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Pollination strategies in Cretan Arum lilies
Abstract
Flowers of the genus Arum are known to attract dung-breeding flies and beetles through olfactory deceit. In addition to this strategy, the genus has evolved several other pollination mechanisms. The present study aimed to characterize the pollination strategies of the Cretan Arum species by investigating the flowering phenology, thermogeny, inflorescence odours, and the pollinating fauna. The results obtained show that Arum cyrenaicum and Arum concinnatum emit a strong dung smell and exhibit the distinctive features associated with this pollination syndrome. Both species are highly thermogenic, have a similar odour profile and attract small-bodied Diptera. Although sharing the same habitat, these two plant species are never found growing sympatrically as a result of the early blooming period of A. cyrenaicum. By contrast, Arum creticum and Arum idaeum have evolved a more traditional and mutually beneficial pollination mechanism. The stinking smell has been replaced by a more flower-like odour that attracts bees (Lasioglossum sp.) and, occasionally, bugs (Dionconotus cruentatus). Although attracting the same pollinator, the main compound present in the odour of A. creticum is different from that of A. idaeum. Principal component analysis (PCA), based on physiologically active components of the flower odours determined by testing on the antenna of the Lasioglossum bee, revealed two different clusters, indicating that pollinators can potentially discriminate between the odours of the two species. A further PCA on the main floral odour volatiles as identified by gas chroatography-mass spectroscopy from all the Arum species under investigation displayed odour-based similarities and differences among the species. The PCA-gas chomotography-electroantennographic detection active peaks analysis showed that the two species, A. creticum and A. idaeum, form two groups and are clearly separated from A. cyrenaicum and A. concinnatum, which, conversely, cluster together. The evolutionary forces and selective pressures leading to diversification of pollination mechanisms in the Cretan Arum spp. are discussed.~copyright 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 991--1001
... This is accompanied by a single bout of intense warming of the appendix to over 30uC. When the appendix temperature reaches its peak, accompanied by spathe opening and scent volatilization, several insect families of Diptera (e.g., Sphaeroceridae, Sciaridae, and Drosophilidae) and a family of Coleoptera (Ceratopogonidae) are attracted to the inflorescence 42 . The insects remain in the floral chamber where the thermogenic male florets provide warmth overnight. ...
... The jasmonic acid signaling pathway is involved in defense responses to injury and in programmed cell death and senescence 61 . When the appendix temperature rises and reaches its peak, accompanied by floral scent volatilization, several species of pollinator insects are attracted to the inflorescence 42 . In the only other study of the transcriptome in thermogenic plants, Ito-Inaba et al. demonstrated that genes involved in stress responses and protein degradation are up-regulated during the post-thermogenic stages in skunk cabbage (S. renifolius) 62 . ...
... As a distinctive phenomenon associated with thermogenesis in A. concinnatum, the flowers volatilize a strong dung/urine-like smell at D-day 42 . Metabolome analysis by gas chromatography/mass spectrometry (GC-MS) on the volatile compounds showed that terpenoids (3,7-dimethyl-1, 6-octadine, 2,7-dimethyl-1,7-octadiene, and 3-7-dimethyl-1-octane) mainly account for the smell of A. concinnatum 42,63 . Because the transcripts of the first step of the mevalonate pathway showed lower correlation with the thermogenic level compared with transcripts of the first step of the MEP pathway (Fig. 6), the MEP pathway seems to be the main biosynthetic route for producing these three basic scent monoterpenes in this plant. ...
Several plant species can generate enough heat to increase their internal floral temperature above ambient temperature. Among thermogenic plants, Arum concinnatum shows the highest respiration activity during thermogenesis. However, an overall understanding of the genes related to plant thermogenesis has not yet been achieved. In this study, we performed de novo transcriptome analysis of flower organs in A. concinnatum. The de novo transcriptome assembly represented, in total, 158,490 non-redundant transcripts, and 53,315 of those showed significant homology with known genes. To explore genes associated with thermogenesis, we filtered 1266 transcripts that showed a significant correlation between expression pattern and the temperature trend of each sample. We confirmed five putative alternative oxidase transcripts were included in filtered transcripts as expected. An enrichment analysis of the Gene Ontology terms for the filtered transcripts suggested over-representation of genes involved in 1-deoxy-D-xylulose-5-phosphate synthase (DXS) activity. The expression profiles of DXS transcripts in the methyl-D-erythritol 4-phosphate (MEP) pathway were significantly correlated with thermogenic levels. Our results suggest that the MEP pathway is the main biosynthesis route for producing scent monoterpenes. To our knowledge, this is the first report describing the candidate pathway and the key enzyme for floral scent production in thermogenic plants.
... E-mail: david.broederbauer@univie. ac.at Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/ onlineopen#OnlineOpen_Terms bs_bs_banner extent to which these trapping devices are under selection based on the type of pollinator caught is currently an unexplored question. The genus Arum L. (Araceae) offers an excellent opportunity to explore the relationship between pollinators and floral structure as it comprises 29 species (Boyce, 1993; Linz et al., 2010), which attract various types of pollinators (reviewed in Gibernau, Macquart & Przetak, 2004 ). All Arum spp. ...
... were available for our study. These species cover the majority of the clades in the genus (Espíndola et al., 2010) and represent all pollination syndromes found in Arum (Linz et al., 2010). Voucher specimens are preserved in spirit collections of the Herbarium of the University of Vienna (WU) (seeTable 1). ...
... We found that, in the genus Arum, species pollinated by different types of insects differ significantly in the size of the slippery papillate surfaces and lacunae. Although several of the taxa sharing the same pollinator type are closely related, similarities in trapping devices are unlikely to be a result of common ancestry alone, as our sample species belong to different clades of the genus and pollination syndromes in these clades have been shown to have evolved in convergence independently of the phylogenetic relationship (Linz et al., 2010). Therefore, we conclude that the differences in trapping devices in Arum are most probably attributable to adaptation to the respective pollinator types. ...
Pollinators have long been known to select for floral traits, but the nature of this relationship has been little investigated in trap pollination systems. We investigated the trapping devices of 15 Arum spp. and compared them with the types of insects trapped. Most species shared a similar general design of trap chamber walls covered in downward-pointing papillate cells, lacunose cells in the chamber wall and elongated sterile flowers partially blocking the exit of the trap. However, there was significant variation in all these morphological features between species. Furthermore, these differences related to the type of pollinator trapped. Most strikingly, species pollinated by midges had a slippery epidermal surface consisting of smaller papillae than in species pollinated by other insects. Midge-pollinated species also had more elongated sterile flowers and tended to have a larger lacunose area. We conclude that pollination traps evolve in response to the type of insect trapped and that changes to the slippery surfaces of the chamber wall are an important and previously little recognized variable in the design of pollination traps.
© 2013 The Linnean Society of London,2013, 385-397.
... Pollinator-mediated selection is known to influence floral morphology (Bröderbauer et al. 2013;Gervasi and Schiestl 2017) and colour (Schemske and Bradshaw 1999;Newman et al. 2012;Trunschke et al. 2021), and recent studies have also identified strong evidence for variation in VOC emissions driven by pollinator preferences. Notably, comparative community ecology data and gas chromatographymass spectrometry (GC-MS) have been combined to identify convergent VOC bouquets in unrelated plant species with similar pollinators (Fenster et al. 2004;Schiestl and Johnson 2013;Junker and Parachnowitsch 2015), and divergent VOC bouquets in related species with different pollinators (Dobson et al. 1997;Urru et al. 2010;Byers et al. 2014;Friberg et al. 2019). Moreover, the discovery of biochemical pathways underlying floral VOCs has greatly accelerated by next-generation sequencing (NGS) technologies such as mRNA sequencing (Dhandapani et al. 2017;Wong et al. 2017b;Xiao et al. 2019). ...
... To date, the biosynthetic pathways underlying the production of p-cresol and skatole have only been characterized in bacteria (Selmer and Andrei 2001;Liu et al. 2018), and it is unclear whether A. maculatum and other angiosperms use similar aromatic amino acid fermentation pathways to produce these VOCs. Furthermore, tissue-specific RNA-seq of Arum concinnatum identified more diverse transcript expression in male floret tissue on the day of anthesis rather than in the appendix (Onda et al. 2015), even though A. concinnatum also emits dung-like VOCs from its appendix (Urru et al. 2010). Consequently, many questions remain regarding the specific biosynthetic pathways underlying A. maculatum VOCs, the localization of their expression, and whether mRNA expression related to VOC production varies with geographic distance or pollinator community composition. ...
Deceptive pollination often involves volatile organic compound (VOC) emissions that mislead insects into performing non-rewarding pollination. Among deceptively pollinated plants, Arum maculatum is particularly well-known for its potent dung-like VOC emissions and specialized floral chamber, which traps pollinators—mainly Psychoda phalaenoides and P. grisescens—overnight. However, little is known about the genes underlying the production of many A. maculatum VOCs, and their influence on variation in pollinator attraction rates. Therefore, we performed de novo transcriptome sequencing of A. maculatum appendix and male floret tissue collected during- and post-anthesis, from ten natural populations across Europe. These RNA-seq data were paired with GC-MS analyses of floral scent composition and pollinator data collected from the same inflorescences. Differential expression analyses revealed candidate transcripts in appendix tissue linked to malodourous VOCs including indole, p-cresol, and 2-heptanone. Additionally, we found that terpene synthase expression in male floret tissue during anthesis significantly covaried with sex- and species-specific attraction of Psychoda phalaenoides and P. grisescens. Taken together, our results provide the first insights into molecular mechanisms underlying pollinator attraction patterns in A. maculatum, and highlight floral chamber sesquiterpene (e.g. bicyclogermacrene) synthases as interesting candidate genes for further study.
