Skip to main content
Log in

Innate and Learned Prey-Searching Behavior in a Generalist Predator

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Early colonization by Zyginidia scutellaris leafhoppers might be a key factor in the attraction and settling of generalist predators, such as Orius spp., in maize fields. In this paper, we aimed to determine whether our observations of early season increases in field populations of Orius spp. reflect a specific attraction to Z. scutellaris-induced maize volatiles, and how the responses of Orius predators to herbivore-induced volatiles (HIPVs) might be affected by previous experiences on plants infested by herbivorous prey. Therefore, we examined the innate and learned preferences of Orius majusculus toward volatiles from maize plants attacked by three potential herbivores with different feeding strategies: the leafhopper Z. scutellaris (mesophyll feeder), the lepidopteran Spodoptera littoralis (chewer), and another leafhopper Dalbulus maidis (phloem feeder). In addition, we examined the volatile profiles emitted by maize plants infested by the three herbivores. Our results show that predators exhibit a strong innate attraction to volatiles from maize plants infested with Z. scutellaris or S. littoralis. Previous predation experience in the presence of HIPVs influences the predator’s odor preferences. The innate preference for plants with cell or tissue damage may be explained by these plants releasing far more volatiles than plants infested by the phloem-sucking D. maidis. However, a predation experience on D. maidis-infested plants increased the preference for D. maidis-induced maize volatiles. After O. majusculus experienced L3-L4 larvae (too large to serve as prey) on S. littoralis-infested plants, they showed reduced attraction toward these plants and an increased attraction toward D. maidis-infested plants. When offered young larvae of S. littoralis, which are more suitable prey, preference toward HIPVs was similar to that of naive individuals. The HIPVs from plants infested by herbivores with distinctly different feeding strategies showed distinguishable quantitative differences in (Z)-3-hexenal, (E)-2-hexenal, and methyl salicylate. These compounds might serve as reliable indicators of prey presence and identity for the predator. Our results support the idea that feeding by Z. scutellaris results in the emission of maize’s HIPVs that initially recruit Orius spp. into maize fields.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albajes R, Lumbierres B, Pons X (2011) Two heteropteran predators in relation to weed management in herbicide-tolerant corn. Biol Control 59:30–36

    Article  CAS  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Alivizatos AS (1982) Feeding behavior of the spiroplasma vectors Dalbulus maidis and Euscelidius variegatus in vivo and in vitro. Annales de l’Institut Phytopathologique Benaki 13:128–144

    CAS  Google Scholar 

  • Allison JD, Hare JD (2009) Learned and naïve natural enemy responses and the interpretation of volatile organic compounds as cues or signals. New Phytol 184:768–782

    Article  CAS  PubMed  Google Scholar 

  • Backus EA, Serrano MS, Ranger CM (2005) Mechanisms of hopperburn: an overview of insect taxonomy, behavior, and physiology. Annu Rev Entomol 50:125–151

    Article  CAS  PubMed  Google Scholar 

  • Chabaane Y, Laplanche D, Turlings TCJ, Desurmont GA (2014) Impact of exotic insect herbivores on native tritrophic interactions: A case study of the African cotton leafworm, Spodoptera littoralis and insects associated with the field mustard Brassica rapa. J Ecol 103:109–117

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • D’alessandro M, Turlings TCJ (2005) In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30:739–753

    Article  PubMed  Google Scholar 

  • Dávila AM, Thomas F, Bernal JS (2013) Facilitated by nature and agriculture : performance of a specialist herbivore improves with host plant life history evolution, domestication, and breeding. Oecol 173:1425–1437

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH, Pare PW (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Deboer J, Snoeren T, Dicke M (2005) Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim Behav 69:869–879

    Article  Google Scholar 

  • Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012

    Article  CAS  PubMed  Google Scholar 

  • Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol Exp App 91:131–142

  • Dicke M, Sabelis MW (1987) How plants obtain predatory mites as bodyguards. Netherlands J Zool 38:148–165

    Article  Google Scholar 

  • Drukker B, Bruin J, Sabelis MW (2000) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol 25:260–265

    Article  CAS  Google Scholar 

  • Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Foresti N, Turlings TCJ (2010) A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol 10:247

    Article  PubMed  PubMed Central  Google Scholar 

  • Glinwood R, Ahmed E, Qvarfordt E, Ninkovic V (2011) Olfactory learning of plant genotypes by a polyphagous insect predator. Oecol 166:637–647

    Article  Google Scholar 

  • González I, Lé Cao K-A and Déjean S (2011) mixOmics: Omics Data Integration Project. URL:http://www.mixomics.org

  • Gosset V, Harmel N, Göbel C, Francis F, Haubruge E, Wathelet JP, Du Jardin P, Feussner I, Fauconnier ML (2009) Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J Exp Bot 60:1231–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu H, Dorn S (2000) Genetic variation in behavioral response to herbivore-infested plants in the parasitic wasp, Cotesia glomerata (L.) (hymenoptera: Braconidae). J Insect Behav 13:141–156

    Article  Google Scholar 

  • Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180

    Article  CAS  PubMed  Google Scholar 

  • Hare JD, Sun JJ (2011) Production of induced volatiles by Datura wrightii in response to damage by insects: effect of herbivore species and time. J Chem Ecol 37:751–764

