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(3S,6E)-Nerolidol-Mediated Rendezvous of Cyclocephala Paraguayensis Beetles in Bottle Gourd Flowers

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(3S,6E)-Nerolidol-Mediated Rendezvous of Cyclocephala Paraguayensis Beetles in Bottle Gourd Flowers PLOS ONE RESEARCH ARTICLE (3S,6E)-nerolidol-mediated rendezvous of Cyclocephala paraguayensis beetles in bottle gourd flowers 1 1 1 2 Arodõ P. FavarisID , Amanda C. Tu lerID , Weliton D. SilvaID , SeÂrgio R. Rodrigues , Walter 3 1 S. LealID *, Jose M. S. BentoID 1 Department of Entomology and Acarology, ªLuiz de Queirozº College of Agriculture, University of São Paulo (USP), Piracicaba, São Paulo, Brazil, 2 State University of Mato Grosso do Sul, CassilaÃndia, Mato Grosso do Sul, Brazil, 3 Department of Molecular and Cellular Biology, University of California, Davis, California, United States of America * [email protected] a1111111111 a1111111111 Abstract a1111111111 a1111111111 Cyclocephalini beetles of the genus Cyclocephala (Coleoptera: Melolonthidae: Dynastinae) a1111111111 use flowers of some plants as food, shelter, and mating sites. However, little is known about floral scent chemistry involved in this interaction. Here we show that a sesquiterpene alcohol mediates attraction of Cyclocephala paraguayensis Arrow, on bottle gourd flowers, Lagen- aria siceraria (Cucurbitaceae). Both males and females started to aggregate on the flowers OPEN ACCESS at twilight; after that, mating began and remained for the entire night. GC-FID/EAD analysis Citation: Favaris AP, TuÂler AC, Silva WD, of the L. siceraria floral scent collected in the field revealed that only the major constituent of Rodrigues SR, Leal WS, Bento JMS (2020) the airborne volatiles elicited electroantennographic responses on male and female anten- (3S,6E)-nerolidol-mediated rendezvous of nae of C. paraguayensis. This compound was identified as (3S,6E)-nerolidol, which was Cyclocephala paraguayensis beetles in bottle gourd flowers. PLoS ONE 15(12): e0235028. https://doi. tested in two field trapping trials in Brazil. In the first bioassay, traps baited with nerolidol org/10.1371/journal.pone.0235028 (mix of isomers) captured significantly more adult C. paraguayensis than control traps. In Editor: Guy Smagghe, Ghent University, BELGIUM the second field trial, catches in traps baited with a mixture of isomers or enantiopure neroli- dol were significantly higher than captures in control traps, but the treatments did not differ Received: June 6, 2020 significantly. Analysis from the gut content of adult C. paraguayensis showed the presence Accepted: November 29, 2020 of pollen, suggesting that they also use bottle gourd flowers for their nourishment. Taken Published: December 23, 2020 together, these results suggest that (3S,6E)-nerolidol plays an essential role in the repro- Copyright: © 2020 Favaris et al. This is an open ductive behavior of C. paraguayensis by eliciting aggregation, mating, and feeding. access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All data are contained Introduction in the manuscript. Floral scents have been reported as essential assets for the visitation of beetles of the tribe Funding: This research was supported by INCT- Cyclocephalini (Melolonthidae: Dynastinae) [1±4]. The interaction of beetles and flowers may SemioquõÂmicos na Agricultura (FAPESP 2014/ result in mutualistic pollination typically by the cantharophilous floral syndrome of basal 50871-0 and CNPq 465511/2014-7). angiosperms, whose flowers are usually bisexual, protogynous, very scented, and thermogenic Competing interests: The authors declare no [4, 5]. The Cyclocephalini beetles are primarily attracted by strong odors released by flowers as conflict of interest. chemical cues to indicate a rendezvous site for food, shelter, and mating sites [4, 6, 7]. PLOS ONE | https://doi.org/10.1371/journal.pone.0235028 December 23, 2020 1 / 13 PLOS ONE Nerolidol-mediated rendezvous of Cyclocephalini beetles The floral volatile organic compounds (VOCs) in the plant families of Araceae, Annona- ceae, Arecaceae, and Magnoliaceae, have been demonstrated to be comprised of pyrazines, ketones, esters, and methoxystyrenes [8±13]. The qualitative chemical profile of theses VOCs has shown little complexity, dominated by uncommon and non-related compounds that are sufficient to ensure the attraction of beetles, which display an efficient olfactory recognition that evokes a specific plant-pollinator interaction [13, 14]. By contrast, VOCs produced by eudicot flowers that are visited by Cyclocephalini beetles of the genus Cyclocephala have never been identified. It has been suggested that some cyclocepha- lines of the genus Cyclocephala are opportunistic eudicot flower visitors, causing at times dam- ages on flower tissues due to feeding and, therefore, compromising