Ceropegieae-Anisotominae): a Generalized System of Floral Deception
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plants Article Fly Pollination of Kettle Trap Flowers of Riocreuxia torulosa (Ceropegieae-Anisotominae): A Generalized System of Floral Deception Annemarie Heiduk 1,* , Ulrich Meve 2 , Frank Menzel 3 , Jean-Paul Haenni 4 , Michael von Tschirnhaus 5, Stefan Dötterl 6 and Steven D. Johnson 1 1 Centre for Functional Biodiversity, School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa; [email protected] 2 Department of Plant Systematics, University of Bayreuth, Universitätsstrasse 30, 95440 Bayreuth, Germany; [email protected] 3 Senckenberg Deutsches Entomologisches Institut, Eberswalder Straße 90, 15374 Müncheberg, Germany; [email protected] 4 Entomology, Muséum d’Histoire Naturelle Neuchâtel, Rue des Terreaux 14, 2000 Neuchâtel, Switzerland; [email protected] 5 Faculty of Biology, University of Bielefeld, Bielefeld, Universitätsstraße 25, 33615 Bielefeld, Germany; [email protected] 6 Department of Biosciences, Plant Ecology, Paris Lodron University of Salzburg, 5020 Salzburg, Austria; [email protected] * Correspondence: [email protected] Citation: Heiduk, A.; Meve, U.; Abstract: Elaborated kettle trap flowers to temporarily detain pollinators evolved independently in Menzel, F.; Haenni, J.-P.; Tschirnhaus, several angiosperm lineages. Intensive research on species of Aristolochia and Ceropegia recently illu- M.v.; Dötterl, S.; Johnson, S.D. Fly minated how these specialized trap flowers attract particular pollinators through chemical deception. Pollination of Kettle Trap Flowers Morphologically similar trap flowers evolved in Riocreuxia; however, no data about floral rewards, of Riocreuxia torulosa pollinators, and chemical ecology were available for this plant group. Here we provide data on (Ceropegieae-Anisotominae): pollination ecology and floral chemistry of R. torulosa. Specifically, we determined flower visitors and A Generalized System of Floral pollinators, assessed pollen transfer efficiency, and analysed floral scent chemistry. R. torulosa flowers Deception. Plants 2021, 10, 1564. are myiophilous and predominantly pollinated by Nematocera. Pollinating Diptera included, in order https://doi.org/10.3390/ of decreasing abundance, male and female Sciaridae, Ceratopogonidae, Scatopsidae, Chloropidae, plants10081564 and Phoridae. Approximately 16% of pollen removed from flowers was successfully exported to conspecific stigmas. The flowers emitted mainly ubiquitous terpenoids, most abundantly linalool, Academic Editor: Diego Demarco furanoid (Z)-linalool oxide, and (E)-β-ocimene—compounds typical of rewarding flowers and fruits. Received: 19 June 2021 R. torulosa can be considered to use generalized food (and possibly also brood-site) deception to Accepted: 12 July 2021 lure small nematocerous Diptera into their flowers. These results suggest that R. torulosa has a less Published: 29 July 2021 specific pollination system than previously reported for other kettle trap flowers but is nevertheless specialized at the level of Diptera suborder Nematocera. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Keywords: Apocynaceae-Asclepiadoideae; electroantennography; Ceropegia; flower scent; fly polli- published maps and institutional affil- nation; gas chromatography/mass spectrometry; kettle trap flower; pollen transfer efficiency iations. 1. Introduction Copyright: © 2021 by the authors. The diversification of angiosperm flowers is driven largely by adaptations to pollina- Licensee MDPI, Basel, Switzerland. tors [1,2]. Some plants have evolved extremely complex floral phenotypes specialized in This article is an open access article pollination by particular pollinators. Among such specialized flowers are sophisticated distributed under the terms and kettle-shaped flowers that temporarily trap pollinators. These evolved independently in conditions of the Creative Commons many different plant lineages, such as Apocynaceae, Aristolochiaceae, and Araceae (see Attribution (CC BY) license (https:// also [3]) and are generally associated strongly with brood-site deception [4,5]. Though creativecommons.org/licenses/by/ similar deceptive strategies, such as food and brood-site deception, tend to be used by such 4.0/). Plants 2021, 10, 1564. https://doi.org/10.3390/plants10081564 https://www.mdpi.com/journal/plants Plants 2021, 10, 1564 2 of 13 Plants 2021, 10, x FOR PEER REVIEW 2 of 13 plants, their chemical profiles are generally highly variable due to the vast diversity of similar deceptive strategies, such as food and brood-site deception, tend to be used by different substrates and/or stages of decay mimicked [5]; however, certain key compounds such plants, their chemical profiles are generally highly