Sour orange, Citrus aurantium, displays higher constitutive and earlier inducible direct defenses against the two-spotted spider mite, Tetranychus urticae, than Cleopatra mandarin, Citrus reshni. Moreover, herbivore-induced plant volatiles (HIPVs) produced by sour orange upon infestation can induce resistance in Cleopatra mandarin but not vice versa. Because the role of these HIPVs in indirect resistance remains ignored, we have carried out a series of behavioral assays with three predatory mites with different levels of specialization on this herbivore, from strict entomophagy to omnivory. We have further characterized the volatile blend associated with T. urticae, which interestingly includes the HIPV methyl salicylate, as well as that produced by induced Cleopatra mandarin plants. Although a preference for less defended plants with presumably higher prey densities (i.e., C. reshni) was expected, this was not always the case. Because predators’ responses changed with diet width, with omnivore predators responding to both HIPVs and prey-related odors and specialized ones mostly to prey, our results reveal that these responses depend on plant genotype, prey presence and predator diet specialization. As the different volatile blends produced by infested sour orange, induced Cleopatra mandarin and T. urticae itself are attractive to T. urticae natural enemies but not to the herbivore, they may provide clues to develop new more sustainable tools to manipulate these agriculturally relevant species.
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Abad-Moyano R, Pina T, Ferragut F, Urbaneja A (2009) Comparative life-history traits of three phytoseiid mites associated with Tetranychus urticae (Acari: tetranychidae) colonies in clementine orchards in eastern Spain: implications for biological control. Exp Appl Acarol 47:121–132
Adar E, Inbar M, Gal S, Doron N, Zhang ZQ, Palevsky E (2012) Plant-feeding and non-plant feeding phytoseiids: differences in behavior and cheliceral morphology. Exp Appl Acarol 58:341–357
Aguilar-Fenollosa E, Ibáñez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas JA (2011) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (I): bottom-up regulation mechanisms. Biol Control 59:158–170
Agut B, Gamir J, Jacas JA, Hurtado M, Flors V (2014) Different metabolic and genetic responses in citrus may explain relative susceptibility to Tetranychus urticae. Pest Manag Sci 70:1728–1741
Agut B, Gamir J, Jaques JA, Flors V (2015) Tetranychus urticae-triggered responses promote genotype-dependent conspecific repellence or attractiveness in citrus. New Phytol 207:790–804
Agut B, Gamir J, Jaques JA, Flors V (2016) Systemic resistance in citrus to Tetranychus urticae induced by conspecifics is transmitted by grafting and mediated by mobile amino acids. J Exp Bot 67:5711–5723
Alfaro C, Vacas S, Zarzo M, Navarro-Llopis V, Primo J (2011) Solid phase microextraction of volatile emissions of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae): influence of fly sex, age, and mating status. J Agric Food Chem 59:298–306
Aljbory Z, Chen MS (2018) Indirect plant defense against insect herbivores: a review. Insect Sci 25:2–23
Andersson J, Borg-Karlson AK, Wiklund C (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B 267:1271
Andersson J, Borg-Karlson AK, Wiklund C (2003) Antiaphrodisiacs in pierid butterflies: a theme with variation! J Chem Ecol 29:1489–1499
Bakke A, Froyen P, Skattebol L (1977) Field response to a new pheromonal compound isolated from Ips typographus. Naturwissenschaften 64:98
Bañuls J, Serna MD, Legaz F, Talon M, Primo-Millo E (1997) Growth and gas exchange parameters of Citrus plants stressed with different salts. J Plant Physiol 150:194–199
Bowers WW, Gries G, Borden JH, Pierce HD (1991) 3-Methyl-3-buten-1-ol: an aggregation pheromone of the four-eyed spruce bark beetle, Polygraphus rufipennis (Kirby) (Coleoptera: Scolytidae). J Chem Ecol 17:1989–2002
Bruessow F, Asins MJ, Jacas JA, Urbaneja A (2010) Replacement of CTV susceptible sour orange rootstock by CTV-tolerant ones may have triggered outbreaks of Tetranychus urticae in Spanish citrus. Agric Ecosyst Environ 137:93–98