... Saprophagous or coprophagous Sphaeroceridae and Psychodidae, common dung-inhabiting families (Campbell, 1976;Bishop et al., 1998), are known pollinators of other araceous brood-site mimics, particularly thermogenic Arum species (e.g. Kite et al., 1998;Albre et al., 2003;Quilichini et al., 2010;Urru et al., 2010). The insects trapped were not typically anthophilous and, also unlike mutualistic brood-site pollination (Chartier et al., 2014), there was no evidence of insect egg or larvae development in inflorescences. ...
... S3), which indicated that colour was likely to be negligible in mediating differences in the pollinator attraction and capture, and that each pollinator group (associated with similar habits, i.e. decomposing substrates) may utilize similar visual stimuli, namely dark colours, to locate rewarding substrates (Chen et al., 2015). A shift in pollinator assemblage was also not associated with a change in anthesis rhythms and the timing, extent and pattern of floral thermogenesis, which can vary markedly between thermogenic plant species including congeneric species (Gibernau and Barabe, 2000;Urru et al., 2010;Sayers, 2019). As found in most thermogenic species (Seymour et al., 2003a), appendix temperature increases in both species were transient and associated with enhanced insect attraction and scent emission related to a circadian rhythm. ...
Background
Flowers which imitate insect oviposition sites likely represent the most widespread form of floral mimicry, exhibit the most diverse floral signals and are visited by two of the most speciose and advanced taxa of insect – beetles and flies. Detailed comparative studies on brood-site mimics pollinated exclusively by each of these insect orders are lacking, limiting our understanding of floral trait adaptation to different pollinator groups in these deceptive systems.
Methods
Two closely related and apparent brood-site mimics Typhonium angustilobum and T. wilbertii (Araceae) observed to trap these distinct beetle and fly pollinator groups were used to investigate potential divergence in floral signals and traits most likely under pollinator-mediated selection. Trapped pollinators were identified and their relative abundances enumerated, and thermogenic, visual, and chemical signals and morphological traits were examined using thermocouples and qRT-PCR, reflectance, gas chromatography-mass spectrometry, floral measurements and microscopy.
Key Results
T. angustilobum and T. wilbertii were functionally specialised to trap saprophagous Coleoptera and Diptera, respectively. Both species shared similar colour and thermogenic traits and contained two highly homologous AOX genes (AOX1a and AOX1b) most expressed in the thermogenic tissue and stage (unlike pUCP). Scent during the pistillate stage differed markedly - T. angustilobum emitted a complex blend of sesquiterpenes, and T. wilbertii, a dung mimic, high relative amounts of skatole, p-cresol, and irregular terpenes. Species differed significantly in floral morphology related to trapping mechanisms.
Conclusions
Functional specialisation and pollinator divergence were not associated with differences in anthesis rhythm and floral thermogenic or visual signals between species, but with significant differences in floral scent and morphological features, suggesting these floral traits are critical for the attraction and filtering of beetle or fly pollinators in these two brood-site mimics.
... Thermogenesis is another key feature of araceous pollination systems, with Araceae containing more thermogenic plant species than any other family (Meeuse & Raskin, 1988). Thermogenesis in Araceae is species-and tissue-specific, and the duration, timing and intensity of heat production also often vary in association with the timing of reproductive phases in protogynous inflorescences (Seymour, Gibernau & Ito, 2003;Urru et al., 2010;Miller et al., 2011). Despite its prevelance in Araceae and other early-diverging plant families, the function of floral thermogenesis in plantpollinator interactions remains contentious. ...
... Other Arum spp. pollinated by Sphaeroceridae or Psychodidae or both also generally contain p-cresol, indole and skatole among other VOCs (Urru et al., 2010;Quilichini et al., 2010;Chartier et al., 2013). Skatole and indole have been found to attract and elicit electroantennographic responses in coprophagous Scarabaeidae, and indole alone is a key floral attractant of Staphylinidae in the western skunk cabbage (Lysichiton americanus Hultén & H.St.John) (Osborne, Penman & Chapman, 1975;Burger & Petersen, 2002;Wurmitzer et al., 2017;Brodie et al., 2018). ...
The process of pollinator-driven evolution is best studied at the level of populations and among closely related plant species. Araceae provide a plant model for investigating plant–pollinator interactions, but few studies have investigated intraspecific variation in their pollination systems. Typhonium brownii (Araceae) is distributed widely across 2000 km from tropical to temperate latitudes in Australia, yet the existence of intraspecific variation and ecotypes has not been investigated. Typhonium brownii from five regions, potentially representing distinct taxa, and populations of the sister species, T. eliosurum, were studied to explore pollinator and floral trait divergence. We characterize significant intraspecific floral trait variation in T. brownii, indicating the existence of a species complex, despite the taxa trapping similar Coleoptera (Staphylinidae, Scarabaeidae). Although all T. brownii showed similar temperature increases in the appendix, there were significant shifts in the timing and pattern of thermogenic and anthesis rhythms between regions (taxa), and all T. brownii taxa had distinct scent compositions, with T. sp. aff. brownii being the most dissimilar to other taxa. In contrast, T. eliosurum inflorescences almost exclusively trapped Diptera (Sphaeroceridae, Psychodidae), had modest temperature increases confined to the staminate zone and had a distinct scent profile which differed from all T. brownii taxa; this scent was confirmed in field bioassays to be important for pollinator attraction. Prevalent volatile organic compounds (VOCs) emitted by T. eliosurum and T. brownii taxa included the common dung constituents skatole, indole and p-cresol. Typhonium eliosurum and T. brownii taxa further differed significantly in morphology and trapping mechanisms, particularly the fly-pollinated T. eliosurum. It is possible that a subset of ubiquitous VOCs identified in T. eliosurum and T. brownii taxa attract local communities of dung-seeking flies and beetles, and that floral morphological features are more important for trapping different insect orders in these dung mimics.
... The biological functions of thermogenesis in Arum include the release of volatile compoundsusually polyamines, indoles and skatolemimicking decaying organic matter, the scents of which are considered to attract insect pollinators belonging mostly in orders of Diptera and Coleoptera (Meeuse and Raskin 1988;Urru et al. 2010). As thermogenesis occurs, the female reproductive organs are receptive and the insects fall into the floral chamber of the inflorescences where they are trapped for at least a day. ...
... Arum concinnatum Schott (Araceae) is a highly thermogenic species, with the temperature of the appendix exceeding 10.9 C above the ambient temperature during thermogenesis, while the rates of respiration of the male florets in intact inflorescences peak at 0.92 mmol s -1 g -1 , which is the highest rate so far measured among the plants (Seymour et al. 2009;Seymour 2010). The floral odour of A. concinnatum inflorescences was first chemically analysed by Urru et al. (2010) in combination to pollination strategies, whereas a recent transcriptome analysis revealed the molecular portrait behind the floral scent in relation to thermogenesis (Onda et al. 2015). ...
Arum concinnatum Schott is a highly thermogenic species, with the temperature of the appendix exceeding ~10.9°C above the ambient temperature during thermogenesis, whereas the rates of respiration of the male florets in intact inflorescences peak at 0.92 μmol s–1 g–1, which is the highest rate so far measured among the plants. Here, we attempt the ex situ exogenous induction of thermogenesis in whole inflorescences and in separate appendices of the spadix, and explore the thermogenic patterns under controlled laboratory conditions of light and temperature. Mature but unopened inflorescences and appendices showed thermogenic responses when treated with salicylic acid (SA), but not when treated with distilled water (control). With regard to light conditions, the responses revealed only one significant difference for inflorescences, which concerns the higher maximum temperature in the continuous light treatment compared with continuous dark. Along the ambient temperature gradient, at the lowest temperature edge individuals remained stable close to ambient temperature and to control. These findings suggest that, in general, ex situ exogenous induction of thermogenesis can be achieved in whole inflorescences and in separate appendices of spadix of A. concinnatum using SA. This study also indicates that SA acts independently of light conditions, while exogenous induction of thermogenesis takes place within an ambient temperature range.
... 4 In addition to many volatile amines that will be presented in next sections, many compound families are represented in these pollination odors. 4,5 Some important compounds are shown in Figure 1. ...
... Detailed study of the floral odor of A. italicum was published earlier in 2004, where several methods of isolation and trapping volatile compounds were used. 6 In this study, very similar results were obtained comparing with the previously cited publications (4,5), and only stereochemical and structural isomerization can be noticed, comparing with the compounds shown in Figure 1. Most texts this property is mentioned and potential users are explicitly warned. ...
