Elevated Atmospheric CO2 Impairs Aphid Escape Responses to Predators and Conspecific Alarm Signals


Research into the impact of atmospheric change on predator–prey interactions has mainly focused on density dependent responses and trophic linkages. As yet, the chemical ecology underpinning predator–prey interactions has received little attention in environmental change research. Group living animals have evolved behavioral mechanisms to escape predation, including chemical alarm signalling. Chemical alarm signalling between conspecific prey could be susceptible to environmental change if the physiology and behavior of these organisms are affected by changes in dietary quality resulting from environmental change. Using Rubus idaeus plants, we show that elevated concentrations of atmospheric CO2 (eCO2) severely impaired escape responses of the aphid Amphorophora idaei to predation by ladybird larvae (Harmonia axyridis). Escape responses to ladybirds was reduced by >50 % after aphids had been reared on plants grown under eCO2. This behavioral response was rapidly induced, occurring within 24 h of being transferred to plants grown at eCO2 and, once induced, persisted even after aphids were transferred to plants grown at ambient CO2. Escape responses were impaired due to reduced sensitivity to aphid alarm pheromone, (E)-β-farnesene, via an undefined plant-mediated mechanism. Aphid abundance often increases under eCO2, however, reduced efficacy of conspecific signalling may increase aphid vulnerability to predation, highlighting the need to study the chemical ecology of predator–prey interactions under environmental change.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3


  1. Awmack CS, Woodcock CM, Harrington R (1997) Climate change may increase vulnerability of aphids to natural enemies. Ecol Entomol 22:366–368. doi:10.1046/j.1365-2311.1997.00069.x

  2. Bezemer TM, Thompson LJ, Jones TH (1998) Poa annua shows inter–generational differences in response to elevated CO2. Glob Chang Biol 4:687–691. doi:10.1046/j.1365-2486.1998.00184.x

  3. Blum MS (1969) Alarm pheromones. Annu Rev Entomol 14:57–80. doi:10.1146/annurev.en.14.010169.000421

  4. Bowers WS, Webb RE, Nault LR, Dutky SR (1972) Aphid alarm pheromone–isolation, identification, synthesis. Science 177:1121–1122. doi:10.1126/science.177.4054.1121

  5. Chen FJ, Ge F, Parajulee MN (2005) Impact of elevated CO2 on tri–trophic interaction of Gossypium hirsutum, Aphis gossypii, and Leis axyridis. Environ Entomol 34:37–46. doi:10.1603/0046-225X-34.1.37

  6. Dixon AFG (2000) Insect–predator prey dynamics. Ladybird beetles and biological control. Cambridge University Press, Cambridge

  7. Docherty M, Hurst DK, Holopainen JK, Whittaker JB, Lea PJ, Watt AD (1996) Carbon dioxide–induced changes in beech foliage cause female beech weevil larvae to feed in a compensatory manner. Glob Chang Biol 2:335–341. doi:10.1111/j.1365-2486.1996.tb00085.x

  8. Douglas AE (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecol Entomol 18:31–38. doi:10.1111/j.1365-2311.1993.tb01076.x

  9. Facey SL, Ellsworth D, Staley JT, Wright DJ, Johnson SN. 2014. Upsetting the order: how atmospheric and climate change affects predator–prey interactions. Curr Opin Insect Sci. doi

  10. Guo H, Sun YC, Li Y, Liu X, Zhang W, Ge F (2013a) Elevated CO2 decreases the response of the ethylene signaling pathway in Medicago truncatula and increases the abundance of the pea aphid. New Phytol 201:279–291. doi:10.1111/nph.12484

  11. Guo H, Sun YC, Li Y, Tong B, Harris M, Zhu–Salzman K, Ge F (2013b) Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Glob Chang Biol 19:3210–3223. doi:10.1111/gcb.12260

  12. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311. doi:10.1016/0022–5193(71)90189–5

  13. Harrington R, Woiwod I, Sparks T (1999) Climate change and trophic interactions. Trends Ecol Evol 14:146–150. doi:10.1016/s0169–5347(99)01604–3

