Lighting in Dark Periods Reduced the Fecundity of Spodoptera frugiperda and Limited Its Population Growth
Abstract
:1. Introduction
2. Materials and Methods
2.1. Insect’s Source and Rearing
2.2. Experimental Design
2.2.1. Development and Survival
2.2.2. Adult Fecundity and Longevity
2.2.3. Life Table Parameters and Population Dynamics
2.3. Statistical Analysis
3. Results
3.1. Development and Survival
3.2. Adult Fecundity and Longevity
3.3. Life Table Parameters
3.4. Population Dynamics
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Savary, S.; Willocquet, L.; Pethybridge, S.J.; Esker, P.; McRoberts, N.; Nelson, A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019, 3, 430. [Google Scholar] [CrossRef]
- IPPC Secretariat; Gullino, M.; Albajes, R.; Al-Jboory, I.; Angelotti, F.; Chakraborty, S.; Garrett, K.; Hurley, B.; Juroszek, P.; Makkouk, K.; et al. Scientific Review of the Impact of Climate Change on Plant Pests—A Global Challenge to Prevent and Mitigate Plant Pest Risks in Agriculture, Forestry and Ecosystems; FAO on behalf of the IPPC Secretariat: Rome, Italy, 2021. [Google Scholar]
- Desneux, N.; Luna, M.G.; Guillemaud, T.; Urbaneja, A. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: The new threat to tomato world production. J. Pest Sci. 2011, 84, 403–408. [Google Scholar] [CrossRef]
- FAO. The Global Action for Fall Armyworm Control: A Resource Mobilization Guide; FAO: Rome, Italy, 2022. [Google Scholar]
- Tay, W.T.; Meagher, R.L., Jr.; Czepak, C.; Groot, A.T. Spodoptera frugiperda: Ecology, Evolution, and Management Options of an Invasive Species. Annu. Rev. Entomol. 2023, 68, 299–317. [Google Scholar] [CrossRef]
- Montezano, D.G.; Specht, A.; Sosa-Gomez, D.R.; Roque-Specht, V.F.; Sousa-Silva, J.C.; Paula-Moraes, S.V.; Peterson, J.A.; Hunt, T.E. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr. Entomol. 2018, 26, 286–300. [Google Scholar] [CrossRef] [Green Version]
- Westbrook, J.K.; Nagoshi, R.N.; Meagher, R.L.; Fleischer, S.J.; Jairam, S. Modeling seasonal migration of fall armyworm moths. Int. J. Biometeorol. 2016, 60, 255–267. [Google Scholar] [CrossRef] [PubMed]
- Baudron, F.; Zaman-Allah, M.A.; Chaipa, I.; Chari, N.; Chinwada, P. Understanding the factors influencing fall armyworm (Spodoptera frugiperda JE Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Protect. 2019, 120, 141–150. [Google Scholar] [CrossRef]
- Li, X.J.; Wu, M.F.; Ma, J.; Gao, B.Y.; Wu, Q.L.; Chen, A.D.; Liu, J.; Jiang, Y.Y.; Zhai, B.P.; Early, R.; et al. Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Manag. Sci. 2020, 76, 454–463. [Google Scholar] [CrossRef]
- Togola, A.; Meseka, S.; Menkir, A.; Badu-Apraku, B.; Boukar, O.; Tamò, M.; Djouaka, R. Measurement of Pesticide Residues from Chemical Control of the Invasive Spodoptera frugiperda (Lepidoptera: Noctuidae) in a Maize Experimental Field in Mokwa, Nigeria. Int. J. Environ. Res. Public Health 2018, 15, 849. [Google Scholar] [CrossRef] [Green Version]