Plants belonging to the genus Arum are being used for nutritional and medicinal purposes for many centuries, despite their toxicity. Few subspecies of this genus were widely investigated by modern research, mainly for potential therapeutic goals and drug discovery. Other subspecies were never studied by current research despite the fact that some of them have known and well documented traditional medicinal and other uses. In this review article, we will present the traditional uses of this plant genus and summarize the published results of modern medicinal and other studies of these plants. Special attention will be drawn to effective, natural products that were isolated from these plants. The toxicity of the plants will be discussed extensively.
... Field studies integrating pollination investigations with an assessment of the floral scent composition in Araceae are few, limited to temperate European Arum (Chartier et al. 2013(Chartier et al. , 2016Kite 1995;Kite et al. 1998;Diaz and Kite 2002;Quilichini et al. 2010;Urru et al. 2010), Neotropical Anthurium (Hentrich et al. 2007(Hentrich et al. , 2010Schwerdtfeger et al. 2002), Neotropical Caladium (Maia et al. 2012(Maia et al. , 2013b, temperate N American Peltandra (Patt et al. 1995), Neotropical Philodendron (Maia et al. 2010;Dötterl et al. 2012;Gottsberger et al. 2013), Neotropical Spathiphyllum (Hentrich et al. 2010, and Neotropical Taccarum (Maia et al. 2013b). Studies of tropical Asian taxa are limited to Miyake and Yafuso (2005) for Alocasia and Kumano and Yamaoka (2006), Kumano-Nomura and Yamaoka (2009), Tung et al. (2010 for Homalomena. ...
... Elsewhere in Araceae, methyl benzoate was reported in Anthurium lindenianum (Kuanprasert et al. 1998) and Anthurium armeniense (Schwerdtfeger et al. 2002). Indole was detected in several Arum species (Kite 1995;Kite et al. 1998;Diaz and Kite 2002;Urru et al. 2010), Amorphophallus eichleri (Kite et al. 1998), and Caladium bicolor (Aiton) (Maia et al. 2012). In a field-trapping experiment, Psychoda (Diptera, Psychodidae) species were attracted to indole (Kite et al. 1998). ...
The flowering mechanism, visiting insect activities, reproductive system, and floral scent composition of Schismatoglottis baangongensis a Northwest Bornean locally endemic limestone-restricted protogynous mesophyte were investigated. Anthesis started at dawn and lasted ca 29 h. Fruit set for open pollination (93 %) and restricted access pollination (88 %) were high. Colocasiomyia (Diptera, Drosophilidae) and Cycreon (Coleoptera, Hydrophilidae) were the main pollinators. Colocasiomyia flies present in much higher numbers than Cycreon beetles individually carried significantly less pollen load. Chaloenus (Chrysomelidae, Galerucinae) was inadvertent pollinators, and Atheta (Coleoptera, Staphylinidae) passive visitors. Pollen transferal between dissimilar insect genera (Colocasiomyia and Chaloenus) is reported for the first time. Low pollen/ovule ratio of S. baangongensis indicated an efficient pollination mechanism. Ester compound class floral odours, especially the dominant compounds 3-butenoic acid, 3-methyl-, methyl ester, were decisive in attracting pollinators. The spadix appendix of S. baangongensis was the main olfactory body although the spathe was detected to release an additional N-containing compound, an indole. An increase in the total amount of floral scent from the pistillate flower zone during pistillate phase of anthesis from Period I (06:00–08:00 h) to Period II (08:00–10:00 h) was postulated to detain insects in the lower chamber of the inflorescence.
... Only one genus of this tribe has not been studied from a pollination point of view, namely Lazarum. The pollination of all the other eight genera has been studied (Arum, Biarum, Dracunculus, Eminium, Helicodiceros, Sauromatum, Theriophonum and Typhonium), and it's achieved by necrophilous or saprophilous flies and/or beetles (review in Gibernau, 2003;Blackith & Blackith, 1993;Yadav, 1998;Angioy et al., 2004;Gibernau et al., 2004;Sivadasan & Kavalan, 2005;Boyce, 2008;Espindola et al., 2010;Linz et al., 2010;Stökl et al., 2010;Quilichini et al., 2010;Urru et al., 2010) except for one known exception (Diaz & Kite, 2006;Urru et al., 2010). ...
... Only one genus of this tribe has not been studied from a pollination point of view, namely Lazarum. The pollination of all the other eight genera has been studied (Arum, Biarum, Dracunculus, Eminium, Helicodiceros, Sauromatum, Theriophonum and Typhonium), and it's achieved by necrophilous or saprophilous flies and/or beetles (review in Gibernau, 2003;Blackith & Blackith, 1993;Yadav, 1998;Angioy et al., 2004;Gibernau et al., 2004;Sivadasan & Kavalan, 2005;Boyce, 2008;Espindola et al., 2010;Linz et al., 2010;Stökl et al., 2010;Quilichini et al., 2010;Urru et al., 2010) except for one known exception (Diaz & Kite, 2006;Urru et al., 2010). ...
Data on aroid pollinators or inflorescence visitors were reviewed lately by Gibernau (2003), documenting the pollinators of 49 genera and about 125 species. This addendum adds information on 35 genera, of which 9 are newly documented, and about 60 species. In summary, we have actually some information on pollinators or inflorescence visitors on 58 genera and about 165 species. Such numbers are very still low in comparison of the family diversity (more than 110 genera and about 4,000 species). The pollination of entire groups of Araceae is still unknown. The knowledge on the pollination of each tribe is discussed. 2 KEY WORDS Araceae, Coleoptera, Diptera, Hymenoptera, Pollination DEDICATION I would like to dedicate this paper to Patricia Frank and Julius Boos.
... However, since no data is available, neither regarding pollinators nor on scent, from these species, they will be excluded from further discussion. The pollination biology of several Arum species has been described in general terms (Braverman and Koach, 1982;Drummond and Hammond, 1993;Koach and Feinbrun-Dothan, 1986;Lack and Diaz, 1991;Ollerton and Diaz, 1999), and for some brood-site mimicking species in quite some detail (Lack and Diaz, 1991;Quilichini et al., 2010;Stökl et al., 2010;Urru et al., 2010). Below we provide a review of the present state of knowledge regarding these brood-site mimicking species. ...
... Within the non-alkene producers, three species (A. cyrenaicum, A. concinnatum and A. pictum) are attracting the most diverse entomofauna (Quilichini et al., 2010;Urru et al., 2010). In A. cyrenaicum and A. concinnatum more than eleven diptera families, e.g., Sphaeroceridae, Drosophilidae and Cecidomyidae, have been recorded in the floral chamber . ...
... Nonanal (12%) and decanal (33%) were also primarily found in A. cylindraceum, a Cretan Arum lilies growing on the island of Crete, producing a very weak odour (to a human nose). 27 Emitting a urine-like smell is a very known characteristics of the flowers of Arum species to prevent themselves from many insects (flies and beetles) to oviposit as being their brood-site-mimicking pollination system. Because the insect communication are based on chemical signals, the ability have evolved by other organisms by emitting a dummy floral scent so equal chemically to sexual pheromones of insects to copulate. ...
Aim: Arum rupicola Boiss. var. rupicola with a vernacular name of Dağ Sorsalı, are used etnobotanically for hemorroid, eczema, rheumatism, and cancer. Essential oil combination of A. rupicola var. rupicola, under the lower risk (lc) threatened category because of the excess gathering was investigated. Methods: The above ground samples of Arum rupicola Boiss. var. rupicola was collected from Palamut province of Antalya (Kaş) and essential oil was taken by hydrodistillation method with Clevenger apparatus. The essential oil composition was analysed by Gas chromatography (GC) and Gas chromatography/Mass Spectrometry (GC/MS) systems simultaneously. Results: As a result of, (E)-geranyl acetone (15%) was the main compound while hexahydrofarnesyl acetone (9.2%), nonanal (6.8%), heptacosan (6.5%), farnesyl acetone (5.0%), tricosan (4.9%), ve 2-dodecanone (3.8%) followed. Conclusion: Farnesyl acetone (5%) and hexahydrofarnesyl acetone (9.2%) sesquiterpenes were new records for A. rupicola var. rupicola volatile oil content. The only species is Arum creticum consisting α-farnesene (95%) as its taxonomical feature. A. rupicola var. rupicola has farnesyl acetone and hexahydrofarnesyl aceton being known a flagy and odourless species.
... These compounds and those EAD-active ones shared with the pollinators' breeding substrates (e.g., UNK1415, 3-octanone) are the most promising candidates for future behavioural assays. As the tested Diptera species (Psychodidae, Sphaeroceridae) are also known pollinators of other (similarly-scented) species of Arum (e.g., A. italicum, A. concinnatum 31,66 ) as well as other species/genera of Araceae (e.g., Typhonium eliosurum 28 ), our study should also help to elucidate the chemical interactions between these plants and their fly pollinators. Future research is now needed to test the behavioural function of physiologically active floral volatiles, which is crucial for a better understanding of olfactory cues mediating plant-animal interactions in general, and in sapromyiophilous species, in particular. ...
