Abstract
More than 140 years ago Darwin proposed that leaf-trap of carnivorous plants could produce odor to increase prey attraction; however, even now, there is limited information on the role of flower and leaf-trap volatile organic compounds (VOCs) in the attraction to pollinators and prey in carnivorous plants. Here, we recorded the floral visitors and prey of Pinguicula moranensis, a carnivorous plant with adhesive leaf-traps. In addition, the VOCs from flowers and leaf-traps were analyzed. Their role in the attraction of floral visitors and prey was experimentally tested using the skipper butterfly Thorybes dorantes and the fruit fly Drosophila melanogaster as models, respectively. In the field, flowers of P. moranensis were only visited by butterflies and most of the prey were dipterans. Six VOCs, predominantly benzenoids, were identified from floral scent samples. Twelve VOCs were identified from leaf-trap scent samples, mainly monoterpenoids and benzenoids. In experimental conditions, D. melanogaster significantly preferred the scent given off by the leaf-trap over the clean air, whereas the main floral visitor, T. dorantes significantly preferred the floral scent source over the clean air. However, D. melanogaster did not show preferences for the leaf-trap scent compared to the flower scent. These results showed that leaf-traps and flowers of P. moranensis emitted a specific composition and relative abundance of VOCs. In addition, we experimentally showed that floral VOCs attracted the main floral visitor species and leaf-traps attracted D. melanogaster, as a potential prey. The VOCs play a relevant role in attracting pollinators and prey in carnivorous plants.
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References
Adams RP (2007) Identification of essential oils by gas chromatography/Mass spectrometry, 4th edn. Allured Publication, Carol Stream
Akol AM, Njagi PGN, Sithanantham S, Mueke JM (2003) Effects of two neem insecticide formulations on the attractiveness, acceptability and suitability of diamondback moth larvae to the parasitoid, Diadegma mollipla (Holmgren)(Hym., Ichneumonidae). J Appl Entomol 127:325–331. https://doi.org/10.1046/j.1439-0418.2003.00771.x
Alcalá RE, Domínguez CA (2003) Patterns of prey capture and prey availability among populations of the carnivorous plant Pinguicula moranensis (Lentibulariaceae) along an environmental gradient. Am J Bot 90:1341–1348
Andersson S (2003) Antennal responses to floral scents in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae). Chemoecology 13:13–20. https://doi.org/10.1007/s000490300001
Andersson S, Nilsson LA, Groth I, Bergström G (2002) Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Botanical J Linnean Soc 140:129–153. https://doi.org/10.1046/j.1095-8339.2002.00068.x
Brückner A, Heethoff M (2017) A chemo-ecologists’ practical guide to compositional data analysis. Chemoecology 27:33–46. https://doi.org/10.1007/s00049-016-0227-8
Clavijo Mccormick A, Gershenzon J, Unsicker SB (2014) Little peaks with big effects: establishing the role of minor plant volatiles in plant–insect interactions. Plant Cell Environ 37:1836–1844
Darwin C (1875) Insectivorous plants. John Murray, London
Di Giusto B, Grosbois V, Fargeas E, Marshall D, Gaume L (2008) Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from Borneo. J Biosci 33:121–136
Di Giusto B, Bessière JM, Guéroult M, Lim LB, Marshall DJ, Hossaert-McKey M, Gaume L (2010) Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. J Ecol 98:845–856. https://doi.org/10.1111/j.1365-2745.2010.01665.x
Díaz-Osorio AC, Bonilla-Díaz C, Valle JRM, Sánchez-López A, Sandoval-Ruíz CA (2016) Diversidad de presas de la planta carnívora Pinguicula moranensis (Lentibulariaceae). Entomología Mexicana 3:596–601
Dobson H (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton
Ellison AM, Adamec L (2018) Carnivorous plants: physiology, ecology, and evolution. Oxford University Press, Oxford
El-Sayed AM, Byers JA, Suckling DM (2016) Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death. Sci Rep 6:1–11. https://doi.org/10.1038/srep21065
El-Sayed AM (2021) The pherobase: Database of insect pheromones and semiochemicals: Available at http://www.pherobase.com
García MB, Antor RJ, Villar L (1994) Phenomorphology and reproductive biology of Pinguicula longifolia Ramond ex DC. subsp. longifolia (Lentibulariaceae), a carnivorous endemic plant of the Pyrenees. Acta Botanica Gallica 141:343–349. https://doi.org/10.1080/12538078.1994.10515167
Gershenzon J, Fontana A, Burow M, Wittstock U, Degenhardt J (2012) Mixtures of plant secondary metabolites: metabolic origins and ecological benefits. In: Iason GR, Hartley M, Dicke SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 56–77
Gervasi DDL, Schiestl FP (2017) Real-time divergent evolution in plants driven by pollinators. Nature Communication 8:14691. https://doi.org/10.1038/ncomms14691
