Abstract
Plant defenses that respond to the threat of herbivory require accurate sensing of the presence of herbivores. Herbivory cues include mechanical damage, elicitors from insect saliva or eggs, and airborne volatiles emitted by wounded plants. Plants can also respond to the leaf vibrations produced by chewing herbivores. However, previous studies of the influence of feeding vibrations on plant defenses have been limited to single species pairs. In this study we test the hypothesis that chewing vibrations differ among herbivore species, both in their acoustic features and in their potential effect on plant defense responses. We first compare the acoustic traits of larval feeding vibrations in ten species from six families of Lepidoptera and one family of Hymenoptera. We then test responses of Arabidopsis thaliana plants to variation among feeding vibrations of different individuals of one species, and to feeding vibrations of two species, including a pierid butterfly and a noctuid moth. All feeding vibrations consisted of repetitive pulses of vibration associated with leaf tissue removal, although chewing rates varied between species and between large and small individuals within species. The frequency spectra of the vibrations generated by leaf feeding were similar across all ten species. Induced increases in anthocyanins in A. thaliana did not differ when plants were played vibrations from different individuals, or vibrations of two species of herbivores with different chewing rates, when amplitude was held constant. These results suggest that feeding vibrations provide a consistent set of cues for plant recognition of herbivores.
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References
Appel HM, Cocroft RB (2014) Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–1266. https://doi.org/10.1007/s00442-014-2995-6
Baldwin IT, Kessler A, Halitschke R (2002) Volatile signaling in plant-plant-herbivore interactions: what is real? Curr Opin Plant Biol 5:1–4. https://doi.org/10.1016/S1369-5266(02)00263-7
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Berens ML, Wolinska KZ, Spaepen S, Ziegler J, Nobori T, Nair A, Krüler V, Winkelmüller TM, Wang Y, Mine A, Becker D, Garrido-Otera R, Schulze-Lefert P, Tsuda K (2019) Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. PNAS 116:2364–2373. https://doi.org/10.1073/pnas.1817233116
Bernays EA (1997) Feeding by lepidopteran larvae is dangerous. Ecol Entomol 22:121–123. https://doi.org/10.1046/j.1365-2311.1997.00042.x
Bernays EA, Janzen DH (1988) Saturniid and sphingid caterpillars: two ways to eat leaves. Ecology 69:1153–1160. https://doi.org/10.2307/1941269
Bernays EA, Jarzembowski RA, Malcolm SB (1991) Evolution of insect morphology in relation to plants. Philos Trans Biol Sci 333:257–264. https://doi.org/10.1098/rstb.1991.0075
Bernays EA, Singer MS, Rodrigues D (2004) Foraging in nature: Foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecol Entomol 29:389–397. https://doi.org/10.1111/j.0307-6946.2004.00615.x
Body MJA, Neer WC, Vore C, Lin C-H, Vu D, Cocroft RB, Appel HA (2019a) Caterpillar chewing vibrations cause changes in plant hormones and volatile emissions in Arabidopsis thaliana. Front Plant Sci 10:810. https://doi.org/10.3389/fpls.2019.00810
Body MJA, Dave DF, Coffman CM, Paret TY, Koo AJ, Cocroft RB, Appel HM (2019b) Use of YFP fluorescence to track OPR3 expression in A. thaliana responses to insect herbivory. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01586
Bown AW, Hall DE, MacGregor KB (2002) Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiol 129:1430–1434. https://doi.org/10.1104/pp.006114
Brumm H, Slabbekoorn H (2005) Acoustic com-munication in noise. Adv Study Behav 35:151–209. https://doi.org/10.1016/S0065-3454(05)35004-2