Insect-pollinated plants often release complex mixtures of floral scents to attract their pollinators. Yet scent compounds eliciting physiological or behavioural responses in pollinators have only been identified in few plant species. The sapromyiophilous aroid Arum maculatum releases a highly diverse dung-like scent with overall more than 300 different compounds recorded so far to attract its psychodid and other fly pollinators. The volatiles’ role in pollinator attraction is mostly unknown. To identify potential behaviourally active compounds, we recorded electroantennographic responses of four Psychodidae and one Sphaeroceridae species to (1) inflorescence scents of A. maculatum and (2) the scents released by cow dung, likely imitated by the plant species. Here we show that these flies are sensitive to 78 floral volatiles of various chemical classes, 18 of which were also found in cow dung. Our study, which for the first time determined physiologically active compounds in the antennae of Psychoda spp. and Sphaeroceridae, identified various volatiles not known to be biologically active in any floral visitors so far. The obtained results help deciphering the chemical basis that enables A. maculatum and other plants, pollinated by psychodids and sphaerocerids, to attract and deceive their pollinators.
... In some species with morphologically very similar flowers, the flowers might differ in other than morphological traits such as the quality of their rewards (e.g. odour, nectar composition) leading at least to partially different pollinator spectra and thus further species separation (Urru et al. 2010). Due to the rather uniform appearance of these systems at first sight they remain little investigated regarding their current degree of differentiation and their ecological-evolutionary background. ...
Background and aims – Diversification in plant-pollinator interactions based on floral diversity is potentially a mechanism of coexistence in angiosperms. However, besides high floral diversity, some genera seemingly exhibit the same floral type in many of their species. This contradicts some expectations of competitive exclusion. We thus tested on a finer flower morphological scale whether five sympatric Aframomum species (61 spp., Zingiberaceae) in southeastern Gabon exhibiting the same general floral type (trumpet) were differentiated, and whether this resulted in different “pollinator niches”.Material and methods – We carried out a detailed survey measuring 18 flower morphological parameters as well as nectar volume (μl) and sugar concentration (% Brix) on five flowers per species and locality. Furthermore, we observed inflorescence phenology and pollinator activity from 8 am to 4 pm for 12 to 50 hours per species and conducted pollinator exclusion experiments.Key results – This study proves fine-scale flower morphological and resource differentiation within the trumpet floral type. Pollination-relevant parts of the flowers, however, remain constant across species. Our pollinator observations reveal the same broad bee pollinator spectrum for all observed simultaneously flowering sympatric species.Conclusion – As we could not detect a pollinator-based differentiation in the studied sympatric Aframomum species we assume that species boundaries developed randomly by genetic drift during geographic isolation in the past. The trumpet floral type and its pollinator guild, however, were maintained due to similar selection pressures in comparable habitats during isolation and are potentially an advantage for increased pollinator attraction through co-flowering.
... Similarly, gas chromatography-electroantennography (GC-EAD; Cork et al. 1990) could be used to identify all VOCs which elicit a physiological response in different pollinator species. The A. maculatum populations with unique patterns in pollinator attraction identified in this study may be useful targets for future research testing whether selection is acting on specific compounds (Stensmyr et al. 2002, Urru et al. 2010, or on 'superattractive mixtures' (e.g. in A. palaestinum; Stökl et al. 2010). ...
Flowering plants emit complex bouquets of volatile organic compounds (VOCs) to mediate interactions with their pollinators. These bouquets are undoubtedly influenced by pollinator‐mediated selection, particularly in deceptively‐pollinated species that rely on chemical mimicry. However, many uncertainties remain regarding how spatially and temporally heterogeneous pollinators affect the diversity and distribution of floral odour variation. Here, we characterized and compared the floral odours of ten populations of deceptively‐pollinated Arum maculatum (Araceae), and inter‐annual and decadal variation in pollinator attraction within these populations. Additionally, we transplanted individuals from all sampled populations to two common garden sites dominated by different pollinator species (Psychoda phalaenoides or Psycha grisescens), and compared pollinator attraction rates to investigate whether populations maintained odour blends adapted to a specific pollinator. We identified high within‐ and among‐population variation in a common blend of VOCs found across the range of A. maculatum. We also observed shifts in pollinator community composition within several populations over 1–2 years, as well as over the past decade. Common garden experiments further revealed that transplanted inflorescences generally attracted the dominant local pollinator species in both transplant sites. However, one population (Forêt du Gâvre, France) appears to exclusively attract P. grisescens, even when transplanted to a P. phalaenoides‐dominated site. Together, our results suggest that maintaining diverse floral odour bouquets within populations may be advantageous when pollinator communities vary over short timescales. We propose that temporally‐replicated ecological data are one potential key to understanding variation in complex traits such as floral odour, and in some cases may reveal resiliency to shifting pollinator communities.
... Also within Araceae, outside Australia staphylinids were noted as potential vectors of Biarum carduchorum, Englerarum hypnosum, and Symplocarpus renifolius; and potential secondary vectors of several Arum species and Schismatoglottis muluensis, the majority of which are characterised by fetid odours (Uemura et al. 1993;Boyce 2008;Quilichini et al. 2010;Urru et al. 2010;Nauheimer and Boyce 2013;Hoe et al. 2018;Oguri et al. 2019). Kite et al. (1998) provide additional accounts of visitation by Staphylinidae to several Arum species, amongst other beetle and fly visitors, not referred to in Table 1 and ESM 1. Due to the inaccessibility of this primary literature, however, it is unknown whether further details are provided on the pollination effectiveness of particular insect visitors (Knoll 1926;Kullenberg 1953;Hammond 1991, 1993). ...
Beetles (Coleoptera) are a diverse group of overlooked pollinators, considered particularly important in tropical ecosystems. The role of the most diverse beetle family, Staphylinidae, as pollinators is generally considered minor, yet their relationships
with plants are mostly unknown. Although often referred to as opportunistic visitors, it is arguable that the true extent of rove beetle pollination is underestimated given their frequency of visitation to flowers. This review comprehensively analysed the
plant–pollinator or visitor interactions of the Staphylinidae and uncovered 108 well-described staphylinid–flower interactions across 27 seed plant families. Of these interactions, Staphylinidae were considered either potential or conclusive pollinators
for 56 plant species, having either a primary or secondary role in pollination. Conversely, Staphylinidae were visitors to 40 plant species with a negligible role in pollination. For the remaining 12 interactions and additional anecdotal reports, the role of staphylinids as pollinators was unresolved. Staphylinid–flower interactions were most prevalent in the monocots and magnoliids (families: Araceae, Annonaceae, Arecaceae, and Magnoliaceae) involving predominantly generalist pollination systems, and interactions were limited to six staphylinid subfamilies (Omaliinae, Tachyporinae, Aleocharinae, Oxytelinae,
Paederinae, and Staphylininae). Trends in the involvement of staphylinid subfamilies with particular plant lineages were identified, associated with differences in insect habit and floral rewards. Overall this review indicates that the role of Staphylinidae as pollinators, and Coleoptera as a whole, is underestimated. Caution, however, must be given to inferring the role of staphylinids in pollination because rove beetles commonly function as inadvertent secondary pollinators or antagonists there to fulfil other ecological roles.
... The pollination biology of relatively few species in the Araceae has been documented (Grayum 1986;Mayo et al. 1997;Kite 1995;Gibernau et al. 2003). To achieve pollination, plants in the Araceae "advertise" with a variety of cues that have olfactory (Borg-Karlson et al. 1994;Stökl et al. 2010;Urru et al. 2010;Dötterl et al. 2012;Maia et al. 2012Maia et al. , 2013Gottsberger et al. 2013), visual (Gottsberger and Silberbauer-Gottsberger 1991;Pellmyr and Patt 1986) and thermal (Moodie 1976;Gibernau and Barabé 2000;Ivancic et al. 2005) characteristics. While many plants trick pollinators into pollination by mimicry of a reward without supplying one (Renner 2006), others have a mutualistic relationship with "their" pollinators, rewarding them with food, rendezvous sites for mates and oviposition resources. ...
Western skunk cabbage, Lysichiton americanus (Araceae), is pollinated mainly by the rove beetle Pelecomalium testaceum (Staphylinidae). Our objective was to determine the floral semiochemical(s) of L. americanus that attract(s) P. testaceum. Porapak Q headspace volatile extracts of L. americanus inflorescences were analyzed by gas chromatographic–electroantennographic detection (GC–EAD) and GC–mass spectrometry. In GC–EAD analyses, three floral odorants [(E)-4 nonene, (E)-5-undecene, indole] elicited consistent responses from the antennae of female P. testaceum. In field experiments, traps baited with a blend of these three components (“3-CB”) captured significantly more P. testaceum than unbaited control traps. Traps baited with the 3-CB, the two hydrocarbons, or indole, each captured significantly more beetles than unbaited control traps, indicating redundancy in the semiochemical blend. Moreover, traps baited with indole captured significantly more beetles than traps baited with either the 3-CB, or the hydrocarbons, indicating that indole is a key floral attractant for P. testaceum. Many necrophilous and coprophilous insects respond to indole in search of carrion or feces, but P. testaceum has never been associated with these types of resources. Both electrophysiological and behavioral responses of P. testaceum to two hydrocarbon semiochemicals, which are not signature odorants of carrion or feces, may indicate that the beetles recognize the odor of L. americanus as an honest signal, seek and pollinate its inflorescences, and get rewarded with pollen and on-plant mating opportunities.
