Alien interference: Disruption of infochemical networks by invasive insect herbivores

Plant, Cell and Environment

Volumn 37, Issue 8, 2014, Pages 1854-1865

  Desurmont, Gaylord A ^a   Harvey, Jeff ^b   Van Dam, Nicole M ^c,h   Cristescu, Simona M ^c   Schiestl, Florian P ^d   Cozzolino, Salvatore ^e   Anderson, Peter ^f   Larsson, Mattias C ^f   Kindlmann, Pavel ^g   Danner, Holger ^c   Turlings, Ted C J ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e CNR Institute of Plant Protection   (Italy)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^g Charles University   (Czech Republic)

^h GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

Invasive species; Multitrophic interactions; Plant volatiles; Plant insect interactions

Indexed keywords

BIOLOGICAL INVASION; ECOSYSTEM FUNCTION; INTERFERENCE COMPETITION; INVASIVE SPECIES; NATIVE SPECIES; NATURAL ENEMY; PHYTOCHEMISTRY; PLANT-HERBIVORE INTERACTION; PLANT-INSECT INTERACTION; PLANT-POLLINATOR INTERACTION; TRITROPHIC INTERACTION; VOLATILE SUBSTANCE;

HEXAPODA;

VOLATILE ORGANIC COMPOUND;

ADAPTATION; ANIMAL; CHEMISTRY; ECOSYSTEM; HERBIVORY; INSECT; INTRODUCED SPECIES; INVASIVE SPECIES; MULTITROPHIC INTERACTIONS; PHYSIOLOGY; PLANT; PLANT VOLATILES; PLANT-INSECT INTERACTIONS; POLLINATION; REVIEW;

INVASIVE SPECIES; MULTITROPHIC INTERACTIONS; PLANT VOLATILES; PLANT-INSECT INTERACTIONS;

ADAPTATION, BIOLOGICAL; ANIMALS; ECOSYSTEM; HERBIVORY; INSECTS; INTRODUCED SPECIES; PLANTS; POLLINATION; VOLATILE ORGANIC COMPOUNDS;

EID: 84904352377     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12333     Document Type: Review

References (132)