    Article  CAS  PubMed  Google Scholar 

  • Hervé M (2014) RVAideMemoire: diverse basic statistical and graphical functions. R package version 0:9–32

    Google Scholar 

  • James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628

    Article  CAS  PubMed  Google Scholar 

  • Janssen A, Fonseca JO, Colares F, Silva L, Pedrosa ARP, Lima ER, Van Wijk M, Pallini A, Oliveira CM, Sabelis MW, Lesna I (2014) Time scales of associating food and odor by predator communities in the field. Behav Ecol 25:1123–1130

    Article  Google Scholar 

  • Lattin JD (1999) Bionomics of the Anthocoridae. Annu Rev Entomol 44:207–231

    Article  CAS  PubMed  Google Scholar 

  • Leitner M, Boland W, Mithöfer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167:597–606

    Article  CAS  PubMed  Google Scholar 

  • Lins JC, Van Loon JJA, Bueno VHP, Lucas-Barbosa D, Dicke M, Van Lenteren JC (2014) Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics. BioControl 59:707–718

    Article  Google Scholar 

  • Madeira F, Di Lascio A, Carlino P, Costantini ML, Rossi L, Pons X (2014) Stable carbon and nitrogen isotope signatures to determine predator dispersal between alfalfa and maize. Biol Control 77:66–75

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Margolies DC, Sabelis MW, Boyer JE (1997) Response of a phytoseiid predator to herbivore-induced plant volatiles: selection on attraction and effect on prey exploitation. J Insect Behav 10:695–709

    Article  Google Scholar 

  • Marion-Poll F, Della GW, Mauchamp B (1987) Changes of electric patterns related to feeding in a mesophyll feeding leafhopper. Entomol Exp Appl 43:115–124

    Article  Google Scholar 

  • Montserrat M, Albajes R, Castañé C (2004) Behavioral responses of three plant-inhabiting predators to different prey densities. Biol Control 30:256–264

    Article  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: Caterpillar saliva beats plant defences. Nature 416:599–600

    Article  CAS  PubMed  Google Scholar 

  • Nault LR, Delong DM (1980) Evidence for co-evolution of leafhoppers in the genus Dalbulus (Cicadellidae: Homoptera) with maize and its ancestors. Ann Entomol Soc Am 73:349–353

    Article  Google Scholar 

  • Oluwafemi S, Bruce TJA, Pickett JA, Ton J, Birkett MA (2011) Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J Chem Ecol 37:40–48

    Article  CAS  PubMed  Google Scholar 

  • Papaj DR, Lewis AC (eds) (1993) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York

  • Pons X, Albajes R (2002) Control of maize pests with imidacloprid seed dressing treatment in Catalonia (NE Iberian peninsula) under traditional crop conditions. Crop Prot 21:943–950

    Article  CAS  Google Scholar 

  • Pons X, Núñez E, Lumbierres B, Albajes R (2005) Epigeal aphidophagous predators and the role of alfalfa as a reservoir of aphid predators for arable crops. Eur J Entomol 102:519–525

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • 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

    Article  CAS  Google Scholar 

  • Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci U S A 103:1129–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Khan A, Subrahmanyam S, Raman A, Taylor GS, Fletcher MJ (2014) Salivary proteins of plant-feeding hemipteroids - implication in phytophagy. Bull Entomol Res 104:117–136

    Article  CAS  PubMed  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  CAS  PubMed  Google Scholar 

  • Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, Van Wijk M (2006) Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol Res 21:3–8

    Article  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  CAS  PubMed  Google Scholar 

  • Turlings TCL, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids, pp. 51–78, Insect learning. Chapman & Hall, New York

  • Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129

    Article  Google Scholar 

  • Turlings TCJ, Davison AC, Tamò C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29:45–55

    Article  Google Scholar 

  • Van Dam NM, Poppy GM (2008) Why plant volatile analysis needs bioinformatics - detecting signal from noise in increasingly complex profiles. Plant Biol 10:29–37

    Article  PubMed  Google Scholar 

  • Van den Boom CEM, 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

    Article  PubMed  Google Scholar 

  • Venzon M, Janssen A, Sabelis MW (2002) Prey preference and reproductive success of the generalist predator Orius laevigatus. Oikos 97:116–124

    Article  Google Scholar 

  • Vet LEM, Lewis WJ, Carde RT (1995) Parasitoid foraging and learning, pp. 65–101, Chemical ecology of insects 2. Chapman & Hall, New York

  • Walling L (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Julio Bernal for kindly sharing the D. maidis colony, Hao Xu for help with olfactometer assays, Gregory Röder for help with the GC-MS analyses, and Angela Köhler for maintaining the Dalbulus colony. A.A. was funded with an FPU scholarship and a visiting grant to FARCE laboratory from the Ministerio de Educación. The work was partially funded by the Spanish Government project AGL2011-23996.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Agnès Ardanuy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ardanuy, A., Albajes, R. & Turlings, T.C.J. Innate and Learned Prey-Searching Behavior in a Generalist Predator. J Chem Ecol 42, 497–507 (2016). https://doi.org/10.1007/s10886-016-0716-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0716-9

Keywords

Navigation