... Also interesting is the persistence of the complex pollination system of many endemic Araceae of the Mediterranean islands, which attract flies and beetles through olfactory deceit and thermal claim (Quilichini et al. 2010;Urru et al. 2010). The thermogenesis of several island Arum species has actually been examined in detail in several studies (Seymour et al. 2009 and references therein). ...
The c. 12,000 islands and islets that encompass the Mediterranean basin represent a biodiversity hotspot. They have been disconnected from each other and from the continent for hundreds of thousands to millions of years and entail a high incidence of endemic plant species, with values that can exceed 20% of the local flora. Despite this, relatively few studies have been carried out to unravel ecological and evolutionary aspects of plant reproduction. We synthesize here the available information on the breeding systems, pollination and seed dispersal mode of the Mediterranean island flora. The main objective is to identify general patterns as well as to detect the main gaps of information on reproductive ecology in these particular and vulnerable systems in the face of global change. We also briefly review the information on impacts of invasive species on plant reproduction and dispersal as this is one of the main threats to island biodiversity in general and Mediterranean island plant diversity in particular. The review has revealed that most available information is much geographically biased towards the western Mediterranean islands, especially the Balearic Islands, although a good fraction of studies have been carried out also on the eastern islands in the Aegean archipelago. Moreover, the large majority of data come from species-focused studies, mainly endemic species of restricted range, whereas only a small fraction have been performed at a community level. Relatively little work has involved genetic analyses, mainly focused at assessing the genetic differentiation and variability on narrow endemics. Contrary to our expectations, most island species do not rely on autonomous selfing, what might be related to the relatively high diversity of pollinators. The small, uninhabited, islands might be the last refuges of peculiar interactions evolved in them in ancient times; they thus should be considered as sanctuaries of extraordinary biodiversity. We end up by pointing out the main gaps of information and formulating a set of hypotheses that we believe are worth testing in future studies if we are to advance the knowledge on the reproductive biology of Mediterranean island plants.
... K. Koch), often appear dark red and emit decomposition odorants including dimethyl disulfide and dimethyl trisulfide. These odorants are reminiscent of carrion odor [28,29], and thus are particularly attractive to gravid female blow flies seeking oviposition sites [30]. Unlike sapromyophilous flowers, myophilous flowers reward visitors with nectar, and possibly pollen, and produce a broad range of colors and typically sweet smelling fragrances [31]. ...
The common green bottle fly Lucilia sericata (Meigen) and other filth flies frequently visit pollen-rich composite flowers such as the Oxeye daisy, Leucanthemum vulgare Lam. In laboratory experiments with L. sericata, we investigated the effect of generic floral scent and color cues, and of Oxeye daisy-specific cues, on foraging decisions by recently eclosed flies. We also tested the effect of a floral pollen diet with 0-35% moisture content on the ability of females to mature their oocytes. Our data indicate that (1) young flies in the presence of generic floral scent respond more strongly to a uniformly yellow cue than to any other uniform color cue (green, white, black, blue, red) except for ultraviolet (UV); (2) the floral scent of Oxeye daisies enhances the attractiveness of a yellow cue; and (3) moisture-rich pollen provides nutrients that facilitate ovary maturation of flies. With evidence that L. sericata exploits floral cues during foraging, and that pollen can be an alternate protein source to animal feces and carrion, Pollen apparently plays a major role in the foraging ecology of L. sericata and possibly other filth flies. These flies, in turn, may play a significant role as pollinators, as supported by a recently published study.
... Thousands of plant species across a wide range of families are suspected to attract fly and beetle pollinators through chemical mimicry of their oviposition sites (Dobson, 2006;Urru et al., 2011;J€ urgens et al., 2013;Schiestl & Johnson, 2013). Studies of the chemical signalling evolved by independent plant lineagesfor example in cycads (Proches & Johnson, 2009), aroids (Stensmyr et al., 2002;Urru et al., 2011) and stapeliads (J€ urgens et al., 2006) have led to the identification of several general categories of oviposition sites mimicked by plants, such as carrion (Stensmyr et al., 2002;van der Niet et al., 2011;J€ urgens et al., 2013), dung (Johnson & J€ urgens, 2010;Urru et al., 2010;Humeau et al., 2011), mushrooms (Kaiser, 2006;Ren et al., 2011), rotting fruits Proches & Johnson, 2009;Maia et al., 2012) and yeasts . These biological substrates are largely ephemeral, and insects that use them have a low probability of finding suitable sites for laying their eggs. ...
Many plant species attract insect pollinators through chemical mimicry of their oviposition sites, often detaining them in a trap chamber that ensures pollen transfer. These plant mimics are considered to be unspecialized at the pollinator species level, yet field observations of a mycoheterotrophic rainforest orchid (Gastrodia similis), which emits an odour reminiscent of rotting fruit, indicate that it is pollinated by a single drosophilid fly species (Scaptodrosophila bangi). We investigated the roles of floral volatiles and the dimensions of the trap chamber in enforcing this specialization, using gas chromatography-mass spectrometry analyses, bioassays and scanning electron microscopy. We showed that G. similis flowers predominantly emit three fatty-acid esters (ethyl acetate, ethyl isobutyrate and methyl isobutyrate) that were shown in experiments to attract only Scaptodrosophila flies. We additionally showed that the trap chamber, which flies enter into via a touch-sensitive 'trapdoor', closely matches the body size of the pollinator species S. bangi and plays a key role in pollen transfer. Our study demonstrates that specialization in oviposition site mimicry is due primarily to volatile chemistry and is reflected in the dimensions of the trapping apparatus. It also indicates that mycoheterotrophic plants can be specialized both on mycorrhizal fungi and insect pollinators.
© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.
... Rewarding mutualisms in Araceae are pollination interactions that involve a food reward, such as stigmatic exudates, small amounts of nectar (Vogel and Martens 2000;Diaz and Kite 2006), or liquid floral perfume for male euglossine bees (Hentrich et al. 2007(Hentrich et al. , 2010. Mating/oviposition site mutualisms involve flies or beetles that mate or oviposit in the inflorescences (Gibernau et al. 1999;Sakai 2002;Urru et al. 2010;our Table S2). Antagonistic interactions involve the attraction and trapping of pollinators without either a food reward or a suitable site for larval development (Urru et al. 2011). ...
Most plant/pollinator interactions are mutualistic, involving rewards provided by flowers or inflorescences to pollinators. Antagonistic plant/pollinator interactions, in which flowers offer no rewards, are rare and concentrated in a few families including Araceae. In the latter, they involve trapping of pollinators, which are released loaded with pollen but unrewarded. To understand the evolution of such systems, we compiled data on the pollinators and types of interactions, and coded 21 characters, including interaction type, pollinator order, and 19 floral traits. A new phylogenetic framework comes from a matrix of plastid and new nuclear DNA sequences for 135 species from 119 genera (5342 nucleotides). The ancestral pollination interaction in Araceae was reconstructed as probably rewarding albeit with low confidence since information is available for only 56 of the 120-130 genera. Bayesian stochastic trait mapping showed that spadix zonation, presence of an appendix, and flower sexuality were correlated with pollination interaction type. In the Araceae, having unisexual flowers appears to have provided the morphological precondition for the evolution of traps. Compared with the frequency of shifts between deceptive and rewarding pollination systems in orchids, our results indicate less lability in the Araceae, probably because of morphologically and sexually more specialized inflorescences. This article is protected by copyright. All rights reserved.
The chapters open with theories of insect–plant association where several theories were discussed. A flow chart of coevolution of plants and insects from the evolution point of view is given with a special note on “hexapod gap.” The structural and functional coevolution of insects in relation to plant evolution is briefly discussed. Evolution of herbivory in insects considering plant as the source of food material to insects and several theories of insect herbivory has been outlined and discussed. Role of insects belonging to different orders, as principal pollinator agent of several terrestrial cross-pollinated plants is reviewed under “Entomophily.” A brief note on deceptive pollination in insects is also touched upon. Plants through the process of evolution has learnt to defend themselves from herbivore attack particularly insects and accordingly role of plant secondary metabolites as a defense against insect herbivore has been discussed in length. Several plant secondary metabolites, their by-products and their role as defense against insect herbivore has been discussed in length.KeywordsCoevolution theoriesCoevolution of plants and insectsMonophagyPolyphagyFeeding strategiesNitrogen limitation theoryStress hypothesisClimate release hypothesisPlant vigor hypothesisEntomophilyFig-wasp associationDeceptive pollinationTerpenesPhenolsAlkaloidsCyanogenic glucosidesGlucosinolatesLectinsNon-protein amino acids
Allium is a large monocotyledonous genus, with many species of high economic importance. Knowledge of the pollination biology and the chemical ecology of pollination in this genus is far from being complete. We studied flower visitors of some Allium species in their native habitat and how these interaction partners communicate by olfactory cues. Floral volatiles of five Mediterranean species were investigated by dynamic headspace and thermal desorption-gas chromatography/mass spectrometry. Floral visitors were observed and captured. The physiological activity of scent components in antennae of flower visitors and congeneric species was tested by gas chromatographic/electroantennographic detections. In the scent samples of the five species, 36 volatile organic compounds (VOCs) were detected. The species-specific scent profiles were dominated either by one or two aromatic compounds, or by a monoterpene. We recorded several insects on the flowers/ inflorescences of the different Allium species, mainly bees and flies, with only a few visitor taxa shared among the studied species. In the physiological measurements, specific/congeneric visitors did not only respond to VOCs of the species they visited, but also to VOCs of species on which they were not recorded. Our study shows that inflorescence scent and visitor patterns do not correlate, and that although single visitors detected compounds of various Allium species, there was only a limited overlap in visitor spectrum among the species. Our study also adds several compounds to the list of floral scents being EAD-active in bees and flies.