1. Adler L.S., Karban R. & Strauss S.Y. (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82, 2032-2044.
2. Agrawal A.A. (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89, 493-500.
3. Akhtar Y. & Isman M. (2003) Larval exposure to oviposition deterrents alters subsequent oviposition behavior in generalist, Trichoplusia ni and specialist, Plutella xylostella moths. Journal of Chemical Ecology 29, 1853-1870.
4. Allison J.D. & Hare D.J. (2009) Learned and naive natural enemy responses and the interpretation of volatile organic compounds as cues or signals. New Phytologist 184, 768-782.
5. Arimura G.-I., Ozawa R., Horiuchi J.-I., Nishioka T. & Takabayashi J. (2001) Plant-plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochemical Systematics and Ecology 29, 1049-1061.
6. Arimura G.-I., Köpke S., Kunert M., Volpe V., David A., Brand P., ... Boland W. (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiology 146, 965-973.
7. Arimura G.-I., Matsui K. & Takabayashi J. (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant and Cell Physiology 50, 911-923.
8. Balbyshev N.F. & Lorenzen J.H. (1997) Hypersensitivity and egg drop: a novel mechanism of host plant resistance to Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 90, 652-657.
9. Bartkowska M.P. & Johnston M.O. (2012) Pollinators cause stronger selection than herbivores on floral traits in Lobelia cardinalis (Lobeliaceae). New Phytologist 193, 1039-1048.
10. Becerra J.X. (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276, 253-256.
11. Behmer S.T. (2008) Insect herbivore nutrient regulation. Annual Review of Entomology 54, 165-187.
12. Behmer S.T. & Elias D.O. (2000) Sterol metabolic constraints as a factor contributing to the maintenance of diet mixing in grasshoppers (Orthoptera: Acrididae). Physiological and Biochemical Zoology 73, 219-230.
13. Bernays E.A. & Chapman R.F. (1994) Host-Plant Selection by Phytophagous Insects, Springer, Berlin.
14. Bidart-Bouzat M.G. & Kliebenstein D. (2011) An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167, 677-689.
15. Blight M., Pickett J., Wadhams L. & Woodcock C. (1995) Antennal perception of oilseed rape, Brassica napus (Brassicaceae), volatiles by the cabbage seed weevil Ceutorhynchus assimilis (Coleoptera, Curculionidae). Journal of Chemical Ecology 21, 1649-1664.
16. Bruce T.J., Wadhams L.J. & Woodcock C.M. (2005) Insect host location: a volatile situation. Trends in Plant Science 10, 269-274.
17. Bukovinszky T., van Veen F.F., Jongema Y. & Dicke M. (2008) Direct and indirect effects of resource quality on food web structure. Science 319, 804-807.
18. Bukovinszky T., Poelman E.H., Kamp A., Hemerik L., Prekatsakis G. & Dicke M. (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Animal Behaviour 83, 501-509.
19. Callaway R.M. & Aschehoug E.T. (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290, 521-523.
20. Cardel Y.J. & Koptur S. (2010) Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant. International Journal of Plant Sciences 171, 283-292.
21. Chen Y., Schmelz E.A., Wäckers F. & Ruberson J.R. (2008) Cotton plant, Gossypium hirsutum L., defense in response to nitrogen fertilization. Journal of Chemical Ecology 34, 1553-1564.
22. Christensen S.A., Nemchenko A., Borrego E., Murray I., Sobhy I.S., Bosak L., ... Vaughn K.A. (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. The Plant Journal 74, 59-73.
23. Clavijo McCormick A., Unsicker S.B. & Gershenzon J. (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends in Plant Science 17, 303-310.
24. Colazza S., Cusumano A., Giudice D.L. & Peri E. (2014) Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59, 1-17.
25. Connor E.C., Rott A.S., Samietz J. & Dorn S. (2007) The role of the plant in attracting parasitoids: response to progressive mechanical wounding. Entomologia Experimentalis et Applicata 125, 145-155.
26. Cunningham J.P., Moore C.J., Zalucki M.P. & West S.A. (2004) Learning, odour preference and flower foraging in moths. Journal of Experimental Biology 207, 87-94.
27. Danderson C.A. & Molano-Flores B. (2010) Effects of herbivory and inflorescence size on insect visitation to Eryngium yuccifolium (Apiaceae) a prairie plant. The American Midland Naturalist 163, 234-246.
