Pupal and Adult Experience Affect Adult Response to Food Odour Components in the Flower-Visiting Butterfly Tirumala limniace
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Animals
2.2. Compounds of Food Odours
2.3. Pupal Odour Exposure
2.4. Adult Stage Experience
2.5. The Effects of Adult Experience on Earlier Pupal Experience
2.6. Adult Behavioural Assays
2.7. Scanning Electron Microscope
2.8. Electroantennogram (EAG) Recordings
2.9. Statistical Analysis
3. Results
3.1. Exposure to α-Pinene during the Pupal Stage Affects Adult Feeding Preference
3.2. Adult Learning Experience with α-Pinene Affects Feeding Preference
3.3. Odour Preferences from Exposure to α-Pinene or Ethyl Acetate (EA) in Males and Females
3.4. Electrophysiological Responses of Males and Females to α-Pinene and Ethyl Acetate
3.5. Morphology and Number of Antennal Sensilla in Males and Females
4. Discussion
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Fan, R.J.; Anderson, P.; Hansson, B.S. Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J. Exp. Biol. 1997, 200, 2969–2976. [Google Scholar] [CrossRef] [PubMed]
- Jones, P.L.; Agrawal, A.A. Learning in insect pollinators and herbivores. Annu. Rev. Entomol. 2017, 62, 53–71. [Google Scholar] [CrossRef] [PubMed]
- Anderson, P.; Anton, S. Experience-based modulation of behavioural responses to plant volatiles and other sensory cues in insect herbivores. Plant Cell Environ. 2014, 37, 1826–1835. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Shan, S.; Gu, S.; Huang, X.; Li, Z.; Khashaveh, A.; Zhang, Y. Prior experience with food reward influences the behavioral responses of the honeybee Apis mellifera and the bumblebee Bombus lantschouensis to tomato floral scent. Insects 2020, 11, 884. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.S.; Li, Y.H.; Liu, Y.q.; Zalucki, M.P. Experience-induced preference for oviposition repellents derived from a non-host plant by a specialist herbivore. Ecol. Lett. 2005, 8, 722–729. [Google Scholar] [CrossRef]
- Kemp, D.J. Manipulation of natal host modifies adult reproductive behaviour in the butterfly Heliconius charithonia. P. Roy. Soc. B-Biol. Sci. 2019, 286, 20191225. [Google Scholar] [CrossRef]
- Braem, S.; Van Dyck, H. Larval and adult experience and ecotype affect oviposition behavior in a niche-expanding butterfly. Behav. Ecol. 2023, 34, 547–561. [Google Scholar] [CrossRef]
- Dion, E.; Pui, L.X.; Weber, K.; Monteiro, A. Early-exposure to new sex pheromone blends alters mate preference in female butterflies and in their offspring. Nat. Commun. 2020, 11, 53. [Google Scholar] [CrossRef]
- Barragán-Fonseca, K.Y.; Van Loon, J.J.; Dicke, M.; Lucas-Barbosa, D. Use of visual and olfactory cues of flowers of two brassicaceous species by insect pollinators. Ecol. Entomol. 2020, 45, 45–55. [Google Scholar] [CrossRef]
- Blackiston, D.; Briscoe, A.D.; Weiss, M.R. Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J. Exp. Biol. 2011, 214, 509–520. [Google Scholar] [CrossRef]
- Balamurali, G.; Rose, S.; Somanathan, H.; Kodandaramaiah, U. Complex multi-modal sensory integration and context specificity in colour preferences of a pierid butterfly. J. Exp. Biol. 2020, 223, jeb223271. [Google Scholar] [CrossRef] [PubMed]
- Kroutov, V.; Mayer, M.; Emmel, T. Olfactory conditioning of the butterfly Agraulis vanillae (L.) (Lepidoptera, Nymphalidae) to floral but not host-plant odors. J. Insect Behav. 1999, 12, 833–843. [Google Scholar] [CrossRef]
