Biological Invasions

, Volume 15, Issue 11, pp 2387–2401 | Cite as

A tritrophic approach to the preference–performance hypothesis involving an exotic and a native plant

  • Taiadjana M. FortunaEmail author
  • Jozef B. Woelke
  • Cornelis A. Hordijk
  • Jeroen J. Jansen
  • Nicole M. van Dam
  • Louise E. M. Vet
  • Jeffrey A. Harvey
Original Paper


Exotic plants often generate physical and chemical changes in native plant communities where they become established. A major challenge is to understand how novel plants may affect trophic interactions in their new habitats, and how native herbivores and their natural enemies might respond to them. We compared the oviposition preference and offspring performance of the crucifer specialist, Pieris brassicae, on an exotic plant, Bunias orientalis, and on a related native plant, Sinapis arvensis. Additionally, we studied the response of the parasitoid, Cotesia glomerata to herbivore-induced plant volatiles (HIPV) and determined the volatile blend composition to elucidate which compound(s) might be involved in parasitoid attraction. On both host plants we also compared the parasitism rate of P. brassicae by C. glomerata. Female butterflies preferred to oviposit on the native plant and their offspring survival and performance was higher on the native plant compared to the exotic. Although, headspace analysis revealed qualitative and quantitative differences in the volatile blends of both plant species, C. glomerata did not discriminate between the HIPV blends in flight-tent bioassays. Nevertheless, parasitism rate of P. brassicae larvae was higher on the native plant under semi-field conditions. Overall, P. brassicae oviposition preference may be more influenced by bottom-up effects of the host plant on larval performance than by top-down pressure exerted by its parasitoid. The potential for dietary breadth expansion of P. brassicae to include the exotic B. orientalis and the role of top-down processes played by parasitoids in shaping herbivore host shifts are further discussed.


Exotic invasive species Volatiles Plant preference–performance Host shift Multitrophic interactions Bunias orientalis 



We thank Roel Wagenaar for rearing the parasitoid wasps; Leo Westerd for supplying butterfly eggs; Gregor Disveld for the technical assistance in the greenhouse; Olga Kostenko and Koen Verhoeven for the fruitful discussions on the statistical analyses; Keith Clay, Antoine Branca, and two anonymous reviewers for very valuable suggestions; This work was funded by a PhD-fellowship from the Portuguese governmental institution, Fundação para a Ciência e Tecnologia, to T. M. Fortuna (SFRH/BD/40531/2007).

Supplementary material

10530_2013_459_MOESM1_ESM.doc (629 kb)
Supplementary material 1 (DOC 629 kb)