28. De Moraes C.M., Mescher M.C. & Tumlinson J.H. (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577-580.
29. Degenhardt J., Hiltpold I., Köllner T.G., Frey M., Gierl A., Gershenzon J., ... Turlings T.C. (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proceedings of the National Academy of Sciences 106, 13213-13218.
30. Desurmont G.A. & Weston P.A. (2010) Stimuli associated with viburnum leaf beetle (Pyrrhalta viburni) aggregative oviposition behavior. Entomologia Experimentalis et Applicata 135, 245-251.
31. Desurmont G.A. & Weston P.A. (2011) Aggregative oviposition of a phytophagous beetle overcomes egg-crushing plant defences. Ecological Entomology 36, 335-343.
32. Desurmont G.A., Donoghue M.J., Clement W.L. & Agrawal A.A. (2011) Evolutionary history predicts plant defense against an invasive pest. Proceedings of the National Academy of Sciences 108, 7070-7074.
33. Dicke M. (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? In Proceedings of the 10th International Symposium on Insect-Plant Relationships (eds S. Simpson, A.J. Mordue & J. Hardie ), pp. 131-142. Springer, Berlin.
34. Dicke M. & Sabelis M.W. (1988) How plants obtain predatory mites as bodyguards. Netherlands Journal of Zoology 38, 148-165.
35. Dudareva N., Negre F., Nagegowda D.A. & Orlova I. (2006) Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Sciences 25, 417-440.
36. Eigenbrode S.D., Ding H., Shiel P. & Berger P.H. (2002) Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proceedings of the Royal Society of London. Series B: Biological Sciences 269, 455-460.
37. Fadini M.A., Venzon M., Oliveira H., Pallini A. & Vilela E.F. (2010) Response of the predatory mite Phytoseiulus macropilis (Banks) to volatiles produced by strawberry plants in response to attack by tetranychid mites (Acari: Phytoseiidae: Tetranychidae). Neotropical Entomology 39, 248-252.
38. Fatouros N.E., Bukovinszkine'Kiss G., Dicke M. & Hilker M. (2007) The response specificity of Trichogramma egg parasitoids towards infochemicals during host location. Journal of Insect Behavior 20, 53-65.
39. Fenster C.B., Armbruster W.S., Wilson P., Dudash M.R. & Thomson J.D. (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35, 375-403.
40. Fitt G.P. (1989) The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology 34, 17-53.
41. Fordyce J. (2003) Aggregative feeding of pipevine swallowtail larvae enhances hostplant suitability. Oecologia 135, 250-257.
42. Fortuna T.M., Vet L.E. & Harvey J.A. (2012) Effects of an invasive plant on the performance of two parasitoids with different host exploitation strategies. Biological Control 62, 213-220.
43. Gandhi K.J. & Herms D.A. (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biological Invasions 12, 389-405.
44. Geervliet J.B., Vreugdenhil A.I., Dicke M. & Vet L.E. (1998) Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C.rubecula. Entomologia Experimentalis et Applicata 86, 241-252.
45. Gilbert G.S., Magarey R., Suiter K. & Webb C.O. (2012) Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evolutionary Applications 5, 869-878.
46. Girling R.D., Stewart-Jones A., Dherbecourt J., Staley J.T., Wright D.J. & Poppy G.M. (2011) Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles. Proceedings of the Royal Society B: Biological Sciences 278, 2646-2653.
47. Glinwood R., Ahmed E., Qvarfordt E. & Ninkovic V. (2011) Olfactory learning of plant genotypes by a polyphagous insect predator. Oecologia 166, 637-647.
48. Godfray H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology, Princeton University Press, Princeton, NJ.
49. Gouinguené S.P. & Turlings T.C. (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology 129, 1296-1307.
50. Hall D.E., MacGregor K.B., Nijsse J. & Bown A.W. (2004) Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. European Journal of Plant Pathology 110, 441-447.
51. Hare J.D. (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology 56, 161-180.
52. Harvey J.A. & Fortuna T.M. (2012) Chemical and structural effects of invasive plants on herbivore-parasitoid/predator interactions in native communities. Entomologia Experimentalis et Applicata 144, 14-26.