Choi S, Kwon YR, Hossain MA, Hong SW, Lee BH, Lee H (2009) A mutation in ELA1, an age-dependent negative regulator of PAP1/MYB75, causes UV- and cold-stress tolerance in Arabidopsis thaliana seedlings. Plant Sci 176:678–686. https://doi.org/10.1016/j.plantsci.2009.02.010
Clissold F (2007) The biomechanics of chewing and plant fracture: mechanisms and implications. Adv Insect Phys 34:317–372. https://doi.org/10.1016/S0065-2806(07)34006-X
Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334. https://doi.org/10.1641/0006-3568(2005)055[0323:TBEOIV]2.0.CO;2
Coffman CM (2016) Effect of far-red induced shade-avoidance responses on carbon allocation in Arabidopsis thaliana. Dissertation, University of Missouri, p 162
D’Alonzo KT (2004) The Johnson-Neyman procedure as an alternative to ANCOVA. Western J Nurs Res 26:804–812. https://doi.org/10.1177/0193945904266733
De Luca PA, Vallejo-Marín M (2013) What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Curr Opin Plant Biol 16:429–435. https://doi.org/10.1016/j.pbi.2013.05.002
Dengler NG (2006) The shoot apical meristem and development of vascular architecture. Botany 84:1660–1671. https://doi.org/10.1139/b06-126
Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971. https://doi.org/10.1016/j.anbehav.2005.01.016
Estrella Santamaria M, Arnaiz A, Gonzalez-Melendi P, Martinez M, Diaz I (2019) Plant perception and short-term responses to phytophagous insects and mites. Int J Mol Sci 19:1356. https://doi.org/10.3390/ijms19051356
Fedderwitz F, Nordlander G, Ninkovic V, Björklund N (2016) Effects of jasmonate-induced resistance in conifer plants on the feeding behaviour of a bark-chewing insect, Hylobius abietis. J Pest Sci 89:97–105. https://doi.org/10.1007/s10340-015-0684-9
Ferrieri AP, Appel HM, Schultz JC (2015) Plant vascular architecture determines the pattern of herbivore-induced systemic responses in Arabidopsis thaliana. PLoS ONE 10:e0123899. https://doi.org/10.1371/journal.pone.0123899
Fleishman LJ, Leal M, Persons MH (2009) Habitat light and dewlap color diversity in four species of Puerto Rican anoline lizards. J Comp Physiol A 195:1043–1060. https://doi.org/10.1007/s00359-009-0478-8
Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498. https://doi.org/10.1111/j.1461-0248.2007.01043.x
Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem 48:3597–3604. https://doi.org/10.1021/jf000220w
Gibson JS, Cocroft RB (2018) Vibration-guided mate searching in treehoppers: directional accuracy and sampling strategies in a complex sensory environment. J Exp Biol 221:1–13. https://doi.org/10.1242/jeb.175083
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpinski S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615. https://doi.org/10.1104/pp.16.00434
Heil M, Silva-Bueno C (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. PNAS 104:5467–5472. https://doi.org/10.1073/pnas.0610266104
Helms AM, De Moraes CM, Tooker JF, Mescher MC (2013) Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. PNAS 110:199–204. https://doi.org/10.1073/pnas.1218606110
Helms AM, De Moraes CM, Tröger A, Alborn HT, Francke W, Tooker JF, Mescher MC (2017) Identification of an insect-produced olfactory cue that primes plant defenses. Nat Commun 8:337. https://doi.org/10.1038/s41467-017-00335-8
Hill PSM, Wessel A (2016) Biotremology. Curr Biol 6:R187–R191
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
Johnson ET, Dowd PF (2004) Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J Agric Food Chem 52:5135–5138. https://doi.org/10.1021/jf0308049
Karban R (2014) Plant sensing and communication. University of Chicago Press, Chicago
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