- Yin, X.; Yang, G.-F.; Niu, D.-B.; Chen, J.; Liao, M.; Cao, H.-Q.; Sheng, C.-W. Identification and pharmacological characterization of histamine-gated chloride channels in the fall armyworm, Spodoptera frugiperda. Insect Biochem. Mol. Biol. 2022, 140, 103698. [Google Scholar] [CrossRef] [PubMed]
- Shylesha, A.N.; Jalali, S.K.; Gupta, A.; Varshney, R.; Venkatesan, T.; Shetty, P.; Ojha, R.; Ganiger, P.C.; Navik, O.; Subaharan, K.; et al. Studies on new invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) and its natural enemies. J. Biol. Control 2018, 32, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Zhao, H.X.; Xian, X.Q.; Yang, N.W.; Zhang, Y.J.; Liu, H.; Wan, F.H.; Guo, J.Y.; Liu, W.X. Insights from the biogeographic approach for biocontrol of invasive alien pests: Estimating the ecological niche overlap of three egg parasitoids against Spodoptera frugiperda in China. Sci. Total Environ. 2023, 862, 160785. [Google Scholar]
- Cruz-Esteban, S.; Rojas, J.C.; Sánchez-Guillén, D.; Cruz-López, L.; Malo, E.A. Geographic variation in pheromone component ratio and antennal responses, but not in attraction, to sex pheromones among fall armyworm populations infesting corn in Mexico. J. Pest Sci. 2018, 91, 973–983. [Google Scholar] [CrossRef]
- Malo, E.A.; Cruz-Esteban, S.; Gonzalez, F.J.; Rojas, J.C. A Home-Made Trap Baited With Sex Pheromone for Monitoring Spodoptera frugiperda Males (Lepidoptera: Noctuidae) in Corn crops in Mexico. J. Econ. Entomol. 2018, 111, 1674–1681. [Google Scholar] [CrossRef] [PubMed]
- Hailu, G.; Niassy, S.; Zeyaur, K.R.; Ochatum, N.; Subramanian, S. Maize–Legume Intercropping and Push–Pull for Management of Fall Armyworm, Stemborers, and Striga in Uganda. Agron. J. 2018, 110, 2513–2522. [Google Scholar] [CrossRef] [Green Version]
- Harrison, R.D.; Thierfelder, C.; Baudron, F.; Chinwada, P.; Midega, C.; Schaffner, U.; van den Berg, J. Agro-ecological options for fall armyworm (Spodoptera frugiperda JE Smith) management: Providing low-cost, smallholder friendly solutions to an invasive pest. J. Environ. Manag. 2019, 243, 318–330. [Google Scholar] [CrossRef] [PubMed]
- Fatoretto, J.C.; Michel, A.P.; Silva Filho, M.C.; Silva, N. Adaptive Potential of Fall Armyworm (Lepidoptera: Noctuidae) Limits Bt Trait Durability in Brazil. J. Integr. Pest Manag. 2017, 8, 17. [Google Scholar] [CrossRef]
- Moar, W.J.; Pusztai-Carey, M.; Van Faassen, H.; Bosch, D.; Frutos, R.; Rang, C.; Luo, K.; Adang, M.J. Development of Bacillus thuringiensis CryIC Resistance by Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). Appl. Environ. Microbiol. 1995, 61, 2086–2092. [Google Scholar] [CrossRef] [Green Version]
- Wu, K. Management strategies of fall armyworm (Spodoptera frugiperda) in China. Plant Prot. 2020, 46, 1–5. [Google Scholar]
- Yang, P.; Zhu, X.; Guo, J.; Wang, Z. Strategy and advice for managing the fall armyworm in China. Plant Prot. 2019, 45, 1–6. [Google Scholar]
