Abstract
Plants use volatile organic compounds (VOCs) to cue natural enemies to their herbivore prey on plants. Simultaneously, herbivores utilize volatile cues to identify appropriate hosts. Despite extensive efforts to understand sources of variation in plant communication by VOCs, we lack an understanding of how ubiquitous belowground mutualists, such as arbuscular mycorrhizal fungi (AMF), influence plant VOC emissions. In a full factorial experiment, we subjected plants of two milkweed (Asclepias) species under three levels of AMF availability to damage by aphids (Aphis nerii). We then measured plant headspace volatiles and chemical defenses (cardenolides) and compared these to VOCs emitted and cardenolides produced by plants without herbivores. We found that AMF have plant species-specific effects on constitutive and aphid-induced VOC emissions. High AMF availability increased emissions of total VOCs, two green leaf volatiles (3-hexenyl acetate and hexyl acetate), and methyl salicylate in A. curassavica, but did not affect emissions in A. incarnata. In contrast, aphids consistently increased emissions of 6-methyl-5-hepten-2-one and benzeneacetaldehyde in both species, independent of AMF availability. Both high AMF availability and aphids alone suppressed emissions of individual terpenes. However, aphid damage on plants under high AMF availability increased, or did not affect, emissions of those terpenes. Lastly, aphid feeding suppressed cardenolide concentrations only in A. curassavica, and AMF did not affect cardenolides in either plant species. Our findings suggest that by altering milkweed VOC profiles, AMF may affect both herbivore performance and natural enemy attraction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agrawal AA (2004) Plant defense and density dependence in the population growth of herbivores. Am Nat 164:113–120. https://doi.org/10.1086/420980
Agrawal AA, Petschenka G, Bingham RA et al (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45. https://doi.org/10.1111/j.1469-8137.2011.04049.x
Agrawal AA, Hastings AP, Patrick ET, Knight AC (2014) Specificity of herbivore-induced hormonal signaling and defensive traits in five closely related milkweeds (Asclepias spp.). J Chem Ecol 40:717–729. https://doi.org/10.1007/s10886-014-0449-6
Ali JG, Agrawal AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol 28:1404–1412. https://doi.org/10.1111/1365-2435.12271
Anacker BL, Klironomos JN, Maherali H et al (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17:1613–1621. https://doi.org/10.1111/ele.12378
Arimura GI, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923. https://doi.org/10.1093/pcp/pcp030
Asensio D, Rapparini F, Peñuelas J (2012) AM fungi root colonization increases the production of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77:149–161. https://doi.org/10.1016/j.phytochem.2011.12.012
Babikova Z, Gilbert L, Bruce T et al (2014a) Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Funct Ecol 28:375–385. https://doi.org/10.1111/1365-2435.12181
Babikova Z, Gilbert L, Randall KC et al (2014b) Increasing phosphorus supply is not the mechanism by which arbuscular mycorrhiza increase attractiveness of bean (Vicia faba) to aphids. J Exp Bot 65:5231–5241. https://doi.org/10.1093/jxb/eru283
Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971–980. https://doi.org/10.1111/j.1365-2745.2008.01404.x
Barber NA (2013) Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus. J Plant Ecol 6:171–176. https://doi.org/10.1093/jpe/rts026
Barber NA, Kiers ET, Hazzard RV, Adler LS (2013) Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem. Front Plant Sci 4:338. https://doi.org/10.3389/fpls.2013.00338
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:771–779. https://doi.org/10.1007/s00442-009-1338-5
Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects - finding the right mix. Phytochemistry 72:1605–1611. https://doi.org/10.1016/j.phytochem.2011.04.011
Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci. 10:269–274. https://doi.org/10.1016/j.tplants.2005.04.003
Bucher M, Hause B, Krajinski F, Küster H (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840. https://doi.org/10.1111/nph.12862
Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545. https://doi.org/10.1016/j.tplants.2013.06.004
Carvalho LM, Correia PM, Ryel RJ, Martins-Loução MA (2003) Spatial variability of arbuscular mycorrhizal fungal spores in two natural plant communities. Plant Soil 251:227–236. https://doi.org/10.1023/A:1023016317269
de Roode JC, Rarick RM, Mongue AJ et al (2011) Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant. Ecol Lett 14:453–461. https://doi.org/10.1111/j.1461-0248.2011.01604.x
Danner H, Desurmont GA, Cristescu SM, van Dam NM (2018) Herbivore-induced plant volatiles accurately predict history of coexistence, diet breadth, and feeding mode of herbivores. New Phytol 220:726–738. https://doi.org/10.1111/nph.14428