Givnish TJ (2015) New evidence on the origin of carnivorous plants. Proc Natl Acad Sci 112:10–11. https://doi.org/10.1073/pnas.1422278112
Guleria N, Nebapure SM, Kamala JPD, Suby SB, Kumar PS (2021) Identification of male-specific active host plant volatiles for maize stem borer, Chilo partellus Swinhoe. Curr Sci 121:578–658
Hatcher CR, Ryves DB, Millett J (2020) The function of secondary metabolites in plant carnivory. Ann Bot 125:399–411
Joel DM, Juniper BE, Dafni A (1985) Ultraviolet patterns in the traps of carnivorous plants. New Phytol 101:585–593. https://doi.org/10.1111/j.1469-8137.1985.tb02864.x
Jürgens A, El-Saye AM, Suckling DM (2009) Do carnivorous plants use volatiles for attracting prey insects? Funct Ecol 23:875–887. https://doi.org/10.1111/j.1365-2435.2009.01626.x
Jürgens A, Sciligo A, Witt T, El-Sayed AM, Suckling DM (2012) Pollinator-prey conflict in carnivorous plants. Biol Rev 87:602–615
Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017) Community-wide integration of floral color and scent in a Mediterranean scrubland. Nat Ecol Evolut 1:1502–1510. https://doi.org/10.1038/s41559-017-0298-0
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1. https://doi.org/10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2
Kreuzwieser J, Scheerer U, Kruse J, Burzlaff T, Honsel A, Alfarraj S, Georgiev P, Schnitzler JP, Ghirardo A, Kreuzer I, Hedrich R, Rennenberg H (2014) The Venus flytrap attracts insects by the release of volatile organic compounds. J Exp Bot 65:755–766
Kristensen TN, Henningsen AK, Aastrup C, Bech-Hansen M, Bjerre LB, Carlsen B, Hagstrup M, Jensen SG, Karlsen P, Kristensen L, Lundsgaard C, Møller T, Nielsen LD, Starcke C, Sørensen CR, Schou MF (2016) Fitness components of Drosophila melanogaster developed on a standard laboratory diet or a typical natural food source. Insect Science 23:771–779
Molau U (1993) Reproductive ecology of the three Nordic Pinguicula species (Lentibulariaceae). Nord J Bot 13:149–157. https://doi.org/10.1111/j.1756-1051.1993.tb00025.x
Ojeda F, Carrera C, Paniw M, García-Moreno L, Barbero GF, Palma M (2021) Volatile and semi-volatile organic compounds may help reduce pollinator-prey overlap in the carnivorous plant Drosophyllum lucitanicum (Drosophyllaceae). J Chem Ecol 47:73–86. https://doi.org/10.1007/s10886-020-01235-w
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Oksanen MJ (2013) Package ‘vegan.’ Commun Ecol Package Version 2:1–295
Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Ann Rev Ecol Evolut Syst 39:549–569. https://doi.org/10.1146/annurev.ecolsys.38.091206.0956018
Schiestl FP (2015) Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytol 206:571–577. https://doi.org/10.1111/nph.13243
Shimai H, Setoguchi H, Roberts DL, Sun M (2021) Biogeographical patterns and speciation of the genus Pinguicula (Lentibulariaceae) inferred by phylogenetic analyses. PLoS ONE 16(6):e0252581. https://doi.org/10.1371/journal.pone.0252581
Tóth P, Undas AK, Verstappen F, Bouwmeester H (2016) Floral volatiles in parasitic plants of the Orobanchaceae. Ecological and taxonomic implications. Front Plant Sci 7:312. https://doi.org/10.3389/fpls.2016.00312
Triplehorn CA, Johnson NF., Borror DJ (2005) Borror and DeLong's Introduction to the Study of Insects (No. QL463 B69 2005)
Villegas SG, Alcalá RE (2018) Reproductive ecology of the carnivorous plant Pinguicula moranensis (Lentibulariaceae). Plant Biol 20:205–212
Wang P, Zhang N, Zhou LL, Si SY, Lei CL, Ai H, Wang XP (2014) Antennal and behavioral responses of female Maruca vitrata to the floral volatiles of Vigna unguiculata and Lablab purpureus. Entomol Exp Appl 152:248–257. https://doi.org/10.1111/eea.12216
Zamora R (1999) Conditional outcomes of interactions: the pollinator–prey conflict of an insectivorous plant. Ecology 80:786–795
Zamudio S (2005) Familia Lentibulariaceae. Flora del Bajío y Regiones Adyacentes. Instituto de Ecología. A.C.
Acknowledgements
We thank the comments and suggestions made by the two anonymous reviewers that improved previous versions of the manuscript. This research was funded by the Institute of Science, Technology and Innovation (ICTI) project No. 13 to E. Cuevas and the Coordinación de la Investigación Científica (CIC), Universidad Michoacana de San Nicolás de Hidalgo.
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EC, YM-D designed the experiments, wrote the manuscript and analyzed data. ADM, EC made fieldwork. FJE-G, YM-D analyzed the samples by gas chromatography/spectrometry mass.
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Cuevas, E., Martínez-Díaz, Y., Montes, A.D. et al. Floral and leaf-trap volatiles and their relationship to pollinator and prey attraction in Pinguicula moranensis (Lentibulariaceae). Arthropod-Plant Interactions 17, 687–694 (2023). https://doi.org/10.1007/s11829-023-09984-7
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DOI: https://doi.org/10.1007/s11829-023-09984-7