Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination

Heiduk A, Brake I, von Tschirnhaus M, Goehl M, Juergens A, Johnson SD, Meve U, Doetterl S (2016)
CURRENT BIOLOGY 26(20): 2787-2793.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Heiduk, Annemarie; Brake, Irina; von Tschirnhaus, MichaelUniBi; Goehl, Matthias; Juergens, Andreas; Johnson, Steven D.; Meve, Ulrich; Doetterl, Stefan
Abstract / Bemerkung
Four to six percent of plants, distributed over different angiosperm families, entice pollinators by deception [1]. In these systems, chemical mimicry is often used as an efficient way to exploit the olfactory preferences of animals for the purpose of attracting them as pollinators [2,3]. Here, we report a very specific type of chemical mimicry of a food source. Ceropegia sandersonii (Apocynaceae), a deceptive South African plant with pitfall flowers, mimics attacked honeybees. We identified kleptoparasitic Desmometopa flies (Milichiidae) as the main pollinators of C. sandersonii. These flies are well known to feed on honeybees that are eaten by spiders, which we thus predicted as the model chemically mimicked by the plant. Indeed, we found that the floral scent of C. sandersonii is comparable to volatiles released from honeybees when under simulated attack. Moreover, many of these shared compounds elicited physiological responses in antennae of pollinating Desmometopa flies. A mixture of four compounds geraniol, 2-heptanone, 2-nonanol, and (E)-2-octen-1-yl acetate was highly attractive to the flies. We conclude that C. sandersonii is specialized on kleptoparasitic fly pollinators by deploying volatiles linked to the flies' food source, i.e., attacked and/or freshly killed honeybees. The blend of compounds emitted by C. sandersonii is unusual among flowering plants and lures kleptoparasitic flies into the trap flowers. This study describes a new example of how a plant can achieve pollination through chemical mimicry of the food sources of adult carnivorous animals.
Page URI


Heiduk A, Brake I, von Tschirnhaus M, et al. Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination. CURRENT BIOLOGY. 2016;26(20):2787-2793.
Heiduk, A., Brake, I., von Tschirnhaus, M., Goehl, M., Juergens, A., Johnson, S. D., Meve, U., et al. (2016). Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination. CURRENT BIOLOGY, 26(20), 2787-2793. doi:10.1016/j.cub.2016.07.085
Heiduk, A., Brake, I., von Tschirnhaus, M., Goehl, M., Juergens, A., Johnson, S. D., Meve, U., and Doetterl, S. (2016). Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination. CURRENT BIOLOGY 26, 2787-2793.
Heiduk, A., et al., 2016. Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination. CURRENT BIOLOGY, 26(20), p 2787-2793.
A. Heiduk, et al., “Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination”, CURRENT BIOLOGY, vol. 26, 2016, pp. 2787-2793.
Heiduk, A., Brake, I., von Tschirnhaus, M., Goehl, M., Juergens, A., Johnson, S.D., Meve, U., Doetterl, S.: Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination. CURRENT BIOLOGY. 26, 2787-2793 (2016).
Heiduk, Annemarie, Brake, Irina, von Tschirnhaus, Michael, Goehl, Matthias, Juergens, Andreas, Johnson, Steven D., Meve, Ulrich, and Doetterl, Stefan. “Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination”. CURRENT BIOLOGY 26.20 (2016): 2787-2793.

