Adult Nutrition Stress Modulates the Energy Allocation Between Migration and Reproduction in Cnaphalocrocis medinalis
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Insect Rearing
2.2. Evaluation of Migratory Behavior
2.3. Flight Performance Assessment
2.4. Fecundity Assay
2.5. Ovarian Developmental Assay
2.6. Determination of Triglyceride and Glycogen Contents
2.7. Statistical Analysis
3. Results
3.1. Starved MG Individuals Exhibit Enhanced Flight Performance Compared with NMG Individuals
3.2. Starved MG Individuals Show Delayed Reproduction
3.3. Starved Migratory Individuals Prioritize Energy Allocation to Migration
4. Discussion
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Dingle, H.; Drake, V.A. What is migration? BioScience 2007, 57, 113–121. [Google Scholar] [CrossRef]
- Hu, G.; Lim, K.S.; Horvitz, N.; Clark, S.J.; Reynolds, D.R.; Sapir, N.; Chapman, J.W. Mass seasonal bioflows of high-flying insect migrants. Science 2016, 354, 1584–1587. [Google Scholar] [CrossRef]
- Chapman, J.W.; Reynolds, D.R.; Wilson, K.; Holyoak, M. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 2015, 18, 287–302. [Google Scholar] [CrossRef]
- Holland, R.A.; Wikelski, M.; Wilcove, D.S. How and why do insects migrate? Science 2006, 313, 794–796. [Google Scholar] [CrossRef] [PubMed]
- Beenakkers, A.M.; Van der Horst, D.J.; Van Marrewijk, W.J. Insect lipids and lipoproteins, and their role in physiological processes. Prog. Lipid Res. 1985, 24, 19–67. [Google Scholar] [CrossRef]
- Arrese, E.L.; Soulages, J.L. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 2010, 55, 207–225. [Google Scholar] [CrossRef]
- Xu, C.-F.; Liu, P.-C.; Chapman, J.W.; Wotton, K.R.; Qi, G.-J.; Wang, Y.-M.; Hu, G. Energy reserve allocation in the trade-off between migration and reproduction in fall armyworm. Insects 2024, 15, 809. [Google Scholar] [CrossRef] [PubMed]
- Rankin, M.; Burchsted, J. The cost of migration in insects. Annu. Rev. Entomol. 1992, 37, 533–559. [Google Scholar] [CrossRef]
- Kennedy, J. A turning point in the study of insect migration. Nature 1961, 189, 785–791. [Google Scholar] [CrossRef]
- Zera, A.J.; Denno, R.F. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 1997, 42, 207–230. [Google Scholar] [CrossRef] [PubMed]
- Azizi, T.; Johnston, J.S.; Vinson, S.B. Initiation of flight muscle apoptosis and wing casting in the red imported fire ant Solenopsis invicta. Physiol. Entomol. 2009, 34, 79–85. [Google Scholar] [CrossRef]
- Tigreros, N.; Davidowitz, G. Flight-fecundity tradeoffs in wing-monomorphic insects. Adv. Insect Phys. 2019, 56, 1–41. [Google Scholar]
- Johnson, C.G. Physiological factors in insect migration by flight. Nature 1963, 198, 423–427. [Google Scholar] [CrossRef]
- Johnson, C.G. Migration and Dispersal of Insects by Flight; Methuen & Co., Ltd.: London, UK, 1969; 763p. [Google Scholar]
- Zhang, X.X.; Wang, M.T. Studies on the relationship between variation of ovary canal number and takeoff behavior in green peach aphid. J. Plant Prot. 1991, 18, 161–166. [Google Scholar]
- Liu, X.D.; Zhai, B.P.; Zhang, X.X.; Xiong, F. The relationship between flight behavior and ovary development in the cotton aphid, Aphis gossypii. Entomol. Knowl. 2003, 40, 39–42. [Google Scholar]
- Saglam, I.K.; Roff, D.A.; Fairbairn, D.J. Male sand crickets trade-off flight capability for reproductive potential. J. Evol. Biol. 2008, 21, 997–1004. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.-C.; Diao, Y.-H.; Guo, J.-W.; Gao, B.-Y.; Hu, G. Insect migration behavior and its regulation. Chin. J. Appl. Entomol. 2021, 58, 520–529. [Google Scholar]
