Abstract
We explored the effects of elevated CO2 on the population performance and interspecific interactions of three thrips pests. The dominance of the three thrips in the field was Frankliniella occidentalis ≈ Frankliniella intonsa > Thrips hawaiiensis. The performance of these thrips, alone and in combination, was evaluated in the laboratory under elevated CO2 (800 μl L−1) and ambient CO2. Compared with ambient CO2, elevated CO2 significantly accelerated the developmental rates and decreased the survival rates of all thrips species. Significant differences in fecundity, intrinsic rate of increase (rm), and net reproductive rate (R0) were observed among these thrips, and their values were significantly increased in F. occidentalis but decreased in F. intonsa and T. hawaiiensis under elevated CO2, compared that in the ambient CO2 treatments. In treatments where thrips species coexisted, F. occidentalis and F. intonsa accounted for similar proportions of the population, and both were dominant over T. hawaiiensis within 10 generations under ambient CO2. Under elevated CO2, F. occidentalis was the dominant species and completely displaced F. intonsa and T. hawaiiensis by the ninth or eighth generation. Where the three species coexisted, no displacement occurred within 10 generations, but the pattern of dominance shifted to F. occidentalis > F. intonsa > T. hawaiiensis. Our results show that the population development of F. occidentalis benefits from elevated CO2 and that it can become the dominant species in interspecific interactions with native thrips species. Thus, compared with native thrips species, F. occidentalis has greater adaptability and competitive capacity under elevated CO2, and it may become a more dangerous crop pest under environmental change in the future.
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References
Alim MA, Song J, Seo HJ, Choi JJ (2018) Monitoring thrips species with yellow sticky traps in astringent persimmon orchards in Korea. Appl Entomol Zool 53(1):75–84. https://doi.org/10.1007/s13355-017-0530-z
Atakan E, Uygur S (2005) Winter and spring abundance of Frankliniella spp. and Thrips tabaci Lindeman (Thysan., Thripidae) on weed host plants in Turkey. J Appl Entomol 129(1):17–26. https://doi.org/10.1111/j.1439-0418.2005.00918.x
Bhuyain MMH, Lim UT (2019) Interference and exploitation competition between Frankliniella occidentalis and F. intonsa (Thysanoptera: Thripidae) in laboratory assays. Fla Entomol 102(2):322–328. https://doi.org/10.1653/024.102.0206
Cao Y, Zhi JR, Cong CL, Margolies DC (2014) Olfactory cues used in host selection by Frankliniella occidentalis (Thysanoptera: Thripidae) in relation to host suitability. J Insect Behav 27(1):41–56. https://doi.org/10.1007/s10905-013-9405-5
Cao Y, Zhi JR, Zhang RZ, Li C, Liu Y, Lv ZY, Gao YL (2018) Different population performances of Frankliniella occidentalis and Thrips hawaiiensis on fowers of two horticultural plants. J Pest Sci 91(1):79–91. https://doi.org/10.1007/s10340-017-0887-3
Cao Y, Yang H, Gao YL, Wang LJ, Li J, Wang C, Li C (2021) Effect of elevated CO2 on the population development of the invasive species Frankliniella occidentalis and native species Thrips hawaiiensis and activities of their detoxifying enzymes. J Pest Sci 94(1):29–42. https://doi.org/10.1007/s10340-020-01224-8
Cao Y, Qi GL, Jiang FY, Meng YL, Wang C, Gu ZY, Gao YL, Reitz SR, Li C (2023) Population performance and detoxifying and protective enzyme activities of four thrips species feeding on flowers of Magnolia grandiflora (Ranunculales: Magnolia). Pest Manag Sci. https://doi.org/10.1002/ps.7509
Carey JR (2001) Insect biodemography. Annu Rev Entomol 46(1):79–110. https://doi.org/10.1146/annurev.ento.46.1.79
Deutsch CA, Tewksbury JJ, Tigchelaar M, Battisti DS, Merrill SC, Huey RB, Naylor RL (2018) Increase in crop losses to insect pests in a warming climate. Science 361(6405):916–919. https://doi.org/10.1126/science.aat3466
Gai HT, Zhi JR, Jiang YJ, Li ZX (2009) Comparison of development and growth between invasive species Frankliniella occidentalis and native species Frankliniella intonsa. China Plant Prot 29(3):9–12. https://doi.org/10.3969/j.issn.1672-6820.2009.03.002
