Skip to main content

Deceptive Behavior in Plants. I. Pollination by Sexual Deception in Orchids: A Host–Parasite Perspective

  • Chapter
  • First Online:
Plant-Environment Interactions

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Sexually deceptive orchids attract male insects as pollinators by mimicking the reproductive signals emitted by the targeted females. Since this mimicry system involves the imitation of female mating signals of certain insects, and since mating signals, especially sex pheromones, generally act on a species-specific basis, theory holds that each sexually deceptive orchid is usually pollinated by only one or a few male insect species. While these orchids rely exclusively on their specialized pollinators for their own reproduction, the male insects derive no benefit from this interaction. In this chapter, I will argue that incorporating questions relevant to the field of animal-centered host–parasite interactions into investigations on the evolutionary ecology of orchid pollination by deception will provide important insights at both the proximate (or mechanistic) and at the ultimate (or evolutionary) levels.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ackerman JD (1986) Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana 1:108–113

    Google Scholar 

  • Aigner PA (2006) The evolution of specialized floral phenotypes in a fine-grained pollination environment. In: NM Waser, J Ollerton (eds) Plant–pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago, pp 23–46

    Google Scholar 

  • Alcock J (2005) An enthusiasm for orchids: sex and deception in plant evolution. Oxford University Press, Oxford

    Google Scholar 

  • Alcock J, Barrows EN, Gordh G, Hubbard J, Kirkendall L, Pyle DW, Ponder TL, Zalom FG (1978) The ecology and evolution of male reproductive behaviour in the bees and wasps. Zool J Linn Soc 64:293–326

    Google Scholar 

  • Ayasse M (2006) Floral scent and pollinator attraction in sexually deceptive orchids. In: N Dudareva E Pichersky (eds) Biology of floral scent. CRC, Boca Raton, pp 219–241

    Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Erdmann D, Francke W (1997) Chemical communication in the reproductive biology of Ophrys sphegodes. Mitt D Ges Allg Ang Ent 11:473–476

    Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson BS, 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 

  • Ayasse M, Schiestl FP, Paulus HF, Ibarra F, Francke W (2003) Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proc R Soc Lond B 270:517–522

    CAS  Google Scholar 

  • Barnard CJ, 1990. Parasitic relationships. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor and Francis, London, pp 1–33

    Google Scholar 

  • Bateman RM, Hollingsworth PM, Preston J, Yi-Bo L, Pridgeon AM, Chase MW (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Bot J Linn Soc 142:1–40

    Google Scholar 

  • Blanco MA, Barboza G (2005) Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Ann Bot 95:763–772

    PubMed  Google Scholar 

  • Borg-Karlson A-K, Groth I, Agren L, Kullenberg B (1993) Form-specific fragrances from Ophrys insectifera (Orchidaceae) attract species of different pollinator genera. Evidence of sympatric speciation? Chemoecology 4:39–45

    CAS  Google Scholar 

  • Bower CC (1996) Demonstration of pollinator-mediated reproductive isolation in sexually deceptive species of Chiloglottis (Orchidaceae: Caladeniinae). Austr J Bot 44:15–33

    Google Scholar 

  • Bower CC (2006) Specific pollinators reveal a cryptic taxon in the bird orchid, Chiloglottis valida sensu lato (Orchidaceae) in south-eastern Australia. Austr J Bot 54:53–64

    Google Scholar 

  • Brooks DR, McLennan DA (1991) Phylogeny, ecology, and behavior: a research program in comparative biology. University of Chicago Press, Chicago

    Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 70:315–316

    Google Scholar 

  • Ciotek L, Giorgis P, Benitez-Vieyra S, Cocucci AA (2006) First confirmed case of pseudocopulation in terrestrial orchids of South America: pollination of Geoblasta pennicillata (Orchidaceae) by Campsomeris bistrimacula (Hymenoptera, Scoliidae). Flora 201:365–369

