Advertisement

Oecologia

, Volume 174, Issue 2, pp 479–491 | Cite as

Genetic variation in plant volatile emission does not result in differential attraction of natural enemies in the field

  • Elizabeth L. Wason
  • Mark D. Hunter
Plant-microbe-animal interactions - Original research

Abstract

Volatile organic chemical (VOC) emission by plants may serve as an adaptive plant defense by attracting the natural enemies of herbivores. For plant VOC emission to evolve as an adaptive defense, plants must show genetic variability for the trait. To date, such variability has been investigated primarily in agricultural systems, yet relatively little is known about genetic variation in VOCs emitted by natural populations of native plants. Here, we investigate intraspecific variation in constitutive and herbivore-induced plant VOC emission using the native common milkweed plant (Asclepias syriaca) and its monarch caterpillar herbivore (Danaus plexippus) in complementary field and common garden greenhouse experiments. In addition, we used a common garden field experiment to gauge natural enemy attraction to milkweed VOCs induced by monarch damage. We found evidence of genetic variation in the total constitutive and induced concentrations of VOCs and the composition of VOC blends emitted by milkweed plants. However, all milkweed genotypes responded similarly to induction by monarchs in terms of their relative change in VOC concentration and blend. Natural enemies attacked decoy caterpillars more frequently on damaged than on undamaged milkweed, and natural enemy visitation was associated with higher total VOC concentrations and with VOC blend. Thus, we present evidence that induced VOCs emitted by milkweed may function as a defense against herbivores. However, plant genotypes were equally attractive to natural enemies. Although milkweed genotypes diverge phenotypically in their VOC concentrations and blends, they converge into similar phenotypes with regard to magnitude of induction and enemy attraction.

Keywords

Common milkweed Asclepias syriaca Indirect defense Monarch butterfly Danaus plexippus Plant–herbivore interactions Volatile organic chemicals 

Notes

Acknowledgments

This work was supported by funding from NSF grants (DEB 0814340 to MDH and IGERT BART to ELW), with additional funding from the Department of Ecology and Evolutionary Biology at the University of Michigan, Ann Arbor. Steve Bertman, Mary Anne Caroll, Huijie Gan, Doug Jackson, Dave Karowe, Andre Kessler, Beth Pringle, Tony Sutterley, Leiling Tao, Shino Toma, Rachel Vannette, Chris Vogel, and all of the staff at the University of Michigan Biological Station provided invaluable advice and support that improved this work. These experiments comply with the current laws of the United States of America, in which the experiments were performed.