Li G, Bartram S, Guo H, Mithöfer A, Kunert M, Boland W (2019) SpitWorm, an herbivorous robot: mechanical leaf wounding with simultaneous application of salivary components. Plants 8:318. https://doi.org/10.3390/plants8090318
Lundborg L, Fedderwitz F, Björklund N, Nordlander G, Borg-Karlson AK (2016) Induced defenses change the chemical composition of pine seedlings and influence meal properties of the pine weevil Hylobius abietis. Phytochemistry 130:99–105. https://doi.org/10.1016/j.phytochem.2016.06.002
Magal C, Schoeller M, Tautz J, Casas J (2000) The role of leaf structure in vibration propagation. J Acoust Soc Am 108:2412–2418. https://doi.org/10.1121/1.1286098
Malone LA, Barraclough EI, Lin-Wang K, Stevenson DE, Allan AC (2009) Effects of red-leaved transgenic tobacco expressing a MYB transcription factor on two herbivorous insects, Spodoptera litura and Helicoverpa armigera. Entomol Exp Appl 133:127–137. https://doi.org/10.1111/j.1570-7458.2009.00910.x
Mancinelli AL, Hoff AM, Cottrell M (1988) Anthocyanin production in Chl-rich and Chl-poor seedlings. Plant Physiol 86:652–654. https://doi.org/10.1104/pp.86.3.652
McNett GD, Luan L, Cocroft RB (2010) Wind-induced noise alters signaler and receiver behavior in vibrational communication. Behav Ecol Sociobiol 64:2043–2051. https://doi.org/10.1007/s00265-010-1018-9
Meyhöfer R, Casas J, Dorn S (1994) Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host. Physiol Entomol 19:349–359. https://doi.org/10.1111/j.1365-3032.1994.tb01062.x
Michael SCJ, Appel HM, Cocroft RB (2019) Methods for replicating leaf vibrations induced by insect herbivores. In: Gassmann W (ed) Methods in molecular biology: plant innate immunity. Springer, New York, pp 141–157
Michelsen A, Fink F, Gogala M, Traue D (1982) Plants as transmission channels for insect vibrational songs. Behav Ecol Sociobiol 11:269–281. https://doi.org/10.1007/BF00299304
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. https://doi.org/10.1016/j.tplants.2011.03.007
Ohse B, Hammerbacher A, Seele C, Meldau S, Reichert M, Ortmann S, Wirth C (2017) Salivary cues: simulated roe deer browsing induces systemic changes in phytohormones and defence chemistry in wild-grown maple and beech saplings. Funct Ecol 31:340–349. https://doi.org/10.1111/1365-2435.12717
Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, van Loon JJA, Dicke M (2014) Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. J Exp Bot 65:2203–2217. https://doi.org/10.1093/jxb/eru096
Pinto CF, Torrico-Bazoberry D, Penna M, Cossio-Rodriguez R, Cocroft RB, Appel HA, Niemeyer HM (2019) Chemical responses of Nicotiana tabacum (Solanaceae) induced by vibrational signals of a generalist herbivore. J Chemical Ecol 45:708–714. https://doi.org/10.1007/s10886-019-01089-x
Sanson G (2006) The biomechanics of browsing and grazing. Am J Bot 93:1531–1545. https://doi.org/10.3732/ajb.93.10.1531
Shao L, Shu Z, Peng CL, Lin ZF, Yang CW, Gu Q (2008) Enhanced sensitivity of Arabidopsis anthocyanin mutants to photooxidation: a study with fluorescence imaging. Funct Plant Biol 35:714–724. https://doi.org/10.1071/FP08069
Shiojiri K, Ozawa R, Takabayashi J (2006) Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar. PLoS Biol 4:e164. https://doi.org/10.1371/journal.pbio.0040164
Shuman MR, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61:373–394. https://doi.org/10.1146/annurev-ento-010715-023851
Tianzi G, Congcong Z, Changyu C, Shuo T, Xudong Z, Dejun H (2018) Effects of exogenous methyl jasmonate-induced resistance in Populus × euramericana ‘Nanlin895’ on the performance and metabolic enzyme activities of Clostera anachoreta. Arth Plant Interact 12:247–255. https://doi.org/10.1007/s11829-017-9564-y
