Abstract
Some parasitoids oviposit in nonhosts. Parasitization of nonhosts potentially wastes gametes, risks the death of offspring, and reduces fitness. Associative learning, a strategy for efficient reproduction, has been observed in various parasitoid species. We conducted two types of experiments to reveal whether larval parasitoid wasps, Cotesia kariyai (Hymenoptera: Braconidae), learn associatively by ovipositing in nonhosts. In dissection experiments, we found wasp eggs in both host [Mythimna separata (Lepidoptera: Noctuidae)] and nonhost [Spodoptera litura (Lepidoptera: Noctuidae)] caterpillars. However, the mean number of eggs in nonhosts was significantly smaller than in hosts. In oviposition experiments, most naive C. kariyai females attacked both hosts and nonhosts. On the other hand, wasps that had previously attacked nonhosts tended to avoid them thereafter. We conclude that C. kariyai females may be able to detect and identify nonhost metabolites and/or cuticular hydrocarbons. Negative associative learning enhances C. kariyai reproductive success when hunting in complex host habitats.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
References
Costa A, Ricard I, Davison AC, Turlings TCJ (2010) Effects of rewarding and unrewarding experiences on the response to host-induced plant odors of the generalist parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). J Insect Behav 23:303–318
De Rijk M, Dicke M, Poelman EH (2013) Foraging behaviour by parasitoids in multiherbivore communities. Anim Behav 85:1517–1528
Feng Y, Wratten S, Sandhu H, Keller M (2015) Host plants affect the foraging success of two parasitoids that attack light brown apple moth Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae). PLoS One 10:e0124773
Gentry GL, Dyer LA (2002) On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119
Giunti G, Canale A, Messing RH, Donati E, Stefanini C, Michaud JP, Benelli G (2015) Parasitoid learning: current knowledge and implications for biological control. Biol Control 90:208–219
Goubault M, Cortesero AM, Paty C, Fourrier J, Dourlot S, Ralec AL (2011) Abdominal sensory equipment involved in external host discrimination in a solitary parasitoid wasp. Micros Res Techniq 74:1145–1153
Hayakawa Y, Yazaki K (1997) Envelope protein of parasitic wasp symbiont virus, polydnavirus, protects the wasp eggs from cellular immune reactions by the host insect. Eur J Biochem 246:820–826
Islam KS, Copland MJW (2000) Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci (Hymenoptera: Encyrtidae), a solitary endoparasitoid of citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). Bull Entomol Res 90:69–75
Koyama J, Matsumura M (2019) Ecology and control of armyworm, Mythimna separata (Lepidoptera: Noctuidae) in Japan, with special reference to outbreak and migration. Jpn J Appl Entomol Zool 63:39–56
McDonald H, Reed DA, Ahmadian S, Paine TD (2015) Parasitoid discrimination between suitable and unsuitable congener hosts. J Insect Behav 28:417–425
Obonyo M, Schulthess F, Gerald J, Wanyama O, Rü BL, Calatayud P-A (2008) Location, acceptance and suitability of lepidopteran stemborers feeding on a cultivated and wild host-plant to the endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae). Biol Control 45:36–47
Obonyo M, Schulthess F, Ru BL, Van Den Berg J, Silvain J-F, Calatayud P-A (2010) Importance of contact chemical cues in host recognition and acceptance by the braconid larval endoparasitoids Cotesia sesamiae and Cotesia flavipes. Biol Control 54:270–275
Ohara Y, Takabayashi J, Takahashi S (1996) Oviposition kairomones in the cuticular wax of host larvae, Pseudaletia separata, toward its parasitic wasp, Cotesia kariyai. Appl Entomol Zool 31:271–277
Potting RPJ, Vermeulen NE, Conlong DE (1999) Active defence of herbivorous hosts against parasitism: adult parasitoid mortality risk involved in attacking a concealed stemboring host. Entomol Exp Appl 91:143–148
Quicke DLJ (2015) The ovipositor and ovipositor sheaths. In: Quicke DLJ (ed) The braconid and ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. WileyChichester, pp. 35–56
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ruschioni S, van Loon JJA, Smid HM, van Lenteren JC (2015) Insects can count: sensory basis of host discrimination in parasitoid wasps revealed. PLoS One 10:e0138045
Sato Y, Tanaka T (1984) Effect of the number of parasitoid (Apanteles kariyai) eggs [Hym. : Braconidae] on the growth of host (Leucania separata) larvae [Lep. : Noctuidae]. Entomophaga 29:21–28
Takabayashi J (2014) Infochemical webs and tritrophic interactions. In : eLS 2014, John Wiley & Sons Ltd : Chichester http://www.els.net/
Takabayashi J, Takahashi S (1990) An allelochemical elicits arrestment in Apanteles kariyai in feces of nonhost larvae Acantholeucania loreyi. J Chem Ecol 16:2009–2017
Takasu K, Lewis WJ (2003) Learning of host searching cues by the larval parasitoid Microplitis croceipes. Entomol Exp Appl 108:77–86
Thanikkul P, Piyasaengthong N, Menezes-Netto AC, Taylor D, Kainoh Y (2017) Effects of quantitative and qualitative differences in volatiles from host- and non-host-infested maize on the attraction of the larval parasitoid Cotesia kariyai. Entomol Exp Appl 163:60–69
Ueno T (1999) Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch. Evol Ecol 13:33–44
van Lenteren JC, Ruschioni S, Romani R, van Loon JJA, Qiu YT, Smid HM, Isidoro N, Bin F (2007) Structure and electrophysiological responses of gustatory organs on the ovipositor of the parasitoid Leptopilina heterotoma. Arthropod Struct Dev 36:271–276
Vet LEM, Lewis WJ, Papaj DR, van Lenteren JC (1990) A variable-response model for parasitoid foraging behavior. J Insect Behav 3:471–490
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
Zaidi MA, Ye G, Yao H, You TH, Loit E, Dean DH, Riazuddin S, Altosaar I (2009) Transgenic rice plants expressing a modified cry1Ca1 gene are resistant to Spodoptera litura and Chilo suppressalis. Mol Biotechnol 43:232–242
Acknowledgements
We thank Profs. Hiroshi Honda and DeMar Taylor, and Drs. Seiichi Furukawa, Shigeru Matsuyama, and Natsuko Kinoshita for giving us valuable counsel. We are grateful to all members of the Laboratory of Applied Entomology and Zoology, University of Tsukuba for helping with this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
There are no conflicts of interest to declare.
Ethics Approval
Not applicable.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Code Availability
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Supplementary Material
Female parasitoid wasps (Cotesia kariyai) consistently oviposit more eggs per attack upon host (Mythimna separata) larvae than upon nonhost (Spodoptera litura) larvae, and attacks in which few eggs (0–2) were deposited occurred nearly 3 times more often in S. litura. The frequency distribution of C. kariyai eggs found by dissecting (a) M. separata and (b) S. litura larvae that had been attacked once. (PPTX 351 kb)
Rights and permissions
About this article
Cite this article
Aikawa, F.K., Kuramitsu, K. & Kainoh, Y. Oviposition Experience by the Larval Parasitoid, Cotesia kariyai, on Nonhost, Spodoptera litura, Can Deter Subsequent Attacks. J Insect Behav 33, 91–96 (2020). https://doi.org/10.1007/s10905-020-09749-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-020-09749-7