Journal of Chemical Ecology

, Volume 39, Issue 8, pp 1101–1111 | Cite as

A Genetically-Based Latitudinal Cline in the Emission of Herbivore-Induced Plant Volatile Organic Compounds

  • Elizabeth L. Wason
  • Anurag A. Agrawal
  • Mark D. Hunter


The existence of predictable latitudinal variation in plant defense against herbivores remains controversial. A prevailing view holds that higher levels of plant defense evolve at low latitudes compared to high latitudes as an adaptive plant response to higher herbivore pressure on low-latitude plants. To date, this prediction has not been examined with respect to volatile organic compounds (VOCs) that many plants emit, often thus attracting the natural enemies of herbivores. Here, we compared genetically-based constitutive and herbivore-induced aboveground vegetative VOC emissions from plants originating across a gradient of more than 10° of latitude (>1,500 km). We collected headspace VOCs from Asclepias syriaca (common milkweed) originating from 20 populations across its natural range and grown in a common garden near the range center. Feeding by specialist Danaus plexippus (monarch) larvae induced VOCs, and field environmental conditions (temperature, light, and humidity) also influenced emissions. Monarch damage increased plant VOC concentrations and altered VOC blends. We found that genetically-based induced VOC emissions varied with the latitude of plant population origin, although the pattern followed the reverse of that predicted—induced VOC concentration increased with increasing latitude. This pattern appeared to be driven by a greater induction of sesquiterpenoids at higher latitudes. In contrast, constitutive VOC emission did not vary systematically with latitude, and the induction of green leafy volatiles declined with latitude. Our results do not support the prevailing view that plant defense is greater at lower than at higher latitudes. That the pattern holds only for herbivore-induced VOC emission, and not constitutive emission, suggests that latitudinal variation in VOCs is not a simple adaptive response to climatic factors.


Common milkweed Asclepias syriaca Herbivory Indirect defense Latitudinal gradient Monarch butterfly Danaus plexippus Volatile organic compounds 



This work was supported by funding from NSF grants (DEB 0814340 to MDH, IGERT BART to ELW, and DEB 0447550 and 1118783 to AAA). We thank Ellen Woods and Amy Hastings for establishing the common garden and for logistical support, Andre Kessler and Rayko Halitschke for sharing advice about VOC collection and analysis, Tony Sutterley for assistance in constructing the VOC sampling equipment, Christoph Vogel for help with LI-COR instruments, and M. Jahi Chappell and Lela for hospitable lodging. We also thank Richard Karban for feedback regarding our results and Robert Raguso, Martin Heil, and an anonymous reviewer for constructive comments on this manuscript.