Tooker JF, Peiffer M, Luthe DS, Felton GW (2010) Trichomes as sensors: Detecting activity on the leaf surface. Plant Signal Behav 5:73–75. https://doi.org/10.4161/psb.5.1.10234
Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361:1112–1115. https://doi.org/10.1126/science.aat7744
Veits M, Khait I, Obolski U, Zinger E, Boonman A, Goldshtein A, Saban K, Seltzer R, Ben-Dor U, Estlein P, Kabat A (2019) Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration. Ecol Lett 22:1483–1492. https://doi.org/10.1111/ele.13331
Virant-Doberlet M, Cokl A (2004) Vibrational communication in insects. Neotrop Entomol 33:121–134. https://doi.org/10.1590/s1519-566X2004000200001
von Dahl CC, Winz RA, Halitschke R, Kühnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J 51:293–307. https://doi.org/10.1111/j.1365-313X.2007.03142.x
Warren J (2015) Is wind-mediated passive leaf movement an effective form of herbivore defence? Plant Ecol Evol 148:52–56. https://doi.org/10.5091/plecevo.2015.1042
Wei S, Hannoufa A, Soroka J, Xu N, Li X, Zebarjadi A, Gruber M (2011) Enhanced β-ionone emission in Arabidopsis over-expressing AtCCD1 reduces feeding damage in vivo by the Crucifer Flea Beetle. Environ Entomol 40:1622–1630. https://doi.org/10.1603/EN11088
Yamazaki K (2011) Gone with the wind: trembling leaves may deter herbivory. Biol J Linnean Soc 104:738–747. https://doi.org/10.1111/j.1095-8312.2011.01776.x
Yang F, Zhang Y, Huang Q, Yin G, Pennerman KK, Yu J, Liu Z, Li D, Guo A (2015) Analysis of key genes of jasmonic acid mediated signal pathway for defense against insect damages by comparative transcriptome sequencing. Sci Rep 5:16500. https://doi.org/10.1038/srep16500
Zhang YT, Zhang YL, Chen SX, Yin GH, Yang ZZ, Lee S, Liu CG, Zhao DD, Ma YK, Song FQ, Bennett JW (2015) Proteomics of methyl jasmonate induced defense response in maize leaves against Asian corn borer. BMC Genom 16:224. https://doi.org/10.1186/s12864-015-1363-1
Acknowledgements
We thank Dhruveesh Dave, Tessa Foti, Sabrina Michael, Taylor Paret and Daniel Torrico for logistical support and assistance in recording caterpillars, Barb Sondermann for help in growing plants, Melissa Mitchum for soybean seeds, and Bruce McClure for tobacco seeds. We thank Lada Micheas of the University of Missouri Statistical Consulting Center for assistance in choosing statistical models and writing SAS code. We also thank two reviewers and editors R. Karban and C. Ballaré for comments that substantially improved the manuscript. The work was supported by National Science Foundation grant IOS-1359593 to HMA and RBC, Comisión Nacional de Ciencia y Tecnología postdoctoral project 3160356 to CFP, and International Science Programs at Uppsala University project BOL-01 to CFP.
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AMK, HMA and RBC conceived and designed the experiments. AMK and CFP made the vibration recordings and AMK, ARAK and RBC performed the playback experiments. RBC, AMK and ARAK analyzed the data. RBC and AMK wrote the manuscript and produced the figures, and HMA, MJAB and CFP edited the manuscript and figures.
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Communicated by Richard Karban.
We show that feeding vibrations of leaf-chewing insect larvae provide a consistent acoustic cue of herbivory and that vibrations of two species induce similar responses in Arabidopsis plants.
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Kollasch, A.M., Abdul-Kafi, AR., Body, M.J.A. et al. Leaf vibrations produced by chewing provide a consistent acoustic target for plant recognition of herbivores. Oecologia 194, 1–13 (2020). https://doi.org/10.1007/s00442-020-04672-2
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DOI: https://doi.org/10.1007/s00442-020-04672-2