    Google Scholar 

  • Coleman E (1928) Pollination of Cryptostylis leptochila. Vict Nat 44:333–340

    Google Scholar 

  • Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Correvon H, Pouyanne M (1916) Un curieux cas de mimétisme chez les Ophrydées. J Soc Nat Hortic France 4:29–47

    Google Scholar 

  • Correvon H, Pouyanne M (1923) Nouvelles observations sur le mimétisme et la fécondation chez les Ophrys speculum et lutea. J Soc Nat Hortic France 4:372–377

    Google Scholar 

  • Cortis P, Vereecken NJ, Schiestl FP, Barone Lumaga MR, Scrugli A, Cozzolino S (2008) Floral odour convergence and the nature of species boundaries in sympatric Sardinian Ophrys (Orchidaceae). Annals of Botany doi:10.1093/aob/mcn219

    Google Scholar 

  • Cozzolino S, Schiestl FP, Müller A, De Castro O, Nardella AM, Widmer A (2005) Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of pre-mating barriers? Proc R Soc Lond B 272:1271–1278

    Google Scholar 

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

    Google Scholar 

  • Dafni A (1987) Pollination in Orchis and related genera: evolution from reward to deception. In: Arditti J (ed) Orchid biology: reviews and perspectives IV. Cornell University Press, Ithaca, pp 80–104

    Google Scholar 

  • Dafni A, Ivri Y (1981) Floral mimicry between Orchis israelitica Baumann and Dafni (Orchidaceae) and Bellevalia flexuosa BOISS (Liliaceae). Oecologia 49:229–232

    Google Scholar 

  • Damiens D, Boivin G (2006) Why do sperm-depleted parasitoid males continue to mate? Behav Ecol 17:138–143

    Google Scholar 

  • Danesch O, Danesch E (1972) Orchideen Europas, Ophrys-hybriden. Hallwag, Bern

    Google Scholar 

  • Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects. John Murray, London

    Google Scholar 

  • Delforge P (2005) Guide des orchidées d'Europe, d'Afrique du Nord et du Proche-Orient. Delachaux and Niestlé, Paris

    Google Scholar 

  • Dickson CR, Petit S (2006) Effect of individual height and labellum colour on the pollination of Caladenia (syn. Arachnorchis) behrii (Orchidaceae) in the northern Adelaide region, South Australia. Plant Syst Evol 262:65–74

    Google Scholar 

  • Dod DD (1976) Oncidium henekenii: bee orchid pollinated by bee. Am Orch Soc Bull 45:792–794

    Google Scholar 

  • Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1435

    PubMed  CAS  Google Scholar 

  • Ebert D (2000) Experimental evidence for rapid parasite adaptation and its consequences for the evolution of virulence. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host–parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 163–184

    Google Scholar 

  • Galizia CG, Kunze J, Gumbert A, Borg-Karlson A-K, Sachse S, Markl C, Menzel R (2005) Relationship of visual and olfactory signal parameters in a food-deceptive flower mimicry system. Behav Ecol 16:159–168

    Google Scholar 

  • Gaskett AC, Herberstein ME (2006) Flowering, pollination and fruit set in tongue orchids, Cryptostylis spp. Vict Nat 123:128–133

    Google Scholar 

  • Gaskett AC, Winnick CG, Herberstein ME (2008) Orchid sexual deceit provokes ejaculation. Am Nat 171(6):E206–E212

    PubMed  CAS  Google Scholar 

  • Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proc Natl Acad Sci USA 91:3–10

    PubMed  CAS  Google Scholar 

  • Hadley NF (1981) Cuticular lipids of terrestrial plants and arthropods: a comparison of their structure, composition and waterproofing function. Biol Rev 56:23–47

    CAS  Google Scholar 

  • Herrera CM, Castellanos MC, Medrano M (2006) Geographical context of floral evolution: towards an improved research programme in floral diversification. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, New York, pp 278–294

    Google Scholar 

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

    Google Scholar 

  • Johnson SD (1994) Evidence for Batesian mimicry in a butterfly pollinated orchid. Biol J Linn Soc 53:91–104