Supplementary material

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  1. Agrawal AA (2004) Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation. Ecology 85:2118–2133CrossRefGoogle Scholar
  2. Agrawal AA, Konno K (2009) Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331CrossRefGoogle Scholar
  3. Agrawal AA, van Zandt PA (2003) Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. J Ecol 91:1049–1059CrossRefGoogle Scholar
  4. Araújo MB, Luoto M (2007) The importance of biotic interactions for modeling species distributions under climate change. Glob Ecol Biogeogr 16:743–753CrossRefGoogle Scholar
  5. Arimura G, Ozawa R, Horiuchi J, Nishioka T, Takabayashi J (2001) Plant-plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem Syst Ecol 29:1049–1061CrossRefGoogle Scholar
  6. Bergström G, Rothschild M, Groth I, Crighton C (1995) Oviposition by butterflies on young leaves: investigation of leaf volatiles. Chemoecology 5(6):147–158Google Scholar
  7. Bingham RA, Agrawal AA (2010) Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. J Ecol 98:1014–1022CrossRefGoogle Scholar
  8. Bruce TJA, Midega CAO, Birkett MA, Pickett JA, Khan ZR (2010) Is quality more important than quantity? Insect behavioural responses to changes in a volatile blend after stemborer oviposition on an African grass. Biol Lett 6:314–317PubMedCrossRefGoogle Scholar
  9. Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384–2392PubMedCrossRefGoogle Scholar
  10. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  11. Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24PubMedGoogle Scholar
  12. Das PD, Raina R, Prasad AR, Sen A (2007) Electroantennogram responses of the potato tuber moth, Phthorimaea operculella (Lepidoptera; Gelichiidae) to plant volatiles. J Biosci 32:339–349PubMedCrossRefGoogle Scholar
  13. Davis MA (1984) The flight and migration ecology of the red milkweed beetle (Tetraopes tetraophthalmus). Ecology 65:230–234CrossRefGoogle Scholar
  14. Davis AJ, Jenkinson LS, Lawton JH, Shorrocks B, Wood S (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature 391:783–786PubMedCrossRefGoogle Scholar
  15. de Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  16. Delphia CM, Rohr JR, Stephenson AG, de Moraes CM, Mescher MC (2009) Effects of genetic variation and inbreeding on volatile production in a field population of horsenettle. Int J Plant Sci 170:12–20CrossRefGoogle Scholar
  17. Dicke M (1994) Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J Plant Physiol 143:465–472CrossRefGoogle Scholar
  18. Dicke M, Takabayashi J, Posthumus MA, Shütte C, Krips OE (1998) Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp Appl Acarol 22:311–333CrossRefGoogle Scholar
  19. Dyer LA, Coley PD (2004) Tritrophic interactions in tropical versus temperate communities. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 67–88Google Scholar
  20. Engelkes T, Morriën E, Verhoeven KJF, Bezemer TM, Biere A, Harvey JA, McIntyre LM, Tamis WLM, van der Putten WH (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456:946–948PubMedCrossRefGoogle Scholar
  21. Farmer EE (2001) Surface-to-air signals. Nature 411:854–856PubMedCrossRefGoogle Scholar
  22. Frost CJ, Appel HM, Carlson JE, de Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498PubMedCrossRefGoogle Scholar
  23. Geron C, Rasmussen R, Arnts RR, Guenther A (2000) A review and synthesis of monoterpene speciation from forests in the United States. Atmos Environ 34:1761–1781CrossRefGoogle Scholar
  24. Gols R, Rossjen M, Dijkman H, Dicke M (2003) Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J Chem Ecol 29:2651–2666PubMedCrossRefGoogle Scholar
  25. Gols R, van Dam NM, Raaijmakers CE, Dicke M, Harvey JA (2009) Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps? Oikos 118:733–742CrossRefGoogle Scholar
  26. Guernier V, Hochberg ME, Guégan J-F (2004) Ecology drives the worldwide distribution of human diseases. PLoS Biol 2:e141PubMedCrossRefGoogle Scholar
  27. Halitschke R, Kessler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124:408–417CrossRefGoogle Scholar
  28. Hare JD (2007) Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J Chem Ecol 33:2028–2043PubMedCrossRefGoogle Scholar
  29. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144PubMedCrossRefGoogle Scholar
  30. Helmig D (1997) Ozone removal techniques in the sampling of atmospheric volatile organic trace gases. Atmos Environ 31:3635–3651CrossRefGoogle Scholar
  31. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184PubMedCrossRefGoogle Scholar
  32. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsid thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008PubMedCrossRefGoogle Scholar
  33. Hunter MD, Malcolm SB, Hartley SE (1996) Population-level variation in plant secondary chemistry, and the population biology of herbivores. Chemoecology 7:45–56CrossRefGoogle Scholar
  34. Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88CrossRefGoogle Scholar
  35. Kessler A, Baldwin IT (2001) Herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  36. Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292PubMedCrossRefGoogle Scholar
  37. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102PubMedCrossRefGoogle Scholar
  38. Loughrin JH, Manukian A, Heath RR, Tumlinson JH (1995) Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J Chem Ecol 21:1217–1227CrossRefGoogle Scholar
  39. Marei GIK, Rasoul MAA, Abdelgaleil SAM (2012) Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi. Pestic Biochem Physiol 103:56–61CrossRefGoogle Scholar
