Ceropegia sandersonii Mimics Attacked Honeybees to Attract Kleptoparasitic Flies for Pollination

Abstract

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.

Interpopulation variation in pollinators and floral scent of the lady’s-slipper orchid Cypripedium calceolus L.

“…Olfactory cues are most important for plants pollinated at night (Cordeiro et al 2017;Dobson 2006;Dötterl et al 2012), and for highly specialized pollination systems (Heiduk et al 2016;Milet-Pinheiro et al 2013;Schäffler et al 2015;Schiestl et al 1999).…”

“…The analyses were performed with an Agilent 7890A (Santa Clara, California, USA) gas chromatograph as described by Heiduk et al (2015Heiduk et al ( , 2016. The GC was equipped with a flame ionization detector (FID) and an EAD setup (heated transfer line, 2-channel USB acquisition controller) provided by Syntech (Kirchzarten, Germany).…”

“…To identify EAD-active compounds (see below), S samples were analyzed by GC/MS using a Shimadzu GCMS-QP2010 Ultra equipped with an AOC-20i auto injector (Shimadzu, Tokyo, Japan) and again a ZB-5 fused silica column (5% phenyl polysiloxane; length: 30 m, inner diameter: 0.32 mm, film thickness: 0.25 μm, Phenomenex) as described by Heiduk et al (2015Heiduk et al ( , 2016. 1.0 μl of the samples was injected at 220 °C with a split ratio 1:1, and the column flow (carrier gas: helium) was set at 3 ml/min.…”

Diversity of Diptera families that pollinate Ceropegia (Apocynaceae) trap flowers: An update in light of new data and phylogenetic analyses

“…The tribe Ceropegieae of the Apocynaceae is remarkable for its high proportion of fly pollinated species, particularly in the large genus Ceropegia and within the closely related stapeliads (Vogel, 1961;Meve & Liede, 1994;Ollerton & Liede, 1997). However the full diversity of fly families and genera exploited by Ceropegia, and the exact nature of the relationship between flowers and pollinators, has only recently been appreciated (Masinde, 2004;Ollerton et al, 2009;Coombs et al, 2011;Heiduk et al, 2010Heiduk et al, , 2015Heiduk et al, , 2016Heiduk et al, , 2017.…”

“…In addition to the studies of pollination in Ceropegia there has been a growing body of work aimed at understanding the complex evolutionary history of the genus in relation to related genera of Ceropegieae (Meve & Liede-Schumann, 2007;Bruyns et al, 2015;Meve et al, 2016). All studies agree that the long-tubed trap flowers of What is particularly remarkable about this clade of plants is that they have diversified without major shifts between pollinator types, such as switches between bee, bird, bat and butterfly pollination, as has been observed in other taxa, e.g.…”