    Google Scholar 

  • Johnson SD (2000) Batesian mimicry in the nonrewarding orchid Disa pulchra, and its consequences for pollinator behaviour. Biol J Linn Soc 71:119–132

    Google Scholar 

  • Johnson SD, Shelah M (2006) Lying to Pinocchio: floral deception in an orchid pollinated by long-proboscid flies. Bot J Linn Soc 152:271–278

    Google Scholar 

  • Johnson SD, Peter CI, Agren J (2004) The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proc R Soc Lond B 271:803–809

    Google Scholar 

  • Jones DL (1988) Native orchids of Australia. American Orchid Society, Delray Beach

    Google Scholar 

  • Kasumovic MM, Bruce MJ, Andrade MCB, Herberstein ME (2008) Spatial and temporal demographic variation drives within-season fluctuations in sexual selection. Evolution 62(9):2316–2325

    PubMed  Google Scholar 

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

    Google Scholar 

  • Lehnebach CA, Robertson AW, Hedderley D (2005) Pollination studies of four New Zealand terrestrial orchids and the implication for their conservation. New Zeal J Bot 43:467–477

    Google Scholar 

  • Lorella B, Mahé G, Séité F (2002) Pollinisateurs d'Ophrys en Bretagne. L'Orchidophile 151:91–96

    Google Scholar 

  • Mant J, Schiestl FP, Peakall R, Weston PH (2002) A phylogenetic study of pollinator conservatism among sexually deceptive orchids. Evolution 56:888–898

    PubMed  CAS  Google Scholar 

  • Mant JG, Peakall R, Schiestl FP (2005a) Does selection on floral odour promote differentiation among populations and species of the sexually deceptive genus Ophrys? Evolution 59:1449–1463

    Google Scholar 

  • Mant J, Brown GR, Weston PH (2005b) Opportunistic pollinator shifts among sexually deceptive orchids indicated by a phylogeny of pollinating and non-pollinating thynnine wasps (Tiphiidae). Biol J Linn Soc 86:381–395

    Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Moccia MD, Widmer A, Cozzolino S (2007) The strength of reproductive isolation in two hybridizing food-deceptive orchid species. Mol Ecol 16:2855–2866

    PubMed  Google Scholar 

  • Neiland MRM, Wilcock CC (1995) Maximization of reproductive success by European Orchidaceae under conditions of infrequent pollination. Protoplasma 187:39–48

    Google Scholar 

  • Neiland MRM, Wilcock CC (1998) Fruit set, nectar reward, and rarity in the Orchidaceae. Am J Bot 85:1657–1671

    Google Scholar 

  • Nilsson LA (1983) Processes of isolation and introgressive interplay between Platanthera bifolia (L.) RICH and P. chlorantha. Bot J Linn Soc 87:325–350

    Google Scholar 

  • Nilsson LA (1992) Orchid pollination biology. Trends Ecol Evol 7:255–259

    Google Scholar 

  • Pasteur G (1982) A classificatory review of mimicry systems. Ann Rev Ecol Syst 13:169–199

    Google Scholar 

  • Paulus HF, Gack C (1990) Pollinators as prepollinating isolation factors: evolution and speciation in Ophrys (Orchidaceae). Isr J Bot 39:43–79

    Google Scholar 

  • Paxton RJ (2005) Male mating behaviour and mating systems of bees: an overview. Apidologie 36:145–156

    Google Scholar 

  • Peakall R (1990) Responses of male Zaspilothynnus trilobatus Turner wasps to females and the sexually deceptive orchid it pollinates. Funct Ecol 4:159–167

    Google Scholar 

  • Peakall R (2007) Speciation in the Orchidaceae: confronting the challenges. Mol Ecol 16:2834–2837

    PubMed  Google Scholar 

  • Peakall R, Handel SN (1993) Pollinators discriminate among floral heights of a sexually deceptive orchid: implications for selection. Evolution 47:1681–1687

    Google Scholar 

  • Peakall R, Beattie AJ (1996) Ecological and genetic consequences of pollination by sexual deception in the orchid Caladenia tentactulata. Evolution 50:2207–2220