Bruin J, Dicke M, Sabelis MW (1992) Plants are better protected against spider-mites after exposure to volatiles from infested conspecifics. Experientia 48:525–529
Bruinsma M, Van Broekhoven S, Poelman EH, Posthumus MA, Müller MJ, Van Loon JJ, Dicke M (2010) Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects. Oecologia 162:393–404
Cambra M, Gorris MT, Marroquın C, Román MP, Olmos A, Martınez MC, Hermoso de Mendoza A, López A, Navarro L (2000) Incidence and epidemiology of Citrus tristeza virus in the Valencian community of Spain. Virus Res 71:85–95
Castro-Vázquez L, Díaz-maroto MC, González-Viñas MA, Pérez-Coello M (2009) Differentiation of monofloral citrus, rosemary, eucalyptus, lavender, thyme and heather honeys based on volatile composition and sensory descriptive analysis. Food Chem 112:1022–1030
Clavijo McCormick A, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310
Cortés LE, Weldegergis BT, Boccalandro HE, Dicke M, Ballaré CL (2016) Trading direct for indirect defense? Phytochrome B inactivation in tomato attenuates direct anti-herbivore defenses whilst enhancing volatile-mediated attraction of predators. New Phytol 212:1057–1071
De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271
Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthumus MA (1990) Plant strategies of manipulating predatorprey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118
Dötterl S, Jürgens A (2005) Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Syst Evol 255:99–109
Dötterl S, Burkhardt D, Weißbecker B, Jürgens A, Schütz S, Mosandl A (2006) Linalool and lilac aldehyde/alcohol in flower scents: electrophysiological detection of lilac aldehyde stereoisomers by a moth. J Chromatogr A 1113:231–238
Gómez-Martínez MA, Jaques JA, Ibáñez-Gual MV, Pina T (2018) When the ground cover brings guests: is Anaphothrips obscurus a friend or a foe for the biological control of Tetranychus urticae in clementines? J Pest Sci 91:613–623
Hoy MA (2011) Agricultural acarology: introduction to integrated mite management. CRC Press (Taylor and Francis Group), Boca Raton
Huffaker C, Van de Vrie M, McMurtry J (1970) Ecology of tetranychid mites and their natural enemies: a review: II. Tetranychid populations and their possible control by predators: an evaluation. Hilgardia 40:391–458
Jacas JA, Urbaneja A (2010) Biological control in citrus in Spain: from classical to conservation biological control. In: Ciancio A, Mukerij KG (eds) Integrated management of arthropod pests and insect borne diseases. Springer, Dordrecht, pp 61–72
Jerković I, Molnar M, Vidović S, Vladić J, Jokić S (2017) Supercritical CO2 extraction of Lavandula angustifolia Mill. Flowers: optimisation of oxygenated monoterpenes, coumarin and herniarin content. Phytochem Anal 28:558–566
Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495
Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc R Soc Lond B Biol Sci 275:443–452
Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol Control 60:77–89
Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, Seo S, Mitsuhara I (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact 6:221–230
Kiefer E, Heller W, Ernst D (2000) A simple and efficient protocol for isolation of functional RNA from plant tissues rich in secondary metabolites. Plant Mol Biol Rep 18:33–39
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
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
McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321
McMurtry JA, Moraes GJD, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320
Migeon A, Dorkeld F (2006–2017) Spider Mites Web: a comprehensive database for the Tetranychidae. http://www.montpellier.inra.fr/CBGP/spmweb. Accessed 13 April 2018
Oku K, Weldegergis BT, Poelman EH, De Jong PW, Dicke M (2015) Altered volatile profile associated with precopulatory mate guarding attracts spider mite males. J Chem Ecol 41:187–193
