Abstract
Insects often rely on olfaction to communicate with conspecifics. While the chemical language of insects has been deciphered in recent decades, few studies have assessed how changes in atmospheric greenhouse gas concentrations might impact pheromonal communication in insects. Here, we hypothesize that changes in the concentration of atmospheric carbon dioxide affect the whole dynamics of alarm signaling in aphids, including: (1) the production of the active compound (E)-β-farnesene (Eβf), (2) emission behavior when under attack, (3) perception by the olfactory apparatus, and (4) the escape response. We reared two strains of the pea aphid, Acyrthosiphon pisum, under ambient and elevated CO2 concentrations over several generations. We found that an increase in CO2 concentration reduced the production (i.e., individual content) and emission (released under predation events) of Eβf. While no difference in Eβf neuronal perception was observed, we found that an increase in CO2 strongly reduced the escape behavior expressed by an aphid colony following exposure to natural doses of alarm pheromone. In conclusion, our results confirm that changes to greenhouse gases impact chemical communication in the pea aphid, and could potentially have a cascade effect on interactions with higher trophic levels.
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References
Awmack C, Woodcock C, Harrington R (1997) Climate change may increase vulnerability of aphids to natural enemies. Ecol Entomol 22:366–368
Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol 50:1339–1354
Boullis A, Verheggen FJ (2016) Chemical ecology of aphids (Hemiptera: Aphididae). In: Vilcinskas A (ed) Biology and ecology of aphids. CRC press, Boca Ranton, pp 171–198
Boullis A, Francis F, Verheggen FJ (2015) Climate change and tritrophic interactions: will modifications to greenhouse gas emissions increase the vulnerability of herbivorous insects to natural enemies? Environ Entomol 44:277–286
Boullis A, Detrain C, Francis F, Verheggen FJ (2016) Will climate change affect insect pheromonal communication? Curr Opin Insect Sci 17:87–91
Coviella CE, Trumble JT (1999) Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conserv Biol 13:700–712
DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160:1677–1685
Fassotte B, Fischer C, Durieux D, Lognay G, Haubruge E, Francis F, Verheggen FJ (2014) First evidence of a volatile sex pheromone in lady beetles. PLoS One 9:e115011
Fischer CY, Lognay GC (2012) Simple and automatic closed grinding and extraction system. J Chem Educ 89:1611–1612
Francis F, Vandermoten S, Verheggen FJ, Lognay G, Haubruge E (2005) Is the (E)-β-farnesene only volatile terpenoid in aphids? J Appl Entomol 129:6–11
Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178
Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–16
Hansson BS, Wicher D (2016) Chemical ecology in insects. In: Zufall F, Munger SD (eds) Chemosensory transduction: the detection of odors, tastes, and other chemostimuli. Academic press, London, pp 29–45
Hatano E, Kunert G, Michaud JP, Weisser WW (2008) Chemical cues mediating aphid location by natural enemies. Eur J Entomol 105:797–806
Hentley WT, Vanbergen AJ, Hails RS, Jones TH, Johnson SN (2014) Elevated atmospheric CO2 impairs aphid escape responses to predators and conspecific alarm signals. J Chem Ecol 40:1110–1114
Heuskin S, Godin B, Leroy P et al (2009) Fast gas chromatography characterization of purified semiochemicals from essential oils of Matricaria chamomilla L. (Asteraceae) and Nepeta cataria L. (Lamiaceae). J Chromatogr A 1216:2768–2775
Heuskin S, Lorge S, Godin B et al (2012) Optimisation of a semiochemical slow-release alginate formulation attractive towards Aphidius ervi Haliday parasitoids. Pest Manag Sci 68:127–136
Hughes L, Bazzaz FA (2001) Effects of elevated CO2 on five plant-aphid interactions. Entomol Exp Appl 99:87–96
Joachim C, Hatano E, David A, Kunert M, Linse C, Weisser WW (2013) Modulation of aphid alarm pheromone emission of pea aphid prey by predators. J Chem Ecol 39:773–782
Kislow CJ, Edwards LJ (1972) Repellent odour in aphids. Nature 235:108–109
Kunert G, Otto S, Röse US, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8:596–603
Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391