53. Harvey J.A., Bukovinszky T. & van der Putten W.H. (2010) Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biological Conservation 143, 2251-2259.
54. Hassell M. & May R. (1986) Generalist and specialist natural enemies in insect predator-prey interactions. The Journal of Animal Ecology 55, 923-940.
55. Heil M. (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). Journal of Chemical Ecology 30, 1289-1295.
56. Heil M. & Karban R. (2010) Explaining evolution of plant communication by airborne signals. Trends in Ecology & Evolution 25, 137-144.
57. Hilker M. & Meiners T. (2010) How do plants 'notice' attack by herbivorous arthropods? Biological Reviews 85, 267-280.
58. Holopainen J.K. (2004) Multiple functions of inducible plant volatiles. Trends in Plant Science 9, 529-533.
59. Horiuchi J.-I., Arimura G.-I., Ozawa R., Shimoda T., Takabayashi J. & Nishioka T. (2003) A comparison of the responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T.urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Applied Entomology and Zoology 38, 109-116.
60. Horiuchi J.-I., Arimura G.-I., Ozawa R., Shimoda T., Dicke M., Takabayashi J. & Nishioka T. (2003) Lima bean leaves exposed to herbivore-induced conspecific plant volatiles attract herbivores in addition to carnivores. Applied Entomology and Zoology 38, 365-368.
61. Johnson S.N. & Nielsen U.N. (2012) Foraging in the dark chemically mediated host plant location by belowground insect herbivores. Journal of Chemical Ecology 38, 604-614.
62. Kappers I.F., Aharoni A., Van Herpen T.W., Luckerhoff L.L., Dicke M. & Bouwmeester H.J. (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science Signaling 309, 2070-2072.
63. Karban R. (2001) Communication between sagebrush and wild tobacco in the field. Biochemical Systematics and Ecology 29, 995-1005.
64. Karban R., Agrawal A.A. & Mangel M. (1997) The benefits of induced defenses against herbivores. Ecology 78, 1351-1355.
65. Keane R.M. & Crawley M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164-170.
66. Keeler M.S. & Chew F.S. (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156, 559-568.
67. Kenis M., Auger-Rozenberg M.-A., Roques A., Timms L., Péré C., Cock M.J., ... Lopez-Vaamonde C. (2009) Ecological effects of invasive alien insects. In Ecological Impacts of Non-Native Invertebrates and Fungi on Terrestrial Ecosystems (eds Langor, David, Sweeney & Jon), pp. 21-45. Springer, Berlin.
68. Kessler A. & Baldwin I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141-2144.
69. Kessler A. & Halitschke R. (2007) Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Current Opinion in Plant Biology 10, 409-414.
70. Kessler A. & Halitschke R. (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Functional Ecology 23, 901-912.
71. Kessler A., Halitschke R. & Poveda K. (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92, 1769-1780.
72. Kessler D., Diezel C. & Baldwin I.T. (2010) Changing pollinators as a means of escaping herbivores. Current Biology 20, 237-242.
73. Lehtilä K. & Strauss S.Y. (1997) Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum. Oecologia 111, 396-403.
74. Leimu R., Muola A., Laukkanen L., Kalske A., Prill N. & Mutikainen P. (2012) Plant-herbivore coevolution in a changing world. Entomologia Experimentalis et Applicata 144, 3-13.
75. Lohman D., Zangerl A. & Berenbaum M. (1996) Impact of floral herbivory by parsnip webworm (Oecophoridae: Depressaria pastinacella Duponchel) on pollination and fitness of wild parsnip (Apiaceae: Pastinaca sativa L. American Midland Naturalist 136, 407-412.
76. Lucas-Barbosa D., van Loon J.J.A. & Dicke M. (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72, 1647-1654.
77. Lürling M. & Scheffer M. (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends in Ecology & Evolution 22, 374-379.
78. McCall A.C. & Irwin R.E. (2006) Florivory: the intersection of pollination and herbivory. Ecology Letters 9, 1351-1365.
79. Meiners T., Hacker N., Anderson P. & Hilker M. (2005) Response of the elm leaf beetle to host plants induced by oviposition and feeding: the infestation rate matters. Entomologia Experimentalis et Applicata 115, 171-177.