Pascual-Ruiz S, Aguilar-Fenollosa E, Ibáñez-Gual V, Hurtado-Ruiz MA, Martínez-Ferrer MT, Jacas JA (2014) Economic threshold for Tetranychus urticae (Acari: Tetranychidae) in clementine mandarins Citrus clementina. Exp Appl Acarol 62:337–362
Pellissier L, Moreira X, Danner H, Serrano M, Salamin N, Dam NM, Rasmann S (2016) The simultaneous inducibility of phytochemicals related to plant direct and indirect defences against herbivores is stronger at low elevation. J Ecol 104:1116–1125
Pérez-Sayas C, Pina T, Gómez-Martínez MA, Camañes G, Ibáñez-Gual MV, Jaques JA, Hurtado MA (2015) Disentangling mite predator-prey relationships by multiplex PCR. Mol Ecol Resour 15:1330–1345
Peron G, Baldan V, Sut S, Faggian M, Roccabruna L, Zanini D, Manzini P, Maggi F, Dall’Acqua S (2017) Phytochemical investigations on Artemisia alba Turra growing in the North-East of Italy. Nat Prod Res 31:1861–1868
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308
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
Reddy GV, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261
Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343
Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303
Rowen E, Gutensohn M, Dudareva N, Kaplan I (2017) Carnivore attractant or plant elicitor? Multifunctional roles of methyl salicylate lures in tomato defense. J Chem Ecol 43:573–585
Sabelis MW, Baan HVD (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol Exp Appl 33:303–314
Sabelis MW, Vermaat JE, Groeneveld A (1984) Arrestment responses of the predatory mite, Phytoseiulus persimilis, to steep odour gradients of a kairomone. Physiol Entomol 9:437–446
Salamanca J, Souza B, Lundgren JG, Rodriguez-Saona C (2017) From laboratory to field: electro-antennographic and behavioral responsiveness of two insect predators to methyl salicylate. Chemoecology 27:51–63
Shimoda T (2010) A key volatile infochemical that elicits a strong olfactory response of the predatory mite Neoseiulus californicus, an important natural enemy of the two-spotted spider mite Tetranychus urticae. Exp Appl Acarol 50:9–22
Stoakley JT, Bakke A, Renwick JAA, Vité JP (1978) The aggregation pheromone system of the larch beetle, lps cembrae Heer. Z Angew Entomol 86:174–177
Van Den Boom CE, Van Beek TA, Posthumus MA, De Groot A, Dicke M (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J Chem Ecol 30:69–89
Van Wijk M, De Bruijn PJ, Sabelis MW (2008) Predatory mite attraction to herbivore-induced plant odors is not a consequence of attraction to individual herbivore-induced plant volatiles. J Chem Ecol 34:791–803
Van Wijk M, De Bruijn PJ, Sabelis MW (2011) Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS ONE 6:e21742
Wallis C, Eyles A, Chorbadjian R, McSpadden-Gardener B, Hansen R, Cipollini D, Herms DA, Bonello P (2008) Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytol 177:767–778
Zhurov V, Navarro M, Bruinsma KA, Arbona V, Santamaria ME, Cazaux M, Wybouw N, Osborne EJ, Ens C, Rioja C, Vermeirssen V (2014) Reciprocal responses in the interaction between Arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol 164:384–399
The research leading to these results was partially funded by the Spanish Ministry of Economy and Competitiveness (AGL2014-55616-C3; AGL2015-64990-2R). The authors thank M. Piquer (UJI) for technical assistance. MC received a pre-doctoral fellowship from the Spanish Ministry of Economy and Competitiveness (BES-2015-074570), and MP was the recipient of a research fellowship from INIA, Spain (subprogram DOC INIA-CCAA).
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Marc Cabedo-López and Joaquín Cruz-Miralles should be considered joint first author.
Communicated by I. Hiltpold.
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Cabedo-López, M., Cruz-Miralles, J., Vacas, S. et al. The olfactive responses of Tetranychus urticae natural enemies in citrus depend on plant genotype, prey presence, and their diet specialization. J Pest Sci 92, 1165–1177 (2019). https://doi.org/10.1007/s10340-019-01107-7
- Sour orange
- Cleopatra mandarin
- Phytoseiulus persimilis
- Neoseiulus californicus
- Euseius stipulatus