6 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study.
Ollerton J, Liede-Schumann S, Endress ME, Meve U, Rech AR, Shuttleworth A, Keller HA, Fishbein M, Alvarado-Cárdenas LO, Amorim FW, Bernhardt P, Celep F, Chirango Y, Chiriboga-Arroyo F, Civeyrel L, Cocucci A, Cranmer L, da Silva-Batista IC, de Jager L, Deprá MS, Domingos-Melo A, Dvorsky C, Agostini K, Freitas L, Gaglianone MC, Galetto L, Gilbert M, González-Ramírez I, Gorostiague P, Goyder D, Hachuy-Filho L, Heiduk A, Howard A, Ionta G, Islas-Hernández SC, Johnson SD, Joubert L, Kaiser-Bunbury CN, Kephart S, Kidyoo A, Koptur S, Koschnitzke C, Lamborn E, Livshultz T, Machado IC, Marino S, Mema L, Mochizuki K, Morellato LPC, Mrisha CK, Muiruri EW, Nakahama N, Nascimento VT, Nuttman C, Oliveira PE, Peter CI, Punekar S, Rafferty N, Rapini A, Ren ZX, Rodríguez-Flores CI, Rosero L, Sakai S, Sazima M, Steenhuisen SL, Tan CW, Torres C, Trøjelsgaard K, Ushimaru A, Vieira MF, Wiemer AP, Yamashiro T, Nadia T, Queiroz J, Quirino Z., Ann Bot 123(2), 2019
PMID: 30099492
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
Nocturnal Bee Pollinators Are Attracted to Guarana Flowers by Their Scents.
Krug C, Cordeiro GD, Schäffler I, Silva CI, Oliveira R, Schlindwein C, Dötterl S, Alves-Dos-Santos I., Front Plant Sci 9(), 2018
PMID: 30108601
Complex Sexual Deception in an Orchid Is Achieved by Co-opting Two Independent Biosynthetic Pathways for Pollinator Attraction.
Xu H, Bohman B, Wong DCJ, Rodriguez-Delgado C, Scaffidi A, Flematti GR, Phillips RD, Pichersky E, Peakall R., Curr Biol 27(13), 2017
PMID: 28625782

48 References

Daten bereitgestellt von Europe PubMed Central.

Rewardless flowers in the angiosperms and the role of insect cognition in their evolution
Renner, 2006
Cheaters and liars: chemical mimicry at its finest
Vereecken, Can. J. Zool. 88(), 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
Ceropegia (Apocynaceae, Ceropegieae, Stapeliinae): Paraphyletic but still taxonomically sound
Meve, Ann. Mo. Bot. Gard. 94(), 2007
Fly pollination in Ceropegia (Apocynaceae: Asclepiadoideae): biogeographic and phylogenetic perspectives
Ollerton, Ann. Bot. (Lond.) 103(), 2009
Die Bestäubung der Kesselfallen-Blüten von Ceropegia
Vogel, Beitr. Biol. Pflanz. 36(), 1961
Chemical attraction of kleptoparasitic flies to heteropteran insects caught by orb-weaving spiders.
Eisner T, Eisner M, Deyrup M., Proc. Natl. Acad. Sci. U.S.A. 88(18), 1991
PMID: 1896468
Associations between flies and spiders: bibiocommensalism and dipsoparasitism
Robinson, Psyche (Stuttg.) 84(), 1977
A synopsis of the world species of Desmometopa Loew (Diptera, Milichiidae)
Sabrosky, Contrib. Am. Entomol. Inst. 19(), 1983
Kleptoparasitism and phoresy in the diptera.
Sivinski J, Marshall S, Petersson E., Fla. Entomol. 82(2), 1999
PMID: IND22014621
A kleptoparasitic cecidomyiid and other flies associated with spiders
Sivinski, Psyche (Stuttg.) 87(), 1980
Chemical attraction of male crab spiders (Araneae, Tomisidae) and kleptoparasitic flies (Diptera, Milichidae and Chloropidae)
Aldrich, J. Arachnol. 23(), 1995
Synthetic attractants for some dipteran species
Beavers, J. Econ. Entomol. 65(), 1972
Attraction of scavenging chloropid and milichiid flies (Diptera) to metathoracic scent gland compounds of plant bugs (Heteroptera: Miridae)
Zhang, Environ. Entomol. 33(), 2004
Scent chemistry and pollinator attraction in the deceptive trap flowers of Ceropegia dolichophylla
Heiduk, S. Afr. J. Bot. 76(), 2010
Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent
Heiduk, Front. Ecol. Evol. (), 2015
The betrayed thief - the extraordinary strategy of Aristolochia rotunda to deceive its pollinators.
Oelschlagel B, Nuss M, von Tschirnhaus M, Patzold C, Neinhuis C, Dotterl S, Wanke S., New Phytol. 206(1), 2014
PMID: 25488155