80. Mithöfer A. & Boland W. (2008) Recognition of herbivory-associated molecular patterns. Plant Physiology 146, 825-831.
81. Mithöfer A. & Boland W. (2012) Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology 63, 431-450.
82. Mithöfer A., Wanner G. & Boland W. (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiology 137, 1160-1168.
83. Mori N. & Yoshinaga N. (2011) Function and evolutionary diversity of fatty acid-amino acid conjugates in insects. Journal of Plant Interactions 6, 103-107.
84. Mumm R. & Dicke M. (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Canadian Journal of Zoology 88, 628-667.
85. Nottingham S.F., Hardie J., Dawson G.W., Hick A.J., Pickett J.A., Wadhams L.J. & Woodcock C.M. (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. Journal of Chemical Ecology 17, 1231-1242.
86. Pare P.W., Farag M.A., Krishnamachari V., Zhang H., Ryu C.-M. & Kloepper J.W. (2005) Elicitors and priming agents initiate plant defense responses. Photosynthesis Research 85, 149-159.
87. Pearse I.S., Harris D.J., Karban R. & Sih A. (2013) Predicting novel herbivore-plant interactions. Oikos 122, 1554-1564.
88. Pearson D.E. & Callaway R.M. (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biological Control 35, 288-298.
89. Peñuelas J. & Llusià J. (2004) Plant VOC emissions: making use of the unavoidable. Trends in Ecology & Evolution 19, 402-404.
90. Pichersky E. & Gershenzon J. (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5, 237-243.
91. Pierre P.S., Jansen J.J., Hordijk C.A., van Dam N.M., Cortesero A.-M. & Dugravot S. (2011) Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground. Journal of Chemical Ecology 37, 368-377.
92. Poelman E.H., Broekgaarden C., Van Loon J.J.A. & Dicke M. (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Molecular Ecology 17, 3352-3365.
93. Poelman E.H., Zheng S.-J., Zhang Z., Heemskerk N.M., Cortesero A.-M. & Dicke M. (2011) Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proceedings of the National Academy of Sciences 108, 19647-19652.
94. Poelman E.H., Bruinsma M., Zhu F., Weldegergis B.T., Boursault A.E., Jongema Y., ... Dicke M. (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biology 10, e1001435.
95. Poveda K., Steffan-Dewenter I., Scheu S. & Tscharntke T. (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601-605.
96. Quicke D.L. (1997) Parasitic wasps, Chapman & Hall Ltd., London.
97. Radville L., Chaves A. & Preisser E.L. (2011) Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis). Journal of Chemical Ecology 37, 592-597.
98. Raffa K.F., Phillips T.W. & Salom S.M. (1993) Strategies and mechanisms of host colonization by bark beetles. In Beetle-Pathogen Interactions in Conifer Forests (eds T.O. Schowalter & G. Filip ), pp. 103-128. Academic Press, New York, NY, USA.
99. Raguso R.A. (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution, and Systematics 39, 549-569.
100. Rasmann S., Köllner T.G., Degenhardt J., Hiltpold I., Toepfer S., Kuhlmann U., ... Turlings T.C. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732-737.
101. Reaser J.K., Meyerson L.A., Cronk Q., De Poorter M., Eldrege L., Green E., ... Mauremootoo J. (2007) Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environmental Conservation 34, 98-111.
102. Reymond P. (2013) Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238, 247-258.
103. Riffell J.A. (2011) The neuroecology of a pollinator's buffet: olfactory preferences and learning in insect pollinators. Integrative and Comparative Biology 51, 781-793.
104. de Rijk M., Dicke M. & Poelman E.H. (2013) Foraging behaviour by parasitoids in multiherbivore communities. Animal Behaviour 85, 1517-1528.
105. Robert C.A.M., Erb M., Hibbard B.E., French B.W., Zwahlen C. & Turlings T.C.J. (2012) A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Functional Ecology 26, 1429-1440.
106. Sakai A.K., Allendorf F.W., Holt J.S., Lodge D.M., Molofsky J., With K.A., ... Ellstrand N.C. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305-332.
107. Schiestl F.P. (2010) The evolution of floral scent and insect chemical communication. Ecology Letters 13, 643-656.