Deceptive orchids typically employ food or sexual deception of male insects. Brood-site deception, when flowers are pollinated by female flies fooled into attempting oviposition, is less well characterized for orchids but is probably common among New Zealand terrestrial orchid species. Helmet orchids (Corybas, Nematoceras and related genera) are considered specialist brood-site deceivers that mimic mushrooms and are pollinated by ovipositing female fungus gnats (Mycetophilidae). We monitored pollination in the endemic spurred helmet orchid, Corybas cheesemanii, and trapped insects visiting orchids and sympatric mushrooms. Flowering occurred from mid-May to early July, each flower lasted 23.14 d, 78.5% of the population flowered (147/194 plants), and c.25% of these set seed naturally (50% of bagged orchids set seed via autonomous self-pollination). Traps caught mostly flies (Mycetophilidae, Anisopodidae and Lauxaniidae), but orchid, mushroom and control traps did not attract significantly different fauna. Seven mycetophilids (of both sexes) visited both orchids and mushrooms, but we found no compelling evidence that C. cheesemanii was pollinated by these. Only some mycetophilid individuals caught above orchids were small enough to enter orchids, but none carried orchid pollinia. If C. cheesemanii is fungus gnat-pollinated, the range of species and sexes attracted suggests a more generalist pollination strategy than assumed.
A gas chromatographic detector is described which uses an insect antenna as a sensing element and permits the continuous monitoring of pheromones and other compounds with olfactory activity. In high resolution gas chromatography allowing separations of positional and geometrical isomers, the electroantennographic detector gives precise information on the retention times of active compounds and permits the analysis of insect pheromones with exceedingly small amounts of material.
This study describes the interaction between Hormathophylla spinosa, a crucifer shrub, and its pollinators, analyzing the spatiotemporal variability of the pollinator assemblage as well as the foraging behavior and effectiveness of the common pollinators. The study was carried out in the high mountains of the Sierra Nevada, Spain, over four years (1988-1991). We selected three populations of H. spinosa located along a wide altitudinal gradient. This plant species was visited during the four years of the study by at least 70 species of insects belonging to five orders and 19 families. The assemblage of floral visitors of H. spinosa was composed mainly of ants and different species of solitary bees and flies, although most pollinators were comparatively rare. There were striking similarities between most pollinator species in the distributions of flight distance between consecutive flowers, which were leptokurtic and highly skewed. Moreover, almost all visitors acted as pollinators, depositing pollen grains enough for seed production. Insects visiting flowers of H. spinosa can be divided into two guilds: nectarivores (small flies and ants) and pollinivores (bees and hoverflies), which differ in pollination attributes. Flower-visitation rates were quite different between the faster pollinivores and the slower nectarivores. All nectarivorous species moved almost exclusively between flowers of the same plant, whereas pollinivores sometimes moved between plants; and pollinivores deposited more pollen grains per visit than did nectarivores. H. spinosa interacted most frequently with the nectarivorous Proformica longiseta, Fannia scalaris, and Exechia dorsalis in the two lowest elevation populations of Sierra Nevada, and with the pollinivorous Colletes sp. and Eristalis tenax in the highest elevation population. The mutualistic interaction between H. spinosa and its pollinators is a generalized system, where the traits of the flower allow almost every floral visitor to act as a true, effective, pollinator. The lack of differences in per-visit pollination effectiveness and the functional equivalence of very different pollinators may help to maintain this generalized system.
One view of pollination systems is that they tend toward specialization. This view is implicit in many discussions of angiosperm evolution and plant-pollinator coevolution and in the long-standing concept of "pollination syndromes." But actual pollination systems often are more generalized and dynamic than these traditions might suggest, To illustrate the range of specialization and generalization in pollinators' use of plants and vice versa, we draw on studies of two floras in the United States, and of members of several plant families and solitary bee genera, We also summarize a recent study of one local flora which suggests that, although the colors of flowers are aggregated in "phenotype space," there is no strong association with pollinator types as pollination syndromes would predict. That moderate to substantial generalization often occurs is not surprising on theoretical grounds. Plant generalization is predicted by a simple model as long as temporal and spatial variance in pollinator quality is appreciable, different pollinator species do not fluctuate in unison, and they are similar in their pollination effectiveness. Pollinator generalization is predicted when floral rewards are similar across plant species, travel is costly, constraints of behavior acid morphology are minor, and/or pollinator lifespan is long relative to flowering of individual plant species. Recognizing that pollination systems often are generalized has important implications. In ecological predictions of plant reproductive success and population dynamics it is useful to widen the focus beyond flower visitors within the "correct" pollination syndrome, and to recognize temporal and spatial fluidity of interactions. Behavioral studies of pollinator foraging choices and information-processing abilities will benefit from understanding the selective advantages of generalization. In studies of floral adaptation, microevolution, and plant speciation one should recognize that selection and gene flow vary in time and space and that the contribution of pollinators to reproductive isolation of plant species may be overstated. In conservation biology, generalized pollination systems imply resilience to linked extinctions, but also the possibility for introduced generalists to displace natives with a net loss of diversity.
The flowers of Ophrys orchids mimic receptive females of usually only one pollinator species. Males of this species are attracted primarily by the odour of a flower and transfer the pollinia during so-called 'pseudocopulations' with the flowers1, 2, 3. We have found that flowers of O. sphegodes produce the same compounds and in similar relative proportions as are found in the sex pheromone of its pollinator species, the solitary bee Andrena nigroaenea. Common straight-chain saturated and unsaturated hydrocarbons are the key components in this chemical mimicry, which seems to be an economical means of pollinator attraction.
We studied the pollination ecology and assemblage structure of 31 species of Stylidium (Stylidiaceae) at 25 sites in Western Australia. The number of species per study site varied between two and size. Stylidium species are pollinated by a variety of nectar-seeking solitary bees and bombyliid flies. Within and among species there is significant variation in nectar-tube length (and therefore in the insects that visit the flowers) and in pollen placement on pollinators. Pollen is placed "explosively" on the insect by a motile column of fused staminate and pistillate tissues; the position and reach of the column varies within and among species, thereby causing variation in site of pollen deposition. When discrete pollination niches were defined for all species, only one niche overlap was observed across the 86 interacting pairs of Stylidium species at the 25 sites. To determine whether this was a nonrandom assemblage structure we compared our observation with the outcome of null models. We developed three null models to cover the most likely structuring processes: that communities are organized by (1) ecological sorting, (2) evolution of plant phenotypes, or (3) both processes. We concluded that it was unlikely (P = .055-.002) that so few overlaps in pollination niches would occur by chance. We developed another null model to test whether chance could have created the apparent pattern of character displacement in pollination niches exhibited by the nine species showing intraspecific variation. The analysis indicated that character displacement has probably occurred (P = .014). This study is one of the clearest demonstrations to date of reproductive interactions generating assemblage structure and character displacement in plants.
The pollination ecology of Arum italicum was studied in south-western France. This plant attracts olfactory dung-breeding flies through deceit. These insects are principally represented by Diptera, all belonging to saprophyte families. The volatilization of the odouriferous compounds, responsible for their attraction, is achieved through the production of heat by the appendix. The insects are trapped for 24 h in order to participate in both sexual phases of the protogynous inflorescence. The male flowers produce three heat events during flowering. These peaks of heat seem to be involved in the spathe movements, since they occur during the opening of the inflorescence and the liberation of the insects. The last male heat event may be linked with the liberation of pollen and its dispersion by stimulating trapped flies. According to their frequency and pollen-load, two Psychoda species appear to be the most efficient pollinators (P. crassipenis and P. pusilla). Nevertheless, each of the other attracted species could play a significant role under different spatio-temporal conditions. Experiments on self-pollination have shown that obligate cross-pollination is necessary for A. italicum to set seeds. Moreover, hand- and natural-pollinated plants showed similarly high abortion frequencies suggesting that seed set may be more constrained by resources rather than by pollination limitation. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 141, 205–214.
The relationship between flowering time and reproductive success was investigated in the fly-pollinated, monoecious perennial
herb Arum maculatum L. (Araceae). This species temporarily traps its principle pollinator, a psychodid midge. Probability of fruit set was analysed
in relation to early, peak and late periods of the flowering phenology of four British populations between 1992 and 1997.