- Zhao, X.C.; Feng, H.Q.; Wu, B.; Wu, X.F.; Liu, Z.F.; Wu, K.F.; McNeil, J.N. Does the onset of sexual maturation terminate the expression of migratory behaviour in moths? A study of the oriental armyworm, Mythimna separata. J. Insect Physiol. 2009, 55, 1039–1043. [Google Scholar] [CrossRef] [PubMed]
- Hill, J.K.; Gatehouse, A.G. Effects of temperature and photoperiod on development and pre-reproductive period of the silver Y moth Autographa gamma (Lepidoptera: Noctuidae). Bull. Entomol. Res. 1992, 82, 335–341. [Google Scholar] [CrossRef]
- Gatehouse, A.; Zhang, X. Migratory potential in insects: Variation in an uncertain environment. In Insect Migration: Tracking Resources Through Space and Time; Drake, V.A., Gatehouse, A.G., Eds.; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
- Jiang, X.F.; Luo, L.Z.; Zhang, L.; Sappington, T.W.; Hu, Y. Regulation of migration in Mythimna separata (Walker) in China: A review integrating environmental, physiological, hormonal, genetic, and molecular factors. Environ. Entomol. 2011, 40, 516–533. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.J.; Zheng, M.L.; Zhu, Y.Y.; Li, H.L.; Dong, D.F.; Yu, X.Y.; Li, X.S. Nutritional resources regulate the reproduction or migration of Spodoptera frugiperda through juvenile hormones and 20-hydroxyecdysone. J. Agric. Food Chem. 2024, 72, 27062–27074. [Google Scholar] [CrossRef] [PubMed]
- Hari, N.S.; Jindal, J.; Malhi, N.S.; Khosa, J.K. Effect of adult nutrition and insect density on the performance of spotted stem borer, Chilo partellus in laboratory cultures. J. Pest Sci. 2008, 81, 23–27. [Google Scholar] [CrossRef]
- Zhang, L.; Luo, L.Z.; Jiang, X.F. Starvation influences allatotropin gene expression and juvenile hormone titer in the female adult oriental armyworm, Mythimna separata. Arch. Insect Biochem. Physiol. 2008, 68, 63–70. [Google Scholar] [CrossRef]
- Kaufmann, C.; Collins, L.F.; Brown, M.R. Influence of age and nutritional status on flight performance of the Asian tiger mosquito Aedes albopictus (Diptera: Culicidae). Insects 2013, 4, 404–412. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Yin, J.; Cao, Y.Z.; Li, K.B. The effect of feeding and mating on the development of flight muscle in Agrotis ypsilon. Chin. J. Appl. Entomol. 2013, 50, 1573–1585. [Google Scholar]
- Sappington, T.W.; Showers, W.B. Influence of larval starvation and adult diet on long-duration flight behavior of the migratory moth Agrotis ipsilon (Lepidoptera: Noctuidae). Environ. Entomol. 1993, 22, 141–148. [Google Scholar] [CrossRef]
- Force, E.; Dacher, M.; Debernard, S. How the diet influences lepidopteran reproduction: Morpho-functional, behavioral, and endocrine aspects. J. Insect Physiol. 2025, 164, 104838. [Google Scholar] [CrossRef]
- Boggs, C.L. Reproductive strategies of female butterflies: Variation in and constraints on fecundity. Ecol. Entomol. 2008, 11, 7–15. [Google Scholar]
- Fei, H.; Martin, T.R.; Jaskowiak, K.M.; Hatle, J.D.; Whitman, D.W.; Borst, D.W. Starvation affects vitellogenin production but not vitellogenin mRNA levels in the lubber grasshopper, Romalea microptera. J. Insect Physiol. 2005, 51, 435–443. [Google Scholar] [CrossRef]
- Xuan, J.L.; Lu, S.L.; Cheng, X.Q.; Wan, F.H.; Liu, W.X. Observation of ovary anatomy and impact oogenesis on adult nutrition in female Liriomyza sativae (Diptera: Agromyzidae). J. Environ. Entomol. 2017, 39, 660–666. [Google Scholar]
- Vandekerkhove, B.; Baal, E.V.; Bolckmans, K.; Clercq, P.D. Effect of diet and mating status on ovarian development and oviposition in the polyphagous predator Macrolophus caliginosus (Heteroptera: Miridae). Biol. Control 2006, 39, 532–538. [Google Scholar] [CrossRef]
