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

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• 作者：Simcha Lev-Yadun (1)
  Gidi Ne’eman (1)
  
• 关键词：Batesian mimicry ; Bees ; Defense ; Herbivory ; Ophrys ; Wasps
• 刊名：Arthropod-Plant Interactions
• 出版年：2012
• 出版时间：September 2012
• 年：2012
• 卷：6
• 期：3
• 页码：327-332
• 全文大小：180KB
• 参考文献：1. Ayasse M, Schiestl FP, Paulus HF, L?fstedt 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 54:1995-006
  2. Bain RS, Rashed A, Cowper VJ, Gilbert FS, Sherratt TN (2007) The key mimetic features of hoverflies through avian eyes. Proc R Soc B 274:1949-954 CrossRef
  3. Benson WW, Brown KS, Gilbert LE (1975) Coevolution of plants and herbivores: passion flower butterflies. Evolution 29:659-80 CrossRef
  4. 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 331-71
  5. Breed MD, Guzmán-Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271-98 CrossRef
  6. Brodmann J, Twele R, Francke W, H?lzler G, Zhang Q-H, Ayasse M (2008) Orchids mimic green-leaf volatiles to attract prey-hunting wasps for pollination. Curr Biol 18:740-44 CrossRef
  7. 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 19:1368-372 CrossRef
  8. Brown VK, Lawton JH, Grubb PJ (1991) Herbivory and the evolution of leaf size and shape. Phil Trans R Soc Lond B 333:265-72 CrossRef
  9. Chittka L, Osorio D (2007) Cognitive dimensions of predator responses to imperfect mimicry. PLoS Biol 5:e339 CrossRef
  10. Cott HB (1940) Adaptive coloration in animals. Methuen & Co Ltd, London
  11. Dafni A (1984) Mimicry and deception in pollination. Annu Rev Ecol Syst 15:259-78 CrossRef
  12. Dirzo R (2002) Lying leaves. Science 297:1119
  13. Dixon AFG (1998) Aphid ecology. An optimization approach. Chapman and Hall, London
  14. Dodson C (1962) The importance of pollination in the evolution of the orchids of tropical America. Am Orchid Soc Bull 31:525-34, 641-49, 731-35
  15. Dodson C, Frymire G (1961) Natural pollination of orchids. Missouri Bot Gard Bull 49:133-52
  16. Edmunds M (1974) Defence in animals. A survey of anti-predator defences. Longman Group Ltd, Harlow
  17. Eisner T, Eisner M (2000) Defensive use of a fecal thatch by a beetle larva ( / Hemisphaerota cyanea). Proc Natl Acad Sci USA 97:2632-636 CrossRef
  18. Eisner T, Eisner M, Siegler M (2005) Secret weapons. Defenses of insects, spiders, scorpions, and other many-legged creatures. Harvard University Press, Cambridge
  19. Feinbrun-Dothan N, Danin A (1991) Analytical flora of Eretz-Israel. Cana Publishing House Ltd., Jerusalem
  20. Finch S, Jones TH (1989) An analysis of the deterrent effect of Aphids on cabbage root fly ( / Delia radicum) egg-laying. Ecol Entomol 14:387-91 CrossRef
  21. Forbes P (2009) Dazzled and deceived: mimicry and camouflage. Yale University Press, New Haven
  22. Gaskett AC, Herberstein ME (2010) Colour mimicry and sexual deception by Tongue orchids ( / Cryptostylis). Naturwiss 97:97-02 CrossRef
  23. 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 210-40
  24. Gilbert LE (1982) The coevolution of a butterfly and a vine. Sci Am 247(8):102-07
  25. Hinton HE (1973) Natural deception. In: Gregory RL, Gombrich EH (eds) Illusion in nature and art. Duckworth, London, pp 97-59
  26. Howarth B, Edmunds M (2000) The phenology of Syrphidae (Diptera): are they Batesian mimics of Hymenoptera? Biol J Linn Soc 71:437-57 CrossRef
  27. Huxley CR, Cutler DF (1991) Ant-plant interactions. Oxford University Press, London
  28. Inbar M, Doostdar H, Mayer RT (1999) Effects of sessile Whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environ Entomol 28:353-57
  29. Janzen DH, Hallwachs W, Burns JM (2010) A tropical horde of counterfeit predator eyes. Proc Natl Acad Sci USA 107:11659-1665 CrossRef
  30. Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev 81:219-35 CrossRef
  31. Jolivet P (1998) Interrelationship between insects and plants. CRC Press, Boca Raton
  32. Kauppinen J, Mappes J (2003) Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: / Aeshna grandis). Anim Behav 66:505-11 CrossRef
  33. King LE, Douglas-Hamilton I, Vollrath F (2007) African elephants run from the sound of disturbed bees. Curr Biol 17:R832–R833 CrossRef
  34. King LE, Lawrence A, Douglas-Hamilton I, Vollrath F (2009) Beehive fence deters crop-raiding elephants. Afr J Ecol 47:131-37 CrossRef
  35. 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 49:431-39 CrossRef
  36. Kullenberg B (1950) Investigation on the pollination of / Ophrys species. Oikos 2:1-9 CrossRef
  37. Kullenberg B (1956) On the scents and colours of / Ophrys flowers and their specific pollinators among the aculeate Hymenoptera. Svensk Bot Tidskr 50:25-6
  38. Kullenberg B (1961) Studies in / Ophrys pollination. Zool Bidrag Uppsala 34:1-40
  39. Lee D (2007) Nature’s palette. The science of plant color. University Chicago Press, Chicago
  40. Lev-Yadun S (2003) Why do some thorny plants resemble green zebras? J Theor Biol 244:483-89 CrossRef