- Silva, A.K.; Gonçalves, G.L.; Moreira, G.R.P. Larval feeding choices in heliconians: Induced preferences are not constrained by performance and host plant phylogeny. Anim. Behav. 2014, 89, 155–162. [Google Scholar] [CrossRef]
- Bernays, E.; Weiss, M. Induced food preferences in caterpillars: The need to identify mechanisms. Entomol. Exp. Appl. 1996, 78, 1–8. [Google Scholar] [CrossRef]
- Gowri, V.; Dion, E.; Viswanath, A.; Piel, F.M.; Monteiro, A. Transgenerational inheritance of learned preferences for novel host plant odors in Bicyclus anynana butterflies. Evolution 2019, 73, 2401–2414. [Google Scholar] [CrossRef] [PubMed]
- Janz, N.; Söderlind, L.; Nylin, S. No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): On the persistence of Hopkins’ host selection principle. Ecol. Entomol. 2009, 34, 50–57. [Google Scholar] [CrossRef]
- Gegear, R.J. Exploring the role of cognition in the annual fall migration of the monarch butterfly (Danaus plexippus). Insects 2021, 12, 760. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Wang, F.; Chen, X.; Zhou, C.; Yao, J. Adult behavior of Tirumala limniace (Lepidoptera: Danaidae). J. Insect Sci. 2015, 15, 76. [Google Scholar] [CrossRef] [PubMed]
- Tang, Y.; Zhou, C.; Chen, X.; Zheng, H. Visual and olfactory responses of seven butterfly species during foraging. J. Insect Behav. 2013, 26, 387–401. [Google Scholar] [CrossRef]
- Tang, Y. The Research of Olfactory Andvisualresponses·during Butterflies Foraging; Chinese Academy of Forestry: Beijing, China, 2013. [Google Scholar]
- Lin, M.; Chen, J.; Wu, D.; Chen, K. Volatile profile and biosynthesis of post-harvest apples are affected by the mechanical damage. J. Agric. Food Chem. 2021, 69, 9716–9724. [Google Scholar] [CrossRef]
- Schneider, D. Insect antennae. Annu. Rev. Entomol. 1964, 9, 103–122. [Google Scholar] [CrossRef]
- Yuan, X.; Gao, K.; Yuan, F.; Zhang, Y. Ultrastructure of antennal sensilla of four skipper butterflies in Parnara sp. and Pelopidas sp. (Lepidoptera, Hesperiidae). ZooKeys 2014, 399, 35–45. [Google Scholar] [CrossRef]
- Limberger, G.M.; Brugnera, R.; da Fonseca, D.B. Antennal morphology and sensilla ultrastructure of Ascia monuste (Linnaeus) (Lepidoptera: Pieridae). Micron 2021, 142, 103000. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Wang, H.; Chen, X.; Yao, J.; Deng, J. Visual cues and body volatile β-ocimene are used by the blue tiger butterfly Tirumala limniace to identify conspecifics during courtship. Behav. Ecol. Sociobiol. 2022, 76, 163. [Google Scholar] [CrossRef]
- Kandori, I.; Yamaki, T. Reward and non-reward learning of flower colours in the butterfly Byasa alcinous (Lepidoptera: Papilionidae). Naturwissenschaften 2012, 99, 705–713. [Google Scholar] [CrossRef]
- Kandori, I.; Yamaki, T.; Okuyama, S.-i.; Sakamoto, N.; Yokoi, T. Interspecific and intersexual learning rate differences in four butterfly species. J. Exp. Biol. 2009, 212, 3810–3816. [Google Scholar] [CrossRef] [PubMed]
- Rankin, M.; Burchsted, J. The cost of migration in insects. Annu. Rev. Entomol. 1992, 37, 533–559. [Google Scholar] [CrossRef]
- Karlsson, B.; Wickman, P.-O. Increase in reproductive effort as explained by body size and resource allocation in the speckled wood butterfly, Pararge aegeria (L.). Funct. Ecol. 1990, 4, 609–617. [Google Scholar] [CrossRef]
