The betrayed thief – the extraordinary strategy ofAristolochia rotundato deceive its pollinators

Abstract

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.

Deceptive Ceropegia dolichophylla fools its kleptoparasitic fly pollinators with exceptional floral scent

“…Milichiidae and Chloropidae have rarely been described as pollinators in other angiosperms, but are known as pollinators from other Apocynaceae (Raspi et al, 2009;Pisciotta et al, 2011), rewarding and non-rewarding orchid species (Borba and Semir, 2001;Chase et al, 2014;Nunes et al, 2014), and several species of Aristolochia (Brantjes, 1980;Wolda and Sabrosky, 1986;Oelschlägel et al, 2015). Lower Diptera were the most abundant flower visitors but did not carry pollinia and, therefore, are no pollinators of C. dolichophylla.…”

“…Oelschlägel et al (2015) described it for the first time for a deceptive Aristolochia species pollinated by kleptoparasitic Chloropidae. Independently from each other, the early diverged lineage Aristolochia (39.5 million years ago; Naumann et al, 2013) and the much younger group Ceropegia (10 million years ago; Rapini et al, 2007) evolved both, the trap flowers and the kleptomyiophilous pollination strategy.…”

Spatial and temporal variation in volatile composition suggests olfactory division of labor within the trap flowers of Aristolochia gigantea

“…In a bizarre twist on fly pollination, flowers of the European A. rotunda specifically attract chloropid flies with a chemical blend (hexyl esters and short chain alkanes) that mimics the wound volatiles emitted by recently killed mirid bugs (Hemiptera). These kleptoparasitic flies (Trachysiphonella ruficeps) steal food from other insects, and in this case specifically imbibe the secretions from mirid bugs killed by other arthropods (Oelschlägel et al, 2015). Finally, the larger Aristolochiaceae, which now includes the former Piperaceae, Saururaceae and Hydnoraceae (APG, 2016), includes additional pollinator niches, including fungal mimicry in the ground-blooming genus Asarum and the cauliflorous Aristolochia arborea (Kaiser, 2006;Sinn et al, 2015;Vogel, 1978).…”

“…Kettle trap flowers are thought to have first evolved in the basal angiosperm genus Aristolochia (Aristolochiaceae) (Oelschlägel et al, 2009), which includes some of the world's largest flowers (Davis et al, 2008) and most unusual floral scent blends (Oelschlägel et al, 2015). Aristolochia is a diverse genus consisting of roughly 450 species of vines, lianas, shrubs, or herbs with a predominately pantropical (but also warm-temperate) distribution (Endress, 1994;Judd et al, 2009;Wagner et al, 2014).…”

Plantas, polinizadores e algumas articulações da biologia da polinização com a teoria ecológica

“…Tradicionalmente essas flores tem sido encaixadas dentro da síndrome de sapromiiofila ou micromiiofilia mediada pelo odor floral (Faegri & van der Pijl 1979). Porém, um estudo mostrou que a espécie Aristolochia rotunda explora as preferências inatas de moscas ao produzir odores semelhantes à hemolinfa de hemípteros da ordem Miridae da qual geralmente essas moscas se alimentam (Oelschlägel et al 2015).…”