- Feng, H.; Wu, X.; Bo, W.; Kongming, W. Seasonal Migration of Helicoverpa armigera (Lepidoptera: Noctuidae) Over the Bohai Sea. J. Econ. Entomol. 2009, 102, 95–104. [Google Scholar] [CrossRef]
- Maelzer, D.A.; Zalucki, M.P. Analysis of long-term light-trap data for Helicoverpa spp. (Lepidoptera: Noctuidae) in Australia: The effect of climate and crop host plants. Bull. Entomol. Res. 1999, 89, 455–463. [Google Scholar] [CrossRef]
- Di Cara, F.; King-Jones, K. How Clocks and Hormones Act in Concert to Control the Timing of Insect Development. Curr. Top. Dev. Biol. 2013, 105, 1–36. [Google Scholar]
- Yamaguchi, S.; Desplan, C.; Heisenberg, M. Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc. Natl. Acad. Sci. USA 2010, 107, 5634–5639. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hori, M.; Shibuya, K.; Sato, M.; Saito, Y. Lethal effects of short-wavelength visible light on insects. Sci. Rep. 2014, 4, 7383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Y.R.; Wei, W.L.; Tzeng, D.T.W.; Owens, A.C.S.; Tang, H.C.; Wu, C.S.; Lin, S.S.; Zhong, S.; Yang, E.C. Effects of artificial light at night (ALAN) on gene expression of Aquatica ficta firefly larvae. Environ. Pollut. 2021, 281, 116944. [Google Scholar] [CrossRef]
- Yan, S.; Liu, Y.-J.; Zhu, J.-L.; Cui, W.-N.; Zhang, X.-F.; Yang, Y.-H.; Liu, X.-M.; Zhang, Q.-W.; Liu, X.-X. Daily expression of two circadian clock genes in compound eyes of Helicoverpa armigera: Evidence for peripheral tissue circadian timing. Insect Sci. 2019, 26, 217–228. [Google Scholar] [CrossRef] [PubMed]
- Philogene, B.; McNeil, J. The influence of light on the non-diapause related aspects of development and reproduction in insects. Photochem. Photobiol. 2008, 40, 753–762. [Google Scholar] [CrossRef]
- Leather, S.; Walters, K.; Bale, J.S. The Ecology of Insect Overwintering; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
- Cardé, R.T.; Roelofs, W.L. Temperature modification of male sex pheromone response and factors affecting female calling in Holomelina immaculata (Lepidoptera: Arctiidae). Can. Entomol. 1973, 105, 1505–1512. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Wang, F.; Wan, X.; Xu, J.; Ye, H. Reproductive behavior and circadian rhythms of Spodoptera frugiperda. J. Environ. Entomol. 2022, 44, 509–522. [Google Scholar]
- Sun, X.; Xu, R.; Ge, S.; Fu, X.; Xincheng, Z.; Wu, K. Effects of photoperiod on the eclosion, reproduction and flight performance of Helicoverpa armigera (Lepidoptera: Noctuidae). J. Environ. Entomol. 2019, 41, 1045–1056. [Google Scholar]
- Jiang, Y.; Wu, Y.; Li, T.; Miao, J.; Gong, Z.; Duan, Y.; Mei, S.; Wang, X.; Liu, Q. Light and dark adaptation of adult compound eyes of Spodoptera frugiperda (Lepidoptera:Noctuidae) and their transformation rate to light-adapted stateunder yellow light. Acta Entomol. Sin. 2021, 64, 1120–1126. [Google Scholar]
