (1975) Coevolution of plants and herbivores: passion flower butterflies. Evolution 29:659–680

    Article  Google Scholar 

  • Bowers DM (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, New York, pp 331–371

    Google Scholar 

  • Breed MD, Guzmán-Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298

    Article  PubMed  CAS  Google Scholar 

  • Brodmann J, Twele R, Francke W, Hölzler G, Zhang Q-H, Ayasse M (2008) Orchids mimic green-leaf volatiles to attract prey-hunting wasps for pollination. Curr Biol 18:740–744

    Article  PubMed  CAS  Google Scholar 

  • Brodmann J, Twele R, Francke W, Yi-bo L, Xi-qiang S, Ayasse M (2009) Orchids mimics honey bee alarm pheromone in order to attract hornets for pollination. Curr Biol 19:1368–1372

    Article  PubMed  CAS  Google Scholar 

  • Brown VK, Lawton JH, Grubb PJ (1991) Herbivory and the evolution of leaf size and shape. Phil Trans R Soc Lond B 333:265–272

    Article  Google Scholar 

  • Chittka L, Osorio D (2007) Cognitive dimensions of predator responses to imperfect mimicry. PLoS Biol 5:e339

    Article  PubMed  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen & Co Ltd, London

    Google Scholar 

  • Dafni A (1984) Mimicry and deception in pollination. Annu Rev Ecol Syst 15:259–278

    Article  Google Scholar 

  • Dirzo R (2002) Lying leaves. Science 297:1119

    Google Scholar 

  • Dixon AFG (1998) Aphid ecology. An optimization approach. Chapman and Hall, London

    Google Scholar 

  • Dodson C (1962) The importance of pollination in the evolution of the orchids of tropical America. Am Orchid Soc Bull 31:525–534, 641–649, 731–735

    Google Scholar 

  • Dodson C, Frymire G (1961) Natural pollination of orchids. Missouri Bot Gard Bull 49:133–152

    Google Scholar 

  • Edmunds M (1974) Defence in animals. A survey of anti-predator defences. Longman Group Ltd, Harlow

    Google Scholar 

  • Eisner T, Eisner M (2000) Defensive use of a fecal thatch by a beetle larva (Hemisphaerota cyanea). Proc Natl Acad Sci USA 97:2632–2636

    Article  PubMed  CAS  Google Scholar 

  • Eisner T, Eisner M, Siegler M (2005) Secret weapons. Defenses of insects, spiders, scorpions, and other many-legged creatures. Harvard University Press, Cambridge

  • Feinbrun-Dothan N, Danin A (1991) Analytical flora of Eretz-Israel. Cana Publishing House Ltd., Jerusalem

    Google Scholar 

  • Finch S, Jones TH (1989) An analysis of the deterrent effect of Aphids on cabbage root fly (Delia radicum) egg-laying. Ecol Entomol 14:387–391

    Article  Google Scholar 

  • Forbes P (2009) Dazzled and deceived: mimicry and camouflage. Yale University Press, New Haven

    Google Scholar 

  • Gaskett AC, Herberstein ME (2010) Colour mimicry and sexual deception by Tongue orchids (Cryptostylis). Naturwiss 97:97–102

    Article  PubMed  CAS  Google Scholar 

  • Gilbert LE (1980) Ecological consequences of a coevolved mutualism between butterflies and plants. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 210–240

    Google Scholar 

  • Gilbert LE (1982) The coevolution of a butterfly and a vine. Sci Am 247(8):102–107

    Google Scholar 

  • Hinton HE (1973) Natural deception. In: Gregory RL, Gombrich EH (eds) Illusion in nature and art. Duckworth, London, pp 97–159

    Google Scholar 

  • Howarth B, Edmunds M (2000) The phenology of Syrphidae (Diptera): are they Batesian mimics of Hymenoptera? Biol J Linn Soc 71:437–457

    Article  Google Scholar 

  • Huxley CR, Cutler DF (1991) Ant-plant interactions. Oxford University Press, London

    Google Scholar 

  • Inbar M, Doostdar H, Mayer RT (1999) Effects of sessile Whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environ Entomol 28:353–357

    Google Scholar 

  • Janzen DH, Hallwachs W, Burns JM (2010) A tropical horde of counterfeit predator eyes. Proc Natl Acad Sci USA 107:11659–11665