  41. 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 292-99
  42. 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 167-02
  43. Lev-Yadun S (2010) Ant mimicry by / Passiflora flowers? Isr J Entomol 39:159-63
  44. 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 21-8
  45. Lev-Yadun S, Inbar M (2002) Defensive ant, aphid and caterpillar mimicry in plants. Biol J Linn Soc 77:393-98 CrossRef
  46. Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, Izhaki I, Katzir G, Ne`eman G (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126-130 CrossRef
  47. 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 31:84-8 CrossRef
  48. Madden D, Young YP (1992) Symbiotic ants as an alternative defense against giraffe herbivory in spinescent / Acacia drepanolobium. Oecologia 91:235-38 CrossRef
  49. Niemel? P, Tuomi J (1987) Does the leaf morphology of some plants mimic caterpillar damage? Oikos 50:256-57 CrossRef
  50. Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483:461-66 CrossRef
  51. Perevolotsky A, Schwartz-Tzachor R, Yonathan R, Ne’eman G (2011) Geophytes-herbivore interactions: reproduction and population dynamics of / Anemone coronaria L. Plant Ecol 212:563-71 CrossRef
  52. Plowright RC, Owen RE (1980) The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution 34:622-37 CrossRef
  53. Rolfe RA (1910) The bee-orchis. Orch Rev 10:261
  54. Rothschild M (1972) Some observations on the relationship between plants, toxic insects and birds. In: Harborne JB (ed) Phytochemical ecology. Academic Press, London, pp 1-2
  55. Rothschild M (1974) Modified stipules of / Passiflora which resemble horned caterpillars. Proc R Entomol Soc Lond 39:16
  56. Rothschild M (1984) Aide mémoire mimicry. Ecol Entomol 9:311-19 CrossRef
  57. Rothschild M (1986) The red smell of danger. New Sci 111(September 4):34-6
  58. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals & mimicry. Oxford University Press, Oxford
  59. Schaefer HM, Ruxton GD (2009) Deception in plants: mimicry or perceptual exploitation? Trends Ecol Evol 24:676-85 CrossRef
  60. Schaefer HM, Ruxton GD (2011) Plant-animal communication. Oxford University Press, New York
  61. Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwiss 92:255-64 CrossRef
  62. 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 126:531-34 CrossRef
  63. Schiestl FP, Ayasse M, Paulus HF, L?fstedt 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 186:567-74 CrossRef
  64. Shapiro AM (1981a) Egg-mimics of / Streptanthus (Cruciferae) deter oviposition by / Pieris sisymbrii (Lepidoptera: Pieridae). Oecologia 48:142-43 CrossRef
  65. Shapiro AM (1981b) The pierid red-egg syndrome. Am Nat 117:276-94 CrossRef
  66. Smith AP (1986) Ecology of leaf color polymorphism in a tropical forest species: habitat segregation and herbivory. Oecologia 69:283-87 CrossRef
  67. Soltau U, D?tterl S, Liede-Schumann S (2009) Leaf variegation in / Caladium steudneriifolium (Araceae): a case of mimicry? Evol Ecol 23:503-12 CrossRef
  68. Spaethe J, Chittka L (2003) Interindividual variation of eye optics and single object resolution in bumblebees. J Exp Biol 206:3447-453
  69. Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to airborne vibration. Behav Ecol Sociobiol 4:101-10 CrossRef
  70. Tautz J, Rostás M (2008) Honeybee buzz attenuates plant damage by caterpillars. Curr Biol 18:R1125–R1126 CrossRef
  71. van der Pijl L, Dodson CH (1966) Orchid flowers. Their pollination and evolution. University of Miami Press, Coral Gables
  72. Vereecken NJ, Schiestl FP (2009) On the roles of colour and scent in a specialized floral mimicry system. Ann Bot 104:1077-084 CrossRef
  73. Vereecken NJ, Teng J, Kullenberg G, Bergstr?m G (2009) Bertil Kullenberg (1913-2007) and his / Ophrys orchids. J Eur Orch 41:3-8
  74. Vollrath F, Douglas-Hamilton I (2002) African bees to control African elephants. Naturwiss 89:508-11 CrossRef
  75. Warren J, James P (2008) Do flowers wave to attract pollinators? A case study with / Silene maritima. J Evol Biol 21:1024-029 CrossRef
  76. Weiss MR (2006) Defecation behavior and ecology of insects. Annu Rev Entomol 51:635-61 CrossRef
  77. Wickler W (1968) Mimicry in plants and animals. Weidenfeld and Nicolson, London
  78. Wiens D (1978) Mimicry in plants. Evol Biol 11:365-03
  79. Williams KS, Gilbert LE (1981) Insects as selective agents on plant vegetative morphology: egg mimicry reduces egg laying by butterflies. Science 212:467-69 CrossRef
  80. Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82:440-52
  81. Yamazaki K (2010) Leaf mines as visual defensive signals to herbivores. Oikos 119:796-01 CrossRef
  82. Yamazaki K (2011) Gone with the wind: trembling leaves may deter herbivory. Biol J Linn Soc 104:738-47 CrossRef
  
• 作者单位：Simcha Lev-Yadun (1)
  Gidi Ne’eman (1)
  
  1. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, 36006, Tivon, Israel
  

文摘

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.