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help”. Trends Plant Sci 15:167–175. https://doi.org/10.1016/j.tplants.2009.12.002
Du YJ, Poppy GM, Powell W et al (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368. https://doi.org/10.1023/A:1021278816970
Fontana A, Reichelt M, Hempel S et al (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843. https://doi.org/10.1007/s10886-009-9654-0
Fordyce JA, Malcolm SB (2000) Specialist weevil, Rhyssomatus lineaticollis, does not spatially avoid cardenolide defenses of common milkweed by ovipositing into pith tissue. J Chem Ecol 26:2857–2874. https://doi.org/10.1023/A:1026450112601
Fox J, Weisberg S (2014) An R Companion to Applied Regression, Second edition. Sage, Thousand Oaks, CA
Frost CJ, Appel HM, Carlson JE et al (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
Garrido E, Bennett AE, Fornoni J, Strauss SY (2010) Variation in arbuscular mycorrhizal fungi colonization modifies the expression of tolerance to above-ground defoliation. J Ecol 98:43–49. https://doi.org/10.1111/j.1365-2745.2009.01586.x
Gouinguené SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307. https://doi.org/10.1104/pp.001941
Grman E (2012) Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711–718. https://doi.org/10.1890/11-1358.1
Guerrieri E, Lingua G, Digilio MC et al (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756. https://doi.org/10.1111/j.0307-6946.2004.00644.x
Gutjahr C (2014) Phytohormone signaling in arbuscular mycorhiza development. Curr Opin Plant Biol 20:26–34. https://doi.org/10.1016/j.pbi.2014.04.003
Halitschke R, Stenberg JA, Kessler D et al (2008) Shared signals - “alarm calls” from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34. https://doi.org/10.1111/j.1461-0248.2007.01123.x
Hardie J, Isaacs R, Pickett JA et al (1994) Methyl salicylate and (-)-(1R,5S)-myrtenal are plant-derived repellents for black bean aphid, Aphis fabae Scop. (Homoptera: Aphididae). J Chem Ecol 20:2847–2855. https://doi.org/10.1007/BF02098393
Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180. https://doi.org/10.1146/annurev-ento-120709-144753
Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342. https://doi.org/10.1146/annurev.ento.54.110807.090614
Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272. https://doi.org/10.1016/j.tplants.2008.03.005
Helms SE, Connelly SJ, Hunter MD (2004) Effects of variation among plant species on the interaction between a herbivore and its parasitoid. Ecol Entomol 29:44–51. https://doi.org/10.1111/j.0307-6946.2004.00566.x
Hoeksema JD, Chaudhary VB, Gehring CA et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184. https://doi.org/10.1016/j.tplants.2010.01.006
James DG (2005) Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495. https://doi.org/10.1007/s10886-005-2020-y
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664. https://doi.org/10.1007/s10886-012-0134-6
Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1-18. https://doi.org/10.18637/jss.v025.i01
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press
Karban R, Wetzel WC, Shiojiri K et al (2014a) Deciphering the language of plant communication: volatile chemotypes of sagebrush. J Physiol 204:380–385. https://doi.org/10.1111/nph.12887
Karban R, Yang LH, Edwards KF (2014b) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52. https://doi.org/10.1111/ele.12205
Karban R, Wetzel WC, Shiojiri K et al (2016) Geographic dialects in volatile communication between sagebrush individuals. Ecology 97:2917–2924. https://doi.org/10.1002/ecy.1573
Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300. https://doi.org/10.1111/j.1365-2435.2009.01647.x
Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88. https://doi.org/10.1023/A:1006127516791
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141-2144 https://doi.org/10.1126/science.291.5511.2141
Klironomos JH (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. https://doi.org/10.2307/3450135
Koide RT, Mooney HA (1987) Spatial variation in inoculum potential of vesicular-arbuscular mycorrhizal fungi caused by rormation of gopher mounds. New Phytol 107:173–182. https://doi.org/10.1111/j.1469-8137.1987.tb04891.x
Koricheva J, Nykänen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75. https://doi.org/10.1086/382601
Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097. https://doi.org/10.1890/08-1555.1
Kunert M, Biedermann A, Koch T, Boland W (2002) Ultrafast sampling and analysis of plant volatiles by a hand-held miniaturised GC with pre-concentration unit: kinetic and quantitative aspects of plant volatile production. J Sep Sci 25:677–684. https://doi.org/10.1002/1615-9314(20020701)25:10/11<677::AID-JSSC677>3.0.CO;2-5
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. doi: 10.18637/jss.v082.i13
Leitner M, Kaiser R, Hause B et al (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101. https://doi.org/10.1007/s00572-009-0264-z
Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204. https://doi.org/10.1111/j.1469-8137.2005.01490.x
Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166. https://doi.org/10.1016/j.tplants.2009.12.006
Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant, Cell Environ 29:1820–1828. https://doi.org/10.1111/j.1365-3040.2006.01561.x
Malcolm SB (1992) Prey Defence and Predator Foraging. In: Crawley MJ (ed) Natural Enemies: The Population Biology of Predators, Parasites, and Diseases. Blackwell Scientific Publications, Oxford, UK, pp 458–475
Mallinger RE, Hogg DB, Gratton C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124. https://doi.org/10.1603/EC10253
McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM Software Design. Gleneden Beach, OR
McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Meier AR, Hunter MD (2018a) Arbuscular mycorrhizal fungi mediate herbivore-induction of plant defenses differently above and belowground. Oikos 127:1759–1775. https://doi.org/10.1111/oik.05402
Meier AR, Hunter MD (2018b) Mycorrhizae alter toxin sequestration and performance of two specialist herbivores. Front Ecol Evol 6:33. https://doi.org/10.3389/fevo.2018.00033
Mohl EK, Santa-Martinez E, Heimpel GE (2016) Interspecific differences in milkweeds alter predator density and the strength of trophic cascades. Arthropod Plant Interact 10:249–261. https://doi.org/10.1007/s11829-016-9430-3
Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644. https://doi.org/10.1126/science.1184814
Natale D, Mattiacci L, Hern A et al (2003) Response of female Cydia molesta (Lepidoptera: Tortricidae) to plant derived volatiles. Bull Entomol Res 93:335–342. https://doi.org/10.1079/BER2003250
Oksanen J, Blanchet FG, Kindt R, et al (2015) Vegan: community ecology package, version 2.2-1. R package vegan, vers. 2.2-1
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790. https://doi.org/10.1111/j.1365-2745.2006.01136.x
Pareja M, Mohib A, Birkett MA et al (2009) Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim Behav 77:901–909. https://doi.org/10.1016/j.anbehav.2008.12.016
Pettersson J, Pickett JA, Pye BJ et al (1987) Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (homoptera, aphididae), and other aphids in cereal fields. J Chem Ecol 20:2565–2574. https://doi.org/10.1007/BF02036192
Pope TW, Campbell CAM, Hardie J et al (2007) Interactions between host-plant volatiles and the sex pheromones of the bird cherry-oat aphid, Rhopalosiphum padi and the damson-hop aphid, Phorodon humuli. J Chem Ecol 33:157–165. https://doi.org/10.1007/s10886-006-9199-4
Quiroz A, Pettersson J, Pickett JA et al (1997) Semiochemicals mediating spacing behavior of bird cherry-oat aphid, Rhopalosiphum padi feeding on cereals. J Chem Ecol 23:2599–2607. https://doi.org/10.1023/B:JOEC.0000006669.34845.0d
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/.
Rapparini F, Llusià J, Peñuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122. https://doi.org/10.1055/s-2007-964963
Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483. https://doi.org/10.1111/j.1461-0248.2011.01609.x
Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): Trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99:16–25. https://doi.org/10.1111/j.1365-2745.2010.01713.x
Rasmann S, Bennett A, Biere A et al (2017) Root symbionts: powerful drivers of plant above- and belowground indirect defenses. Insect Sci 24:947–960. https://doi.org/10.1111/1744-7917.12464
Rodriguez-Saona C, Kaplan I, Braasch J et al (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303. https://doi.org/10.1016/j.biocontrol.2011.06.017
Rowen E, Kaplan I (2016) Eco-evolutionary factors drive induced plant volatiles: a meta-analysis. New Phytol 210:284–294. https://doi.org/10.1111/nph.13804
Schaub A, Blande JD, Graus M et al (2010) Real-time monitoring of herbivore induced volatile emissions in the field. Physiol Plant 138:123–133. https://doi.org/10.1111/j.1399-3054.2009.01322.x
Schausberger P, Peneder S, Jürschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449. https://doi.org/10.1111/j.1365-2435.2011.01947.x
Schwartzberg EG, Böröczky K, Tumlinson JH (2011) Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. J Chem Ecol 37:1055–1062. https://doi.org/10.1007/s10886-011-0006-5
Schweiger R, Müller C (2015) Leaf metabolome in arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 26:120–126. https://doi.org/10.1016/j.pbi.2015.06.009
Schweiger R, Baier MC, Persicke M, Müller C (2014) High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nat Commun 5:3886. https://doi.org/10.1038/ncomms4886
Shrivastava G, Ownley BH, Augé RM et al (2015) Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis 65:65–74. https://doi.org/10.1007/s13199-015-0319-1
Smith SE, Read D (2008) Mycorrhizal symbiosis, Third edition. Academic Press, London
