The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators

Oelschlaegel B, Nuss M, von Tschirnhaus M, Paetzold C, Neinhuis C, Doetterl S, Wanke S (2015)
New Phytologist 206(1): 342-351.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Oelschlaegel, Birgit; Nuss, Matthias; von Tschirnhaus, MichaelUniBi; Paetzold, Claudia; Neinhuis, Christoph; Doetterl, Stefan; Wanke, Stefan
Abstract / Bemerkung
Pollination of several angiosperms is based on deceit. In such systems, the flowers advertise a reward that ultimately is not provided. We report on a previously unknown pollination/mimicry system discovered in deceptive Aristolochia rotunda (Aristolochiaceae). Pollinators were collected in the natural habitat and identified. Flower scent and the volatiles of insects (models) potentially mimicked were analyzed by chemical analytical techniques. Electrophysiological and behavioral tests on the pollinators identified the components that mediate the plant-pollinator interaction and revealed the model of the mimicry system. The main pollinators of A.rotunda were female Chloropidae. They are food thieves that feed on secretions of true bugs (Miridae) while these are eaten by arthropod predators. Freshly killed mirids and Aristolochia flowers released the same scent components that chloropids use to find their food sources. Aristolochia exploits these components to deceive their chloropid pollinators.Aristolochia and other trap flowers were believed to lure saprophilous flies and mimic brood sites of pollinators. We demonstrate for A.rotunda, and hypothesize for other deceptive angiosperms, the evolution of a different, kleptomyiophilous pollination strategy. It involves scent mimicry and the exploitation of kleptoparasitic flies as pollinators. Our findings suggest a reconsideration of plants assumed to show sapromyiophilous pollination.
Croatia; chemical mimicry; Aristolochia; kleptoparasites; deception; pollination system; Chloropidae
New Phytologist
Page URI


Oelschlaegel B, Nuss M, von Tschirnhaus M, et al. The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytologist. 2015;206(1):342-351.
Oelschlaegel, B., Nuss, M., von Tschirnhaus, M., Paetzold, C., Neinhuis, C., Doetterl, S., & Wanke, S. (2015). The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytologist, 206(1), 342-351. doi:10.1111/nph.13210
Oelschlaegel, B., Nuss, M., von Tschirnhaus, M., Paetzold, C., Neinhuis, C., Doetterl, S., and Wanke, S. (2015). The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytologist 206, 342-351.
Oelschlaegel, B., et al., 2015. The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytologist, 206(1), p 342-351.
B. Oelschlaegel, et al., “The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators”, New Phytologist, vol. 206, 2015, pp. 342-351.
Oelschlaegel, B., Nuss, M., von Tschirnhaus, M., Paetzold, C., Neinhuis, C., Doetterl, S., Wanke, S.: The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators. New Phytologist. 206, 342-351 (2015).
Oelschlaegel, Birgit, Nuss, Matthias, von Tschirnhaus, Michael, Paetzold, Claudia, Neinhuis, Christoph, Doetterl, Stefan, and Wanke, Stefan. “The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators”. New Phytologist 206.1 (2015): 342-351.

13 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Flower scent of Ceropegia stenantha: electrophysiological activity and synthesis of novel components.
Heiduk A, Haenni JP, Meve U, Schulz S, Dötterl S., J Comp Physiol A Neuroethol Sens Neural Behav Physiol 205(3), 2019
PMID: 30868226
Deep into the Aristolochia Flower: Expression of C, D, and E-Class Genes in Aristolochia fimbriata (Aristolochiaceae).
Suárez-Baron H, Pérez-Mesa P, Ambrose BA, González F, Pabón-Mora N., J Exp Zool B Mol Dev Evol 328(1-2), 2017
PMID: 27507740
Novel Consequences of Bird Pollination for Plant Mating.
Krauss SL, Phillips RD, Karron JD, Johnson SD, Roberts DG, Hopper SD., Trends Plant Sci 22(5), 2017
PMID: 28412035
The Spider Orchid Caladenia crebra Produces Sulfurous Pheromone Mimics to Attract its Male Wasp Pollinator.
Bohman B, Phillips RD, Flematti GR, Barrow RA, Peakall R., Angew Chem Int Ed Engl 56(29), 2017
PMID: 28470835
Evolutionary relationships among pollinators and repeated pollinator sharing in sexually deceptive orchids.
Phillips RD, Brown GR, Dixon KW, Hayes C, Linde CC, Peakall R., J Evol Biol 30(9), 2017
PMID: 28714217
More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids.
Nunes CEP, Wolowski M, Pansarin ER, Gerlach G, Aximoff I, Vereecken NJ, Salvador MJ, Sazima M., Naturwissenschaften 104(11-12), 2017
PMID: 29028068
Introduction to a Virtual Special Issue on plant volatiles.
Kessler A., New Phytol 209(4), 2016
PMID: 26840247
Spatio-temporal patterns in pollination of deceptive Aristolochia rotunda L. (Aristolochiaceae).
Oelschlägel B, von Tschirnhaus M, Nuss M, Nikolić T, Wanke S, Dötterl S, Neinhuis C., Plant Biol (Stuttg) 18(6), 2016
PMID: 27566447
Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination.
Heiduk A, Brake I, von Tschirnhaus M, Göhl M, Jürgens A, Johnson SD, Meve U, Dötterl S., Curr Biol 26(20), 2016
PMID: 27720617