- Ray, S. Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosci. Lett. 1999, 259, 37–40. [Google Scholar] [CrossRef]
- Truman, J.W.; Price, J.; Miyares, R.L.; Lee, T. Metamorphosis of memory circuits in Drosophila reveals a strategy for evolving a larval brain. Elife 2023, 12, e80594. [Google Scholar] [CrossRef]
- Gandolfi, M.; Mattiacci, L.; Dorn, S. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 2623–2629. [Google Scholar] [CrossRef] [PubMed]
- Blackiston, D.J.; Silva Casey, E.; Weiss, M.R. Retention of memory through metamorphosis: Can a moth remember what it learned as a caterpillar? PLoS ONE 2008, 3, e1736. [Google Scholar] [CrossRef] [PubMed]
- Signorotti, L.; Jaisson, P.; d’Ettorre, P. Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis. P. Roy. Soc. B-Biol. Sci. 2014, 281, 20132579. [Google Scholar] [CrossRef]
- Gowri, V.; Monteiro, A. Acquired preferences for a novel food odor do not become stronger or stable after multiple generations of odor feeding in Bicyclus anynana butterfly larvae. Ann. N. Y. Acad. Sci. 2024, 1531, 84–94. [Google Scholar] [CrossRef] [PubMed]
- Couto, A.; Young, F.J.; Atzeni, D.; Marty, S.; Melo-Flórez, L.; Hebberecht, L.; Monllor, M.; Neal, C.; Cicconardi, F.; McMillan, W.O. Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies. Nat. Commun. 2023, 14, 4024. [Google Scholar] [CrossRef] [PubMed]
- Stanton, M.L. Short-term learning and the searching accuracy of egg-laying butterflies. Anim. Behav. 1984, 32, 33–40. [Google Scholar] [CrossRef]
- Papaj, D.R.; Prokopy, R.J. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 1989, 34, 315–350. [Google Scholar] [CrossRef]
Compounds | 1 μg/μL | 100 μg/μL | ||
---|---|---|---|---|
♀ | ♂ | ♀ | ♂ | |
α-pinene | 0.98 ± 0.13Ab | 1.92 ± 0.25Aa | 0.95 ± 0.16Ab | 2.09 ± 0.41Aa |
ethyl acetate | 1.25 ± 0.23Aa | 1.99 ± 0.32Aa | 1.36 ± 0.17Aa | 2.04 ± 0.35Aa |
Böhm Bristles (BB) | Sensilla Squamiformia (SQ) | Sensilla Trichodea (ST) | Sensilla Coeloconica (SCo) | Sensilla Chaetica (SCh) | |
---|---|---|---|---|---|
♂ | 146.0 ± 25.5A | 27.5 ± 0.7A | 2924.5 ± 287.8A | 16,583.0 ± 222.0A | 251.5 ± 12.0B |
♀ | 153.0 ± 25.5A | 33.0 ± 2.8A | 2343.0 ± 11.3B | 14,047.5 ± 185.5B | 280.5 ± 20.5A |
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Li, C.; Wang, H.; Bian, F.; Yao, J.; Shi, L.; Chen, X. Pupal and Adult Experience Affect Adult Response to Food Odour Components in the Flower-Visiting Butterfly Tirumala limniace. Insects 2024, 15, 231. https://doi.org/10.3390/insects15040231
Li C, Wang H, Bian F, Yao J, Shi L, Chen X. Pupal and Adult Experience Affect Adult Response to Food Odour Components in the Flower-Visiting Butterfly Tirumala limniace. Insects. 2024; 15(4):231. https://doi.org/10.3390/insects15040231
Chicago/Turabian StyleLi, Chengzhe, Hua Wang, Fangyuan Bian, Jun Yao, Lei Shi, and Xiaoming Chen. 2024. "Pupal and Adult Experience Affect Adult Response to Food Odour Components in the Flower-Visiting Butterfly Tirumala limniace" Insects 15, no. 4: 231. https://doi.org/10.3390/insects15040231
APA StyleLi, C., Wang, H., Bian, F., Yao, J., Shi, L., & Chen, X. (2024). Pupal and Adult Experience Affect Adult Response to Food Odour Components in the Flower-Visiting Butterfly Tirumala limniace. Insects, 15(4), 231. https://doi.org/10.3390/insects15040231