Abstract
Plants can influence the effectiveness of microbial insecticides through numerous mechanisms. One of these mechanisms is the oxidation of plant phenolics by plant enzymes, such as polyphenol oxidases (PPO) and peroxidases (POD). These reactions generate a variety of products and intermediates that play important roles in resistance against herbivores. Oxidation of the catecholic phenolic compound chlorogenic acid by PPO enhances the lethality of the insect-killing bacterial pathogen, Bacillus thuringiensis var. kurstaki (Bt) to the polyphagous caterpillar, Helicoverpa zea. Since herbivore feeding damage often triggers the induction of higher activities of oxidative enzymes in plant tissues, here we hypothesized that the induction of plant defenses would enhance the lethality of Bt on those plants. We found that the lethality of a commercial formulation of Bt (Dipel® PRO DF) on tomato plants was higher if it was applied to plants that were induced by H. zea feeding or induced by the phytohormone jasmonic acid. Higher proportions of H. zea larvae killed by Bt were strongly correlated with higher levels of PPO activity in the leaflet tissue. Higher POD activity was only weakly associated with higher levels of Bt-induced mortality. While plant-mediated variation in entomopathogen lethality is well known, our findings demonstrate that plants can induce defensive responses that work in concert with a microbial insecticide/entomopathogen to protect against insect herbivores.
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References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a
Acevedo FE, Peiffer M, Tan C-W et al (2017) Fall armyworm-associated gut bacteria modulate plant defense responses. Mol Plant-Microbe Interact 30:127–137. https://doi.org/10.1094/MPMI-11-16-0240-R
Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432. https://doi.org/10.1111/j.1365-2435.2010.01796.x
Ali MI, Felton GW, Meade T, Young SY (1998) Influence of interspecific and intraspecific host plant variation on the susceptibility of Heliothines to a baculovirus. Biol Control 12:42–49. https://doi.org/10.1006/bcon.1998.0619
Ali MI, Young SY, McNew RC (2004) Host plant influence on activity of Bacillus thuringiensis Berliner against lepidopterous pests of crops. J Entomol Sci 39:311–317. https://doi.org/10.18474/0749-8004-39.3.311
Appel HM, Schultz JC (1994) Oak tannins reduce effectiveness of Thuricide (Bacillus thuringiensis) in the gypsy moth (Lepidoptera: Lymantriidae). J Econ Entomol 87:1736–1742
Bauce É, Bidon Y, Berthiaume R (2002) Effects of food nutritive quality and Bacillus thuringiensis on feeding behaviour, food utilization and larval growth of spruce budworm Choristoneura fumiferana (Clem.) when exposed as fourth- and sixth-instar larvae. Agric For Entomol 4:57–70. https://doi.org/10.1046/j.1461-9563.2002.00123.x
Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530. https://doi.org/10.1007/BF02035149
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brar SK, Verma M, Tyagi RD et al (2007) Bacillus thuringiensis proteases: production and role in growth, sporulation and synergism. Process Biochem 42:773–790. https://doi.org/10.1016/j.procbio.2007.01.015
Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435. https://doi.org/10.1016/j.toxicon.2006.11.022
Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431. https://doi.org/10.1016/j.ibmb.2011.02.006
Broadway RM, Duffey SS, Pearce G, Ryan CA (1986) Plant proteinase inhibitors: a defense against herbivorous insects? Entomol Exp Appl 41:33–38. https://doi.org/10.1111/j.1570-7458.1986.tb02168.x
Bukovinszky T, Poelman EH, Gols R et al (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308. https://doi.org/10.1007/s00442-009-1308-y
Carisey N, Bauce É, Dupont A, Miron S (2004) Effects of bud phenology and foliage chemistry of balsam fir and white spruce trees on the efficacy of Bacillus thuringiensis against the spruce budworm, Choristoneura fumiferana. Agric For Entomol 6:55–69. https://doi.org/10.1111/j.1461-9555.2004.00204.x
