Abstract
Natural enemies of agricultural pests, such as parasitoids and predators, often use chemical and visual cues in search of their hosts and prey, and they can learn the association between the cues and the host and prey presence. The braconid, egg-larval endoparasitoid wasp Ascogaster reticulata is a promising biological control agent for tortricid pests, such as Adoxophyes honmai, in tea plantations. Although previous studies revealed that A. reticulata uses contact chemicals released by tea plants in response to tortricid egg oviposition and that it can learn the associated cues, the diurnal wasp is also expected to use visual cues, especially color. Therefore, in this study, we investigated the innate color preference and associative color learning ability of A. reticulata. When a green paper and a paper of a different color (black, blue, red or yellow) was offered together to naive females of the wasp, the females spent less time on a black and blue papers. However, wasps trained to associate black or blue with the presence of a host egg-mass showed increased preference for these colors, whereas red- and yellow-trained wasps did not show changes in preference. Our findings indicate that A. reticulata uses colors, in addition to chemical cues, in host searching behavior and has the ability to learn colors associated with host presence.
Similar content being viewed by others
References
Benelli G, Canale A (2012) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). BioControl 57:767–777
Blackiston D, Briscoe AD, Weiss MR (2011) Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J Exp Biol 214:509–520
Chiu-Alvarado P, Barrera JF, Rojas JC (2009) Attraction of Prorops nasuta (Hymenoptera: Bethylidae), a parasitoid of the coffee berry borer (Coleoptera: Curculionidae), to host-associated olfactory cues. Ann Entomol Soc Am 102:166–171
Chiu-Alvarado P, Valle-Mora J, Rojas JC (2010) Chemical cues from the coffee berry borer influence the locomotory behaviour of its bethylid parasitoids. Bull Entomol Res 100:707–714
de Aquino MFS, Dias AM, Borges M et al (2012) Influence of visual cues on host-searching and learning behaviour of the egg parasitoids Telenomus podisi and Trissolcus basalis. Entomol Exp Appl 145:162–174
DeLury NC, Gries R, Gries G et al (1999) Moth scale-derived kairomones used by egg-larval parasitoid Ascogaster quadridentata to locate eggs of its host, Cydia pomonella. J Chem Ecol 25:2419–2431
Deshpande SA, Kainoh Y (2012) Herbivore egg deposition induces tea leaves to arrest the egg-larval parasitoid Ascogaster reticulata. Entomol Exp Appl 144:172–180
Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton
Gutiérrez-Ibáñez C, Villagra CA, Niemeyer HM (2007) Pre-pupation behaviour of the aphid parasitoid Aphidius ervi (Haliday) and its consequences for pre-imaginal learning. Naturwissenschaften 94:595–600
Honda T, Kainoh Y, Honda H (1998) Enhancement of learned response to plant chemicals by the egg-larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Appl Entomol Zool 33:271–276
Iizuka T, Takasu K (1998) Olfactory associative learning of the pupal parasitoid Pimpla luctuosa Smith (Hymenoptera: Ichneumonidae). J Insect Behav 11:743–760
Jang EB, Messing RH, Klungness LM, Carvalho LA (2000) Flight tunnel responses of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) to olfactory and visual stimuli. J Insect Behav 13:525–538
Kainoh Y (1997) Learning of plant’s contact chemicals by the egg-larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Appl Entomol Zool 32:416–418
Kawakami T, Kainoh Y (1986) Host specificity of the egg-larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera : Braconidae) among five tortricid and one noctuid species. Appl Entomol Zool 21:8–14
Kelber A (2001) Receptor based models for spontaneous colour choices in flies and butterflies. Entomol Exp Appl 99:231–244
Lobdell CE, Yong T-H, Hoffmann MP (2005) Host color preferences and short-range searching behavior of the egg parasitoid Trichogramma ostriniae. Entomol Exp Appl 116:127–134
Minamikawa H, Osakabe K (1979) Pest insects of tea tree. Japan Plant Protection Association Press, Tokyo [in Japanese]
Oliai SE, King BH (2000) Associative learning in response to color in the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). J Insect Behav 13:55–69
Piyasaengthong N, Kinoshita N, Sato Y, Kainoh Y (2016) Sex-specific elicitor from Adoxophyes honmai (Lepidoptera: Tortricidae) induces tea leaf to arrest the egg-larval parasitoid Ascogaster reticulata (Hymenoptera: Braconidae). Appl Entomol Zool 51:353–362
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Segura DF, Viscarret MM, Carabajal Paladino LZ, Ovruski SM, Cladera JL (2007) Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts. Anim Behav 74:131–142
Seino H, Kainoh Y (2008) Associative learning and discrimination of 10 plant species by the egg-larval parasitoid, Ascogaster reticulata Watanabe (Hymenoptera: Braconidae). Appl Entomol Zool 43:83–90
Takemoto H, Powell W, Pickett J, Kainoh Y, Takabayashi J (2009) Learning is involved in the response of parasitic wasps Aphidius ervi (Haliday) (Hymenoptera: Braconidae) to volatiles from a broad bean plant, Vicia faba (Fabaceae), infested by aphids Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Appl Entomol Zool 44:23–28
Takemoto H, Powell W, Pickett J, Kainoh Y, Takabayashi J (2012) Two-step learning involved in acquiring olfactory preferences for plant volatiles by parasitic wasps. Anim Behav 83:1491–1496
Uefune M, Kugimiya S, Shimoda T, Takabayashi J (2013) Starvation and herbivore-induced plant volatiles affect the color preferences of parasitic wasps. BioControl 58:187–193
Wäckers FL (1994) The effect of food deprivation on the innate visual and olfactory preferences in the parasitoid Cotesia rubecula. J Insect Physiol 40:641–649
Wäckers FL, Lewis WJ (1994) Olfactory and visual learning and their combined influence on host site location by the parasitoid Microplitis croceipes (Cresson). Biol Control 4:105–112
Wajnberg E, Colazza S (2013) Chemical ecology of insect parasitoid. Wiley, West Sussex
Acknowledgements
We thank Prof. Hiroshi Honda, Prof. DeMar Taylor, and Dr. Sei-ichi Furukawa at the University of Tsukuba for their helpful comments and discussions on the experiments and the manuscript. We thank Mr. Yoshiaki Tokushima for his help for measuring reflectance spectra of colored papers, and also Ms. Rumi Yoshimura and our colleagues in the Laboratory of Applied Entomology, University of Tsukuba, for their help and support in conducting the experiments. We thank the two referees for their comments and suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kawamata, R., Sato, Y., Suzuki, M. et al. Color Preference and Associative Color Learning in a Parasitoid Wasp, Ascogaster reticulata (Hymenoptera: Braconidae). J Insect Behav 31, 523–534 (2018). https://doi.org/10.1007/s10905-018-9696-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-018-9696-7