Abstract
Nesidiocoris tenuis Reuter (Heteroptera: Miridae) is an omnivorous mirid bug that preys on diverse generalist herbivorous arthropods. N. tenuis adults are attracted to volatiles from plants induced by their prey, such as tobacco cutworms (CCW) (Spodoptera litura larvae) and two-spotted spider mites (Tetranychus urticae). N. tenuis adults also induce volatiles when they infest plants. In this study, we focused on olfactory responses of N. tenuis males and females to volatiles from eggplants and sesame plants induced by conspecifics of the same or different gender by using a Y-tube olfactometer. Males were attracted to volatiles from plants of both species induced by either males or females. The male preference was biased to volatiles from plants of both species induced by females, probably because the biased response would facilitate their mate-finding. Females were attracted only to volatiles from plants of both species induced by females. Mating occurs multiple times in this species. Thus, the responses would indirectly affect mating of males and females. Slight but significant qualitative and quantitative differences were detected between the volatiles of plants of both species induced by N. tenuis females and those of the plants induced by conspecific males. N. tenuis might use such differences in their gender-specific responses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Addesso KM, McAuslane HJ (2009) Pepper weevil attraction to volatiles from host and nonhost plants. Environ Entomol 38:216–224. https://doi.org/10.1603/022.038.0127
Arimura G, 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
Arnó J, Castane C, Riudavets J, Gabarra R (2006) Characterization of damage to tomato plants produced by the zoophytophagous predator Nesidiocoris tenuis. IOBC wprs Bull 29:249
Bengtsson M, Jaastad G, Knudsen G, Kobro S, Bäckman A-C, Pettersson E, Witzgall P (2006) Plant volatiles mediate attraction to host and non-host plant in apple fruit moth, Argyresthia conjugella. Entomol Exp Appl 118:77–85. https://doi.org/10.1111/j.1570-7458.2006.00359.x
Cabello T, Rodriguez-Manzaneque MA, Gallego JR (2017) Can the pheromones of predators modulate responses to herbivore-induced plant volatiles? Ann Appl Biol 170:369–378. https://doi.org/10.1111/aab.12341
Calvo FJ, Bolckmans K, Belda JE (2009) Development of a biological control-based integrated pest management method for Bemisia tabaci for protected sweet pepper crops. Entomol Exp Appl 133:9–18. https://doi.org/10.1111/j.1570-7458.2009.00896.x
Calvo FJ, Lorente MJ, Stansly PA, Belda JE (2012) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisa tabaci in greenhouse tomato. Entomol Exp Appl 143:111–119. https://doi.org/10.1111/j.1570-7458.2012.01238.x
Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924. https://doi.org/10.1007/s10886-006-9117-9
Carroll MJ, Schmelz E, Teal PA (2008) The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J Chem Ecol 34:291–300. https://doi.org/10.1007/s10886-007-9414-y
Dicke M (1986) Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider mite Tetranychus urticae. Physiol Entomol 11:251–262. https://doi.org/10.1111/j.1365-3032.1986.tb00412.x
Dicke M, Beek TA, Posthumus MA, Ben Dom N, Bokhoven H, Groot A (1990) Isolation and identification of volatile kairomone that affects acarine predatorprey interactions Involvement of host plant in its production. J Chem Ecol 16:381–396. https://doi.org/10.1007/BF01021772
Franco K, Jauset A, Castañé C (2011) Monogamy and polygamy in two species of mirid bugs: a functional-based approach. J Insect Physiol 57:307–315. https://doi.org/10.1016/j.jinsphys.2010.11.020
Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Nishioka T (2003) A comparison of the responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl Entomol Zool 38:109–116. https://doi.org/10.1303/aez.2003.109
Itou M, Watanabe M, Watanabe E, Miura K (2013) Gut content analysis to study predatory efficacy of Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) by molecular methods. Entomol Sci 16:145–150. https://doi.org/10.1111/j.1479-8298.2012.00552.x
