Sublethal effect of thermal stress on reproduction parameters and sexual attraction of Plodia interpunctella

Document Type : Research Paper

Authors

1 Department of Plant Protection, Faculty of Agriculture, University of Zanjan, Iran

2 Zanjan Agricultural and Natural Resources Research and Education Center, AREEO, Zanjan, Iran

10.22124/iprj.2026.31811.1660

Abstract

The present study was designed to evaluate the impact of minimal thermal stress on some reproductive activities of the Indian meal moth, Plodia interpunctella (Hübner, 1813). Adults at ages of one, three, and five days were exposed to a temperature of 44°C for 18 minutes. The results indicated a significant effect of thermal stress on male insects. The highest and lowest fertility were observed in three-day-old insects in the control and heat-stressed males (144.4 and 16 eggs respectively), representing approximately a 90% reduction in egg production. Additionally, the fecundity rate in the control treatment was 88±2%, while the lowest value in the heat-stressed male treatment was 42±12%. Heat treatments had no effect on mating frequency but influenced the duration of mating in 3-day-old insects. Furthermore, heat stress resulted in a 40-50% reduction in attraction to pheromone traps in wind tunnel. For instance, in the control and one-day-old heat-stressed male treatments, attraction rates were reported as 96.67 ± 3.3% and 53.33 ± 3.3%, respectively. According to the obtained results, the simultaneous 90% reduction in fertility and 58% reduction in egg hatching in the heat-stressed male treatment compared to the control led to a 96% decrease in net progeny. The results indicated that applying sublethal heat stress to adult Indian meal moths can disrupt reproductive activities and meanwhile reduce the number of offspring produced.