  1. Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured Publishing CorporationGoogle Scholar
  2. Benrey B, Denno RF (1997) The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999Google Scholar
  3. Bernards MA (2010) Plant natural products: a primer. Can J Zool 88:601–614CrossRefGoogle Scholar
  4. Bukovinszky T, Gols R, Posthumus MA, Vet LEM, van Lenteren JC (2005) Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). J Chem Ecol 31:461–480PubMedCrossRefGoogle Scholar
  5. Bylesjo M, Rantalainen M, Cloarec O, Nicholson JK, Holmes E, Trygg J (2006) OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. J Chemometr 20:341–351CrossRefGoogle Scholar
  6. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  7. Camara MD (1997) A recent host range expansion in Junonia coenia Hubner (Nymphalidae): oviposition preference, survival, growth, and chemical defense. Evolution 51:873–884CrossRefGoogle Scholar
  8. Chew FS (1977) Coevolution of pierid butterflies and their cruciferous foodplants. II. The distribution of eggs on potential foodplants. Evolution 31:568–579CrossRefGoogle Scholar
  9. Cronin JT, Haynes KJ (2004) An invasive plant promotes unstable host-parasitoid patch dynamics. Ecology 85:2772–2782CrossRefGoogle Scholar
  10. Croteau RB, Davis EM, Ringer KL, Wildung MR (2005) (−)-Menthol biosynthesis and molecular genetics. Naturwissenschaften 92:562–577PubMedCrossRefGoogle Scholar
  11. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  12. Dicke M, Vet LEM (1999) Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore. In: Olff H, Brown VK, Drent RH (eds) Herbivores between plants and predators. Blackwell Science, London, pp 483–520Google Scholar
  13. Dietz H, Steinlein T, Ullmann I (1999) Establishment of the invasive perennial herb Bunias orientalis L.: an experimental approach. Acta Oecol 20:621–632CrossRefGoogle Scholar
  14. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  15. Engelkes T, Wouters B, Bezemer TM, Harvey JA, van der Putten WH (2012) Contrasting patterns of herbivore and predator pressure on invasive and native plants. Basic Appl Ecol 13:725–734CrossRefGoogle Scholar
  16. Feltwell J (1982) Large white butterfly: the biology, biochemistry and physiology of Pieris brassicae (Linnaeus). Dr W. Junk Publishers, The HagueGoogle Scholar
  17. Fortuna TM, Vet LEM, Harvey JA (2012) Effects of an invasive plant on the performance of two parasitoids with different host exploitation strategies. Biol Control 62:213–220CrossRefGoogle Scholar
  18. Geervliet JBF, Vet LEM, Dicke M (1996) Innate responses of the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes. J Insect Behav 9:525–538CrossRefGoogle Scholar
  19. Geervliet JBF, Posthumus MA, Vet LEM, Dicke M (1997) Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J Chem Ecol 23:2935–2954CrossRefGoogle Scholar
  20. Geervliet JBF, Vreugdenhil AI, Dicke M, Vet LEM (1998) Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol Exp Appl 86:241–252CrossRefGoogle Scholar
  21. Geervliet JBF, Verdel MSW, Snellen H, Schaub J, Dicke M, Vet LEM (2000) Coexistence and niche segregation by field populations of the parasitoids Cotesia glomerata and C. rubecula in the Netherlands: predicting field performance from laboratory data. Oecologia 124:55–63CrossRefGoogle Scholar
  22. Gols R, Witjes LMA, van Loon JJA, Posthumus MA, Dicke M, Harvey JA (2008) The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid. Entomol Exp Appl 128:99–108CrossRefGoogle Scholar
  23. Gols R, Bullock JM, Dicke M, Bukovinszky T, Harvey JA (2011) Smelling the wood from the trees: non-linear parasitoid responses to volatile attractants. J Chem Ecol 37:795–807PubMedCrossRefGoogle Scholar
  24. Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433CrossRefGoogle Scholar
  25. Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13:383–393PubMedCrossRefGoogle Scholar
  26. Harvey JA, Fortuna T (2012) Chemical and structural effects of invasive plants on herbivore-parasitoid/predator interactions in native communities. Entomol Exp Appl 144:14–26CrossRefGoogle Scholar
  27. Harvey JA, Biere A, Fortuna T, Vet LEM, Engelkes T, Morrien E, Gols R, Verhoeven K, Vogel H, Macel M, Heidel-Fischer HM, Schramm K, van der Putten WH (2010a) Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis. Biol Invasions 12:3045–3059CrossRefGoogle Scholar
  28. Harvey JA, Bukovinszky T, van der Putten WH (2010b) Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biol Conserv 143:2251–2259CrossRefGoogle Scholar
  29. Hood GM (2010) PopTools version 3.2.3. Available on the internet.
  30. Jaenike J (1978) Optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356PubMedCrossRefGoogle Scholar
  31. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273CrossRefGoogle Scholar