- Meng, L.; Jiang, X.; Li, P.; Xia, J.; Zhang, T.; Cheng, Y.; Zhang, L. Comparison of bisexual life tables of Spodoptera frugiperda in differentphotoperiods. Plant Prot. 2022, 48, 63–73. [Google Scholar]
- Chen, S.; Chen, Q.; Liu, H.; Liu, C.; Liu, Y.; Liu, X. Effects of photoperiod on the growth and development of Spodoptera frugiperda. China Plant Prot. 2021, 41, 5–9. [Google Scholar]
- Wang, F.; Li, L.; Wei, Q.; Gu, Y.; Huang, C.; Liao, R.; Liao, S. Effects of different light environments on oviposition of Conopomorpha sinensis and itscontrol efficacy in field. J. South. Agric. 2020, 51, 313–318. [Google Scholar]
- Liu, Y.; Zhang, D.; Yang, L.; Dong, Y.; Liang, G.; Philip, D.; Ren, G.; Xu, P.; Wu, K. Analysis of phototactic responses in Spodoptera frugiperda using Helicoverpa armigera as control. J. Integr. Agric. 2021, 20, 821–828. [Google Scholar] [CrossRef]
- Su, X.; Li, C.; Huang, S.; Liu, W.; Zhang, Y.; Pan, Z. Optimization of artificial diet and rearing condition of fall armyworm, Spodoptera frugiperda (J.E Smith). J. Environ. Entomol. 2019, 41, 992–998. [Google Scholar]
- Chi, H.; Liu, H.S.I. Two new methods for study of insect population ecology. Bull. Inst. Zool. Acad. Sin. 1985, 24, 225–240. [Google Scholar]
- Chi, H. Life-Table Analysis Incorporating Both Sexes and Variable Development Rates Among Individuals. Environ. Entomol. 1988, 17, 26–34. [Google Scholar] [CrossRef]
- Chi, H. TWOSEX-MSChart: A Computer Program for the Age-Stage, Two-Sex Life Table Analysis; National Chung Hsing University: Taichung, Taiwan, China, 2022. [Google Scholar]
- Merlin, C.; Lucas, P.; Rochat, D.; François, M.-C.; Maïbèche-Coisne, M.; Jacquin-Joly, E. An Antennal Circadian Clock and Circadian Rhythms in Peripheral Pheromone Reception in the Moth Spodoptera littoralis. J. Biol. Rhythm. 2007, 22, 502–514. [Google Scholar] [CrossRef]
- Zhu, L.; Liu, W.; Tan, Q.-Q.; Lei, C.-L.; Wang, X.-P. Differential expression of circadian clock genes in two strains of beetles reveals candidates related to photoperiodic induction of summer diapause. Gene 2017, 603, 9–14. [Google Scholar] [CrossRef]
- Danks, H.V. Insect Dormancy: An Ecological Perspective; Biological Survey of Canada (Terrestrial Arthropods), National Museum of Natural Sciences: Ottawa, ON, Canada, 1987.
- Cymborowski, B.; Giebułtowicz, J.M. Effect of photoperiod on development and fecundity in the flour moth, Ephestia kuehniella. J. Insect Physiol. 1976, 22, 1213–1217. [Google Scholar] [CrossRef]
- Bradshaw, W.E.; Lounibos, L.P. Photoperiodic control of development in the pitcher-plant mosquito, Wyeomyia smithii. Can. J. Zool. 1972, 50, 713–719. [Google Scholar] [CrossRef]
- Bradshaw, W.E.; Holzapfel, C.M. Biology of tree-hole mosquitoes: Photoperiodic control of development in northern Toxorhynchites rutilus (Coq.). Can. J. Zool. 1975, 53, 889–893. [Google Scholar] [CrossRef]
