Insect responses to drought events and salinity stress: unveiling direct and indirect effects

Document Type : Review Article

Authors

1 Department of Plant Protection, Ferdowsi University of Mashhad. Mashhad, , I. R. Iran

2 Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, I. R. Iran

Abstract

The future holds a projection of escalated occurrences of extreme climate events, which are expected to affect insect life substantially. Extensive research efforts in this field have witnessed rapid expansion despite significant gaps in knowledge. This review article addresses a deeper understanding of the impacts of severe climate events on insects that outline promising avenues for future research in this field. Drought has emerged as one of the predominant forms of extreme climate events that have extensively influenced insects, as frequently documented in the literature. The significance of drought occurrences on insects is crucial within the climate change scenario. Furthermore, the increasing occurrence and intensity of drought episodes, which are associated with changes in the climate, can result in elevated salinity levels in water bodies and soils. These changes have far-reaching implications for ecosystems, including impacts on biology, survival, and insect behavior. This review aims to analyze developments in information acquisition with anticipated climate change implications, particularly drought and salinity, on various aspects of insect life.

Keywords

Main Subjects


Article Title [Persian]

پاسخ حشرات به رویدادهای خشکسالی و تنش شوری: آشکار کردن اثرات مستقیم و غیر مستقیم

Authors [Persian]

  • لیدا فکرت 1
  • مریم آل عصفور 2
1 گروه گیاهپزشکی، دانشگاه فردوسی مشهد، مشهد، ج.ا. ایران
2 گروه گیاهپزشکی، دانشکده کشاورزی شیراز، دانشگاه شیراز، ج.ا. ایران
Abstract [Persian]

در آینده پیش‌بینی می‌شود رخدادهای شدید آب و هوایی افزایش یابد و انتظار می‌رود که این رخدادها اثرات قابل‌توجهی بر حشرات داشته باشند. تلاش های تحقیقاتی گسترده در این زمینه در حال انجام است با این حال، شکاف های قابل توجهی در دانش وجود دارد. برای به دست آوردن بینش در مورد اثرات رویدادهای آب و هوایی شدید بر حشرات و ترسیم راه های امیدوارکننده برای تحقیقات آینده در این زمینه، این مرور انجام شد. همانطور که در بررسی منابع دیده می‌شود خشکسالی به عنوان یکی از اشکال غالب رویدادهای شدید آب و هوایی است که به طور گسترده بر حشرات تأثیر می‌گذارد. تأثیر خشکسالی بر حشرات در زمینه تغییرات آب و هوایی مهم است. علاوه بر این، فراوانی و شدت فزاینده رویدادهای خشکسالی، که با تغییرات آب و هوایی مرتبط است، باعث افزایش سطح شوری در بدنه‌های آبی و خاک می‌شود. این تغییرات پیامدهای گسترده ای برای اکوسیستم ها، از جمله تأثیرات بر زیست شناسی، بقا و رفتار حشرات دارد. این بررسی با هدف تجزیه و تحلیل پیامدهای تغییر اقلیم ، به ویژه خشکسالی و شوری، بر جنبه های مختلف زندگی حشرات انجام شده است.

Keywords [Persian]