  32. Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385PubMedCrossRefGoogle Scholar
  33. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  34. Keeler MS, Chew FS (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568PubMedCrossRefGoogle Scholar
  35. Kühnle A, Müller C (2009) Differing acceptance of familiar and unfamiliar plant species by an oligophagous beetle. Entomol Exp Appl 131:189–199CrossRefGoogle Scholar
  36. Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host giant. Oikos 72:155–160CrossRefGoogle Scholar
  37. Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428CrossRefGoogle Scholar
  38. Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–667CrossRefGoogle Scholar
  39. Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75:59–68CrossRefGoogle Scholar
  40. Papaj DR (2000) Ovarian dynamics and host use. Annu Rev Entomol 45:423–448PubMedCrossRefGoogle Scholar
  41. Payne RW, Harding SA, Murray DA, Soutar DM, Baird DB, Glaser AI, Welham SJ, Gilmour AR, Thompson R, Webster R (2011) Guide to regression, nonlinear and generalized linear models in genstat. VSN International, Hemel HempsteadGoogle Scholar
  42. Pierre PS, Jansen JJ, Hordijk CA, van Dam NM, Cortesero AM, Dugravot S (2011) Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground. J Chem Ecol 37:368–377PubMedCrossRefGoogle Scholar
  43. Price PW, Bouton CE, Gross P, Mcpheron BA, Thompson JN, Weis AE (1980) Interactions among 3 trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  44. Rausher MD (1979) Larval habitat suitability and oviposition preference in three related butterflies. Ecology 60:503–511CrossRefGoogle Scholar
  45. Renwick JAA (2002) The chemical world of crucivores: lures, treats and traps. Entomol Exp Appl 104:35–42CrossRefGoogle Scholar
  46. Scheirs J, De Bruyn L, Verhagen R (2003) Host nutritive quality and host plant choice in two grass miners: primary roles for primary compounds? J Chem Ecol 29:1373–1389PubMedCrossRefGoogle Scholar
  47. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecol Lett 5:186–192CrossRefGoogle Scholar
  48. Singer MC, Ng D, Thomas CD (1988) Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977–985CrossRefGoogle Scholar
  49. Smid HM, van Loon JJA, Posthumus MA, Vet LEM (2002) GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176CrossRefGoogle Scholar
  50. Stamp N (2001) Enemy-free space via host plant chemistry and dispersion: assessing the influence of tri-trophic interactions. Oecologia 128:153–163CrossRefGoogle Scholar
  51. Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci 1:109–113CrossRefGoogle Scholar
  52. Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14CrossRefGoogle Scholar
  53. Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89CrossRefGoogle Scholar
  54. Travers-Martin N, Müller C (2008) Matching plant defence syndromes with performance and preference of a specialist herbivore. Funct Ecol 22:1033–1043CrossRefGoogle Scholar
  55. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253PubMedCrossRefGoogle Scholar
  56. Valladares G, Lawton JH (1991) Host-plant selection in the holly leaf-miner: does mother know best? J Anim Ecol 60:227–240CrossRefGoogle Scholar
  57. van Wijk M, de Bruijn PJA, Sabelis MW (2011) Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. Plos One 6:e21742Google Scholar
  58. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172CrossRefGoogle Scholar
  59. Vet LEM, Lewis WJ, Carde RT (1995) Parasitoid foraging and learning. In: Carde RT, Bell WJ (eds) Chemical ecology of insects 2. Chapman & Hall, New York, pp 65–101CrossRefGoogle Scholar
  60. Vet LEM, De Jong AG, Franchi E, Papaj DR (1998) The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Anim Behav 55:1271–1279PubMedCrossRefGoogle Scholar
  61. Vinson SB (1976) Host selection by insect parasitoids. Annu Rev Entomol 21:109–133CrossRefGoogle Scholar
  62. Vos M, Berrocal SM, Karamaouna F, Hemerik L, Vet LEM (2001) Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol Lett 4:38–45CrossRefGoogle Scholar
  63. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Taiadjana M. Fortuna
    • 1
    Email author
  • Jozef B. Woelke
    • 1
  • Cornelis A. Hordijk
    • 1
  • Jeroen J. Jansen
    • 2
  • Nicole M. van Dam
    • 3
  • Louise E. M. Vet
    • 1
  • Jeffrey A. Harvey
    • 1
  1. 1.Department of Terrestrial EcologyNetherlands Institute of EcologyWageningenThe Netherlands
  2. 2.Department of Analytical Chemistry, Institute for Molecules and MaterialsRadboud University NijmegenNijmegenThe Netherlands
  3. 3.Department of Ecogenomics, Institute for Water and Wetland Research (IWWR)Radboud University NijmegenNijmegenThe Netherlands

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