- Yee, D.A.; Juliano, S.A.; Vamosi, S.M. Seasonal Photoperiods Alter Developmental Time and Mass of an Invasive Mosquito, Aedes albopictus (Diptera: Culicidae), Across Its North-South Range in the United States. J. Med. Entomol. 2012, 49, 825–832. [Google Scholar] [CrossRef] [Green Version]
- Chen, W.B.; Weng, Q.F.; Nie, R.; Zhang, H.Z.; Jing, X.Y.; Wang, M.Q.; Li, Y.Y.; Mao, J.J.; Zhang, L.S. Optimizing photoperiod, exposure time, and host-to-parasitoid ratio for mass-rearing of Telenomus remus, an egg parasitoid of Spodoptera frugiperda, on Spodoptera litura eggs. Insects 2021, 12, 1050. [Google Scholar] [CrossRef]
- Hu, S.; Wang, X.-Y.; Yang, Z.-Q.; Duan, J.J. Effects of photoperiod and light intensity on wing dimorphism and development in the parasitoid Sclerodermus pupariae (Hymenoptera: Bethylidae). Biol. Control 2019, 133, 117–122. [Google Scholar] [CrossRef]
- Rwomushana, I. Spodoptera Frugiperda (Fall Armyworm); CABI Compendium; CABI International: Oxfordshire, UK, 2022. [Google Scholar]
- Velarde, R.A.M.; Wiedenmann, R.N.; Voegtlin, D.J. Influence of photoperiod on the overwintering induction of Galerucella calmariensis L. BioControl 2002, 47, 587–601. [Google Scholar] [CrossRef]
- Malaquias, J.B.; Ramalho, F.S.; Fernandes, F.S.; Souza, J.V.S.; Azeredo, T.L. Effects of photoperiod on the development and growth of Podisus nigrispinus, a predator of cotton leafworm. Phytoparasitica 2009, 37, 241–248. [Google Scholar] [CrossRef]
- Riemann, J.G.; Thorson, B.J.; Ruud, R.L. Daily cycle of release of sperm from the testes of the Mediterranean flour moth. J. Insect Physiol. 1974, 20, 195–207. [Google Scholar] [CrossRef]
- Determination of optimum temperature and photoperiod for mass production of Oxya hyla hyla (Serville). Turk. J. Zool. 2012, 36, 329–339.
- Kingsolver, J.G.; Huey, R. Size, temperature, and fitness: Three rules. Evol. Ecol. Res. 2008, 10, 251–268. [Google Scholar]
- Demotes-Mainard, S.; Péron, T.; Corot, A.; Bertheloot, J.; Le Gourrierec, J.; Pelleschi-Travier, S.; Crespel, L.; Morel, P.; Huché-Thélier, L.; Boumaza, R.; et al. Plant responses to red and far-red lights, applications in horticulture. Environ. Exp. Bot. 2016, 121, 4–21. [Google Scholar] [CrossRef]
- Huang, Q.; Xie, S.; Cao, M.; Chen, L.; Li, M.; Qin, J.; Li, W.; Yu, H.; Que, M.; Chen, G. Effects of supplementary illumination at night on leaf nutrition and fruit quality folspring fruit of Kyoho grape. J. South. Agric. 2019, 50, 781–787. [Google Scholar]
- Li, X.; Lu, W.; Hu, G.; Wang, X.C.; Zhang, Y.; Sun, G.X.; Fang, Z. Effects of light-emitting diode supplementary lighting on the winter growth of greenhouse plants in the Yangtze River Delta of China. Bot. Stud. 2016, 57, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Treatment | Photoperiod (L:D) | ||
---|---|---|---|
The First Experiment | The Second Experiment | ||
Egg-Pupal Stage | From Egg-Pupal Stage | To Adult Stage | |
LL | 24:0 | 24:0 | 24:0 |
CK-L | — | 14:10 | 24:0 |
CK | 14:10 | 14:10 | 14:10 |
CK-D | — | 14:10 | 0:24 |
DD | 0:24 | 0:24 | 0:24 |