Chen MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114. https://doi.org/10.1111/j.1744-7917.2008.00190.x
Chippendale GM (1970) Metamorphic changes in fat body proteins of the southwestern corn borer, Diatraea grandiosella. J Insect Physiol 16:1057–1068
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induc. Plant Resist. to Herbiv. Springer Netherlands, Dordrecht, pp 253–269
Cornforth DM, Matthews A, Brown SP, Raymond B (2015) Bacterial cooperation causes systematic errors in pathogen risk assessment due to the failure of the independent action hypothesis. PLOS Pathog 11:e1004775. https://doi.org/10.1371/journal.ppat.1004775
Cory JS, Hoover K (2006) Plant-mediated effects in insect-pathogen interactions. Trends Ecol Evol 21:278–286. https://doi.org/10.1016/j.tree.2006.02.005
De Leo F, Bonadé-Bottino MA, Ceci LR et al (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol 118:997–1004. https://doi.org/10.1104/pp.118.3.997
Deans CA, Sword GA, Behmer ST (2015) Revisiting macronutrient regulation in the polyphagous herbivore Helicoverpa zea (Lepidoptera: Noctuidae): new insights via nutritional geometry. J Insect Physiol 81:21–27. https://doi.org/10.1016/j.jinsphys.2015.06.015
Deans CA, Behmer ST, Tessnow AE et al (2017) Nutrition affects insect susceptibility to Bt toxins. Sci Rep 7:39705. https://doi.org/10.1038/srep39705
Estruch JJ, Warren GW, Mullins MA et al (1996) Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc Natl Acad Sci 93:5389–5394. https://doi.org/10.1073/pnas.93.11.5389
Felton GW, Dahlman DL (1984) Allelochemical induced stress: effects of l-canavanine on the pathogenicity of Bacillus thuringiensis in Manduca sexta. J Invertebr Pathol 44:187–191. https://doi.org/10.1016/0022-2011(84)90011-9
Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694. https://doi.org/10.1007/BF01014725
Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38:277–285. https://doi.org/10.1016/0022-1910(92)90128-Z
Granados RR, Fu Y, Corsaro B, Hughes PR (2001) Enhancement of Bacillus thuringiensis toxicity to Lepidopterous species with the enhancin from Trichoplusia ni granulovirus. Biol Control 20:153–159. https://doi.org/10.1006/bcon.2000.0891
Grizanova EV, Dubovskiy IM, Whitten MMA, Glupov VV (2014) Contributions of cellular and humoral immunity of Galleria mellonella larvae in defence against oral infection by Bacillus thuringiensis. J Invertebr Pathol 119:40–46. https://doi.org/10.1016/j.jip.2014.04.003
Hoover K, Stout MJ, Alaniz SA et al (1998a) Influence of induced plant defenses in cotton and tomato on the efficacy of baculoviruses on noctuid larvae. J Chem Ecol 24:253–271
Hoover K, Yee JL, Schultz CM et al (1998b) Effects of plant identity and chemical constituents on the efficacy of a baculovirus against Heliothis virescens. J Chem Ecol 24:221–252
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825
Hwang SY, Lindhoth RL, Montgomery ME, Shields KS (1995) Aspen leaf quality affects gypsy moth (Lepidoptera: Lymantriidae) susceptibility to Bacillus thuringiensis. J Econ Entomol 88:278–282. https://doi.org/10.1093/jee/88.2.278
Inagaki S, Miyasono M, Yamamoto M et al (1992) Induction of antibacterial activity against Bacillus thuringiensis in the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Appl Entomol Zool 27:565–570. https://doi.org/10.1303/aez.27.565
Jafary M, Karimzadeh J, Farazmand H, Rezapanah M (2016) Plant-mediated vulnerability of an insect herbivore to Bacillus thuringiensis in a plant-herbivore-pathogen system. Biocontrol Sci Technol 26:104–115. https://doi.org/10.1080/09583157.2015.1078872
Janmaat AF, Myers JH (2007) Host-plant effects the expression of resistance to Bacillus thuringiensis kurstaki in Trichoplusia ni (Hubner): an important factor in resistance evolution. J Evol Biol 20:62–69. https://doi.org/10.1111/j.1420-9101.2006.01232.x