Keywords


Bodlah, M. A, Zhu, A. X., & Liu, X. D. (2016). Host choice, settling and folding leaf behaviors of the larval rice leaf folder under heat stress. Bulletin of Entomological Research, 106, 809–817. DOI: https://doi.org/10.1017/S0007485316000584
Bodlah, M. A., Gu, L. L., Tan, Y., & Liu, X. D. (2017). Behavioural adaptation of the rice leaf folder Cnaphalocrocis medinalis to short-term heat stress. Journal of Insect Physiology, 100, 28–34. DOI: https://doi.org/10.1016/j.jinsphys.2017.05.004
Bubliy, O. A., & Loeschcke, V. (2005). Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. European Society for Evolutionary Biology, 18, 789-80. DOI: https://doi.org/10.1111/j.1420-9101.2005.00928.x
Chippindale, A. K., Gibbs, A. G., Sheik, M., Yee, K. J., Djawdan, M., Bradley, T. J., Michael R., & Rose, M. R. (1998). Resource acquisition and the evolution of stress resistance in Drosophila melanogaster. Evolution, 52(5), 1342-1352. DOI: https://doi.org/10.1111/j.1558-5646.1998. tb02016.x
Cook, P. A. (1999). Sperm numbers and female fertility in the moth Plodia interpunctella (Hubner) (Lepidoptera; Pyralidae). Journal of Insect Behavior, 12(6), 767-779. DOI: https:// doi.org/10.1023/ A:1020952909933
Dahlhoff, E. P., Fearnley, S. L., Bruce, D. A., Gibbs, A. G., Stoneking, R., McMillan, D. M., Deiner, K., Smiley, J. T., & Rank, N. E. (2008). Effects of temperature on physiology and reproductive success of a montane leaf beetle: implications for persistence of native populations enduring climate change. Physiological Biochemistry and Zoology, 81, 718–732. DOI: https://doi.org/10.1086/590165
Daly, E. Z., Defourneaux, M., Legrand, C., & Renault, D. (2024). The consequences of heat waves for the reproductive success and physiology of the wingless sub-Antarctic fly Anatalanta aptera. Journal of Thermal Biology, 123, 103910. DOI: https://doi.org/10.1016/j.jtherbio.2024.103910
Defilippo, F., Grisendi, A.,  Savoldelli, S., Torri, D., Dottori, M., & Bonilauri, P. (2019). Effect of temperature and diet on Plodia interpunctella (Lepidoptera: Pyralidae) development with special reference to Isomegalen diagram and accumulated degree days. Journal of Entomological and Acarological Research, 51, 69-73. DOI: https://doi.org/10.4081/jear.2019.7855
Dell, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecological Evolutionary System, 37, 637–669. DOI:10.1146/annurev.ecolsys.37.091305.110100
Fasolo, A. G., & Krebs, R. A. (2004). A comparison of behavioural change in Drosophila during exposure to thermal stress. Biological Journal of the Linnean Society, 83, 197-205. DOI:https:// doi.org/10.1111/ j.1095-8312.2004.00380.x
Gallego, B., Verdú, J. R., Carrascal, L. M., & Lobo, J. M. (2016). A protocol for analysing thermal stress in insects using infrared thermography. Journal of Thermal Biology, 56, 113–121. DOI: https://doi.org/10.1016/j.jtherbio.2015.12.006
Gilchrist, G. W., Huye, R. B., and Parteridge, R. (1997). Thermal sensitivity of Drosophila melanogaster: Evolutionary responses of adults and eggs to laboratory natural selection at different temperatures. Physiological Zoology, 70(4), 403 – 414. DOI: https://doi.org/10.1086/515853
Gomez, F. H., Bertoli, C. I., Sambucetti, P., Scannapieco, A. C., & Norry, F. M. (2009). Heat-induced hormesis in longevity as correlated response to thermal-stress selection in Drosophila buzzatii. Journal of Thermal Biology, 34, 17-22. DOI: https://doi.org/10.1016/j.jtherbio.2008.09.003
Hagstrum, D. W., Klejdysz, T., Subramanyam, B., & Nawrot, J. (2013). Atlas of stored-product insects and mites; American Association of Cereal Chemists International: St. Paul, MN, USA.
Hallman, G. J., Wang, S., & Tang, J. (2005). Reaction orders for thermal mortality of third instars of Mexican fruit fly (Diptera: Tephritidae). Journal of Economic Entomology, 98, 1905–1910. DOI: https://doi.org/10.1603/0022-0493-98.6.1905
Harshman, L. G., Hoffmann, A. A., & Clark, A. G. (1999). Selection for starvation resistance in    Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses. Journal of Evolution Biology, 12, 370-379. DOI: https://doi.org/10.1046/j.1420 9101.1999.00024.x
van der Have, T. M. (2002). A proximate model for thermal tolerance in ectotherms. Oikos, 98, 141–155. DOI: https://doi.org/10.1034/j.1600-0706.2002.980115.x