Sokal RR, Rohlf FJ (2012) Biometry: The principles and practice of statistics in biological research, Fourth edition. W. H. Freeman, New York, NY, USA
Soudzilovskaia NA, Douma JC, Akhmetzhanova AA et al (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382. https://doi.org/10.1111/geb.12272
Staudt M, Jackson B, El-Aouni H et al (2010) Volatile organic compound emissions induced by the aphid Myzus persicae differ among resistant and susceptible peach cultivars and a wild relative. Tree Physiol 30:1320–1334. https://doi.org/10.1093/treephys/tpq072
Sternberg ED, Lefèvre T, Li J et al (2012) Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions. Evolution 66:3367–3376. https://doi.org/10.1111/j.1558-5646.2012.01693.x
Tao L, Ahmad A, de Roode JC, Hunter MD (2016) Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms. J Ecol 104:561–571. https://doi.org/10.1111/1365-2745.12535
Trowbridge AM, Daly RW, Helmig D et al (2014) Herbivory and climate interact serially to control monoterpene emissions from pinyon pine forests. Ecology 95:1591–1603. https://doi.org/10.1890/13-0989.1
Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452. https://doi.org/10.1146/annurev-ento-020117-043507
Vannette RL (2011) Whose phenotype is it anyway? The complex role of species interactions and resource availability in determining plant defense phenotype and community consequences. University of Michigan
Vannette RL, Hunter MD (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76. https://doi.org/10.1111/j.1365-2745.2010.01755.x
Vannette RL, Hunter MD (2013) Mycorrhizal abundance affects the expression of plant resistance traits and herbivore performance. J Ecol 101:1019–1029. https://doi.org/10.1111/1365-2745.12111
Vannette RL, Hunter MD, Rasmann S (2013) Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species. Front Plant Sci 4:361. https://doi.org/10.3389/fpls.2013.00361
Visser JH, Avé DA (1978) General green leaf volatiles in the olfactory orientation of the colorado beetle, Leptinotarsa decemlineata. Entomol Exp Appl 24:738–749. https://doi.org/10.1111/j.1570-7458.1978.tb02838.x
Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866. https://doi.org/10.1104/pp.107.113142
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. https://doi.org/10.1007/s00572-005-0033-6
Wang M, Bezemer TM, van der Putten WH, Biere A (2015) Effects of the timing of herbivory on plant defense induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status. J Chem Ecol 41:1006–1017. https://doi.org/10.1007/s10886-015-0644-0
Wason EL, Hunter MD (2014) Genetic variation in plant volatile emission does not result in differential attraction of natural enemies in the field. Oecologia 174:479–491. https://doi.org/10.1007/s00442-013-2787-4
Watanabe H, Yano E, Higashida K et al (2016) An attractant of the aphidophagous gall midge Aphidoletes aphidimyza from honeydew of Aphis gossypii. J Chem Ecol 42:149–155. https://doi.org/10.1007/s10886-016-0666-2
Wei J, Wang L, Zhu J et al (2007) Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLoS One 2:e852. https://doi.org/10.1371/journal.pone.0000852
Whitman DW, Eller FJ (1990) Parasitic wasps orient to green leaf volatiles. Chemoecology 1:69–76. https://doi.org/10.1007/BF01325231
Wolfe BE, Mummey DL, Rillig MC, Klironomos JN (2007) Small-scale spatial heterogeneity of arbuscular mycorrhizal fungal abundance and community composition in a wetland plant community. Mycorrhiza 17:175–183. https://doi.org/10.1007/s00572-006-0089-y
Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053. https://doi.org/10.1007/s10886-007-9364-4
Zhu J, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746. https://doi.org/10.1007/s10886-005-5923-8
Züst T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:1–9. https://doi.org/10.1038/nplants.2015.206
Acknowledgements
We would like to thank the Matthaei Botanical Gardens for greenhouse space and help with plant care. We gratefully acknowledge Lucas Michelotti, Hillary Streit, Anne Bonds, Kamren Johnson, Jackie Kristofik, and Kathleen Moriarty for help with the experiment and chemical analyses. We thank Christopher Frost and Ken Keefover-Ring for assistance in designing the volatile collection system. We also thank three reviewers for their constructive comments on an earlier draft of the paper. The work was supported by a Block Grant, Matthaei Botanical Gardens Research Award, and Rackham Graduate Student Research Grant from the University of Michigan to ARM, a National Science Foundation Graduate Research Fellowship to ARM, and a National Science Foundation Division of Environmental Biology 1256115 grant to MDH.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 65.1 kb)
Rights and permissions
About this article
Cite this article
Meier, A.R., Hunter, M.D. Mycorrhizae Alter Constitutive and Herbivore-Induced Volatile Emissions by Milkweeds. J Chem Ecol 45, 610–625 (2019). https://doi.org/10.1007/s10886-019-01080-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-019-01080-6