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PLOS Biology  2012 

Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host

DOI: 10.1371/journal.pbio.1001435

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Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.


[1]  Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37: 141–172. doi: 10.1146/annurev.en.37.010192.001041
[2]  Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56: 161–180. doi: 10.1146/annurev-ento-120709-144753
[3]  Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25: 348–357. doi: 10.1111/j.1365-2435.2010.01818.x
[4]  Price PW, Bouton CE, Gross P, Mcpheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11: 41–65. doi: 10.1146/
[5]  Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5: 317–324. doi: 10.1038/nchembio.169
[6]  Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help.”. Trends Plant Sci 15: 167–175. doi: 10.1016/j.tplants.2009.12.002
[7]  Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25: 137–144. doi: 10.1016/j.tree.2009.09.010
[8]  Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—“alarm calls” from plants increase apparency to herbivores and their natural enemies in nature. Ecol Lett 11: 24–34. doi: 10.1111/j.1461-0248.2007.01123.x
[9]  Ohgushi T (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol Exp Appl 128: 217–229. doi: 10.1111/j.1570-7458.2008.00705.x
[10]  Van Loon JJA, de Boer JG, Dicke M (2000) Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol Exp Appl 97: 219–227. doi: 10.1046/j.1570-7458.2000.00733.x
[11]  Fritzsche-Hoballah MEF, Turlings TCJ (2001) Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol Ecol Res 3: 553–565.
[12]  Smallegange RC, van Loon JJA, Blatt SE, Harvey JA, Dicke M (2008) Parasitoid load affects plant fitness in a tritrophic system. Entomol Exp Appl 128: 172–183. doi: 10.1111/j.1570-7458.2008.00693.x
[13]  Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72: 520–531. doi: 10.1046/j.1365-2656.2003.00722.x
[14]  Bukovinszky T, van Veen FJF, Jongema Y, Dicke M (2008) Direct and indirect consequences of resource quality on food web structure. Science 319: 804–807. doi: 10.1126/science.1148310
[15]  Sullivan DJ, V?lkl W (1999) Hyperparasitism: mutitrophic ecology and behaviour. Annu Rev Entomol 44: 291–315. doi: 10.1146/annurev.ento.44.1.291
[16]  V?lkl W, Sullivan DJ (2000) Foraging behaviour, host plant and host location in the aphid hyperparasitoid Euneura augarus. Entomol Exp Appl 97: 47–56. doi: 10.1046/j.1570-7458.2000.00715.x
[17]  Harvey JA, Wagenaar R, Bezemer TM (2009) Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources. J Anim Ecol 78: 686–692. doi: 10.1111/j.1365-2656.2008.01516.x
[18]  Fatouros NE, Van Loon JJA, Hordijk KA, Smid HM, Dicke M (2005) Herbivore-induced plant volatiles mediate in-flight host discrimination by parasitoids. J Chem Ecol 31: 2033–2047. doi: 10.1007/s10886-005-6076-5
[19]  Poelman EH, Gols R, Snoeren TAL, Muru D, Smid HM, Dicke M (2011) Indirect plant-mediated interactions among parasitoid larvae. Ecol Lett 14: 670–676. doi: 10.1111/j.1461-0248.2011.01629.x
[20]  Poelman EH, Zheng S-J, Zhang Z, Heemskerk NM, Cortesero A-M, Dicke M (2011) Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc Natl Acad Sci USA 108: 19647–19652. doi: 10.1073/pnas.1110748108
[21]  McDonald RC, Kok LT (1991) Hyperparasites attacking Cotesia glomerata (L.) and Cotesia rubecula (Marshall) (Hymenoptera: Braconidae) in Southwestern Virginia. Biol Control 1: 170–175. doi: 10.1016/1049-9644(91)90116-h
[22]  Brodeur J, Geervliet JBF, Vet LEM (1998) Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol Exp Appl 86: 145–152. doi: 10.1046/j.1570-7458.1998.00275.x
[23]  Le Masurier AD (1987) A comparative study of the relationship between host size and brood size in Apanteles spp. (Hymenoptera: Braconidae). Ecol Entomol 12: 383–393. doi: 10.1111/j.1365-2311.1987.tb01019.x
[24]  Mattiacci L, Dicke M, Posthumus MA (1995) β-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92: 2036–2040. doi: 10.1073/pnas.92.6.2036
[25]  D'Alessandro M, Turlings TCJ (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131: 24–32. doi: 10.1039/b507589k
[26]  Harvey JA (2000) Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness. Ecol Entomol 25: 267–278. doi: 10.1046/j.1365-2311.2000.00265.x
[27]  Adamo SA, (1997) How parasites alter the behavior of their insect hosts. In: Parasitic effects on host hormones and behavior, Beckage NE (Ed.). New York: Chapman & Hall. pp. 231–245.
[28]  Godfray HCJ (1994) Parasitoids: behaviour and evolutionary ecology. Princeton, NJ: Princeton University Press.
[29]  Harvey JA, Jervis MA, Gols R, Jiang N, Vet LEM (1999) Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation. J Insect Physiol 45: 173–182. doi: 10.1016/s0022-1910(98)00113-9
[30]  Harvey JA (2008) Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Evol Ecol 22: 153–166. doi: 10.1007/s10682-007-9164-x
[31]  Harvey JA, Wagenaar R, Gols R (2011) Differing host exploitation efficiencies in two hyperparasitoids: when is a “match made in heaven”? J Insect Behav 24: 282–292. doi: 10.1007/s10905-010-9254-4
[32]  Poelman EH, Oduor AMO, Broekgaarden C, Hordijk CA, Jansen JJ, et al. (2009) Field parasitism of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct Ecol 23: 951–962. doi: 10.1111/j.1365-2435.2009.01570.x
[33]  Poelman EH, van Loon JJA, Dicke M (2008) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13: 534–541. doi: 10.1016/j.tplants.2008.08.003
[34]  Meyer KM, Vos M, Mooij WM, Gera Hol WH, Termorshuizen AJ, et al. (2009) Quantifying the impact of above- and belowground higher trophic levels on plant and herbivore performance by modeling. Oikos 118: 981–990. doi: 10.1111/j.1600-0706.2009.17220.x
[35]  Orre GUS, Wratten SD, Jonsson M, Hale RJ (2010) Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biol Control 53: 62–67. doi: 10.1016/j.biocontrol.2009.10.010
[36]  Geervliet JBF, Verdel MSW, Snellen H, Schaub J, Dicke M, et al. (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: 55–63. doi: 10.1007/s004420050024
[37]  Takabayashi J, Dicke M (1992) Response of predatory mites with differing rearing histories to volatiles of uninfested plants. Entomol Exp Appl 64: 187–193. doi: 10.1111/j.1570-7458.1992.tb01608.x


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