    Article  PubMed  CAS  Google Scholar 

  • Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev 81:219–235

    Article  PubMed  Google Scholar 

  • Jolivet P (1998) Interrelationship between insects and plants. CRC Press, Boca Raton

    Google Scholar 

  • Kauppinen J, Mappes J (2003) Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: Aeshna grandis). Anim Behav 66:505–511

    Article  Google Scholar 

  • King LE, Douglas-Hamilton I, Vollrath F (2007) African elephants run from the sound of disturbed bees. Curr Biol 17:R832–R833

    Article  PubMed  CAS  Google Scholar 

  • King LE, Lawrence A, Douglas-Hamilton I, Vollrath F (2009) Beehive fence deters crop-raiding elephants. Afr J Ecol 47:131–137

    Article  Google Scholar 

  • King LE, Lawrence A, Douglas-Hamilton I, Vollrath F (2011) Beehive fences as effective deterrents for crop-raiding elephants: field trials in northern Kenya. Afr J Ecol 49:431–439

    Article  Google Scholar 

  • Kullenberg B (1950) Investigation on the pollination of Ophrys species. Oikos 2:1–19

    Article  Google Scholar 

  • Kullenberg B (1956) On the scents and colours of Ophrys flowers and their specific pollinators among the aculeate Hymenoptera. Svensk Bot Tidskr 50:25–46

    Google Scholar 

  • Kullenberg B (1961) Studies in Ophrys pollination. Zool Bidrag Uppsala 34:1–340

    Google Scholar 

  • Lee D (2007) Nature’s palette. The science of plant color. University Chicago Press, Chicago

    Google Scholar 

  • Lev-Yadun S (2003) Why do some thorny plants resemble green zebras? J Theor Biol 244:483–489

    Article  Google Scholar 

  • Lev-Yadun S (2006) Defensive coloration in plants: a review of current ideas about anti-herbivore coloration strategies. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, vol IV. Global Science Books, London, pp 292–299

  • Lev-Yadun S (2009) Aposematic (warning) coloration in plants. In: Baluska F (ed) Plant-environment interactions. From sensory plant biology to active behavior, vol II. Springer, Berlin, pp 167–202

    Google Scholar 

  • Lev-Yadun S (2010) Ant mimicry by Passiflora flowers? Isr J Entomol 39:159–163

    Google Scholar 

  • Lev-Yadun S, Gould KS (2009) Role of anthocyanins in plant defense. In: Gould KS, Davies KM, Winefield C (eds) Life’s colorful solutions: the biosynthesis, functions, and applications of anthocyanins. Springer, Berlin, pp 21–48

    Google Scholar 

  • Lev-Yadun S, Inbar M (2002) Defensive ant, aphid and caterpillar mimicry in plants. Biol J Linn Soc 77:393–398

    Article  Google Scholar 

  • Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, Izhaki I, Katzir G, Ne`eman G (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130

    Article  PubMed  Google Scholar 

  • Lev-Yadun S, Ne’eman G, Shanas U (2009) A sheep in wolf’s clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores? BioEssays 31:84–88

    Article  PubMed  Google Scholar 

  • Madden D, Young YP (1992) Symbiotic ants as an alternative defense against giraffe herbivory in spinescent Acacia drepanolobium. Oecologia 91:235–238

    Article  Google Scholar 

  • Niemelä P, Tuomi J (1987) Does the leaf morphology of some plants mimic caterpillar damage? Oikos 50:256–257

    Article  Google Scholar 

  • Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483:461–466

    Article  PubMed  CAS  Google Scholar 

  • Perevolotsky A, Schwartz-Tzachor R, Yonathan R, Ne’eman G (2011) Geophytes-herbivore interactions: reproduction and population dynamics of Anemone coronaria L. Plant Ecol 212:563–571

    Article  Google Scholar 

  • Plowright RC, Owen RE (1980) The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution 34:622–637

    Article  Google Scholar 

  • Rolfe RA (1910) The bee-orchis. Orch Rev 10:261

    Google Scholar 

  • Rothschild M (1972) Some observations on the relationship between plants, toxic insects and birds. In: Harborne JB (ed) Phytochemical ecology. Academic Press, London, pp 1–12

    Google Scholar 

  • Rothschild M (1974) Modified stipules of Passiflora which resemble horned caterpillars. Proc R Entomol Soc Lond 39:16

    Google Scholar 

  • Rothschild M (1984) Aide mémoire mimicry. Ecol Entomol 9:311–319

    Article  Google Scholar 

  • Rothschild M (1986) The red smell of danger. New Sci 111(September 4):34–36

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals & mimicry. Oxford University Press, Oxford