71 References

Daten bereitgestellt von Europe PubMed Central.

Adams RP., 2007
Chemical ecology of the Heteroptera
Aldrich JR., 1988
Chemical attraction of male crab spiders (Araneae, Thomisidae) and kleptoparasitic flies (Diptera, Milichiidae and Chloropidae)
Aldrich JR, Barros TM., 1995
Scuttle flies (Diptera: Phoridae) imprisoned by Aristolochia baenzigeri (Aristolochiaceae) in Thailand
Bänziger H, Disney R., 2006
Aristolochia grandiflora Sw. (Aristolochiaceae): Desarrollo y morfología de la flor más larga del mundo
Bello MA, Valois-Cuesta H, González F., 2006

Beshovski VL., 1985
Pollinator specificity and convergence in fly-pollinated Pleurothallis (Orchidaceae) species: a multiple population approach
Borba E, Semir J., 2001
Orchids mimic green-leaf volatiles to attract prey-hunting wasps for pollination.
Brodmann J, Twele R, Francke W, Holzler G, Zhang QH, Ayasse M., Curr. Biol. 18(10), 2008
PMID: 18472423
Orchid mimics honey bee alarm pheromone in order to attract hornets for pollination.
Brodmann J, Twele R, Francke W, Yi-bo L, Xi-qiang S, Ayasse M., Curr. Biol. 19(16), 2009
PMID: 19664924
Pollination biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico
Burgess K, Singfield J, Melendez V, Kevan P., 2004
The British genera and species of Oscinellinae (Diptera, Chloropidae)
Collin JE., 1946
Beiträge zur biologischen Anatomie der Aristolochia-Blüthe
Correns C., 1891
Mimicry and deception in pollination
Dafni A., 1984
Zur Bestäubungsökologie von Aristolochia clematitis L
Daumann E., 1971
Revision der palaearktischen Arten der Gattung Aphanotrigonum Duda, 1932, und Aphanotrigonella Nartshuk, 1964 (Diptera: Chloropidae)
Dely-Draskovits Á., 1981

Derzhansky VV, Péricart J., 2005
1,4-Dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee.
Dotterl S, Fussel U, Jurgens A, Aas G., J. Chem. Ecol. 31(12), 2005
PMID: 16258713
Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides?
Dötterl S, Jürgens A., 2005
Qualitative and quantitative analyses of flower scent in Silene latifolia.
Dotterl S, Wolfe LM, Jurgens A., Phytochemistry 66(2), 2005
PMID: 15652577
Chemical attraction of kleptoparasitic flies to heteropteran insects caught by orb-weaving spiders
Eisner T, Eisner M, Deyrup M., 1991

Faegri K, van L., 1979
Perianth development and systematics of Aristolochia
González F, Stevenson D., 2000
Scent chemistry and pollinator attraction in the deceptive trap flowers of Ceropegia dolichophylla
Heiduk A, Brake I, Tolasch T, Frank J, Jürgens A, Meve U, Dötterl S., 2010
Pollination biology and genetic variability of a giant perfumed flower (Aristolochia gigantea Mart. and Zucc., Aristolochiaceae) visited mainly by small Diptera
Hipólito J, Viana BF, Selbach-Schnadelbach A, Galetto L, Kevan PG., 2012
Early steps of angiosperm–pollinator coevolution
Hu S, Dilcher D, Jarzen D, Winship D., 2008
Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism
Iyengar EV., 2008
Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus
Johnson SD, Jürgens A., 2010
Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms.
Jurgens A, Wee SL, Shuttleworth A, Johnson SD., Ecol. Lett. 16(9), 2013
PMID: 23841830

