Effect of Leaf Maturity on Host Habitat Location by the Egg-Larval Parasitoid Ascogaster reticulata

Abstract

Adoxophyes honmai, a serious pest of tea plants, prefers to lay eggs on mature tea leaves rather than young leaves. Here, we examined a hypothesis that Ascogaster reticulata, an egg-larval parasitoid of A. honmai, increases the likelihood of encountering host egg masses by searching mature tea leaves when host-derived cues are not available. In a dual-choice bioassay using a four-arm olfactometer, A. reticulata preferred odor from intact, mature leaves versus young leaves. Based on volatile analysis with gas chromatography-mass spectrometry (GC-MS), we identified 5 and 10 compounds from mature and young leaf volatiles, respectively. The 5 components in the extract from intact mature leaves included (Z)-3-hexenyl acetate, (E)-β-ocimene, linalool, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and methyl salicylate. When each individual compound, or quaternary and quintenary blends of them, ratios of which were adjusted to match those of mature leaf volatiles, were provided, parasitoids preferred the full mixture and the quaternary blend devoid of DMNT to the solvent control. Methyl salicylate, one of the components of preferred blends, was not detected among young leaf volatiles. We concluded that the volatile composition of tea leaves changes, depending on their maturity, and that this composition affects foraging behavior of the parasitoid, which is closely related to the host herbivore’s oviposition preference.

This is a preview of subscription content, access via your institution.

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

Data Availability

All data and materials from this study are available from the corresponding author upon request.

References

  1. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  2. Bell WJ (1990) Locating patches and distant resources. In: Bell WJ (ed) Searching behaviour: the behavioural ecology of finding resources. Chapman and Hall, London, pp 69–82

    Google Scholar 

  3. Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904. https://doi.org/10.1111/pce.12352

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Colazza S, Salerno G, Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control 16:310–317

    Article  Google Scholar 

  5. Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400. https://doi.org/10.1146/annurev.ento.52.110405.091407

    CAS  Article  PubMed  Google Scholar 

  6. Crawley MJ (2007) The R book. Wiley, Chichester

    Google Scholar 

  7. Deshpande SA, Kainoh Y (2012) Herbivore egg deposition induces tea leaves to arrest the egg-larval parasitoid Ascogaster reticulata Watanabe (Hymenoptera: Braconidae). Entomol Exp Appl 144:172–180. https://doi.org/10.1111/j.1570-7458.2012.01275.x

    Article  Google Scholar 

  8. Faraway JJ (2006) Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  9. Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689. https://doi.org/10.1093/beheco/arn011

    Article  Google Scholar 

  10. Fujinuma M, Kainoh Y, Nemoto H (2010) Borago officinalis attracts the aphid parasitoid Aphidius colemani (Hymenoptera: Braconidae). Appl Entomol Zool 45:615–620. https://doi.org/10.1303/aez.2010.615

    Article  Google Scholar 

  11. Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515. https://doi.org/10.1146/annurev-ento-010814-020620

    CAS  Article  PubMed  Google Scholar 

  12. Hou M, Takabayashi J, Kainoh Y (2005) Effect of leaf age on flight response of a parasitic wasp Cotesia kariyai (Hymenoptera: Braconidae) to a plant-herbivore complex. Appl Entomol Zool 40:113–117. https://doi.org/10.1303/aez.2005.113

    Article  Google Scholar 

  13. Iacovone A, French AS, Tellier F, Cusumano A, Clement G, Gaetner C, Conti E, Salerno G, Marion-Poll F (2016) The role of contact chemoreception in the host location process of an egg parasitoid. J Insect Physiol 91–92:63–75. https://doi.org/10.1016/j.jinsphys.2016.07.001

    CAS  Article  PubMed  Google Scholar 

  14. Jönsson M, Lindkvist A, Anderson P (2005) Behavioural responses in three ichneumonid pollen beetle parasitoids to volatiles emitted from different phenological stages of oilseed rape. Entomol Exp Appl 115:363–369. https://doi.org/10.1111/j.1570-7458.2005.00271.x

    Article  Google Scholar 

  15. Kainoh Y (1988) Some factors influencing sex ratio in Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Appl Entomol Zool 23:35–40. https://doi.org/10.1303/aez.23.35

    Article  Google Scholar 

  16. Kamijo K (1973) The parasite complex of Choristoneura diversana Hübner injurious to todo-fir, Abies sachalinensis masters. Jpn J Appl Entomol Zool 17:77–83 (in Japanese with English summary)

    Article  Google Scholar 

  17. Kawakami T (1985) Development of immature stages of Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae), an egg-larval parasitoid of the smaller tea tortrix moth, Adoxophyes sp. (Lepidoptera: Tortricidae). Appl Entomol Zool 20:380–386. https://doi.org/10.1303/aez.20.380

    Article  Google Scholar 

  18. Kobayashi K, Arai M, Tanaka A, Matsuyama S, Honda H, Ohsawa R (2012) Variation in floral scent compounds recognized by honeybees in Brassicaceae crop species. Breed Sci 62:293–302. https://doi.org/10.1270/jsbbs.62.293

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Liu C, Matsuyama S, Kainoh Y (2019) Synergistic effects of volatiles from host-infested plants on host-searching behavior in the parasitoid wasp Lytopylus rufipes (Hymenoptera: Braconidae). J Chem Ecol 45:684–692. https://doi.org/10.1007/s10886-019-01088-y

