Volatile organic compounds influence prey composition in Sarracenia carnivorous plants

PLOS ONE RESEARCH ARTICLE Volatile organic compounds influence prey composition in Sarracenia carnivorous plants Corentin Dupont ID1, Bruno Buatois ID2☯, Jean-Marie Bessiere3☯, Claire Villemant4☯, Tom Hattermann1☯, Doris Gomez2, Laurence Gaume1* 1 AMAP, Montpellier University, CNRS, CIRAD, INRA, IRD, Montpellier, France, 2 CEFE, Montpellier University, CNRS, EPHE, IRD, Montpellier, France, 3 ENSCM, Montpellier University, Montpellier, France, 4 ISYEB, CNRS, MNHN, EPHE, Sorbonne University, Antilles University, Paris, France ☯ These authors contributed equally to this work. * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Dupont C, Buatois B, Bessiere J-M, Villemant C, Hattermann T, Gomez D, et al. (2023) Volatile organic compounds influence prey composition in Sarracenia carnivorous plants. PLoS ONE 18(4): e0277603. https://doi.org/ 10.1371/journal.pone.0277603 Editor: Renee M. Borges, Indian Institute of Science, INDIA Received: February 23, 2022 Accepted: November 1, 2022 Published: April 19, 2023 Copyright: © 2023 Dupont et al. This is an open 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: The data are available on OSF (Open Science Framework) under the link: https://osf.io/65edk/ (DOI: https://doi.org/10. 17605/OSF.IO/65EDK). Funding: This work was publicly supported by the French National Research Agency & MUSE University (ANR-16-IDEX-0006 to L.G, C.V. and D. G. under the “Investissements d’avenir” program), which funded material and plants, as well as the PhD salary of CD. The funders had no role in study Abstract Sarracenia pitcher plants display interspecific differences in prey, so far only explained by pitcher morphology. We hypothesized that pitcher odours play a role in prey composition. We first compared odour and prey compositions among Sarracenia taxa grown together, forming a kinship gradient from S. purpurea known to capture primarily ants towards S. leucophylla known to capture many flying insects: S. purpurea, S. X mitchelliana, and S. X Juthatip soper & S. X leucophylla horticultural hybrids. We then measured several pitcher traits to disentangle the contributions of morphology and odour to prey variation. The pitcher odours were as diverse as those of generalist-pollinated flowers but with notable differences among taxa, reflecting their relatedness. VOC similarity analyses revealed taxon specificities, that mirrored those revealed by prey similarity analyses. S. X leucophylla stood out by being more specialised in flying insects like bees and moths and by releasing more monoterpenes known to attract flower visitors. S. X Juthatip soper trapped as many bees but fewer moths, sesquiterpenes contributing less to its scent. Ants and Diptera were the main prey of the other two with fatty-acid-derivative-dominated scents. Quantities of the different prey groups can be inferred 98% from quantities of the odour classes and pitcher dimensions. Two syndromes were revealed: ants associated with fatty-acid-derivatives and short pitchers; flying insects associated with monoterpenes, benzenoids and tall pitchers. In S. X leucophylla, emission rate of fatty-acid-derivatives and pitcher length explained most variation in ant captures; monoterpenes and pitcher length explained most variation in bee and moth captures; monoterpenes alone explained most variation in Diptera and wasp captures. Our results suggest that odours are key factors of the diet composition of pitcher plants. They support the hypothesis of perceptual exploitation of insect biases in carnivorous plants and provide new insights into the olfactory preferences of insect groups. Introduction Plants are sedentary organisms and have developed over the course of evolution a particularly diverse and effective language for communicating at a distance with each other or with PLOS ONE | https://doi.org/10.1371/journal.pone.0277603 April 19, 2023 1 / 23 PLOS ONE design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: This work was publicly supported by the French National Research Agency (ANR-16-IDEX-0006 to LG, CV and DG. under the “Investissements d’avenir” program), which funded material, plants and chemical analyses, as well as the PhD salary of CD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Scent contributes to prey partitioning in Sarracenia pitcher plants organisms from other kingdoms: odours with an alphabet made of volatile organic compounds [1,2]. Plants communicate with each other and use particular combinations of VOCs to warn their neighbours of herbivore attacks, or, conversely, to inhibit the germination of their competitors [3]. Plants also communicate with other organisms, by emitting repellent odours to deter pathogens [4,5] and herbivores [6,7] or by emitting COVs attractive to insects, which often perform essential functions in mutualistic relationships with them, such as defense against herbivores [8], pollination [9], seed dispersal [10], and even nutrition in carnivorous plants [11,12]. Carnivorous plants, to overcome the lack of nutrients in the soils where they grow, do indeed supplement their diet with essential nutrients obtained from insects and other arthropods that they attract, capture and digest with their highly-modified leaves [13–15]. Attraction is thus the first, but not least, component of the carnivorous syndrome in these specialised plants [13]. A group of carnivorous plants, the so-called pitcher plants, includes the well-known Sarraceniaceae from the Americas and the Nepenthaceae from Southeast Asia. The results of some studies comparing insect prey or inquiline numbers of pitcher traps versus control traps suggest that pitchers are not simple pitfall traps, highlighting the importance of attraction in these carnivorous plants [16,17]. Attraction in these pitcher plants is actually satisfied not only by olfactory signals [18–20] but also by other lures, such as nectar guides [21,22] and colour patterns [23–25]. Olfactory cues have received comparatively little attention. A few old studies used tissue extraction to investigate the odour of pitcher plants, but this method also collected non-volatile compounds [18,26] and thus did not provide information on the composition of the emitted bouquet. A more recent study used the same method to compare metabolites among Sarraceniaceae species and also investigated their scent profile but the investigation was then focused on the search for the volatile alkaloid coniine [27]. Only a few studies have actually examined the volatile compounds in the odour bouquets of Sarracenia [19,28] and Nepenthes [20] pitchers and have shown some similarity w (...truncated)