  40. Martz F, Peltola R, Fontanay S, Duval RE, Julkunen-Tiitto R, Stark S (2009) Effect of latitude and altitude on the terpenoid and soluble phenolic composition of juniper needles and evaluation of their antibacterial activity in the boreal zone. J Agric Food Chem 57:9575–9584PubMedCrossRefGoogle Scholar
  41. McCauley DE (1983) Gene flow distances in natural populations of Tetraopes tetraophthalmus. Evolution 37:1239–1246CrossRefGoogle Scholar
  42. Menéndez R, González-Megías A, Lewis OT, Shaw MR, Thomas CD (2008) Escape from natural enemies during climate-driven range expansion: a case study. Ecol Entomol 33:413–421CrossRefGoogle Scholar
  43. Moles AT, Bonser SP, Poore AGB, Wallis IR, Foley WJ (2011a) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25:380–388CrossRefGoogle Scholar
  44. Moles AT, Wallis IR, Foley WJ, Warton DI, Stegen JC, Bisigato AJ, Cella-Pizarro L et al (2011b) Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytol 191:777–788PubMedCrossRefGoogle Scholar
  45. Mooney KA, Agrawal AA (2008) Plant genotype shapes ant-aphid interactions: implications for community structure and indirect plant defense. Am Nat 171:E195–E205PubMedCrossRefGoogle Scholar
  46. Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644PubMedCrossRefGoogle Scholar
  47. O’dowd DJ, Willson MF (1991) Associations between mites and leaf domatia. Trends Ecol Evol 6:179–182PubMedCrossRefGoogle Scholar
  48. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2010) Vegan: Community Ecology PackageGoogle Scholar
  49. Pemberton RW (1998) The occurrence and abundance of plants with extrafloral nectaries, the basis for antiherbivore defensive mutualisms, along a latitudinal gradient in east Asia. J Biogeogr 25:661–668CrossRefGoogle Scholar
  50. Pennings SC, Siska EL, Bertness MD (2001) Latitudinal differences in plant palatability in Atlantic Coast salt marshes. Ecology 82:1344–1359CrossRefGoogle Scholar
  51. Pennings SC, Ho C-K, Salgado CS, Wieski K, Davé N, Kunza AE, Wason EL (2009) Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90:183–195PubMedCrossRefGoogle Scholar
  52. Prysby MD (2004) Natural enemies and survival of monarch eggs and larvae. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology & conservation. Cornell University Press, New York, pp 27–37Google Scholar
  53. Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483PubMedCrossRefGoogle Scholar
  54. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737PubMedCrossRefGoogle Scholar
  55. Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99:16–25CrossRefGoogle Scholar
  56. Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175PubMedCrossRefGoogle Scholar
  57. Ruther J, Kleier S (2005) Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-Hexen-1-ol. J Chem Ecol 31:2217–2222PubMedCrossRefGoogle Scholar
  58. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269CrossRefGoogle Scholar
  59. Schuman MC, Heinzel N, Gaquerel E, Svatos A, Baldwin IT (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol 183:1134–1148PubMedCrossRefGoogle Scholar
  60. Späthe A, Reinecke A, Olsson SB, Kesavan S, Knaden M, Hansson BS (2013) Plant species- and status-specific odorant blends guide oviposition choice in the moth Manduca sexta. Chem Senses 38:147–159PubMedCrossRefGoogle Scholar
  61. Staudt M, Mir C, Joffre R, Rambal S, Bonin A, Landais D, Lumaret R (2004) Isoprenoid emissions of Quercus spp. (Q. suber and Q. ilex) in mixed stands contrasting in interspecific genetic introgression. New Phytol 163:573–584CrossRefGoogle Scholar
  62. Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688CrossRefGoogle Scholar
  63. Thompson JN (2005) The geographic Mosaic of Coevolution. The University of Chicago Press, ChicagoGoogle Scholar
  64. Turlings TCJ, Davison AC, Tamó C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29:45–55CrossRefGoogle Scholar
  65. Vannette RL, Hunter MD (2011) Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2. Glob Chang Biol 17:1277–1288CrossRefGoogle Scholar
  66. Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bährmann R, Fabian B, Heinrich W, Köhler G, Lichter D, Marstaller R, Sander FW (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453CrossRefGoogle Scholar
  67. Wason EL (2012) Plants make scents: Variation in plant volatile organic chemical emission at multiple scales. PhD dissertation. University of Michigan, Ann Arbor.Google Scholar
  68. Weber MG, Clement WL, Donoghue MJ, Agrawal AA (2012) Phylogenetic and experimental tests of interactions among mutualistic plant defense traits in Viburnum (Adoxaceae). Am Nat 180:450–463PubMedCrossRefGoogle Scholar
  69. Wiens JA, Cates RG, Rotenberry JT, Cobb N, van Horne B, Redak RA (1991) Arthropod dynamics on sagebrush (Artemisia tridentata): effects of plant chemistry and avian predation. Ecol Monogr 61:299–321CrossRefGoogle Scholar
  70. Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monogr 82:149–168CrossRefGoogle Scholar
  71. Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806–815PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Elizabeth L. Wason
    • 1
  • Anurag A. Agrawal
    • 2
    • 3
  • Mark D. Hunter
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of Michigan, Ann ArborAnn ArborUSA
  2. 2.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  3. 3.Department of EntomologyCornell UniversityIthacaUSA

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