  • Schaefer HM, Ruxton GD (2009) Deception in plants: mimicry or perceptual exploitation? Trends Ecol Evol 24:676–685

    Article  PubMed  Google Scholar 

  • Schaefer HM, Ruxton GD (2011) Plant-animal communication. Oxford University Press, New York

    Google Scholar 

  • Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwiss 92:255–264

    Article  PubMed  CAS  Google Scholar 

  • Schiestl FP, Ayasse M (2001) Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126:531–534

    Article  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (2000) Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deception. J Comp Physiol A 186:567–574

    Article  PubMed  CAS  Google Scholar 

  • Shapiro AM (1981a) Egg-mimics of Streptanthus (Cruciferae) deter oviposition by Pieris sisymbrii (Lepidoptera: Pieridae). Oecologia 48:142–143

    Article  Google Scholar 

  • Shapiro AM (1981b) The pierid red-egg syndrome. Am Nat 117:276–294

    Article  Google Scholar 

  • Smith AP (1986) Ecology of leaf color polymorphism in a tropical forest species: habitat segregation and herbivory. Oecologia 69:283–287

    Article  Google Scholar 

  • Soltau U, Dötterl S, Liede-Schumann S (2009) Leaf variegation in Caladium steudneriifolium (Araceae): a case of mimicry? Evol Ecol 23:503–512

    Article  Google Scholar 

  • Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J Exp Biol 206:3447–3453

    Google Scholar 

  • Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to airborne vibration. Behav Ecol Sociobiol 4:101–110

    Article  Google Scholar 

  • Tautz J, Rostás M (2008) Honeybee buzz attenuates plant damage by caterpillars. Curr Biol 18:R1125–R1126

    Article  PubMed  CAS  Google Scholar 

  • van der Pijl L, Dodson CH (1966) Orchid flowers. Their pollination and evolution. University of Miami Press, Coral Gables

    Google Scholar 

  • Vereecken NJ, Schiestl FP (2009) On the roles of colour and scent in a specialized floral mimicry system. Ann Bot 104:1077–1084

    Article  PubMed  Google Scholar 

  • Vereecken NJ, Teng J, Kullenberg G, Bergström G (2009) Bertil Kullenberg (1913-2007) and his Ophrys orchids. J Eur Orch 41:3–18

    Google Scholar 

  • Vollrath F, Douglas-Hamilton I (2002) African bees to control African elephants. Naturwiss 89:508–511

    Article  PubMed  CAS  Google Scholar 

  • Warren J, James P (2008) Do flowers wave to attract pollinators? A case study with Silene maritima. J Evol Biol 21:1024–1029

    Article  PubMed  CAS  Google Scholar 

  • Weiss MR (2006) Defecation behavior and ecology of insects. Annu Rev Entomol 51:635–661

    Article  PubMed  CAS  Google Scholar 

  • Wickler W (1968) Mimicry in plants and animals. Weidenfeld and Nicolson, London

    Google Scholar 

  • Wiens D (1978) Mimicry in plants. Evol Biol 11:365–403

    Google Scholar 

  • Williams KS, Gilbert LE (1981) Insects as selective agents on plant vegetative morphology: egg mimicry reduces egg laying by butterflies. Science 212:467–469

    Article  PubMed  CAS  Google Scholar 

  • Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82:440–452

    Google Scholar 

  • Yamazaki K (2010) Leaf mines as visual defensive signals to herbivores. Oikos 119:796–801

    Article  Google Scholar 

  • Yamazaki K (2011) Gone with the wind: trembling leaves may deter herbivory. Biol J Linn Soc 104:738–747

    Article  Google Scholar 

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Acknowledgments

We thank Moshe Inbar, Amots Dafni and two anonymous reviewers for valuable and stimulating comments on the manuscript.

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Authors and Affiliations

  1. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, 36006, Tivon, Israel

    Simcha Lev-Yadun & Gidi Ne’eman

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  1. Simcha Lev-Yadun
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  2. Gidi Ne’eman
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Correspondence to Simcha Lev-Yadun.

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Handling Editor: Lars Chittka.

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Lev-Yadun, S., Ne’eman, G. Does bee or wasp mimicry by orchid flowers also deter herbivores?. Arthropod-Plant Interactions 6, 327–332 (2012). https://doi.org/10.1007/s11829-012-9199-y

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