    Google Scholar 

  • Peakall R, Beattie AJ, James SH (1987) Pseudocopulation of an orchid by male ants: a test of two hypotheses accounting for the rarity of ant pollination. Oecologia 73:522–524

    Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Pouyanne M (1917) La fécondation des Ophrys par les Insectes. Bull Soc Hist Nat Afr Nord 43:53–62

    Google Scholar 

  • Proctor M, Yeo P (1972) The pollination of flowers. Taplinger, New York

    Google Scholar 

  • Rotschild M, Clay T (1952) Fleas, flukes and cuckoos. Collins, London

    Google Scholar 

  • Schiestl FP (2004) Floral evolution and pollinator mate choice in a sexually deceptive orchid. J Evol Biol 17:67–75

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422

    CAS  Google Scholar 

  • Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Francke W (2003) The chemistry of sexual deception in an orchid–wasp pollination system. Science 302:437–438

    PubMed  CAS  Google Scholar 

  • Schiestl FP, Ayasse M (2002) Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Syst Evol 234:111–119

    CAS  Google Scholar 

  • Schiestl FP, Peakall R (2005) Two orchids attract different pollinators with the same floral odour compound: ecological and evolutionary implications. Funct Ecol 19:674–680

    Google Scholar 

  • Schiestl FP, Cozzolino S (2008) Evolution of sexual mimicry in the Orchidinae: the role of preadaptations in the attraction of male bees as pollinators. BMC Evolutionary Biology 8: 27

    Google Scholar 

  • Schiestl FP, Vereecken NJ (2008) Andrena combinata, ein neuer Bestäuber von Ophrys araneola. J Eur Orchid 40:501–507

    Google Scholar 

  • Scopece G, Musacchio A, Widmer A, Cozzolino S (2007) Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61:2623–2642

    PubMed  Google Scholar 

  • Singer RB (2002) The pollination mechanism in Trigonidium obtusum LINDL (Orchidaceae: Maxillariinae): sexual mimicry and trap-flowers. Ann Bot 89:157–163

    PubMed  Google Scholar 

  • Singer RB, Flach A, Koehler S, Marsaioli AJ, Amaral ME (2004) Sexual mimicry in Mormolyca ringens (LINDL.) SCHLTR. (Orchidaceae: Maxillariinae). Ann Bot 93:755–762

    PubMed  Google Scholar 

  • Spaethe J, Moser WH, Paulus HF (2007) Increase of pollinator attraction by means of a visual signal in the sexually deceptive orchid, Ophrys heldreichii (Orchidaceae). Plant Syst Evol 264:31–40

    Google Scholar 

  • Stebbins GL, Ferlan L (1956) Population variability, hybridization, and introgression in some species of Ophrys. Evolution 10:32–46

    Google Scholar 

  • Stökl J, 2007. Pollinator driven radiation in sexually deceptive orchids of the genus Ophrys. Dissertation, University of Ulm, Germany

    Google Scholar 

  • Stökl J, Paulus H, Dafni A, Schulz C, Francke W, Ayasse M (2005) Pollinator attracting odour signals in sexually deceptive orchids of the Ophrys fusca group. Plant Syst Evol 254:105–120

    Google Scholar 

  • Steiner KE, Whitehead VB, Johnson SD (1994) Floral and pollinator divergence in two sexually deceptive Cape orchids. Am J Bot 81:185–194

    Google Scholar 

  • Stoutamire WP (1975) Pseudocopulation in Australian terrestrial orchids. Am Orch Soc Bull 44:226–233

    Google Scholar 

  • Taylor I (1999) Monitoring report 1999 for Pterostylis gibbosa. National Parks and Wildlife Service, Hurstville

    Google Scholar 

  • Thornhill R, Alcock J (2000) The evolution of insect mating systems: enlightenment to romanticism. Harvard University Press, Cambridge

    Google Scholar 

  • Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN (2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol J Linn Soc 84:1–54

    Google Scholar 

  • Turner CMR, Aslam N, Dye C (1995) Replication, differentiation, growth and virulence of Trypanosoma brucei infections. Parasitology 111:289–300