  • حشره
  • تنش خشکی
  • تنش شوری
  • جدول زندگی
Ahmed, I. M., Nadira, U. A., Bibi, N., Cao, F., He, X., Zhang, G., & Wu, F. (2015). Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environmental and Experimental Botany, 111, 1-12.‏ doi:10.1016/j.envexpbot.2014.10.003
Aleosfoor, M., Zahediannezhad, M., Minaei, K., Fekrat, L., & Razi, H. (2023). Effects of drought stress and plant cultivar type on demographic characteristics of the rose-grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae). Bulletin of Entomological Research, 113(2), 196-211. doi:10.1017/S0007485322000463
Allen, C. D., Macalady, A. K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., . . . & Cobb, N. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management, 259(4), 660-684. doi: 10.1016/j.foreco.2009.09.001
Anderegg, W. R. L., Hicke, J. A., Fisher, R. A., Allen, C. D., Aukema, J., Bentz, B., . . . & Zeppel, M. (2015). Tree mortality from drought, insects, and their interactions in a changing climate. New Phytologist, 208(3), 674-683. doi: 10.1111/nph.13477
Aslam, T. J., Johnson, S. N., & Karley, A. J. (2013). Plant‐mediated effects of drought on aphid population structure and parasitoid attack. Journal of Applied Entomology, 137(1-2), 136-145.‏ doi: 10.1111/j.1439-0418.2012.01747.x
Banfield-Zanin, J. A., & Leather, S. R. (2015). Drought intensity and frequency have contrasting effects on development time and survival of the green spruce aphid. Agricultural and Forest Entomology, 17(3), 309-316. doi: 10.1111/afe.12109
Banfield-Zanin, J. A., & Leather, S. R. (2016). Prey-mediated effects of drought on the consumption rates of coccinellid predators of Elatobium abietinumInsects, 7(4), 49.‏ doi: 10.3390/insects7040049
Bao, Y., Wang, F., Tong, S., Na, L., Han, A., Zhang, J., ... & Zhang, Q. (2019). Effect of drought on outbreaks of major forest pests, pine caterpillars (Dendrolimus spp.), in Shandong Province, China. Forests, 10(3), 264.‏ doi: 10.3390/f10030264
Bowdish, T. I., & Stiling, P. (1998). The influence of salt and nitrogen on herbivore abundance: Direct and indirect effects. Oecologia, 113(3), 400-405. doi:10.1007/s004420050392
Cabrera, H. M., Argandoña, V. H., Zúñiga, G. E., & Corcuera, L. J. (1995). Effect of infestation by aphids on the water status of barley and insect development. Phytochemistry, 40(4), 1083-1088. doi:10.1016/0031-9422(95)00325-2
Cañedo-Argüelles, M., Kefford, B., & Schäfer, R. (2019). Salt in freshwaters: Causes, effects and prospects- introduction to the theme issue. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1764), 20180002. doi:10.1098/rstb.2018.0002
Carbonell, J. A., Bilton, D. T., Calosi, P., Millán, A., Stewart, A., & Velasco, J. (2017). Metabolic and reproductive plasticity of core and marginal populations of the eurythermic saline water bug Sigara selecta (Hemiptera: Corixidae) in a climate change context. Journal of Insect Physiology, 98, 59-66. doi: 10.1016/j.jinsphys.2016.11.015
Dale, A. G., & Frank, S. D. (2017). Warming and drought combine to increase pest insect fitness on urban trees. PloS one, 12(3), e0173844.‏
Dang, Z., Li, Y., Gao, Z., & Pan, W. (2009). Influence of soil moisture on growth and development of Holotrichia oblita. Chinese Bulletin of Entomology, 46(1), 135-138.‏
Dasgupta, S., Hossain, M. M., Huq, M., & Wheeler, D. (2015). Climate change and soil salinity: The case of coastal Bangladesh. Ambio, 44(8), 815-826. doi:10.1007/s13280-015-0681-5
Descamps, C., Quinet, M., & Jacquemart, A.-L. (2021). The effects of drought on plant–pollinator interactions: What to expect? Environmental and Experimental Botany, 182, 104297. doi: 10.1016/j.envexpbot.2020.104297