Lins JCJ, 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. https://doi.org/10.1007/s10526-014-9602-y
Moayeri HRS, Ashouri A, Brodsgaard HF, Enkegaard A (2007) Males of the predatory mirid bug Macrolophus caliginosus exploit plant volatiles induced by conspecifics as a sexual synomone. Entomol Exp Appl 123:49–55. https://doi.org/10.1111/j.1570-7458.2007.00523.x
Ozawa R, Nishimura O, Yazawa S, Muroi A, Takabayashi J, Arimura G (2012) Temperature-dependent, behavioral, and transcriptional variability of a tritrophic interaction consisting of bean, herbivorous mite, and predator. Mol Ecol 21:5624–5635. https://doi.org/10.1111/mec.12052
Pérez-Hedo M, Bouagga S, Jaques JA, Flors V, Urbaneja A (2015a) Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae). Biol Control 86:46–51. https://doi.org/10.1016/j.biocontrol.2015.04.006
Pérez-Hedo M, Urbaneja-Bernat P, Jaques J, Flors V, Urbaneja A (2015b) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554. https://doi.org/10.1007/s10340-014-0640-0
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rim H, Uefune M. Ozawa R, Takabayashi J (2015) Olfactory response of the omnivorous mirid bug Nesidiocoris tenuis to eggplants infested by prey: specificity in prey developmental stages and prey species. Biol Control 91:47–54. https://doi.org/10.1016/j.biocontrol.2015.07.009
Rim H, Uefune M, Ozawa R, Yoneya K, Takabayashi J (2017) Experience of plant infestation by the omnivorous arthropod Nesidiocoris tenuis affects its subsequent responses to prey-infested plant volatiles. Biocontrol 62:233–242. https://doi.org/10.1007/s10526-017-9791-2
Sabelis M, Takabayashi J, Janssen A, Kant M, Van Wijk M, Sznajder B, Aratchige N, Lesna I, Belliur B, Schuurink R (2007) Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities. In: Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 188–217
Sanchez JA (2008) Zoophytophagy in the plantbug Nesidiocoris tenuis. Agric Forest Entomol 10:75–80. https://doi.org/10.1111/j.1461-9563.2007.00357.x
Shivaramu S, Jayanthi PDK, Kempraj V, Anjinappa R, Nandagopal B (2017) What signals do herbivore-induced plant volatiles provide conspecific herbivores? Arthropod-Plant Interact 11:815–823. https://doi.org/10.1007/s11829-017-9536-2
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman and Company, New York
Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci 1:109–113. https://doi.org/10.1016/S1360-1385(96)90004-7
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. https://doi.org/10.1007/s11284-005-0129-7
Urbaneja A, Tapia G, Fernandez E, Sanchez E, Contreras J, Gallego A, Bielza P (2003). Influence of the prey on the biology of Nesidiocoris tenuis (Hem.: Miridae). IOBC wprs Bull 26(10):159–160
Wiley RH, Poston J (1996) Indirect mate choice, competition for mates, and coevolution on the sexes. Evolution 50:1371–1381. https://doi.org/10.1111/j.1558-5646.1996.tb03911.x
Williams L, Rodriguez-Saona C, Paré PW, Crafts-Brandner SJ (2005) The Piercing-sucking herbivores Lygus hesperus and Nezara viridula induce volatile emissions in plants. Arch Insect Biochem Physiol 58:84–96. https://doi.org/10.1002/arch.20035
Xue M, Pang Y-H, Wang H-T, Li Q-L, Liu T-X (2010) Effects of four host plants on biology and food utilization of the cutworm, Spodoptera litura. J Insect Sci 10:22. https://doi.org/10.1673/031.010.2201
Acknowledgements
This study was supported by the Bio-oriented Technology Research Advancement Institution, by a Grant-in-Aid for Scientific Research (S) and (B) and by Joint Usage/Research Grant of The Center for Ecological Research, Kyoto University. We thank Indranil B. Mukherjee for his comments on the revised manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Jarmo Holopainen.
Rights and permissions
About this article
Cite this article
Rim, H., Uefune, M., Ozawa, R. et al. An omnivorous arthropod, Nesidiocoris tenuis, induces gender-specific plant volatiles to which conspecific males and females respond differently. Arthropod-Plant Interactions 12, 495–503 (2018). https://doi.org/10.1007/s11829-018-9612-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-018-9612-2