variable due to the vast diversity orof compounddifferent substrates groups canand/or often stages be identifiedof decay mimicked especially [5]; for however, brood-site certain deceptive key com- systems [5]. poundsWithin or compound the Apocynaceae, groups can trapoften flowersbe identified have especially evolved for independently brood-site deceptive in two sister subtribessystems [5]. of the tribe Ceropegieae, i.e., in Stapeliinae and Anisotominae [6]. Members of the species-richWithin the subtribe Apocynaceae, Stapeliinae trap (>700flowers spp.) have areevolved distributed independently in Southern in two and sister Eastern sub- Africa, Arabia,tribes of Madagascar,the tribe Ceropegieae, India, Thailand,i.e., in Stapeliinae and China and Anisotominae [7,8]. About [6]. 225 Members species of thereof the have distinctspecies-rich and subtribe highly elaborateStapeliinaekettle-shaped (>700 spp.) are pitfalldistributed flowers in Southern with various and Eastern trapping Af- devices, suchrica, Arabia, as slippery Madagascar, surfaces India, and trappingThailand, trichomes;and China [7,8]. these About species 225 are species traditionally thereof have recognized asdistinctCeropegia and highlyL. (but elaborate see [9]). kettle-shaped Within the strictlypitfall flowers African with subtribe various Anisotominaetrapping devices, (4 genera, ~30such spp.), as slippery species surfaces in the genusand trappingRiocreuxia trichomes;Decne. these have species similar are though traditionally less elaborate recog- kettle trapnized flowers as Ceropegia lacking L. (but trapping see [9]). trichomes Within the and strictly slippery African surfaces. subtribe Anisotominae (4 genera, ~30 spp.), species in the genus Riocreuxia Decne. have similar though less elaborate Riocreuxia was established in 1844 by the French botanist Joseph Decaisne who recog- kettle trap flowers lacking trapping trichomes and slippery surfaces. nizedRiocreuxiaR. torulosa was(E. established Mey.) Decne., in 1844 the by type the French species botanist of thegenus, Joseph asDecaisne distinct who from rec-Ceropegia, whereognized it wasR. torulosa previously (E. Mey.) included Decne., due theto type similarities species of in the floral genus, and as vegetative distinct from characters Ce- [10]. Riocreuxiaropegia, whereis considered it was previously to comprise included eight due to species similarities [11]; in in floral some and thereof vegetative the flowers char- show extensiveacters [10]. intraspecific Riocreuxia is considered variation withto comprise regard eight to corolla species morphology [11]; in some and thereof the structurethe of theflowers gynostegium show extensive and intraspecific corona [6,11 variation]. R. torulosa with regard(Figure to1 corolla) is among morphology the most and widespread the andstructure most of variable the gynostegium species and and is corona considered [6,11]. R. to torulosa be a species (Figure complex 1) is among [6] consisting the most of two varieties:widespreadR. and torulosa most var.variabletorulosa speciesand andR. is torulosa consideredvar. tobolusii. be a speciesAs shown complex by [6] Meve con- et al. [6], thesisting high of levelstwo varieties: of morphological R. torulosa var. variability torulosa and within R. torulosaR. torulosa var. bolusii., and otherAs shown species by of this genus,Meve et are al. not[6], reflectedthe high levels in DNA of morphological sequence variation, variability suggesting within R. rapidtorulosa recent, and other evolution. In sixspecies of the of this eight genus,Riocreuxia are not species,reflected thein DNA corolla sequence is fused variation, to form suggesting a kettle traprapid very recent similar to evolution. In six of the eight Riocreuxia species, the corolla is fused to form a kettle trap that of flowers in Ceropegia [12,13]. In R. aberrans and R. chrysochroma; however, the flowers very similar to that of flowers in Ceropegia [12,13]. In R. aberrans and R. chrysochroma; how- doever, not the seem flowers to functiondo not seem as ato pollinatorfunction as trapa pollinator but are trap rather but campanulateare rather campanulate with spreading corollawith spreading lobe tips corolla [11]. lobe tips [11]. FigureFigure 1. 1. VariabilityVariability in floral in floral shape shape and colouration and colouration of Riocreuxia of Riocreuxia torulosa plants torulosa fromplants different from lo- different calities in KwaZulu-Natal, South Africa: A, Ashburton, where data for the present study were col- localities in KwaZulu-Natal, South Africa: A, Ashburton, where data for the present study were lected; B, Michel’s Pass at Hogsback, flower opened revealing a ceratopogonid fly caught in the act collected;of removing B, a Michel’s pollinarium; Pass C, at Ngome; Hogsback, D, Inanda;