Dong, Y. C., Wang, Z. J., Bu, R. Y., Dai, H. J., Zhou, L. J., Han, P., Amiens-Desneux, E., Bearez, P., & Desneux, N. (2020). Water and salt stresses do not trigger bottom-up effects on plant-mediated indirect interactions between a leaf chewer and a sap-feeder. Journal of Pest Science, 93(4), 1267–1280.
Douglas, A. (2006). Phloem-sap feeding by animals: Problems and solutions. Journal of Experimental Botany, 57(4), 747-754.‏ doi: 10.1093/jxb/erj067
Elnitsky, M. A., Benoit, J. B., Denlinger, D. L., & Lee, R. E. (2008). Desiccation tolerance and drought acclimation in the Antarctic collembolan Cryptopygus antarcticus. Journal of Insect Physiology, 54(10), 1432-1439. doi: 10.1016/j.jinsphys.2008.08.004
Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S. M. A. (2009). Plant Drought Stress: Effects, Mechanisms and Management. In E., Lichtfouse, M., Navarrete, P., Debaeke, S., Véronique, & C., Alberola (Eds.), Sustainable Agriculture (pp. 153-188). Dordrecht: Springer Netherlands.
Filazzola, A., Matter, S. F., & MacIvor, J. S. (2021). The direct and indirect effects of extreme climate events on insects. Science of The Total Environment, 769, 145161. doi: 10.1016/j.scitotenv.2021.145161
Forieri, I., Hildebrandt, U., & Rostás, M. (2016). Salinity stress effects on direct and indirect defense metabolites in maize. Environmental and Experimental Botany, 122, 68-77. doi: 10.1016/j.envexpbot.2015.09.007
Forister, M. L., Fordyce, J. A., Nice, C. C., Thorne, J. H., Waetjen, D. P., & Shapiro, A. M. (2018). Impacts of a millennium drought on butterfly faunal dynamics. Climate Change Responses, 5(1), 3. doi: 10.1186/s40665-018-0039-x
Gely, C., Laurance, S. G. W., & Stork, N. E. (2020). How do herbivorous insects respond to drought stress in trees? Biological Reviews, 95(2), 434-448. doi:10.1111/brv.12571
Guohong, Z., Guangwen, L., Mengyi, M., & Ling, Z. (2001). Effects of temperature and humidity on development of experimental cotton leafworm population. Journal of South China Agricultural University, 22(3), 29-32.‏
Han, P., Wang, Z.-j., Lavoir, A.-V., Michel, T., Seassau, A., Zheng, W.-y., Niu, C.Y., & Desneux, N. (2016). Increased water salinity applied to tomato plants accelerates the development of the leaf miner Tuta absoluta through bottom-up effects. Scientific Reports, 6(1), 32403. doi:10.1038/srep32403
Hoffmann, A. A., Chown, S. L., & Clusella-Trullas, S. (2013). Upper thermal limits in terrestrial ectotherms: How constrained are they? Functional Ecology, 27(4), 934-949. doi: 10.1111/j.1365-2435.2012.02036.x
Huberty, A. F., & Denno, R. F. (2004). Plant water stress and its consequences for herbivorous insects: A new synthesis. Ecology, 85(5), 1383-1398. doi:10.1890/03-0352
Kansman, J. T., Basu, S., Casteel, C. L., Crowder, D. W., Lee, B. W., Nihranz, C. T., & Finke, D. L. (2022). Plant water stress reduces aphid performance: exploring mechanisms driven by water stress intensity. Frontiers in Ecology and Evolution, 10.‏ doi: 10.3389/fevo.2022.846908
Khan, M. A. M., Ulrichs, C., & Mewis, I. (2010). Influence of water stress on the glucosinolate profile of Brassica oleracea var. italica and the performance of Brevicoryne brassicae and Myzus persicae. Entomologia Experimentalis et Applicata, 137(3), 229-236. doi: 10.1111/j.1570-7458.2010.01059.x
Klockmann, M., & Fischer, K. (2017). Effects of temperature and drought on early life stages in three species of butterflies: Mortality of early life stages as a key determinant of vulnerability to climate change? Ecology and Evolution, 7(24), 10871-10879. doi:10.1002/ece3.3588
Kolb, T. E., Fettig, C. J., Ayres, M. P., Bentz, B. J., Hicke, J. A., Mathiasen, R., . . . & Weed, A. S. (2016). Observed and anticipated impacts of drought on forest insects and diseases in the United States. Forest Ecology and Management, 380, 321-334. doi: 10.1016/j.foreco.2016.04.051