Gao YL, Reitz SR (2017) Emerging themes in our understanding of species displacements. Ann Rev Entomol 62:165–183. https://doi.org/10.1146/annurev-ento-031616-035425
Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Ann Rev Entomol 53:161–178. https://doi.org/10.1146/annurev.ento.53.103106.093402
He SQ, Lin Y, Qian L, Li ZH, Chao X, Lu Y, Gui FR (2017) The influence of elevated CO2 concentration on the fitness traits of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae). Environ Entomol 46(3):722–728. https://doi.org/10.1093/ee/nvx083
IPCC (2014) Climate Change 2014: Mitigation of Climate Change. In: Edenhofer OR, Pichs-Madruga Y, Sokona E, Farahani S, Kadner K, Seyboth A et al (eds) Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jensen NB, Zagrobelny M, Hjerno K, Olsen CE, HoughtonLarsen J, Borch J, Moller BL, Bak S (2011) Convergent evolution in biosynthesis of cyanogenic defence compounds in plants and insects. Nat Commun 2:273. https://doi.org/10.1038/ncomms1271
Joussen N, Agnolet S, Lorenz S, Schone SE, Ellinger R, Schneider B, Heckel DG (2012) Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proc Natl Acad Sci USA 109:15206–15211. https://doi.org/10.1073/pnas.1202047109
Kirk WDJ (2002) The pest and vector from the West: Frankliniella occidentalis. In: Marullo R, Mound L (eds) Thrips and tospoviruses. Proceedings of the 7th international symposium on Thysanoptera. AINC, Canberra, pp 33–42
Li WD, Zhang PJ, Zhang JM, Zhang ZJ, Huang F, Bei YW, Lin WC, Lu YB (2015) An evaluation of Frankliniella occidentalis (Thysanoptera: Thripidae) and Frankliniella intonsa (Thysanoptera: Thripidae) performance on different plant leaves based on life history characteristics. J Insect Sci 15(4):1–5. https://doi.org/10.1093/jisesa/ieu167
Liu JY, Qian L, Jiang XC, He SQ, Li ZY, Gui FR (2014) Effects of elevated CO2 concentration on the activities of detoxifying enzymes and protective enzymes in adults of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae). Acta Entomol Sin 57:754–761. https://doi.org/10.1002/ps.6630
Liu JY, Qian L, Ke R, Chen XY, Li ZY, Gui FR (2017) Effects of elevated carbon dioxide on the activities of physiological enzymes in thrips Frankliniella occidentalis and F. intonsa fed on different host plants. J Plant Prot 44(1):45–53. https://doi.org/10.13802/j.cnki.zwbhxb.2017.2015101
Ma CS, Zhang W, Peng Y, Zhao F, Chang XQ, Xing K, Zhu L, Ma G, Yang HP, Rudolf VHW (2021) Climate warming promotes pesticide resistance through expanding overwintering range of a global pest. Nat Commun 12:5351. https://doi.org/10.1038/s41467-021-25505-7
Marullo R, Mound L (eds) (2002) Thrips and tospoviruses. Proceedings of the 7th international symposium on Thysanoptera, Canberra
Marullo R, De Grazia A (2017) Thrips hawaiiensis a pest thrips from Asia newly introduced into Italy. BullInsectol 70(1):27–30
Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89. https://doi.org/10.1146/annurev.ento.51.110104.151044
Myers SS (2014) Increasing CO2 threatens human nutrition. Nature 510(7503):139. https://doi.org/10.1038/nature13179
Nakahara S, Foottit RG (2007) Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae), an invasive insect in North America. Proc Entomol Soc Wash 109(3):733–734. https://doi.org/10.1016/j.pestbp.2007.02.003
Outhwaite CL, Mccann P, Newbold T (2022) Agriculture and climate change are reshaping insect biodiversity worldwide. Nature 605(7908):97–102. https://doi.org/10.1038/s41586-022-04644-x
Qian L, Chen FJ, Liu JN, He SQ, Liu JY, Li ZY, Gui FR (2017) Effects of elevated CO2 on life-history traits of three successive generations of Frankliniella occidentalis and F. intonsa on kidney bean Phaseolus vulgaris. Entomol Exp Appl 165(1):56–61. https://doi.org/10.1111/eea.12606
Qian L, He S, Liu X, Huang Z, Chen F, Gui F (2018) Effect of elevated CO2 on the interaction between invasive thrips, Frankliniella occidentalis, and its host kidney bean, Phaseolus Vulgaris. Pest Manag Sci 74(12):2773–2782. https://doi.org/10.1002/ps.5064
Qian L, Liu XW, Huang ZJ, Wang L, Zhang YF, Gao YL, Gui FR, Chen FJ (2021) Elevated CO2 enhances the host resistance against the western flower thrips, Frankliniella occidentalis, through increased callose deposition. J Pest Sci 94:55–68. https://doi.org/10.1007/s10340-019-01123-7