    PubMed  Google Scholar 

  • Tyteca D, Rois AS, Vereecken NJ (2006) Observations on the pollination of Ophrys fuciflora by pseudocopulating males of Phyllopertha horticola. J Eur Orch 38:203–214

    Google Scholar 

  • Vandewoestijne S, Rois A-S, Caperta A, Baguette M, Tyteca D (2008) Effects of individual and population parameters on reproductive success in three sexually deceptive orchid species. Plant Biol (in press)

    Google Scholar 

  • Van der Cingel NA (1995) An atlas of orchid pollination: European orchids. Balkema, Rotterdam

    Google Scholar 

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

    Google Scholar 

  • Véla E, Tirard A, Renucci M, Suehs CM, Provost E (2007) Floral chemical signatures in the genus Ophrys L. (Orchidaceae): A preliminary test of a new tool for taxonomy and evolution. Plant Mol Biol Rep 25:83–97

    Google Scholar 

  • Vereecken NJ, Patiny S (2005) On the pollination of Ophrys catalaunica (O. Danesch and E. Danesch) by pseudocopulating males of Chalicodoma pyrenaica (Lepeletier) (Hymenoptera, Megachilidae). Natural Belges 86 (Orchid 18):57–64

    Google Scholar 

  • Vereecken NJ, Patiny S (2006) Patrolling males of Andrena bicolor F. (Hymenoptera, Andrenidae) as pollinators of Ophrys massiliensis Viglione and Véla. Natural Belges 87 (Orchid. 19):63–68

    Google Scholar 

  • Vereecken NJ, Schiestl FP (2008) The evolution of imperfect floral mimicry. Proc Natl Acad Sci USA 105:7484–7488

    PubMed  CAS  Google Scholar 

  • Vereecken NJ, Risch S, Cortis P (2007a) Contribution to the pollination biology of Ophrys scolopax Cavanilles (Orchidaceae) in southern France. Natural Belges 88(Orchid 20):17–26

    Google Scholar 

  • Vereecken NJ, Mant J, Schiestl FP (2007b) Population differentiation in female sex pheromone and male preferences in a solitary bee. Behav Ecol Sociobiol 61:811–821

    Google Scholar 

  • Waser NM, Price MV (1998) What plant ecologists can learn from zoology. Persp Plant Ecol Evol Syst 1/2:137–150

    Google Scholar 

  • Waterman RJ, Bidartondo MI (2008) Deception above, deception below: linking pollination and mycorhhizal biology of orchids. J Exp Bot 59:1085–1096

    PubMed  Google Scholar 

  • Westrich P (1990) Die Wildbienen Baden-Wurttembergs, Teil 1 and 2. Eugen Ulmer, Stuttgart

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Williams NH, Dodson CH (1972) Selective attraction of male euglossine bees to orchid floral fragrances and its importance in long-distance pollen flow. Evolution 26:84–95

    Google Scholar 

  • Wong BBM, Schiestl FP (2002) How an orchid harms its pollinator. Proc R Soc Lond B 269:1529–1532

    Google Scholar 

  • Wong BBM, Salzmann CC, Schiestl FP (2004) Pollinator attractiveness increases with distance from flowering orchids. Biol Lett 171:S212–S214

    Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgements

I am grateful to Florian P. Schiestl (University of Zürich, Switzerland) for his continuous support and encouragements during my research, as well as for his comments on this manuscript. I have received financial support from two Belgian institutions, namely the “Fonds pour la formation à la Recherche dans l'Industrie et l'Agriculture” (F.R.I.A.) and the “Royal Academy of Sciences, Humanities and Fine Arts” (Agathon de Potter Foundation).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicolas J. Vereecken .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Vereecken, N.J. (2009). Deceptive Behavior in Plants. I. Pollination by Sexual Deception in Orchids: A Host–Parasite Perspective. In: Balu¿ka, F. (eds) Plant-Environment Interactions. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89230-4_11

Download citation

Publish with us

Policies and ethics