Lin, P.-A., Paudel, S., Afzal, A., Shedd, N. L., & Felton, G. W. (2021). Changes in tolerance and resistance of a plant to insect herbivores under variable water availability. Environmental and Experimental Botany, 183, 104334. doi:10.1016/j.envexpbot.2020.104334
Liu, X., Yang, H., Niu, F., Sun, H., & Li, C. (2023). Impact of water stress on the demographic traits and population projection of Colorado potato beetle. Frontiers in Physiology, 14. doi:10.3389/fphys.2023.1148129
Marček, T., Hamow, K. Á., Végh. B., Janda, T., & Darko, E. (2019) Metabolic response to drought in six winter wheat genotypes. PloS one 14(2), e0212411. doi:10.1371/journal.pone.0212411
Marques, S. C., Primo, A. L., Martinho, F., Azeiteiro, U. M., & Pardal, M. (2014). Shifts in estuarine zooplankton variability following extreme climate events: A comparison between drought and regular years. Marine Ecology Progress Series, 499, 65-76. doi: 10.3354/meps10635
Mattson, W. J., & Haack, R. A. (1987). The role of drought in outbreaks of plant-eating insects. Bio Science, 37(2), 110–118. doi: 10.2307/1310365
McDermott Long, O., Warren, R., Price, J., Brereton, T. M., Botham, M. S., & Franco, A. M. A. (2017). Sensitivity of UK butterflies to local climatic extremes: Which life stages are most at risk? Journal of Animal Ecology, 86(1), 108-116. doi: 10.1111/1365-2656.12594
Muilenburg, V. L., & Herms, D. A. (2012). A review of bronze birch borer (Coleoptera: Buprestidae) life history, ecology, and management. Environmental Entomology, 41(6), 1372-1385. doi:10.1603/en12238
Müller, M., Olsson, P. O., Eklundh, L., Jamali, S., & Ardö, J. (2022). Features predisposing forest to bark beetle outbreaks and their dynamics during drought. Forest Ecology and Management, 523, 120480. doi: 10.1016/j.foreco.2022.120480
Munns, R., & Tester, M. (2008). Mechanisms of Salinity Tolerance. Annual Review of Plant Biology, 59(1), 651-681. doi:10.1146/annurev.arplant. 59.032607.092911
Netherer, S., Matthews, B., Katzensteiner, K., Blackwell, E., Henschke, P., Hietz, P., Pennerstorfer, J., Rosner, S., Kikuta, S., Schume, H, & Schopf, A. (2015). Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytologist, 205(3), 1128-1141. doi:10.1111/nph.13166
Netherer, S., Panassiti, B., Pennerstorfer, J., & Matthews, B. (2019). Acute drought is an important driver of bark beetle infestation in Austrian Norway spruce stands. Frontiers in Forests and Global Change, 2, 39.‏ doi: 10.3389/ffgc.2019.00039
Pineda, A., Pangesti, N., Soler, R., Dam, N. M. v., Loon, J. J. A. v., & Dicke, M. (2016). Negative impact of drought stress on a generalist leaf chewer and a phloem feeder is associated with, but not explained by an increase in herbivore-induced indole glucosinolates. Environmental and Experimental Botany, 123, 88-97. doi:10.1016/j.envexpbot.2015.11.007
Polack, L. A., Pereyra, P. C., & Sarandón, S. J. (2011). Effects of plant stress and habitat manipulation on aphid control in greenhouse sweet peppers. Journal of Sustainable Agriculture, 35(7), 699-725.‏ doi: 10.1080/10440046.2011.606489
Quais, M. K., Ansari, N. A., Wang, G.-Y., Zhou, W.-W., & Zhu, Z.-R. (2019). Host Plant salinity stress affects the development and population parameters of Nilaparvata lugens (Hemiptera: Delphacidae). Environmental Entomology, 48(5), 1149-1161. doi:10.1093/ee/nvz084
Price, P. W. (1991). Plant vigor and herbivore attack. Oikos, 62,244–251.
Rad, F., Aleosfoor, M., Fekrat, L., & Minaei, K. (2023). Water stress decreases the demographic performance of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), on tomato. Arthropod-Plant Interactions. doi:10.1007/s11829-023-09989-2