Lin FJ, Bosquée E, Liu YJ, Chen JL, Yong L, Francis F (2016) Impact of aphid alarm pheromone release on virus transmission efficiency: when pest control strategy could induce higher virus dispersion. J Virol Methods 235:34–40
Misra BB, Chen S (2015) Advances in understanding CO2 responsive plant metabolomes in the era of climate change. Metabolomics 11:1478–1491
Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. P Roy Soc Lond B Biol Sci 271:S341–S343
Mondor EB, Tremblay MN, Awmack CS, Lindroth RL (2004) Divergent pheromone-mediated insect behaviour under global atmospheric change. Glob Change Biol 10:1820–1824
Mondor EB, Tremblay MN, Awmack CS, Lindroth RL (2005) Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres. Glob Change Biol 11:1990–1996
Ode PJ, Johnson SN, Moore BD (2014) Atmospheric change and induced plant secondary metabolites - are we reshaping the building blocks of multi-trophic interactions? Curr Opin Insect Sci 5:57–65
Peñuelas J, Staudt M (2010) BVOCs and global change. Trends Plant Sci 15:133–144
Qiao H, Tuccori E, He X, Gazzano A, Field L, Zhou JJ, Pelosi P (2009) Discrimination of alarm pheromone (E)-β-farnesene by aphid odorant-binding proteins. Insect Biochem Molec Biol 39:414–419
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Sallaud C, Rontein D, Onillon S et al (2009) A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21:301–317
Sentis A, Ramon-Portugal F, Brodeur J, Hemptinne JL (2015) The smell of change: warming affects species interactions mediated by chemical information. Glob Change Biol 21:3586–3594
Sun YC, Su J, Ge F (2010) Elevated CO2 reduces the response of Sitobion avenae (Homoptera: Aphididae) to alarm pheromone. Agric Ecosyst Environ 135:140–147
Sun YC, Guo H, Ge F (2016) Plant-aphid interactions under elevated CO2: some cues from aphid feeding behavior. Front Plant Sci 7:502
Tanaka S, Yasuda A, Yamamoto H, Nozaki H (1975) A general method for the synthesis of 1,3–dienes. Simple syntheses of β- and trans-α-farnesene from farnesol J Am Chem Soc 97:3252–3254
Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ (2012) Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochem Molec Biol 42:155–163
Verheggen FJ, Fagel Q, Heuskin S, Lognay G, Francis F, Haubruge E (2007) Electrophysiological and behavioral responses of the multicolored Asian lady beetle, Harmonia axyridis Pallas, to sesquiterpene semiochemicals. J Chem Ecol 33:2148–2155
Verheggen FJ, Arnaud L, Bartram S, Gohy M, Haubruge E (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. J Chem Ecol 34:301–307
Verheggen FJ, Haubruge E, Mescher MC (2010) Alarm pheromones-chemical signaling in response to danger. Vitam Horm 83:215–239
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172
Vogt RG (2005) Molecular basis of pheromone detection in insects. In: Gilbert LI, Iatro K, Gill S (eds) Comprehensive insect physiology, biochemistry, pharmacology and molecular biology, Endocrinology, vol 3. Elsevier, London, pp 753–804
Vosteen I, Weisser WW, Kunert G (2016) Is there any evidence that aphid alarm pheromones work as prey and host finding kairomones for natural enemies? Ecol Entomol 41:1–12
Wang N, Nobel PS (1995) Phloem exudate collected via scale insect stylets for the CAM species Opuntia ficus-indica under current and doubled CO2 concentrations. Ann Bot 75:525–532
Zavala JA, Nabity PD, DeLucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97
Acknowledgements
Antoine Boullis and Landry Sarles are financially supported by the Fund for Research Training in Industry and Agriculture (FRIA). Bérénice Fassotte is financially supported by a PhD grant from the “Centre Universitaire de Recherche en Agronomie et ingénierie biologique de Gembloux” (CURAGx), University of Liege. Maryse Vanderplanck is a postdoctoral researcher of the Fund for Scientific Research (F.R.S.- FNRS).
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Fig. S1
Calibration curve of (E)-β-farnesene obtained by the least squares fit analysis method. Peak area ratio is presented as the analyte peak area on an internal standard peak area (GIF 6 kb)
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Boullis, A., Fassotte, B., Sarles, L. et al. Elevated Carbon Dioxide Concentration Reduces Alarm Signaling in Aphids. J Chem Ecol 43, 164–171 (2017). https://doi.org/10.1007/s10886-017-0818-z
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DOI: https://doi.org/10.1007/s10886-017-0818-z