Janmaat AF, Ware J, Myers J (2007) Effects of crop type on Bacillus thuringiensis toxicity and residual activity against Trichoplusia ni in greenhouses. J Appl Entomol 131:333–337. https://doi.org/10.1111/j.1439-0418.2007.01181.x
Keating ST, Yendol WG, Schultz JC (1988) Relationship between susceptibility of gypsy moth larvae (Lepidoptera: Lymantriidae) to a baculovirus and host plant foliage constituents. Environ Entomol 17:952–958
Kouassi KC, Lorenzetti F, Guertin C et al (2001) Variation in the susceptibility of the forest tent caterpillar (Lepidoptera: Lasiocampidae) to Bacillus thuringiensis variety kurstaki HD-1: effect of the host plant. J Econ Entomol 94:1135–1141. https://doi.org/10.1603/0022-0493-94.5.1135
Krischik VA, Barbosa P, Reichelderfer CF (1988) Three trophic level interactions: allelochemicals, Manduca sexta (L.), and Bacillus thuringiensis var. kurstaki Berliner. Environ Entomol 17:476–482. https://doi.org/10.1093/ee/17.3.476
Lacey LA, Grzywacz D, Shapiro-Ilan DI et al (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41. https://doi.org/10.1016/j.jip.2015.07.009
Lampert E (2012) Influences of plant traits on immune responses of specialist and generalist herbivores. Insects 3:573–592. https://doi.org/10.3390/insects3020573
Laurentz M, Reudler JH, Mappes J et al (2012) Diet quality can play a critical role in defense efficacy against parasitoids and pathogens in the Glanville fritillary (Melitaea cinxia). J Chem Ecol 38:116–125. https://doi.org/10.1007/s10886-012-0066-1
Lee KP, Raubeneimer D, Behmer ST, Simpson SJ (2003) A correlation between macronutrient balancing and insect host-plant range: evidence from the specialist caterpillar Spodoptera exempta (Walker). J Insect Physiol 49:1161–1171. https://doi.org/10.1016/j.jinsphys.2003.08.013
Lee KP, Cory JS, Wilson K et al (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc B Biol Sci 273:823–829. https://doi.org/10.1098/rspb.2005.3385
Lee KP, Simpson SJ, Wilson K (2008) Dietary protein-quality influences melanization and immune function in an insect. Funct Ecol 22:1052–1061. https://doi.org/10.1111/j.1365-2435.2008.01459.x
Lord JC, Undeen AH (1990) Inhibition of the Bacillus thuringiensis var. israelensis toxin by dissolved tannins. Environ Entomol 19:1547–1551. https://doi.org/10.1093/ee/19.5.1547
Ludlum CT, Felton GW, Duffey SS (1991) Plant defenses: chlorogenic acid and polyphenol oxidase enhance toxicity of Bacillus thuringiensis subsp. kurstaki to Heliothis zea. J Chem Ecol 17:217–237. https://doi.org/10.1007/BF00994435
Lüthy P, Hofmann C, Jaquet F (1985) Inactivation of delta-endotoxin of Bacillus thuringiensis by tannin. FEMS Microbiol Lett 28:31–33
Ma G, Roberts H, Sarjan M et al (2005) Is the mature endotoxin Cry1Ac from Bacillus thuringiensis inactivated by a coagulation reaction in the gut lumen of resistant Helicoverpa armigera larvae? Insect Biochem Mol Biol 35:729–739. https://doi.org/10.1016/j.ibmb.2005.02.011
MacIntosh SC, Kishore GM, Perlak FJ et al (1990) Potentiation of Bacillus thuringiensis insecticidal activity by serine protease inhibitors. J Agric Food Chem 38:1145–1152. https://doi.org/10.1021/jf00094a051
McLeod PJ, Yearian WC, Young SY (1977) Inactivation of Baculovirus heliothis by ultraviolet irradiation, dew, and temperature. J Invertebr Pathol 30:237–241. https://doi.org/10.1016/0022-2011(77)90225-7
Meade T, Hare J (1993) Effects of differential host plant consumption by Spodoptera exigua (Lepidoptera: Noctuidae) on Bacillus thuringiensis efficacy. Environ Entomol 22:432–437
Meade T, Hare JD (1994) Effects of genetic and environmental host-plant variation on the susceptibility of two noctuids to Bacillus thuringiensis. Entomol Exp Appl 70:165–178
Ment D, Shikano I, Glazer I (2017) Abiotic factors. In: Hajek AE, Shapiro-Ilan DI (eds) Ecol. Invertebr. Dis. Wiley, Ltd, Hoboken, pp 143–186