108. Schiestl F.P. & Johnson S.D. (2013) Pollinator-mediated evolution of floral signals. Trends in Ecology & Evolution 28, 307-315.
109. Schiestl F.P., Kirk H., Bigler L., Cozzolino S. & Desurmont G.A. (2014) Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. New Phytologist DOI: 10.1111/nph.12783
110. Shiojiri K., Takabayashi J., Yano S. & Takafuji A. (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecology Letters 5, 186-192.
111. Smallegange R., Van Loon J., Blatt S., Harvey J., Agerbirk N. & Dicke M. (2007) Flower versus leaf feeding by Pieris brassicae: glucosinolate-rich flower tissues are preferred and sustain higher growth rate. Journal of Chemical Ecology 33, 1831-1844.
112. Snoeren T.A., Mumm R., Poelman E.H., Yang Y., Pichersky E. & Dicke M. (2010) The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. Journal of Chemical Ecology 36, 479-489.
113. Sorte C.J., Williams S.L. & Zerebecki R.A. (2010) Ocean warming increases threat of invasive species in a marine fouling community. Ecology 91, 2198-2204.
114. Tamiru A., Bruce T.J., Woodcock C.M., Caulfield J.C., Midega C.A., Ogol C.K., ... Khan Z.R. (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters 14, 1075-1083.
115. Ton J., D'Alessandro M., Jourdie V., Jakab G., Karlen D., Held M., ... Turlings T.C. (2007) Priming by airborne signals boosts direct and indirect resistance in maize. The Plant Journal 49, 16-26.
116. Tumlinson J.H. & Engelberth J. (2008) Fatty acid-derived signals that induce or regulate plant defenses against herbivory. In Induced Plant Resistance to Herbivory (ed. A. Schaller ), pp. 389-407. Springer, Berlin.
117. Turlings T.C., Tumlinson J.H. & Lewis W. (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251-1253.
118. Turlings T.C., Wäckers F.L., Vet L.E., Lewis W.J. & Tumlinson J.H. (1993) Learning of host-finding cues by hymenopterous parasitoids. In Insect Learning (eds D.R. Papaj & A.C. Lewis ), pp. 51-78. Springer, Berlin, Chapman and Hall, New York.
119. Vet L.E. & Dicke M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141-172.
120. Vet L.E., Lewis W.J. & Carde R.T. (1995) Parasitoid foraging and learning. In Chemical Ecology of Insects 2 (eds R.T. Cardé & W.J. Bell ), pp. 65-101. Springer, Berlin.
121. Vilà M., Espinar J.L., Hejda M., Hulme P.E., Jarošík V., Maron J.L., ... Pyšek P. (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecology Letters 14, 702-708.
122. Visser J. & Avé D. (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata. Entomologia Experimentalis et Applicata 24, 738-749.
123. Vos M., Berrocal S.M., Karamaouna F., Hemerik L. & Vet L. (2001) Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecology Letters 4, 38-45.
124. Walther G.-R., Roques A., Hulme P.E., Sykes M.T., Pyšek P., Kühn I., ... Bugmann H. (2009) Alien species in a warmer world: risks and opportunities. Trends in Ecology & Evolution 24, 686-693.
125. Webster B., Qvarfordt E., Olsson U. & Glinwood R. (2013) Different roles for innate and learnt behavioral responses to odors in insect host location. Behavioral Ecology 24, 366-372.
126. White E.M., Wilson J.C. & Clarke A.R. (2006) Biotic indirect effects: a neglected concept in invasion biology. Diversity and Distributions 12, 443-455.
127. Winter T.R. & Rostás M. (2010) Nitrogen deficiency affects bottom-up cascade without disrupting indirect plant defense. Journal of Chemical Ecology 36, 642-651.
128. Woodard A.M., Ervin G.N. & Marsico T.D. (2012) Host plant defense signaling in response to a coevolved herbivore combats introduced herbivore attack. Ecology and Evolution 2, 1056-1064.
129. Wright G.A. & Schiestl F.P. (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology 23, 841-851.
130. Wu J. & Baldwin I.T. (2010) New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44, 1-24.
131. Yoneya K., Kugimiya S. & Takabayashi J. (2009) Can herbivore-induced plant volatiles inform predatory insect about the most suitable stage of its prey? Physiological Entomology 34, 379-386.
132. Yoshinaga N., Alborn H.T., Nakanishi T., Suckling D.M., Nishida R., Tumlinson J.H. & Mori N. (2010) Fatty acid-amino acid conjugates diversification in lepidopteran caterpillars. Journal of Chemical Ecology 36, 319-325.