  14. Hentley WT, Hails RS, Johnson SN, Jones TH, Vanbergen AJ (2014) Top–down control by Harmonia axyridis mitigates the impact of elevated atmospheric CO2 on a plant–aphid interaction. Agric For Entomol Online Early. doi:10.1111/afe.12065

  15. IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner G–K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: The physical science basis contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 3–29

  16. Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant–insect and multitrophic interactions. Plant Physiol 160:1719–1727. doi:10.1104/pp. 112.206524

  17. Johnson SN, McNicol JW (2010) Elevated CO2 and aboveground–belowground herbivory by the clover root weevil. Oecologia 162:209–216. doi:10.1007/s00442-009-1428-4

  18. Johnson SN, Lopaticki G, Hartley SE (2014a) Elevated atmospheric CO2 triggers compensatory feeding by root herbivores on a C3 but not a C4 grass. PLoS One 9:e90251. doi:10.1371/journal.pone.0090251

  19. Johnson SN, Ryalls JMW, Karley AJ (2014b) Global climate change and crop resistance to aphids: contrasting responses of lucerne genotypes to elevated atmospheric carbon dioxide. Ann Appl Biol. doi:10.1111/aab.12115

  20. Martin P, Johnson SN (2011) Evidence that elevated CO2 reduces resistance to the European large raspberry aphid in some raspberry cultivars. J Appl Entomol 135:237–240. doi:10.1111/j.1439-0418.2010.01544.x

  21. Mitchell C, Johnson SN, Gordon SC, Birch ANE, Hubbard SF (2010) Combining plant resistance and a natural enemy to control Amphorophora idaei. Biocontrol 55:321–327. doi:10.1007/s10526-009-9257-2

  22. Mondor EB, Tremblay MN, Awmack CS, Lindroth RL (2004) Divergent pheromone–mediated insect behaviour under global atmospheric change. Glob Chang Biol 10:1820–1824. doi:10.1111/j.1365-2486.2004.00838.x

  23. Pickett JA, Wadhams LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Annu Rev Entomol 37:67–90. doi:10.1146/annurev.en.37.010192.000435

  24. Robinson EA, Ryan GD, Newman JA (2012) A meta–analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336. doi:10.1111/j.1469-8137.2012.04074.x

  25. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack–the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, New York

  26. Sun YC, Ge F (2011) How do aphids respond to elevated CO2? J Asia Pac Entomol 14:217–220. doi:10.1016/j.aspen.2010.08.001

  27. Sun Y, Su J, Ge F (2010) Elevated CO2 reduces the response of Sitobion avenae (Homoptera: Aphididae) to alarm pheromone. Agric Ecosyst Environ 135:140–147. doi:10.1016/j.agee.2009.09.011

  28. Van Emden HF, Bashford MA (1976) Effect of leaf excision on performance of Myzus persicae and Brevicoryne brassicae in relation to nutrient treatment of plants. Physiol Entomol 1:67–71. doi:10.1111/j.1365-3032.1976.tb00887.x

  29. 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 Mol 42:155–163. doi:10.1016/j.ibmb.2011.11.008

  30. Zavala JA, Nabity PD, DeLucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58:79–97. doi:10.1146/annurev-ento-120811-153544

  31. Zuberbuehler K (2009) Survivor signals: the biology and psychology of animal alarm calling. In: Naguib M, Zuberbuhler K, Clayton NS, Janik VM (eds) Advances in the study of behavior, vol 40., pp 277–322

Download references


We thank Alison Dobson, Carolin Schultz, Sheena Lamond, and Scott McKenzie for their assistance on this NERC CASE PhD project (NE/H018247/1).

Author information

Correspondence to William T. Hentley.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hentley, W.T., Vanbergen, A.J., Hails, R.S. et al. Elevated Atmospheric CO2 Impairs Aphid Escape Responses to Predators and Conspecific Alarm Signals. J Chem Ecol 40, 1110–1114 (2014) doi:10.1007/s10886-014-0506-1

Download citation


  • Aphid
  • Chemical signals
  • Climate change
  • Tri-trophic interactions
  • Pheromones