Mohan S, Ma PWK, Pechan T et al (2006) Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28. https://doi.org/10.1016/j.jinsphys.2005.08.011
Navon A, Hare JD, Federici BA (1993) Interactions among Heliothis virescens larvae, cotton condensed tannin and the CryIA(c) δ-endotoxin of Bacillus thuringiensis. J Chem Ecol 19:2485–2499. https://doi.org/10.1007/BF00980685
Ojala K, Julkunen-Tiitto R, Lindström L, Mappes J (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170
Olsen KM, Daly JC, Finnegan EJ, Mahon RJ (2005) Changes in Cry1Ac Bt transgenic cotton in response to two environmental factors: temperature and insect damage. J Econ Entomol 98:1382–1390. https://doi.org/10.1603/0022-0493-98.4.1382
Orpet RJ, Degain BA, Unnithan GC et al (2015) Effects of dietary protein to carbohydrate ratio on Bt toxicity and fitness costs of resistance in Helicoverpa zea. Entomol Exp Appl 156:28–36. https://doi.org/10.1111/eea.12308
Paramasiva I, Krishnayya PV, War AR, Sharma HC (2014) Crop hosts and genotypic resistance influence the biological activity of Bacillus thuringiensis towards Helicoverpa armigera. Crop Prot 64:38–46. https://doi.org/10.1016/j.cropro.2014.05.010
Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci 99:13319–13323. https://doi.org/10.1073/pnas.202224899
Plymale R, Grove MJ, Cox-Foster D et al (2008) Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. J Insect Physiol 54:737–749. https://doi.org/10.1016/j.jinsphys.2008.02.005
Povey S, Cotter SC, Simpson SJ, Wilson K (2014) Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J Anim Ecol 83:245–255. https://doi.org/10.1111/1365-2656.12127
Rahman MM, Roberts HLS, Sarjan M et al (2004) Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc Natl Acad Sci 101:2696–2699. https://doi.org/10.1073/pnas.0306669101
Raymond B, Hails RS (2007) Variation in plant resource quality and the transmission and fitness of the winter moth, Operophtera brumata nucleopolyhedrovirus. Biol Control 41:237–245. https://doi.org/10.1016/j.biocontrol.2007.02.005
Raymond B, Vanbergen A, Pearce I et al (2002) Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus. Oecologia 131:533–541. https://doi.org/10.1007/s00442-002-0926-4
Raymond B, Johnston PR, Nielsen-LeRoux C et al (2010) Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 18:189–194. https://doi.org/10.1016/j.tim.2010.02.006
Robinson DS, Eskin NAM (eds) (1991) Oxidative enzymes in foods. Elsevier Applied Science, London
Schaller A (ed) (2008) Induced Plant Resistance to Herbivory. https://doi.org/10.1007/978-1-4020-8182-8
Shikano I (2017) Evolutionary ecology of multitrophic interactions between plants, insect herbivores and entomopathogens. J Chem Ecol 43:586–598. https://doi.org/10.1007/s10886-017-0850-z
Shikano I, Cory JS (2014) Dietary mechanism behind the costs associated with resistance to Bacillus thuringiensis in the cabbage looper, Trichoplusia ni. PLoS One 9:e105864. https://doi.org/10.1371/journal.pone.0105864
Shikano I, Ericsson JD, Cory JS, Myers JH (2010) Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic Appl Ecol 11:15–22. https://doi.org/10.1016/j.baae.2009.06.008
Shikano I, Oak MC, Halpert-Scanderbeg O, Cory JS (2015a) Trade-offs between transgenerational transfer of nutritional stress tolerance and immune priming. Funct Ecol 29:1156–1164. https://doi.org/10.1111/1365-2435.12422
Shikano I, Olson GL, Cory JS (2015b) Impact of non-pathogenic bacteria on insect disease resistance: importance of ecological context. Ecol Entomol 40:620–628. https://doi.org/10.1111/een.12235
Shikano I, McCarthy EM, Elderd BD, Hoover K (2017a) Plant genotype and induced defenses affect the productivity of an insect-killing obligate viral pathogen. J Invertebr Pathol 148:34–42. https://doi.org/10.1016/j.jip.2017.05.001