- Zhang, S.-Y.; Zhang, Y.-Y.; Yang, F.; Zhou, C.; Shen, H.-M.; Wang, B.-B.; Zeng, J.; Reynolds, D.R.; Chapman, J.W.; Hu, G. Climate change is leading to an ecological trap in a migratory insect. Proc. Natl. Acad. Sci. USA 2025, 122, e2422595122. [Google Scholar] [CrossRef]
- Guo, J.W.; Li, P.; Zhang, J.; Liu, X.-D.; Zhai, B.-P.; Hu, G. Cnaphalocrocis medinalis moths decide to migrate when suffering nutrient shortage on the first day after emergence. Insects 2019, 10, 364. [Google Scholar] [CrossRef]
- Yang, F.; Hu, G.; Shi, J.J.; Zhai, B.P. Effects of larval density and food stress on life-history traits of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J. Appl. Entomol. 2015, 139, 370–380. [Google Scholar] [CrossRef]
- Guo, J.W.; Yang, F.; Zhang, H.Y.; Lin, P.J.; Zhai, B.P.; Lu, Z.X.; Hu, G.; Liu, P.C. Reproduction does not impede the stopover departure to ensure a potent migration in Cnaphalocrocis medinalis moths. Insect Sci. 2022, 29, 1672–1684. [Google Scholar] [CrossRef]
- Yang, F.; Zheng, D.B.; Shi, J.J.; Hu, G.; Zhang, X.X.; Zhai, B.P. Observations on migratory behavior of Cnaphalocrocis medinalis: When will they take-off? Chin. J. Appl. Entomol. 2013, 50, 592–600. [Google Scholar]
- Zhu, A.X.; Qian, Q.; Liu, X.D. A method for rearing the rice leaf folder (Cnaphalocrocis medinalis) using wheat seedlings. Chin. J. Appl. Entomol. 2015, 04, 883–889. [Google Scholar]
- Guo, J.-W.; Yang, F.; Li, P.; Liu, X.-D.; Wu, Q.-L.; Hu, G.; Zhai, B.-P. Female bias in an immigratory population of Cnaphalocrocis medinalis moths based on field surveys and laboratory tests. Sci. Rep. 2019, 9, 18388. [Google Scholar] [CrossRef]
- Chen, H.; Wang, Y.; Huang, L.; Xu, C.-F.; Li, J.-H.; Wang, F.-Y.; Cheng, W.; Gao, B.-Y.; Chapman, J.W.; Hu, G. Flight capability and the low temperature threshold of a chinese field population of the fall armyworm Spodoptera frugiperda. Insects 2022, 13, 422. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.X.; Lu, Z.Q.; Geng, J.G. Application of ovarian dissection of female Cnaphalocrocis medinalis moths in prediction and forecasting system. Chin. Bull. Entomol. 1979, 16, 97–99. [Google Scholar]
- Reynolds, D.R.; Smith, A.D.; Chapman, J.W. A radar study of emigratory flight and layer formation by insects at dawn over southern Britain. Bull. Entomol. Res. 2008, 98, 35–52. [Google Scholar] [CrossRef]
- Luo, J.; Wang, Y.K.; Zhang, X.X.; Zhai, B.P. Migratory biology of the white backed planthopper: Take-off and emigration. Chin. J. Appl. Entomol. 2011, 48, 1202–1212. [Google Scholar]
- Wang, R.; Shen, H.M.; Hu, G.; Chen, X.; Zhai, B.P. The takeoff behavior of Laodelphax striatellus and its relation to the ovarian development. Chin. Bull. Entomol. 2008, 45, 42–45. [Google Scholar]
- Wang, Y.-P.; Tu, X.-B.; Lin, P.-J.; Li, S.; Xu, C.-M.; Wang, X.-Q.; Reynolds, D.R.; Chapman, J.; Zhang, Z.H.; Hu, G. Migratory take-off behaviour of the Mongolian grasshopper Oedaleus asiaticus. Insects 2020, 11, 416. [Google Scholar] [CrossRef]
- Chen, H.; Xu, C.-F.; Wang, Y.-H.; Li, X.-R.; Yu, D.-H.; Chen, A.-D.; Lyu, B.-Q.; Wu, Y.-F.; Wang, Y.-M.; Chapman, J.W.; et al. Characteristics and seasonal variation of fall armyworm migratory behavior in their year-round breeding areas in South China. Pest Manag. Sci. 2025, 81, 4051–4062. [Google Scholar] [CrossRef]
- Luo, L.Z.; Li, G.B.; Cao, Y.Z.; Hu, Y. The influence of larval rearing density on flight capacity and fecundity of adult oriental armyworm, Mythimna separata (Walker). Acta Entomol. Sin. 1995, 38, 38–45. [Google Scholar]