Commensalismus bei Fliegen
Biró, Természetrajzi Füzetek 22(), 1899
Observations on commensal Diptera (Milichiidae and Chloropidae) associated with spiders in Alabama
Landau, J. Arachnol. 15(), 1987
Merkwürdige Beziehungen zwischen Desmometopa m-atrum Meig. aus Europa und Agromyza minutissima v.d., Wulp aus Neu-Guinea
Mik, Wien. Ent. Ztg. 17(), 1898
News on insects considered as spider commensals and their hosts
Lopez, Newsl. Br. Arachnol. Soc. 40(), 1984
Diversity and distribution of floral scent
Knudsen, Bot. Rev. 72(), 2006

The influence of age and task specialization on the production and perception of honey bee pheromones
Allan, J. Insect Physiol. 33(), 1987
Eclectic chemisociality of the honeybee: A wealth of behaviors, pheromones, and exocrine glands
Blum, J. Chem. Ecol. 14(), 1988
Alarm responses caused by newly identified compounds derived from the honeybee sting
Collins, J. Chem. Ecol. 9(), 1983
Chemistry of the sting apparatus of the worker honeybee
Blum, J. Apic. Res. 17(), 1978
Identification of nerolic and geranic acids in the Nassanoff pheromone of the honey bee
Boch, Nature 202(), 1964
Mass spectral identification of the tergal gland secretions of female castes of two African honey bee races (Apis mellifera)
Wossler, J. Apic. Res. 38(), 1999
Trapping pheromonal components with silicone rubber tubes: fatty acid secretions in honeybees (Apis mellifera)
Crewe, Chemoecology 14(), 2004
Volatiles of foraging honeybees Apis mellifera (Hymenoptera: Apidae) and their potential role as semiochemicals
Schmitt, Apidologie (Celle) 38(), 2007
Nucleotide composition of soluble ribonucleic acid of Streptomyces fradiae.
Trentalance A, Amaldi F., Nature 206(983), 1965
PMID: 5831852
Bioassay of compounds derived from the honeybee sting
Collins, J. Chem. Ecol. 8(), 1982
(Z)-11-eicosen-1-ol, an important new pheromonal component from the sting of the honey bee, Apis mellifera L. (Hymenoptera, Apidae.)
Pickett, J. Chem. Ecol. 8(), 1982
The bite of the honeybee: 2-heptanone secreted from honeybee mandibles during a bite acts as a local anaesthetic in insects and mammals.
Papachristoforou A, Kagiava A, Papaefthimiou C, Termentzi A, Fokialakis N, Skaltsounis AL, Watkins M, Arnold G, Theophilidis G., PLoS ONE 7(10), 2012
PMID: 23091624
Identification of geraniol as the active compound in the Nasonoff pheromone of the honeybee
Boch, Nature 194(), 1962
Nasonov pheromone of the honey bee, Apis mellifera L. (Hymenoptera, Apidae). Part I. Chemical characterization
Pickett, J. Chem. Ecol. 6(), 1980
Evidence of Nasonov scenting in colony defence of the Giant honeybee Apis dorsata
Kastberger, Ethology 104(), 1998
Observations on colony defense of Apis nuluensis Tingek, Koeniger and Koeniger, 1996 and predatory behavior of the hornet, Vespa multimaculata Pérez, 1910
Koeniger, Apidologie (Celle) 27(), 1996
Discovery of pyrazines as pollinator sex pheromones and orchid semiochemicals: implications for the evolution of sexual deception.
Bohman B, Phillips RD, Menz MH, Berntsson BW, Flematti GR, Barrow RA, Dixon KW, Peakall R., New Phytol. 203(3), 2014
PMID: 24697806
Chemical basis for the relationship between Ophrys orchids and their pollinators. 1. Volatile compounds of Ophrys lutea and O. fusca as insect mimetic attractants/excitants
Borg-Karlson, Chem. Scr. 25(), 1985
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
(Z)-11-eicosen-1-ol, a major component of Apis cerana venom
Schmidt, J. Chem. Ecol. 23(), 1997
Qualitative and quantitative analyses of flower scent in Silene latifolia.
Dotterl S, Wolfe LM, Jurgens A., Phytochemistry 66(2), 2005
PMID: 15652577


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 27720617
PubMed | Europe PMC

Suchen in

Google Scholar