Treatment | LL | CK | DD |
---|---|---|---|
Egg-larval stage (d) | 18.99 ± 0.19 a | 16.80 ± 0.08 b | 17.31 ± 0.10 b |
Pupal stage (d) | 8.02 ± 0.14 c | 8.65 ± 0.08 b | 9.06 ± 0.07 a |
Pre-adult stage (d) | 23.44 ± 0.09 a | 22.59 ± 0.09 b | 23.42 ± 0.06 a |
Pupal weight (g) | |||
Female | 0.30 ± 0.01 a | 0.25 ± 0.00 b | 0.21 ± 0.00 c |
Male | 0.29 ± 0.00 a | 0.23 ± 0.01 b | 0.23 ± 0.01 b |
Pupal length (mm) | |||
Female | 18.31 ± 0.12 a | 17.14 ± 0.14 b | 16.36 ± 0.14 c |
Male | 18.47 ± 0.12 a | 17.44 ± 0.19 b | 17.22 ± 0.1 b |
Pupation rate (%) | 93.82 ± 0.68 b | 96.40 ± 0.55 ab | 97.07 ± 1.67 a |
Pupal emergence rate (%) | 31.31 ± 7.13 b | 88.79 ± 2.85 a | 94.53 ± 3.02 a |
Treatment | LL | CK-L | CK | CK-D | DD |
---|---|---|---|---|---|
Adult pre-oviposition period (d) | 6.50 ± 0.29 ab | 8.00 ± 1.00 a | 3.27 ± 0.59 b | 6.07 ± 0.69 ab | 4.94 ± 0.57 ab |
Total pre-oviposition period (d) | 30.00 ± 0.00 a | 30.00 ± 0.00 a | 25.93 ± 0.59 a | 28.64 ± 0.70 a | 28.34 ± 0.58 a |
Number of eggs per female moth | 3.57 ± 1.80 c | 5.90 ± 4.92 c | 662.65 ± 70.02 a | 310.43 ± 45.06 b | 327.97 ± 59.73 b |
Oviposition days (d) | 0.07 ± 0.03 c | 0.03 ± 0.02 c | 2.72 ± 0.27 a | 1.63 ± 0.20 b | 1.45 ± 0.22 b |
Oviposition probability (%) | 6.67 ± 3.33 b | 3.33 ± 3.33 b | 83.33 ± 3.33 a | 70.00 ± 10 a | 63.33 ± 9.28 a |
Female longevity (d) | 6.67 ± 0.52 c | 9.53 ± 0.32 b | 12.79 ± 0.76 a | 12.41 ± 0.46 a | 11.51 ± 0.39 a |
Male longevity (d) | 6.22 ± 0.36 c | 9.31 ± 0.25 b | 11.77 ± 0.51 a | 10.66 ± 2.79 a | 10.64 ± 0.32 a |
Treatment | R0 | T (d) | r (d−1) | λ (d−1) |
---|---|---|---|---|
LL | 2.33 ± 1.14 c | 31.00± 0.00 a | 0.0272 ± 0.0181 c | 1.0276 ± 0.0184 c |
CK-L | 3.77 ± 2.97 c | 30.35 ± 0.81 a | 0.0437 ± 0.0277 c | 1.0447 ± 0.0286 c |
CK | 268.68 ± 49.45 a | 26.56 ± 0.34 c | 0.2106 ± 0.0079 a | 1.2344 ± 0.0097 a |
CK-L | 137.87 ± 29.88 b | 28.51 ± 0.61 b | 0.1728 ± 0.0100 b | 1.1886 ± 0.0118 b |
DD | 189.74 ± 40.15 ab | 27.92 ± 0.26 b | 0.1879 ± 0.0088 ab | 1.2067 ± 0.0105 ab |
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Yuan, X.; Wei, S.; Li, D.; Zhang, J. Lighting in Dark Periods Reduced the Fecundity of Spodoptera frugiperda and Limited Its Population Growth. Agronomy 2023, 13, 971. https://doi.org/10.3390/agronomy13040971
Yuan X, Wei S, Li D, Zhang J. Lighting in Dark Periods Reduced the Fecundity of Spodoptera frugiperda and Limited Its Population Growth. Agronomy. 2023; 13(4):971. https://doi.org/10.3390/agronomy13040971
Chicago/Turabian StyleYuan, Xi, Shengbao Wei, Dunsong Li, and Jiaen Zhang. 2023. "Lighting in Dark Periods Reduced the Fecundity of Spodoptera frugiperda and Limited Its Population Growth" Agronomy 13, no. 4: 971. https://doi.org/10.3390/agronomy13040971
APA StyleYuan, X., Wei, S., Li, D., & Zhang, J. (2023). Lighting in Dark Periods Reduced the Fecundity of Spodoptera frugiperda and Limited Its Population Growth. Agronomy, 13(4), 971. https://doi.org/10.3390/agronomy13040971