Raven PH, Wagner DL (2021) Agricultural intensification and climate change are rapidly decreasing insect biodiversity. PNAS 118(2):e2002548117. https://doi.org/10.1073/pnas.2002548117
Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Ann Rev Entomol 47:435–465. https://doi.org/10.1146/annurev.ento.47.091201.145227
Reitz SR, Gao YL, Kirk WDJ, Hoddle MS, Funderburk JE (2020) Invasion biology, ecology, and management of western flower thrips. Ann Rev Entomol 65(1):17–37. https://doi.org/10.1146/annurev-ento-011019-024947
Riley DG, Joseph SV, Srinivasan R, Diffie S (2011) Thrips vectors of tospoviruses. J Integr Pest Manag 1:1–10. https://doi.org/10.1603/IPM10020
Rotenberg D, Jacobson AL, Schneweis DJ, Whitfield AE (2015) Thrips transmission of tospoviruses. Curr Opin Virol 15:80–89. https://doi.org/10.1016/j.coviro.2015.08.003
Stacey DA, Fellowes MDE (2002) Influence of elevated CO2 on interspecific interactions at higher trophic levels. Glob Change Biol 8:668–678. https://doi.org/10.1046/j.1365-2486.2002.00506.x
Sun YC, Chen FJ, Ge F (2009) Elevated CO2 changes interspecific competition among three species of wheat aphids: Sitobion avenae, Rhopalosiphum padi, and Schizaphis graminum. Environ Entomol 38(1):26–34. https://doi.org/10.1603/022.038.0105
Sun YC, Feng L, Gao F, Ge F (2011) Effects of elevated CO2 and plant genotype on interactions among cotton, aphids and parasitoids. Insect Sci 18(4):451–461. https://doi.org/10.1111/j.1744-7917.2010.01328.x
Teulon DAJ, Nielsen MC (2005) Distribution of western (glasshouse strain) and intonsa flower thrips in New Zealand. N Z Plant Prot 58:208–212. https://doi.org/10.30843/NZPP.2005.58.4274
Ullah MS, Lim UT (2015) Life history characteristics of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae) in constant and fluctuating temperatures. J Econ Entomol 108(3):1000–1009. https://doi.org/10.1093/jee/tov035
Varley GC, Gradwell GR (1970) Recent advance in insect population dynamics. Annu Rev Entomol 15:1–24. https://doi.org/10.1146/annurev.en.15.010170.000245
Wu SY, Xing ZL, Ma TT, Xu DW, Li YY, Lei ZR, Gao YL (2021) Competitive interaction between Frankliniella occidentalis and locally present thrips species: a global review. J Pest Sci 94(1):5–16. https://doi.org/10.1007/s10340-020-01212-y
Yuan CM, Zhi JR, Li JZ, Zhang Y (2008) Investigation on the species of thrips in fields of vegetable in Guizhou Province. China Plant Prot 7:8–10. https://doi.org/10.3969/j.issn.1672-6820.2008.07.003
Zavala JA, Nabity PD, Delucia EH (2013) An emerging understanding of mechanisms governing insect herbivory under elevated CO2. Annu Rev Entomol 58(1):79–97. https://doi.org/10.1146/annurev-ento-120811-153544
Zhang YJ, Wu QJ, Xu BY, Zhu GR (2003) The occurrence and damage of Frankliniella occidentalis (Thysanoptera: Thripidae): a dangerous alien invasive pest in Beijing. China Plant Prot 4:58–59. https://doi.org/10.3969/j.issn.0529-1542.2003.04.023
Zhang B, Qian WQ, Qiao X, Xi Y, Wan FH (2019) Invasion biology, ecology, and management of Frankliniella occidentalis in China. Arch Insect Biochem Physiol 102:e21613. https://doi.org/10.1002/arch.21613
Zhao XY, Reitz SR, Yuan HG, Lei ZR, Paini DR, Gao YL (2017) Pesticide-mediated interspecifc competition between local and invasive thrips pests. Sci Rep 7:40512. https://doi.org/10.1038/srep40512
Funding
This study was financially supported by the Key project of Natural Science Foundation of Guizhou Province (ZK[2022]001), Key Laboratory of Surveillance and Management for Alien Invasive Species in Guizhou Province (QJJ[2023]024), the Regional First Class Discipline Construction of Guizhou Province (XKTJ[2020]14), and Academic New Seedling Cultivation and Free Exploration & Innovation Project from Guizhou Provincial Science and Technology Department (2023).
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Zhang, T., Wang, C., Jiang, F. et al. Elevated CO2 affects interspecific competition between the invasive thrips Frankliniella occidentalis and native thrips species. J Pest Sci (2024). https://doi.org/10.1007/s10340-023-01723-4
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DOI: https://doi.org/10.1007/s10340-023-01723-4