    CAS  Article  PubMed  Google Scholar 

  20. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310. https://doi.org/10.1016/j.tplants.2012.03.012

    CAS  Article  Google Scholar 

  21. Meiners T (2015) Chemical ecology and evolution of plant-insect interactions: a multitrophic perspective. Curr Opin Insect Sci 8:22–28. https://doi.org/10.1016/j.cois.2015.02.003

    Article  PubMed  Google Scholar 

  22. Mohammed K, Agarwal M, Du XB, Newman J, Ren YL (2019) Behavioural responses of the parasitoid Aphytis melinus to volatiles organic compounds (VOCs) from Aonidiella aurantii on its host fruit Tahitian lime fruit Citrus latifolia. Biol Control 133:103–109. https://doi.org/10.1016/j.biocontrol.2019.03.015

    CAS  Article  Google Scholar 

  23. Neises B, Steglich W (1978) Simple method for the esterification of carboxylic acids. Angew Chem Int Ed 17:522–524. https://doi.org/10.1002/anie.197805221

    Article  Google Scholar 

  24. Piyasaengthong N, Sato Y, Kinoshita N, Kainoh Y (2016) Oviposition preference for leaf age in the smaller tea tortrix Adoxophyes honmai (Lepidoptera: Tortricidae) as related to performance of neonates. Appl Entomol Zool 51:363–371. https://doi.org/10.1007/s13355-016-0408-5

    Article  Google Scholar 

  25. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/

  26. 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. https://doi.org/10.1303/aez.2008.83

    Article  Google Scholar 

  27. Seino H, Shoji K, Kainoh Y (2010) Utilization of learned plant chemicals in host searching behavior by the egg-larval parasitoid Ascogaster reticulata Watanabe (Hymenoptera: Braconidae). Appl Entomol Zool 45:339–345. https://doi.org/10.1303/aez.2010.339

    Article  Google Scholar 

  28. Šimpraga M, Takabayashi J, Holopainen JK (2016) Language of plants: where is the word? J Integr Plant Biol 58:343–349. https://doi.org/10.1111/jipb.12447

    CAS  Article  PubMed  Google Scholar 

  29. Steidle JLM, van Loon JJA (2002) Chemoecology of parasitoid and predator oviposition behaviour. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell Publishing, Berlin, pp 291–317

    Google Scholar 

  30. Takagi K (1974) Monitoring of hymenopterous parasite in the field. Bull Tea Res Stn 10:91–131 (in Japanese with English summary)

    Google Scholar 

  31. Tamaki Y (1966) Mass rearing of the smaller tea tortrix, Adoxophyes orana Fischer von Röslerstamm, on a simplified artificial diet for successive generations (Lepidoptera: Torticidae). Appl Entomol Zool 1:120–124. https://doi.org/10.1303/aez.1.120

    Article  Google Scholar 

  32. Tamaki Y (1991) Tortricid in tea. In: van der Geest LPS, Evenhuis HH (eds) Tortricids pests: their biology, natural enemies and control. Elsevier, Amsterdam, pp 541–551

    Google Scholar 

  33. Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452. https://doi.org/10.1146/annurev-ento-020117-043507

    CAS  Article  PubMed  Google Scholar 

  34. Uchiyama T, Ozawa A (2014) Rapid development of resistance to diamide insecticides in the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae), in the tea fields of Shizuoka prefecture, Japan. Appl Entomol Zool 49:529–534. https://doi.org/10.1007/s13355-014-0283-x

    CAS  Article  Google Scholar 

  35. van Wijk M, de Bruijn PJA, Sabelis MW (2011) Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS One 6:e21742. https://doi.org/10.1371/journal.pone.0021742

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172. https://doi.org/10.1146/annurev.en.37.010192.001041

    Article  Google Scholar 

  37. Vet LEM, van Lenteren JC, Heymans M, Meelis E (1983) An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol Entomol 8:97–106. https://doi.org/10.1111/j.1365-3032.1983.tb00338.x

    Article  Google Scholar 

  38. Vinson SB (1991) Chemical signals used by parasitoids. Redia 74(3):15–42

    Google Scholar 

  39. Watanabe C (1967) Description of a new species of the genus Ascogaster Wesmael and notes on synonymy of Apanteles species (Hymenoptera: Braconidae). Insecta Mastumurana 29:41–44

    Google Scholar 

  40. Webster B, Cardé RT (2017) Use of habitat odour by host-seeking insects. Biol Rev 92:1241–1249. https://doi.org/10.1111/brv.12281

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We appreciate the helpful comments of Prof. DeMar Taylor and Assoc. Prof. Seiichi Furukawa on this study. We are grateful to Dr. Yukie Sato for her advice on statistical analysis.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yooichi Kainoh.

Ethics declarations

Conflicts of Interest/Competing Interests

Not applicable.

Code Availability

Software packages and codes used for statistical analyses in this study are available from the corresponding author.

Supplementary Information

ESM 1

(PPTX 636 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Komatsuzaki, S., Piyasaengthong, N., Matsuyama, S. et al. Effect of Leaf Maturity on Host Habitat Location by the Egg-Larval Parasitoid Ascogaster reticulata. J Chem Ecol (2021). https://doi.org/10.1007/s10886-021-01250-5

Download citation

Keywords

  • Ascogaster reticulata
  • Adoxophyes honmai
  • Camellia sinensis
  • Host searching behavior
  • Plant volatiles
  • Plant maturity
  • Tritrophic interactions