Rad, F., Aleosfoor, M., Fekrat, L., Minaei, K., Etemadi, M., Afsharifar, A. R., & Eshghi, S. (2024). Life-history parameters of the western flower thrips, Frankliniella occidentalis, are affected by host plant salinity stress. Entomologia Experimentalis et Applicata, 172(1), 15-26. doi:10.1111/eea.13378
Raderschall, C. A., Vico, G., Lundin, O., Taylor, A. R., & Bommarco, R. (2021). Water stress and insect herbivory interactively reduce crop yield while the insect pollination benefit is conserved. Global Change Biology, 27(1), 71-83. doi:10.1111/gcb.15386
Renault, S., Wolfe, S., Markham, J., & Avila-Sakar, G. (2016). Increased resistance to a generalist herbivore in a salinity-stressed non-halophytic plant. AoB PLANTS, 8, plw028. doi:10.1093/aobpla/plw028
Sharma, H. C. (2014). Climate change effects on insects: Implications for crop protection and food security. Journal of Crop Improvement, 28(2), 229-259. doi:10.1080/15427528.2014.881205
Sharma, H. C., Srivastava, C. P., Durairaj, C., & Gowda, C. L. L. (2010). Pest management in grain legumes and climate change. In S. S. Yadav & R. Redden (Eds.), Climate change and management of cool season grain legume crops (pp. 115-139). Dordrecht: Springer Netherlands.
Shehzad, M., Gulzar, A., Staley, J. T., & Tariq, M. (2021). The effects of drought stress and type of fertiliser on generalist and specialist herbivores and their natural enemies. Annals of Applied Biology, 178(2), 377-386.
Sienkiewicz-Paderewska, D., Dmuchowski, W., Baczewska, A. H., Brągoszewska, P., & Gozdowski, D. (2017). The effect of salt stress on lime aphid abundance on Crimean linden (Tilia ‘Euchlora’) leaves. Urban Forestry & Urban Greening, 21, 74-79. doi:10.1016/j.ufug.2016.11.010
Silver, S., & Donini, A. (2021). Physiological responses of freshwater insects to salinity: Molecular, cellular, and organ-level studies. Journal of Experimental Biology, 224(20), jeb222190
Soman, P., Nwanze, K. F., Laryea, K. B., Butler, D. R., & Reddy, Y. V. R. (1994). Leaf surface wetness in sorghum and resistance to shoot fly, Atherigona soccata: Role of soil and plant water potentials. Annals of Applied Biology, 124(1), 97-108.
Timms, J. E., Oliver, T. H., Straw, N. A., & Leather, S. R. (2008). The effects of host plant on the coccinellid functional response: Is the conifer specialist Aphidecta obliterata (L.) (Coleoptera: Coccinellidae) better adapted to spruce than the generalist Adalia bipunctata (L.) (Coleoptera: Coccinellidae)? Biological Control, 47(3), 273-281. doi:10.1016/j.biocontrol.2008.08.009
Van Bael, S. A., Aiello, A., Valderrama, A., Medianero, E., Samaniego, M., & Wright, S. J. (2004). General herbivore outbreak following an El Nino-related drought in a lowland Panamanian forest. Journal of Tropical Ecology, 20(6), 625-633.‏ doi:10.1017/S0266467404001725
Verdugo, J. A., Sauge, M.-H., Lacroze, J.-P., Francis, F., & Ramirez, C. C. (2015). Drought-stress and plant resistance affect herbivore performance and proteome: the case of the green peach aphid Myzus persicae (Hemiptera: Aphididae). Physiological Entomology, 40(4), 265-276. doi:10.1111/phen.12111
Weldegergis, B. T., Zhu, F., Poelman, E. H., & Dicke, M. (2015). Drought stress affects plant metabolites and herbivore preference but not host location by its parasitoids. Oecologia, 177(3), 701-713. doi:10.1007/s00442-014-3129-x
Wotherspoon, K., Wardlaw, T., Bashford, R., & Lawson, S. (2014). Relationships between annual rainfall, damage symptoms and insect borer populations in mid-rotation Eucalyptus nitens and Eucalyptus globulus plantations in Tasmania: Can static traps be used as an early warning device? Australian Forestry, 77(1), 15-24. doi:10.1080/00049158.2013.871090