- Liu, Z.; Chen, Y.Y.; Lyu, B.Q.; Wang, S.C.; Lu, H.; Tang, J.H.; Zhang, Q.K.; Jiao, B.; Liu, S. Larval density-driven cannibalism shapes trade-offs among development, flight, and reproduction in Spodoptera frugiperda. J. Pest Sci. 2025, 99, 6. [Google Scholar] [CrossRef]
- Kong, H.L.; Luo, L.Z.; Jiang, X.F.; Zhang, L. Effects of larval density on flight potential of the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). Environ. Entomol. 2010, 39, 1579–1585. [Google Scholar] [CrossRef] [PubMed]
- Cease, A.J.; Talal, S.; Osgood, G.; Pulver, T.; Millerwise, S.; Overson, R.P.; Harrison, J.F. Energetic constraints on multi-day flights in migratory locusts. J. Exp. Biol. 2025, 229, jeb251191. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Luo, L.Z.; Jiang, X.F.; Hu, Y. Influences of starvation on the first day after emergence on ovarian development and flight potential in adults of the oriental armyworm, Mythimna separata (Walker) (Lepidopterea: Noctuidae). Acta Entomol. Sin. 2006, 06, 895–902. [Google Scholar]
- Riley, J.R.; Reynolds, D.R.; Smith, A.D.; Edwards, A.S.; Zhang, X.-X.; Cheng, X.-N.; Wang, H.-K.; Cheng, J.-Y.; Zhai, B.-P. Observations of the autumn migration of the rice leaf roller Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) and other moths in eastern China. Bull. Entomol. Res. 1995, 85, 397–414. [Google Scholar] [CrossRef]
- Dingle, H. Migration strategies of insects. Science 1972, 175, 1327–1335. [Google Scholar] [CrossRef] [PubMed]
- Gunn, A.; Gatehouse, A.G.; Woodrow, K.P. Trade-off between flight and reproduction in the African armyworm moth, Spodoptera exempta. Physiol. Entomol. 1989, 14, 419–427. [Google Scholar] [CrossRef]
- Chen, R.C.; Chen, X.N.; Yang, L.M.; Yin, X.D. The ovarian development of the brown planthopper (Nilaparvata lugens Stal) and its relation to migration. Acta Entomol. Sin. 1979, 22, 280–288. [Google Scholar]
- Jiang, X.F.; Luo, L.Z.; Sappington, T.W. Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. J. Insect Physiol. 2010, 56, 1631–1637. [Google Scholar] [CrossRef]
- Nation, J.L. Insect Physiology and Biochemistry; CRC Press: Boca Raton, FL, USA, 2016. [Google Scholar]
- Yang, F.; Wang, P.; Zheng, M.; Hou, X.-Y.; Zhou, L.-L.; Wang, Y.; Si, S.-Y.; Wang, X.-P.; Chapman, J.W.; Wang, Y.-M.; et al. Physiological and behavioral basis of diamondback moth Plutella xylostella migration and its association with heat stress. Pest Manag. Sci. 2024, 80, 1751–1760. [Google Scholar] [CrossRef] [PubMed]




| Treatment | Adult Age (Day) | |
|---|---|---|
| 1st | 2nd | |
| Fed | ||
| Starvation | ||
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Xu, C.-M.; Hu, M.-Y.; Wu, Y.; Wu, N.-N.; Hu, G.; Wang, Y.-M. Adult Nutrition Stress Modulates the Energy Allocation Between Migration and Reproduction in Cnaphalocrocis medinalis. Insects 2026, 17, 527. https://doi.org/10.3390/insects17050527
Xu C-M, Hu M-Y, Wu Y, Wu N-N, Hu G, Wang Y-M. Adult Nutrition Stress Modulates the Energy Allocation Between Migration and Reproduction in Cnaphalocrocis medinalis. Insects. 2026; 17(5):527. https://doi.org/10.3390/insects17050527
Chicago/Turabian StyleXu, Chao-Min, Meng-Yu Hu, Yan Wu, Ning-Ning Wu, Gao Hu, and Yu-Meng Wang. 2026. "Adult Nutrition Stress Modulates the Energy Allocation Between Migration and Reproduction in Cnaphalocrocis medinalis" Insects 17, no. 5: 527. https://doi.org/10.3390/insects17050527
APA StyleXu, C.-M., Hu, M.-Y., Wu, Y., Wu, N.-N., Hu, G., & Wang, Y.-M. (2026). Adult Nutrition Stress Modulates the Energy Allocation Between Migration and Reproduction in Cnaphalocrocis medinalis. Insects, 17(5), 527. https://doi.org/10.3390/insects17050527