van Heerwaarden, B., & Sgrò, C. M. (2021). Male fertility thermal limits predict vulnerability to climate warming. Nature Communications, 12, 1–11. DOI: https:// doi. org/10.1038/s4146 7-021-22546-w
Hoffmann, A. A., & Parsons, P. A. (1989). Selection for increased desiccation resistance in Drosophilu melanoguster: Additive genetic control and correlated responses for other stresses. Genetics, 122, 837-845.
Hoffmann, A. A., & Parsons, P. A. (1993). Direct and correlated responses to selection for desiccation resistance: A comparison of Drosophila melanogaster and D. simulans. Journal of Evolution Biology, 6, 643-657. DOI: https://doi.org/10.1242/jeb.076166
Huang, F. & Subramanyam, B., (2003). Effects of delayed mating on reproductive performance of Plodia interpunctella (Hubner) (Lepidoptera: Pyralidae). Journal of Stored Products Research, 39, 53–63.
Iossa, G. (2019). Sex-specific differences in thermal fertility limits. Trends in Ecology & Evolution, 34, 490–492. DOI: https://doi.org/10.1016/j. tree.2019.02.016
Iossa, G., Maury, C., Fletcher, R. M., & Eady, P. E. (2019). Temperature-induced developmental plasticity in Plodia interpunctella: Reproductive behaviour and sperm length. Journal of Evolutionary Biology, 32, 675–682. DOI: https://doi.org/10.1111/jeb.13447
Jones, O.T., Lomer, R.A. & Howse, P.E. (1981). Responses of male Mediterranean fruit flies, Ceratitis
     capitata to trimedlure in a wind tunnel of novel design. Physiological Entomology, 6, 175-181.
Katsuki, M. & Miyatake, T. (2009) Effects of temperature on mating duration, sperm transfer and remating frequency in Callosobruchus chinensis. Journal of Insect Physiology, 55, 113–116. DOI: https://doi.org/ 10.1016/j.jinsphys.2008.10.012
Krebs, R. A. & Thompson, K. A. (2006). Direct and correlated effects of selection on flight after exposure to thermal stress in Drosophila melanogaster. Genetica, 128, 217-225. DOI: https://doi.org/10.1007/s10709-005-5704-x
Kontopoulos, D. G., Carreras, B. G., Sal, S., Smith, T. P., & Pawar, S. (2018). Use and misuse of temperature normalisation in meta-analyses of thermal responses of biological traits. Peer Journal, 6, e4363; DOI: https://doi.org/10.7717/peerj.4363
Liao, H. J., Qian, Q., & Liu, X. D. (2014). Heat shock suppresses mating and sperm transfer in the rice leaf folder Cnaphalocrocis medinalis. Bulletin of Entomological Research, 104, 383–392. DOI: https://doi.org/10.1017/S0007485314000212
Mahroof, R., Subramanyam, B., & Flinn, P. (2005). Reproductive performance of Tribolium castaneum (Coleoptera: Tenebrionidae) exposed to the minimum heat treatment temperature as pupae and adults. Entomologia Experimentalis et Applicata, 98, 626-633. DOI: https://doi.org/10.1603/0022-0493-98.2.626
McAfee, A., Chapman, A., Higo, H., Underwood, R., Milone, J., & Foster, L. J. (2020). Vulnerability of honey bee queens to heat-induced loss of fertility. Nature Sustainability, 3, 367–376. DOI: https://doi.org/10.1038/ s 41893-020-0493-x
Martinet, B., Zambra, E., Przybyla, K., Lecocq, T., Anselmo, A., & Nonclercq, D. (2021). Mating under climate change: Impact of simulated heatwaves on the reproduction of model pollinators. Functional Ecology, 35, 739–752. DOI: https://doi.org/10.1111/1365-2435.13738
Mironidis, G. K., & Savopoulou-Soultani, M. (2010) Effects of heat shock on survival and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) adults. Journal of Thermal Biology, 35, 59–69. DOI: https://doi.org/10.1016/j.jtherbio.2009.11.001
Musolin, D. L. (2007). Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change. Global Change Biology, 13, 1565-1585. DOI:10.1111/j.1365-2486.2007.01395.x
Neven, L. G. (2000). Physiological responses of insects to heat. Postharvest Biology and Technology, 21, 103-111. DOI: https://doi.org/10.1016/S0925-5214(00)00169-1
Parratt, S. R., Walsh, B. S., Metelmann, S., White, N., Manser, A.,Bretman, A. J., Hoffmann, A. A., Snook, R. R., & Price, T. A. (2021). Temperatures that sterilize males better match global species distributions than lethal temperatures. Nature Climate Change, 11, 481–484. DOI: https://doi.org/10.1038/s4155 8-021-01047-0
Przybyla K., Michez D., Zambra E., Anselmo A., Hennebert E., Rasmont P., & Martinet B. (2021). Effects of heat stress on mating behavior and colony development in Bombus terrestris (Hymenoptera: Apidae). Frontiers in Ecology and Evolution, 9, 748405. DOI: https://doi.org/ 10.3389/fevo.2021.748405