the reproductive capability of the plant [3]. However, this hypothesized unspecific attraction is still poorly understood. It has been hypothesized that the detection of floral odors of eudicot plants by Cyclocephala bee- tles could be an acquired preference from larval feeding habitat in the case of roots having a taste similar to that of flowers, thus, preconditioning insects to the adult stage [15]. Alternately, Cyclocephala beetles might visit eudicot plants because flowers, which could be releasing com- pounds commonly found in insect volatiles, as preconized by the hypothesis of pre-existing sensory bias [16, 17]. That means the beetles have developed olfactory sensibility to recognize floral scents which are based on chemicals already produced by the insects for intraspecific communication. Cyclocephala paraguayensis Arrow, is a Neotropical species that is frequently found on eudicot plant species [15, 18]. Here, we observed this beetle visiting flowers of Lagenaria sicer- aria (Molina) Standle (Cucurbitaceae), which incidentally represents a new host flower record for the beetle family Melolonthidae. This plant is originated from Africa and is now spread worldwide [19]; it produces white flowers with separate sexes in the same plant (monoecious) but can assume andromonoecious form when hermaphrodite flowers are present [20]. Anthe- sis occurs throughout the night, at which time lepidopteran pollinators, specially hawkmoths, visit the flowers [21]. We surmised that the volatile components of bottle gourd flowers mediate aggregative behavior of C. paraguayensis for feeding and mating. We studied the floral scent chemistry of L. siceraria flowers and showed that (3S,6E)-nerolidol plays an essential role in the reproduc- tive behavior of C. paraguayensis by eliciting aggregation, mating, and feeding. Results Sexual and feeding behavior of insects The behavior of C. paraguayensis visitation on L. siceraria flowers was observed under field conditions at night for four hours (7:00 p.m. to 11:00 p.m.). Beetles activity started by the twi- light (~7:30 p.m.), when males of C. paraguayensis were the first to land on L. siceraria flowers (n = 36; two-tailed Exact Binomial test; P = 0.011). At 8:00 p.m., the number of visiting males and females was 18.50 ± 5.97 (mean ± SD), increasing until 11:00 p.m. to 26.75 ± 7.46. Paired males and females of C. paraguayensis (2.25 ± 3.2) were present on bottle gourd flowers from 8:00 p.m. until the end of observation period. Both sexes of L. siceraria flowers were visited. Seventy-five percent of bottle gourd flowers harbored more than one mating couple, thus, sug- gesting that aggregation on bottle gourd flowers created mating opportunities for the beetles. These Cyclocephalini beetles usually remained inside the floral receptacles until the next morning, when they were sheltered (Fig 1A and 1B). Bottle gourd flowers presented gnawing marks or even major damages resulted from beetles feeding (Fig 1E and 1F). Of note, pollens of these flowers were found in the gut of beetles (80% females; 50% males, n = 10) when dis- sected (Fig 1G and 1H). PLOS ONE | https://doi.org/10.1371/journal.pone.0235028 December 23, 2020 2 / 13 PLOS ONE Nerolidol-mediated rendezvous of Cyclocephalini beetles Fig 1. Sexual and feeding behavior of Cyclocephalini beetle, Cyclocephala paraguayensis, in bottle gourd flowers, Lagenaria siceraria. A) aggregating and mating on flowers at night; B) C. paraguayensis inside senescent flowers in the next morning of PLOS ONE | https://doi.org/10.1371/journal.pone.0235028 December 23, 2020 3 / 13 PLOS ONE Nerolidol-mediated rendezvous of Cyclocephalini beetles beetleÂs attraction; C) Non-damaged L. siceraria flower in the field; D) Stereoscopic cut view of a non-damaged L. siceraria flower; E) L. siceraria flower damaged by C. paraguayensis in the field; F) Stereoscopic cut view of a damaged flower showing beetle gnawing and excrement signal as a result of feeding activity; G) Fresh pollen grain of L. siceraria; H) Pollen grains of L. siceraria extracted from C. paraguayensis gut (black triangles indicate the pollen grains). https://doi.org/10.1371/journal.pone.0235028.g001 Floral scent identification Gas chromatography linked to electroantennographic detection (GC-EAD) analysis of air- borne volatiles collected from L. siceraria showed the presence of a prominent, antennally active peak at 20.5 min (Fig 2). The correspondent compound was tentatively identified by GC-MS as a nerolidol isomer, which led us to conduct cis and trans identification followed by chiral analysis. The EAD active compound was then identified as trans-nerolidol (i.e., (6E)-nerolidol, IR = 1568) by comparing the mass spectra and retention indexes of the natural product and authentic standards (Fig 3A±3F). Lastly,
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