Evidence for the recruitment of florivorous plant bugs as pollinators.

Angiosperm flowers and their animal visitors have co-evolved for at least 140 Ma, and early flowers were likely used mainly as mating and feeding sites by several groups of insects, including beetles, flies, true bugs, and thrips. Earlier studies suggested that shifts from such neutral or antagonistic relationships toward mutualistic pollination interactions between flowers and insects occurred repeatedly during angiosperm evolution. However, the evolutionary mechanisms and adaptations, which accompanied shifts toward effective pollination, are barely understood, and evidence for such scenarios has been lacking. Here, we show that Syngonium hastiferum (Araceae), a Neotropical representative of an otherwise beetle-pollinated clade, is pollinated by plant bugs (Miridae; Heteroptera), which are florivores of Syngonium schottianum and other Araceae species. We found that S. hastiferum differs in several floral traits from its beetle-pollinated relatives. Scent emission and thermogenesis occur in the morning instead of the evening hours, and its pollen surface is spiny instead of smooth. Furthermore, the floral scent of S. hastiferum includes a previously unknown natural product, (Z)-3-isopropylpent-3-en-1-ol, which we show to have a function in specifically attracting the plant bug pollinators. This is the first known case of a specialized plant bug pollination system and provides clear evidence for the hypothesis that the adoption of antagonistic florivores as pollinators can drive flower diversification. VIDEO ABSTRACT.

Chemical Attraction of Gall Midge Pollinators (Cecidomyiidae: Cecidomyiinae) to Anthurium acutangulum (Araceae).

Flowering plants often use chemical signals to attract their pollinators, and compounds that elicit attraction are known for several groups of pollinators. For other pollinators such as gall midges, however, compounds responsible for their attraction to flowers are largely unknown. Here, we describe the pollination biology of Anthurium acutangulum, a Neotropical aroid species found to be attractive to gall midges. We collected and analyzed its floral scent by dynamic headspace collections and gas chromatography coupled to mass spectrometry, and identified compounds responsible for pollinator attraction. The inflorescences were almost exclusively visited by gall midges (females; Cecidomyiidae: Cecidomyiinae) and released a strong scent reminiscent of freshly cut cucumber, mainly (5S,7S)-trans-conophthorin, (E2,Z6)-2,6-nonadienal, and cis-conophthorin. Behavioral assays with the two most abundant compounds identified (E2,Z6)-2,6-nonadienal as being highly attractive to the female gall midge pollinators, whereas (5S,7S)-trans-conophthorin was not attractive. Overall, we introduce a new specialized gall midge pollination system and identify the chemical mediating communication between the pollinators and their host plants.

Genome Size of Life Forms of Araceae-A New Piece in the C-Value Puzzle.

The genome size of an organism is an important trait that has predictive values applicable to various scientific fields, including ecology. The main source of plant C-values is the Plant DNA C-values database of the Royal Botanic Gardens Kew, which currently contains 12,273 estimates. However, it covers only 2.9% of known angiosperm species and has gaps in the life form and geographic distribution of plants. Only 4.5% of C-value estimates come from researchers in Central and South America. This study provides 41 new C-values for the aroid family (Araceae), collected in the Piedras Blancas National Park area in southern Costa Rica, including terrestrial, epiphytic and aquatic life forms. Data from our study are combined with C-value entries in the RBGK database for Araceae. The analysis reveals a wider range of C-values for terrestrial aroids, consistent with other terrestrial plants, a trend toward slightly lower C-values for epiphytic forms, which is more consistent for obligate epiphytes, and comparatively low C-values for aquatic aroids.

Synthesis, Absolute Configurations, and Biological Activities of Floral Scent Compounds from Night-Blooming Araceae.

The uncommon jasmone derivatives dehydrojasmone, isojasmol, and isojasmyl acetate, floral scent compounds from night-blooming Araceae, were synthesized in a scalable synthesis employing conjugate addition with a selenoacetal as the key step. The stereoselective strategy with subsequent enzymatic kinetic resolution allowed determining the absolute configuration of the natural compounds by GC on a chiral phase. The homoterpene (E)-4,8-dimethyl-1,3,7-nonatrien-5-yl acetate, another uncommon scent compound, was obtained by α-regioselective aldehyde prenylation. The biological activities of dehydrojasmone and isojasmol were investigated in field assays, showing that these unique volatiles are able to selectively attract specific cyclocephaline scarab beetle pollinators.

Novel Floral Scent Compounds from Night-Blooming Araceae Pollinated by Cyclocephaline Scarabs (Melolonthidae, Cyclocephalini).

Nocturnal flowering plants often release strong scents to attract their pollinators. Among night active flower visitors are cyclocephaline scarab beetles, which have been demonstrated to respond to uncommon volatile organic compounds released in high amounts by their host plants. In Araceae, the molecular structure of several such compounds is yet to be unveiled. We investigated headspace floral scent samples of Philodendron squamiferum, Thaumatophyllum mello-baretoanum, and Xanthosoma hylaeae by a variety of approaches, leading to the identification of novel compounds. Dehydrojasmone, (Z)-4-methylene-5-(pent-2-en-1-yl)cyclopent-2-en-1-one (1), (Z)-3-methylene-2-(pent-2-en-1-yl)cyclopentyl acetate (isojasmyl acetate, 3), and (E)-4,8-dimethylnona-1,3,7-trien-5-yl acetate (4) had not been previously reported, while full analytical data of the recently described (Z)-3-methylene-2-(pent-2-en-1-yl)cyclopentan-1-ol (isojasmol, 2) are presented here. All these compounds are derived from more common precursors, (Z)-jasmone and (E)-4,8-dimethyl-1,3,7-nonatriene, likely through biosynthetic "post-processing".

Correction to: Novel floral scent compounds from night-blooming Araceae pollinated by cyclocephaline scarabs (Melolonthidae, Cyclocephalini).

The original version of this article unfortunately contained a mistake. The description of subheadings of Figs. 4c and d have to be interchanged.

Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications.

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.

Nocturnal Plant Bugs Use cis-Jasmone to Locate Inflorescences of an Araceae as Feeding and Mating Site.

Inflorescences of Araceae pollinated by cyclocephaline scarab beetles are visited frequently by a wide array of other arthropods that exploit floral resources without taking part in pollination, including earwigs, flies, and true bugs. To date, nothing is known about the cues these insect visitors use to locate the inflorescences and whether or to what extent floral scents play a role. An aroid visited by large numbers of plant bugs (Miridae) in addition to cyclocephaline scarab beetle pollinators is the Neotropical species Dieffenbachia aurantiaca. We identified the plant bug species and investigated their behavior and arrival time on the inflorescences. To test the importance of olfactory cues in locating their host we conducted experiments with open and gauze-bagged inflorescences as well as natural scent samples of D. aurantiaca. Inflorescence scents were analyzed by gas chromatography linked to mass spectrometry (GC/MS), and the attractive potential of the main scent compound was determined by behavioral assays. Three species of Neella, the most common one being N. floridula, visited the inflorescences at nightfall, shortly after the beginning of scent emission, and showed feeding and copulation activity. Bagged inflorescences as well as natural scent samples attracted similar numbers of plant bugs as the non-bagged inflorescences, showing that olfactory cues are sufficient for them to locate their host. Cis-jasmone was the major component within the inflorescence scent bouquet. In two-choice field bioassays, this compound proved to be highly attractive to Neella, and thus obviously plays a key role in finding host plants.