References

  1. Andersson S (1990) Paternal effects on seed size in a population of Crepis tectorum (Asteraceae). Oikos 59:3–8CrossRefGoogle Scholar
  2. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971–980CrossRefGoogle Scholar
  3. Bergström G, Rothschild M, Groth I, Crighton C (1995) Oviposition by butterflies on young leaves: investigation of leaf volatiles. Chemoecology 5:147–158Google Scholar
  4. 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 6:314–317PubMedCentralPubMedCrossRefGoogle Scholar
  5. D’Alessandro M, Turlings TCJ (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32PubMedCrossRefGoogle Scholar
  6. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  7. Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938PubMedCentralPubMedCrossRefGoogle Scholar
  8. 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
  9. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  10. Fritszche Hoballah ME, Turlings TCJ (2001) Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol Ecol Res 3:553–565Google Scholar
  11. Fritzsche Hoballah ME, Tamo C, Turlings TCJ (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: is quality or quantity important? J Chem Ecol 28:951–968CrossRefGoogle Scholar
  12. Gold JJ, Shore JS (1995) Multiple paternity in Asclepias syriaca using a paired-fruit analysis. Can J Botany 73:1212–1216CrossRefGoogle Scholar
  13. Gols R, Roosjen 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
  14. Gouinguené S, Degen T, Turlings TCJ (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16CrossRefGoogle Scholar
  15. 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
  16. Hare JD (2007) Variation in herbivore and methyl jasmonate-induced volatiles among genetic lines of Datura wrightii. J Chem Ecol 33:2028–2043PubMedCrossRefGoogle Scholar
  17. Hare JD (2010) Ontogeny and season constrain the production of herbivore-inducible plant volatiles in the field. J Chem Ecol 36:1363–1374PubMedCentralPubMedCrossRefGoogle Scholar
  18. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  19. Helmig D (1997) Ozone removal techniques in the sampling of atmospheric volatile organic trace gases. Atmos Environ 31:3635–3651CrossRefGoogle Scholar
  20. Kabat SM, Dick CW, Hunter MD (2010) Isolation and characterization of microsatellite loci in the common milkweed, Asclepias syriaca (Apocynaceae). Am J Bot 97:e37–e38PubMedCrossRefGoogle Scholar
  21. Kahl J, Siemens DH, Aerts RJ, Gäbler R, Kühnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342PubMedCrossRefGoogle Scholar
  22. Kappers IF, Hoogerbrugge H, Bouwmeester HJ, Dicke M (2010) Variation in herbivory-induced volatiles among cucumber (Cucumis sativus L.) varieties has consequences for the attraction of carnivorous natural enemies. J Chem Ecol 37:150–160CrossRefGoogle Scholar
  23. Kariyat RR, Mauck KE, De Moraes CM, Stepheneson AG, Mescher MC (2012) Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.). Ecol Lett 15:301–309CrossRefGoogle Scholar
  24. Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88CrossRefGoogle Scholar
  25. Kessler A, Baldwin IT (2001) Herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  26. 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
  27. Krips OE, Willems PEL, Gols R, Posthumus MA, Gort G, Dicke M (2001) Comparison of cultivars of ornamental crop Gerbera jamesonii on production of spider mite-induced volatiles, and their attractiveness to the predator Phytoseiulus persimilis. J Chem Ecol 27:1355–1372PubMedCrossRefGoogle Scholar
  28. Lou Y, Hua X, Turlings TCJ, Cheng J, Chen X, Ye G (2006) Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. J Chem Ecol 32:2375–2387PubMedCrossRefGoogle Scholar
  29. Loughrin JH, Manukian A, Heath RR, Tumlinson JH (1995) Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J Chem Ecol 21:1217–1227PubMedCrossRefGoogle Scholar
  30. Mazer SJ, Snow AA, Stanton ML (1986) Fertilization dynamics and parental effects upon fruit development in Raphanus raphanistrum: consequences for seed size variation. Am J Bot 73:500–511CrossRefGoogle Scholar
  31. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2010) vegan: community ecology package. http://vegan.r-forge.r-project.org/
  32. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811PubMedCentralPubMedCrossRefGoogle Scholar
  33. Prysby MD (2004) Natural enemies and survival of monarch eggs and larvae. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, New York, pp 27–37Google Scholar
  34. 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
  35. Rudgers JA, Strauss SY, Wendel JF (2004) Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). Am J Bot 91:871–880PubMedCrossRefGoogle Scholar
  36. 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 31:2217–2222Google Scholar
  37. 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
  38. Scriber JM (1977) Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth of Hyalophora cecropia (Lepidoptera: Saturniidae). Oecologia 28:269–287Google Scholar
  39. Skoczylas DR, Muth NZ, Niesenbaum RA (2007) Contribution of insectivorous avifauna to top down control of Lindera benzoin herbivores at forest edge and interior habitats. Acta Oecol 32:337–342CrossRefGoogle Scholar
  40. Staudt M, Mandl N, Joffre R, Rambal S (2001) Intraspecific variability of monoterpene composition emitted by Quercus ilex leaves. Can J Forest Res 31:174–180Google Scholar
  41. Steward JL, Keeler KH (1988) Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)? Oikos 53:79–86CrossRefGoogle Scholar
  42. Strauss SY, Sahli H, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytol 165:81–90PubMedCrossRefGoogle Scholar
  43. Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, van Wijk M (2006) Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol Res 21:3–8CrossRefGoogle Scholar
  44. Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688CrossRefGoogle Scholar
  45. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253PubMedCrossRefGoogle Scholar
  46. 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
  47. Vannette RL, Hunter MD (2011) Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2. Glob Change Biol 17:1277–1288CrossRefGoogle Scholar
  48. Vet LEM, Wäckers FL, Dicke M (1991) How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth J Zool 41:202–213CrossRefGoogle Scholar
  49. Weaver DK, Buteler M, Hofland ML, Runyon JB, Nansen C, Talbert LE, Lamb P, Carlson GR (2009) Cultivar preferences of ovipositing wheat stem sawflies as influenced by the amount of volatile attractant. J Econ Entomol 102:1009–1017PubMedCrossRefGoogle Scholar
  50. 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
  51. Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of Michigan, Ann ArborAnn ArborUSA

Personalised recommendations