In three out of five cases, plants which flowered during early and late periods were significantly less likely to set fruit.
In addition, one population showed a similar relationship for percentage fruit set of individual inflorescences, and seeds
from peak-flowering plants were significantly heavier. There was no variation in number of female flowers per inflorescence
over the flowering season. Probability of fruit set appears to be mediated by the likelihood of trapping psychodid midges
that have previously been trapped and picked up pollen, an unlikely event during early and late flowering periods when few
inflorescences are open. The majority of plants in all populations produce only one inflorescence which means that timing
of flowering may be crucial to reproductive success. We interpret our findings as evidence that stabilising selection may
be acting on some populations and/or during some years. The ultimate cause, however, can be related to the very short (12–18 h)
female phase of each inflorescence, a phylogenetically conservative trait within the Araceae.
For centuries the wonderful looking, but foul smelling, Arum lilies have fascinated botanists. The floral odour of many species is believed to mimic faeces-the oviposition substrate of their pollinators, mainly coprophilous flies and beetles. But not all of the 29 Arum species produce a bad floral smell. The genus has evolved a variety of pollination mechanisms, including sweet and wine-like odours, and maybe even pheromone mimicry. In order to study the evolution of the pollination syndromes in Arum, a detailed and reliable phylogeny is a crucial basis. Here we present the first detailed molecular phylogeny of the genus Arum. By combining three chloroplast and one nuclear loci, as well as AFLPs, a highly resolved tree with good statistical support was obtained. The phylogeny is in most parts in congruence with the traditional classification of the genus. By comparing the phylogeny with the data on the pollination biology of the genus we could show that the mimicry of faeces is the oldest and most basal pollination mechanism, but is also present in the youngest and most derived species. The phylogeny presented here will help to study the evolution of deceptive pollination mechanisms in Arum.
The concept of a generalist flower appears to mean different things to different people, depending upon their background and training. We assess the different meanings of generalist flowers with respect to the ecological "set and setting" of pollination, and then we discuss notions of ecological, functional and phenotypic generalization. These ideas are explored in more detail using examples from our own published and unpublished studies on the pollination ecology of Daucus carota, Hedera helix, and Chamerion angustifolium, and from the published work of other researchers. Finally we relate these ideas and clarified definitions of "generalist" and "specialist" flowers to the pollination syndrome concept.
Approximately one-third of the world's estimated 30,000 orchid species are deceptive and do not reward their pollinators with nectar or pollen. Most of these deceptive orchids imitate the scent of rewarding flowers or potential mates. In this study, we investigated the floral scent involved in pollinator attraction to the rewardless orchid Dendrobium sinense, a species endemic to the Chinese island Hainan that is pollinated by the hornet Vespa bicolor. Via chemical analyses and electrophysiological methods, we demonstrate that the flowers of D. sinense produce (Z)-11-eicosen-1-ol and that the pollinator can smell this compound. This is a major compound in the alarm pheromones of both Asian (Apis cerana) and European (Apis mellifera) honey bees and is also exploited by the European beewolf (Philanthus triangulum) to locate its prey. This is the first time that (Z)-11-eicosen-1-ol has been identified as a floral volatile. In behavioral experiments, we demonstrate that the floral scent of D. sinense and synthetic (Z)-11-eicosen-1-ol are both attractive to hornets. Because hornets frequently capture honey bees to feed to their larvae, we suggest that the flowers of D. sinense mimic the alarm pheromone of honey bees in order to attract prey-hunting hornets for pollination.
Deceit by resource mimicry has evolved as a pollination strategy in several plant species and is particularly elaborate in a plant known as dead-horse arum (Helicodiceros muscivorus; Araceae: Aroideae), which may fool flies into pollinating it by emitting a smell like a dead animal - an important oviposition resource for these insects. Here we confirm that the composition of volatiles from these flowers and from a rotting carcass is strikingly similar and show that the pollinators respond in the same way to chemicals from both sources. This remarkably complex mimicry must have evolved to exploit insects as unrewarded pollinators.
The "sexually deceptive" orchid Chiloglottis trapeziformis attracts males of its pollinator species, the thynnine wasp Neozeleboria cryptoides, by emitting a unique volatile compound, 2-ethyl-5-propylcyclohexan-1,3-dione, which is also produced by female wasps as a male-attracting sex pheromone.
The dead horse arum, Helicodiceros muscivorus, is a conspicuous, foul smelling and thermogenic plant of the Araceae family. This Mediterranean arum lily copies several aspects of a carcass in order to attract carrion blowflies, which are subsequently exploited as unrewarded pollinators. We have previously shown that this plant exhibits a highly accurate olfactory carrion mimicry, which serves to attract the blowflies. In this study, we have investigated the role of thermogeny in the arum. We show that the thermogeny has a direct effect on the pollinators, altering their behaviour. By manipulating heat and odour release of the plant, we can show that the heat, produced along the appendix, is important to lure the flies to this structure, which is vital as the flies from the appendix are more prone to enter the trap chamber that houses the female and male florets. This study provides rare evidence for a direct functional role of thermogeny.
For centuries the wonderful looking, but foul smelling, Arum lilies have fascinated botanists. The floral odour of many species is believed to mimic faeces—the oviposition substrate of their pollinators, mainly coprophilous flies and beetles. But not all of the 29 Arum species produce a bad floral smell. The genus has evolved a variety of pollination mechanisms, including sweet and wine–like odours, and maybe even pheromone mimicry. In order to study the evolution of the pollination syndromes in Arum, a detailed and reliable phylogeny is a crucial basis. Here we present the first detailed molecular phylogeny of the genus Arum. By combining three chloroplast and one nuclear loci, as well as AFLPs, a highly resolved tree with good statistical support was obtained. The phylogeny is in most parts in congruence with the traditional classification of the genus. By comparing the phylogeny with the data on the pollination biology of the genus we could show that the mimicry of faeces is the oldest and most basal pollination mechanism, but is also present in the youngest and most derived species. The phylogeny presented here will help to study the evolution of deceptive pollination mechanisms in Arum.
Learning can enable an animal to find and use its resources more efficiently (Papaj and Prokopy, 1989), but what are the consequences of learning for the evolution of the resource organism? If the resource loses fitness, selection should favor protective or escape mechanisms. If the resource benefits from use, selection should favor traits that make it easier to find and use. An examination of a classic mutualism—the flowering plants and their pollinators—reveals that these simple scenarios do not always hold: flowers advertise their presence, as one would expect, but they hide their rewards. Why?
(1) The pollinating efficiency of moths was examined during four seasons by counting the number of pollen grains that individual moths deposited on the stigmas of virgin female flowers of Silene vulgaris. (2) Experimental pollination showed that c. 150 pollen grains per flower were required to achieve the average natural full seed-set in the plant population. Although 57% of the flower-visiting moths deposited pollen, only about 10% of the moth visits delivered ⩽ 150 pollen grains in one visit to virgin female flowers, indicating that seed-set usually originated from multiple pollinator visits. (3) Pollen receipt indicated pollination by a guild of noctuid and sphingid moths. The abundance of the dominating pollinator species varied strongly between years. (4) Most species deposited about the same mean number of pollen grains, although they were taxonomically diverse and had different flower-visiting behaviours and proboscis lengths. Even noctuid moths of the genus Hadena, known as associated larval seed predators of S. vulgaris, were not especially frequent or efficient pollinators despite the fact that these moths influence their larval food resource through pollination. (5) The annual and seasonal variation in abundance among pollinator species and lack of variation in pollination efficiency among them are factors which counteract specializational trends and control evolutionary retention of plastic and unspecialized floral traits in S. vulgaris. They thereby provide an option for opportunistic responses in this species.
Pollination by the sexual attraction of male insects to non-food rewarding flowers is unique to the orchids. Thynnine wasps are exploited in this manner by more orchid species than any other insects. Experiments were conducted on the mating behaviour of male Zaspilothynnus trilobatus during encounters with the female and the orchid Drakaea glyptodon. The flightless female called for mates by releasing a sex pheromone. Winged males responded rapidly to calling females, locating and carrying away 61% of them within the first minute. All females were taken within 5 min. Similarly. males quickly located experimentally presented flowers with a peak rate of visits occurring within the first minute. Pollination requires the wasps to grasp the flowers but not copulate or ejaculate. While 93% of the wasps landed on flowers, <21% attempted to grasp the female decoy, 6% of males attempted copulation with the flower and ejaculation was never observed. Some flowers were preferentially attractive. Males immediately leave the area after visiting a flower and do not visit nearby flowers within a refractory period. Males moved up to 132 m (mean of 32 m) in their search for females. In larger populations of the orchid, distances of pollen flow could be an order of magnitude greater than food-based pollination systems. -from Author
Since Delpino (1868-74) recognized that flowers sharing similar physiognomies are preferentially visited by certain groups of animals, it has been commonly inferred that these biological groups (flowers and pollinators) have passed a more or less complicated evolutionary process of mutual specialization. The question, however, as to what were the initial angiosperm floral forms remains unanswered. Whatever the form, a broad spectrum of visitors was likely. Each organism needs to be adapted to its environment, for which reason the term "generalized" instead of "non-specialized" is to be preferred. Generalized flowers occur even in otherwise highly evolved families, suggesting that these representatives have developed secondarily from a somewhat specialized pollination type; this points to the fact that "generalized" and "specialized" are relative terms. It also means that a generalized flower is not synonymous with a "primitive flower"! In terms of morphology, the original "primitive flower" form is a subject of debate. Neither in the fossil records nor among extant, archaic angiosperms is there a model organism bearing a flower with a broad spectrum of visitors, and which exhibits all organs in their plesiomorphic state. Nor is it likely that such a plant will ever be discovered. Thus, we must be content with a relative solution; there is one—hitherto only one—magnolioid family, the Winteraceae, some members of which approach the idealized model. Representatives of this family are characterized by many plesiomorphic features and have open flowers visited by a broad spectrum of pollen vectors. An explanation of how these plants could have remained in this generalized condition over long time periods is offered.