Shikano I, Shumaker KL, Peiffer M et al (2017b) Plant-mediated effects on an insect–pathogen interaction vary with intraspecific genetic variation in plant defences. Oecologia 183:1121–1134. https://doi.org/10.1007/s00442-017-3826-3
Sivamani E, Rajendran N, Senrayan R et al (1992) Influence of some plant phenolics on the activity of δ-endotoxin of Bacillus thuringiensis var. galleriae on Heliothis armigera. Entomol Exp Appl 63:243–248. https://doi.org/10.1111/j.1570-7458.1992.tb01580.x
Smilanich AM, Mason PA, Sprung L et al (2011) Complex effects of parasitoids on pharmacophagy and diet choice of a polyphagous caterpillar. Oecologia 165:995–1005. https://doi.org/10.1007/s00442-010-1803-1
Smilanich AM, Langus TC, Doan L et al (2017) Host plant associated enhancement of immunity and survival in virus infected caterpillars. J Invertebr Pathol. https://doi.org/10.1016/j.jip.2017.11.006
Smirnoff WA, Hutchison PM (1965) Bacteriostatic and bacteriocidal effects of extracts of foliage from various plant species on Bacillus thuringiensis var. thuringiensis Berliner. J Invertebr Pathol 7:273–280. https://doi.org/10.1016/0022-2011(65)90001-7
Stevenson PC, D’Cunha RF, Grzywacz D (2010) Inactivation of baculovirus by isoflavonoids on chickpea (Cicer arietinum) leaf surfaces reduces the efficacy of nucleopolyhedrovirus against Helicoverpa armigera. J Chem Ecol 36:227–235. https://doi.org/10.1007/s10886-010-9748-8
Stout M (1996) Temporal and ontogenetic aspects of protein induction in foliage of the tomato, Lycopersicon esculentum. Biochem Syst Ecol 24:611–625. https://doi.org/10.1016/S0305-1978(97)81205-7
Stout MJ, Workman J, Duffey SS (1994) Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20:2575–2594. https://doi.org/10.1007/BF02036193
Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol Exp Appl 86:267–279. https://doi.org/10.1023/A:1003199023355
Tamez-Guerra P, Valadez-Lira JA, Alcocer-González JM et al (2008) Detection of genes encoding antimicrobial peptides in Mexican strains of Trichoplusia ni (Hübner) exposed to Bacillus thuringiensis. J Invertebr Pathol 98:218–227. https://doi.org/10.1016/j.jip.2008.02.008
Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781. https://doi.org/10.1007/BF02028503
Vachon V, Laprade R, Schwartz J-L (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 111:1–12. https://doi.org/10.1016/j.jip.2012.05.001
Vijendravarma RK, Narasimha S, Chakrabarti S et al (2015) Gut physiology mediates a trade-off between adaptation to malnutrition and susceptibility to food-borne pathogens. Ecol Lett 18:1078–1086. https://doi.org/10.1111/ele.12490
Wan N-F, Jiang J-X, Li B (2016) Effect of host plants on the infectivity of nucleopolyhedrovirus to Spodoptera exigua larvae. J Appl Entomol 140:636–644. https://doi.org/10.1111/jen.12298
Young SY, Yearian WC, Kim KS (1977) Effect of dew from cotton and soybean foliage on activity of Heliothis nuclear polyhedrosis virus. J Invertebr Pathol 29:105–111. https://doi.org/10.1016/0022-2011(77)90180-X
Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858. https://doi.org/10.1104/pp.107.112177
Acknowledgements
I.S. acknowledges financial support from the Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship (NSERC PDF-488105-2016), and Q.P. acknowledges financial support from the China Scholarship Council (Grant 201506300111).
Funding
This research was funded by the National Science Foundation, Division of Integrative Organismal Systems, Plant Biotic Interactions Program (Grant 1645548) and the United States Department of Agriculture, Agriculture and Food Research Initiative (AFRI 2017-67013-26596).
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Shikano, I., Pan, Q., Hoover, K. et al. Herbivore-Induced Defenses in Tomato Plants Enhance the Lethality of the Entomopathogenic Bacterium, Bacillus thuringiensis var. kurstaki. J Chem Ecol 44, 947–956 (2018). https://doi.org/10.1007/s10886-018-0987-4
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DOI: https://doi.org/10.1007/s10886-018-0987-4