Kaiser R., 1993
Flowers and fungi use scents to mimic each other.
Kaiser R., Science 311(5762), 2006
PMID: 16469916

Kaiser R., 2006

Kaiser R., 2011
The role of animal pollination in plant speciation: integrating ecology, geography, and genetics
Kay KM, Sargent RD., 2009
Esters from the metathoracic scent gland of two capsid bugs, Pilophorus perplexus Douglas and Scott and Blepharidopterus angulatus (Fallen) (Heteroptera: Miridae)
Knight D, Rossiter M, Staddon B., 1984
Diversity and distribution of floral scent
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B., 2006

McDonald JH., 2009

Moulet P., 1995
99. Sem. Chloropidae – Zlakovye mukhi
Narchuk EP, Smirnov ES, Fedoseeva LI., 1970
30. Order Diptera. 99. Family Chloropidae
Narchuk EP, Smirnov ES, Fedoseeva LI., 1989
The genus Aristolochia L. (Aristolochiaceae) in Italy
Nardi E., 1984
The genus Aristolochia L. (Aristolochiaceae) in Greece
Nardi E., 1991

Nartshuk EP, Andersson H., 2013
Fly pollination in Ceropegia (Apocynaceae: Asclepiadoideae): biogeographic and phylogenetic perspectives.
Ollerton J, Masinde S, Meve U, Picker M, Whittington A., Ann. Bot. 103(9), 2009
PMID: 19339298
How many flowering plants are pollinated by animals?
Ollerton J, Winfree R, Tarrant S., 2011

Oosterbroek P., 2006

Péricart J., 1998

Péricart J., 1998

Péricart J., 1998
Floral organ and stage-specific odors of Aristolochia gigantea: the potential for scent-driven division of labor in trap-pollination
Raguso R., 2006
Rewardless flowers in the Angiosperms and the role of insect cognition in their evolution
Renner SS., 2006
Associations between flies and spiders: bibiocommensalism and dipsoparasitism?
Robinson MH, Robinson B., 1977
Pollination of Aristolochia pallida Willd. (Aristolochiaceae) in the Mediterranean
Rulik B, Wanke S, Nuss M, Neinhuis C., 2008
Orchid pollination by sexual swindle
Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W., 1999
The chemistry of sexual deception in an orchid-wasp pollination system.
Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Francke W., Science 302(5644), 2003
PMID: 14564006
Kleptoparasitism and phoresy in the Diptera
Sivinski J, Marshall S, Petersson E., 1999
Chemical defense in the plant bug Lopidea robiniae (Uhler).
Staples JK, Krall BS, Bartelt RJ, Whitman DW., J. Chem. Ecol. 28(3), 2002
PMID: 11944836
Pollination: Rotting smell of dead-horse arum florets.
Stensmyr MC, Urru I, Collu I, Celander M, Hansson BS, Angioy AM., Nature 420(6916), 2002
PMID: 12478279
A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast.
Stokl J, Strutz A, Dafni A, Svatos A, Doubsky J, Knaden M, Sachse S, Hansson BS, Stensmyr MC., Curr. Biol. 20(20), 2010
PMID: 20933425
Floral biology of Aristolochia argentina (Aristolochiaceae)
Trujillo C, Sérsic A., 2006
Pollination by brood-site deception.
Urru I, Stensmyr MC, Hansson BS., Phytochemistry 72(13), 2011
PMID: 21419464
Pilzmückenblumen als Pilzmimeten. Erster Teil
Vogel S., 1978

Wagner W., 1970
A review of capsid bugs of the genus Notostira Fieb. (Heteroptera, Miridae) of the Caucasus
Zaitzeva IF., 1977
Attraction of scavenging chloropid and milichiid flies (Diptera) to metathoracic scent gland compounds of plant bugs (Heteroptera: Miridae)
Zhang Q, Aldrich J., 2004


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 25488155
PubMed | Europe PMC

Suchen in

Google Scholar