S ummary
The distribution of pollen upon the insect‐visitors to three species of Viola is described and correlated with their feeding and cleaning behaviour. Visitors adopt one of two basic positions while feeding. In the prone position the insect alights on the anterior petal and probes for nectar so that its dorsal surfaces contact the floral genitalia. The supine position may be adopted after alighting on the anterior petal when the insect rotates so that it is virtually standing on its head. While probing for nectar from this position it is the ventral surfaces which contact the floral genitalia. Bumblebees adopt either feeding position; many large solitary bee species almost invariably adopt the supine one while large hoverflies always feed from the prone position. The behaviour of short‐tongued visitors tends to be highly individual with respect to contact with the floral genitalia and many body surfaces may be involved.
The varying activities of insect‐visitors while feeding result in the deposition of pollen at different locations on the integument. Consequently insect‐borne pollen is presented to the stigma in various ways and there is a spectrum of pollination effects: medium and long‐tongued nectar‐seeking insects tend to be systematic cross‐pollinators while short‐tongued or pollengathering species tend to be chance cross‐ or self‐pollinators.
The cleaning behaviour of insect‐visitors strongly influences pollination as it removes much integumental pollen. Two requirements of the pollen deposition mechanism are postulated: that pollen should be placed (a) in a position not occupied by foreign pollen and (b) in a position irregularly or inefficiently cleaned. There were no positions which were free of foreign pollen throughout the visitor‐species. On the other hand, violet pollen was found to be concentrated at locations inaccessible to the cleaning mechanism.
Systematic cross‐pollination results from the visits of a variety of insects with proboscides over 5 mm long including bumblebees, honeybees, solitary bees, hoverflies and beeflies, therefore, the violet flower is not simply a ‘bee flower’ as previously supposed. The widespread practice of generalizing on the role of insect‐visitors in pollination is questioned and the error in labelling flowers according to the taxonomic position of their pollinators is pointed out; the greater relevance of the morphological and behavioural characteristics of the insect‐visitors is emphasized.
Differences in the floral genitalia of these Viola spp. may reflect a shift from allogamy to facultative autogamy which, in turn, may be a response to a paucity of pollinators at certain seasons. However, the diverse range of pollinators may maintain some out‐crossing by the least efficient but more abundant short‐tongued pollinators.
The diversity of pollinators, therefore, provides a mechanism whereby a sexual system can simultaneously produce variation and invariance. The evolutionary versatility of a mating system incorporating this mechanism may have been partially responsible for the success of the genus Viola throughout the temperate regions of the world.
It has been debated whether pollination success in nonrewarding plants that flower in association with nectar-producing plants will be diminished by competition for pollinator visits or, alternatively, enhanced through increased local abundance of pollinators (the magnet species effect). We experimentally evaluated these effects using the nonre-warding bumblebee-pollinated orchid Anacamptis morio and associated nectar-producing plants at a site in Sweden. Pollination success (estimated as pollen receipt and pollen removal) in A. morio was significantly greater for individuals translocated to patches of nectar-producing plants (Geum rivale and Allium schoenoprasum) than for individuals placed outside (20 m away) such patches. These results provide support for the existence of a facilitative magnet species effect in the interaction between certain nectar plants and A. morio. To determine the spatial scale of these interactions, we correlated the visitation rate to flowers of A. morio with the density of sympatric nectar plants in 1-m 2 and 100-m 2 plots centered around groups of translocated plants, and at the level of whole meadows (0.5–2 ha). Visitation rate to flowers of A. morio was not correlated with the 1-m 2 patch density of G. rivale and A. schoenoprasum, but showed a significant positive relationship with density of these nectar plants in 100-m 2 plots. In addition, visitation to flowers of A. morio was strongly and positively related to the density of A. schoenoprasum at the level of the meadow. Choice experiments showed that bees foraging on the purple flowers of A. schoenoprasum (a particularly effective magnet species) visit the purple flowers of A. morio more readily (47.6% of choices) than bees foraging on the yellow flowers of Lotus cor-niculatus (17% of choices). Overall similarity in flower color and shape may increase the probability that a pollinator will temporarily shift from a nectar-producing ''magnet'' plant to a nonrewarding plant. We discuss the possibility of a mimicry continuum between those orchids that exploit instinctive food-seeking behavior of pollinators and those that show an adaptive resemblance to nectar-producing plants.
Plant species of the genus Arum typically have lure-and-trap pollination systems that are saprophilous (i.e. attracting flies or beetles searching for breeding sites in decaying organic matter). They have been assumed to always attract and trap their pollinators by deception because the inflorescences provide unsuitable breeding grounds for pollinators. The present study explored the possibility that one species, Arum creticum Boiss. & Heldr., which has yellow, sweet-smelling inflorescences, rewards its pollinators and that this increases its success in attracting pollinators over its close relative, Arum idaeum Coust. & Gadoger. The relationship between rewards provided, floral structure, insect attraction, and pollen import and export was examined in two naturally occurring sympatric populations of A. creticum, A. idaeum, and their natural hybrids. The results showed that plants providing more pollen were visited by larger numbers of females of a mining bee Lasioglossum marginatum Brullé as well as adults and nymphs of a hemipteran bug Dionconotus cruentatus creticus Heiss. In A. creticum, L. marginatum was found to be a better outcrossing vector than D. cruentatus in areas where both pollinators occurred because L. marginatum individuals carried more pollen on their bodies and travelled greater distances between inflorescences, thus increasing the potential for outcrossing. The finding that floral rewards may result in increased fitness, compared to nonrewarding systems that rely on attracting saprophilic pollinators, suggests that it is possible for rewarding species to evolve from saprophilous systems. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 257–268.
Non-invasive headspace analyses of the odour produced by inflorescences of Arum maculatum L. still attached to plants growing wild in southern England revealed that the major components were 2-heptanone, indole (each comprising 8–23% of the volatiles) and germacrene B (10–14%). p-Cresol (0.2–6%) was also a notable odorous component amongst the 56 compounds present, however, simple amines, reported in previous invasive studies, could not be detected. Although the major odorous organ was the spadix appendix, microheadspace analyses revealed that the germacrene B originated entirely within the spathe chamber, probably from the fertile portion of the spadix. The main pollinator was confirmed as females of Psychoda phalaenoides L. and a comparison of the inflorescence volatiles with those produced by cow dung, the normal breeding microhabitat of the pollinator, identified p-cresol as the major common component.
The majority of species of flowering plants rely on pollination by insects, so that their reproductive success and in part their population structure are determined by insect behaviour. The foraging behaviour of insect pollinators is flexible and complex, because efficient collection of nectar or pollen is no simple matter. Each flower provides a variable but generally small reward that is often hidden, flowers are patchily distributed in time and space, and are erratically depleted of rewards by other foragers. Insects that specialise in visiting flowers have evolved an array of foraging strategies that act to improve their efficiency, which in turn determine the reproductive success of the plants that they visit. This review attempts a synthesis of the recent literature on selectivity in pollinator foraging behaviour, in terms of the species, patch and individual flowers that they choose to visit.
Inflorescences of arum lilies have a three-part spadix with a scent-producing, sterile appendix above two bands of fertile male and female florets. The appendix and male florets are thermogenic, but with different temporal patterns. Heat-production was measured in Arum concinnatum, A. creticum and A. idaeum. The male florets of A. concinnatum showed a 3 d continuous episode of thermogenesis with three waves, and the appendix warmed in a single, 6 h episode. Maximum fresh-mass-specific CO(2) production rate was 0.17 micromol s(-1) g(-1) to achieve a 10.9 degrees C temperature elevation by the appendix, and 0.92 micromol s(-1) g(-1) to achieve a 4.8 degrees C elevation by male florets. Reversible, physiological temperature regulation was not evident in either tissue. Respiration increased with tissue temperatures with Q(10) values of 1.8-3.9, rather than less than 1.0 as occurs in thermoregulatory flowers. Experimental step changes in temperature of appendix and male floret tissues also failed to show thermoregulatory responses. The patterns of thermogenesis therefore appear to be fixed by the temporal sequence of blooming. Thermogenesis in the alpine species, A. creticum and A. idaeum, was significantly lower than in the lowland A. concinnatum, possibly related to difficulty in raising floral temperature in their cold and windy habitat.
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