Rohmer, C., David, J. R., Moreteau, B., & Joly, D. (2004). Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. The Journal of Experimental Biology, 207, 2735-2743. DOI: https://doi.org/10.1242/jeb.01087
Sales, K., Vasudeva, R., Dickinson, M. E., Godwin, J. L., Lumley, A. J., & Michalczyk, Ł. (2018). Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nature Communications, 9, 4771. DOI: https://doi.org/10.1038/s41467-018-07273-z
Sales, K., Vasudeva, R., & Gage, M. J. G. (2021). Fertility and mortality impacts of thermal stress from experimental heat waves on different life stages and their recovery in a model insect. Royal Society Open Science, 8(3) 201717. DOI: https://doi.org/10.1098/rsos.201717rsos
Scannapieco, A. C., Sørensen, J. G., Loeschcke, V., & Norry, F. M. (2007). Heat-induced hormesis in longevity of two sibling Drosophila species. Biogerontology, 8, 315-325. DOI: https://doi.org/10.1007/s10522-006-9075-1
Schou, M. F., Kristensen, T. N., Kellermann, V., Schlötterer, C., & Loeschcke, V. A. (2014). Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future. Journal of Evolutionary Biology, 27, 1859–1868. DOI: https://doi.org/10.1111/jeb.12436
Sentis A., Hemptinne J. L., & Brodeur J. (2017). Non-additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity. Global Change Biology, 23, 4598–4608. DOI: https://doi.org/10.1111/gcb.13674
Siegel, R. W. & Hall, J. C. (1979). Conditioned responses in courtship behavior of normal and mutant Drosophila. Proceeding of the National academy of the United States of America, 76, 3430-3434. DOI: https://doi.org/10.1073/pnas.76.7.3430
Sorensen, J. G., Kristensen, T. N., Kristensen, K. V., & Loeschcke, V. (2007). Gender specific effects of heat induced hormesis in Hsf-deficient Drosophila Melanogaster. Experimental Gerontology, 42(12), 1-27. DOI: https://doi.org/10.1016/j.exger.2007.09.001
Walsh, B. S., Parratt, S. R., Hoffmann, A. A., Atkinson, D., Snook, R. R., Bretman, A., & Price, T. A. R. (2019). The impact of climate change on fertility. Trends in Ecology & Evolution, 34, 249–259. DOI: https://doi.org/10.1016/j.tree.2018.12.002
Wang, X. G., Johnson, M. W., Daane, K. M., & Opp, S. (2009) Combined effects of heat stress and food supply on flight performance of olive fruit fly (Diptera: Tephritidae). Annals of the Entomological Society of America, 102, 727–734. DOI: https://doi.org/10.1603/008.102.0418 
Walsh, B. S., Parratt, S. R., Mannion, N. L. M., Snook, R. R., Bretman, A., & Price, T. A. R. (2021a). Plastic responses of survival and fertility following heat stress in pupal and adult Drosophila virilis. Ecology and Evolution, 11(24), 18238–18247. DOI: https://doi.org/10.1002/ ece3.8418
Walsh, B. S., Mannion, N. L., Price, T. A., & Parratt, S. R. (2021b). Sex-specific sterility caused by extreme temperatures is likely to create cryptic changes to the operational sex ratio in Drosophila virilis. Current Zoology, 67(3), 341–343. DOI: https://doi.org/10.1093/cz/zoaa067
Zhang, G. H., Li, Y. Y., Zhang, K. J., Wang, J. J., Liu, Y. Q., & Liu, H. (2016). Effects of heat stress on copulation, fecundity and longevity of newly-emerged adults of the predatory mite, Neoseiulus barkeri (Acari: Phytoseiidae). Systematic and Applied Acarology, 21, 295–306. DOI: https://doi.org/10.11158/saa.21.3.5
Zhu, G., Xue, M., Luo, Y., Ji, G., Liu, F., Zhao, H., & Sun, X. (2017). Effects of short-term heat shock and physiological responses to heat stress in two Bradysia adults, Bradysia odoriphaga and Bradysia difformis. Scientific Reports, 7, 1-11. DOI: https://doi.org/10.1038/s41598-017-13560-4
Zizzari, Z. V., & Ellers, J. (2011). Effects of exposure to short term heat stress on male reproductive fitness in a soil arthropod. Journal of Insect Physiology, 57, 421–426. DOI: https://doi.org/10.1016/j.jinsphys.2011.01.002
Zouba, J., A., Chermiti, M., Msetra, B., & Bouabidi, H. (2013). Hot Air Treatment for Postharvest Control of the date moth Ectomyelois ceratoniae. Tunisian Journal of Plant Protection, 8, 23-32.
Zwoinska, M. K., Rodrigues, L. R., Slate, J., & Snook, R. R. (2020). Phenotypic responses to and genetic architecture of sterility following exposure to sub-lethal temperature during development. Frontiers in Genetics, 11, 573. DOI: https://doi.org/10.3389/fgene.2020.0057