IMPACTS OF CLIMATE CHANGE ON CROP PRODUCTION, PESTS AND PATHOGENS OF WHEAT AND RICE

Highlights

● An overview of impacts of climate change on wheat and rice crops.

● A review on impacts of climate change on insect pests and fungal pathogens of wheat and rice.

● A selection of adaptation strategies to mitigate impacts of climate change on crop production and pest and disease management.

Abstract

Ongoing climate change is expected to have impacts on crops, insect pests, and plant pathogens and poses considerable threats to sustainable food security. Existing reviews have summarized impacts of a changing climate on agriculture, but the majority of these are presented from an ecological point of view, and scant information is available on specific species in agricultural applications. This paper provides an overview of impacts of climate change on two staple crops, wheat and rice. First, the direct effects of climate change on crop growth, yield formation, and geographic distribution of wheat and rice are reviewed. Then, the effects of climate change on pests and pathogens related with wheat and rice, and their interactions with the crops are summarized. Finally, potential management strategies to mitigate the direct impacts of climate change on crops, and the indirect impacts on crops through pests and pathogens are outlined. The present overview aims to aid agriculture practitioners and researchers who are interested in wheat and rice to better understand climate change related impacts on the target species.

Graphical abstract

Keywords

climate change / pest / pathogen / food security

References

[1] Zhao C, Liu B, Piao S, Wang X, Lobell D B, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand J L, Elliott J, Ewert F, Janssens I A, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane A C, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S. Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114( 35): 9326–9331

[2] Liu B, Asseng S, Müller C, Ewert F, Elliott J, Lobell D B, Martre P, Ruane A C, Wallach D, Jones J W, Rosenzweig C, Aggarwal P K, Alderman P D, Anothai J, Basso B, Biernath C, Cammarano D, Challinor A, Deryng D, Sanctis G D, Doltra J, Fereres E, Folberth C, Garcia-Vila M, Gayler S, Hoogenboom G, Hunt L A, Izaurralde R C, Jabloun M, Jones C D, Kersebaum K C, Kimball B A, Koehler A K, Kumar S N, Nendel C, O’Leary G J, Olesen J E, Ottman M J, Palosuo T, Prasad P V V, Priesack E, Pugh T A M, Reynolds M, Rezaei E E, Rötter R P, Schmid E, Semenov M A, Shcherbak I, Stehfest E, Stöckle C O, Stratonovitch P, Streck T, Supit I, Tao F, Thorburn P, Waha K, Wall G W, Wang E, White J W, Wolf J, Zhao Z, Zhu Y. Similar estimates of temperature impacts on global wheat yield by three independent methods. Nature Climate Change, 2016, 6( 12): 1130–1136

[3] Asseng S, Ewert F, Martre P, Rötter R P, Lobell D B, Cammarano D, Kimball B A, Ottman M J, Wall G W, White J W, Reynolds M P, Alderman P D, Prasad P V V, Aggarwal P K, Anothai J, Basso B, Biernath C, Challinor A J, De Sanctis G, Doltra J, Fereres E, Garcia-Vila M, Gayler S, Hoogenboom G, Hunt L A, Izaurralde R C, Jabloun M, Jones C D, Kersebaum K C, Koehler A K, Müller C, Naresh Kumar S, Nendel C, O’Leary G, Olesen J E, Palosuo T, Priesack E, Eyshi Rezaei E, Ruane A C, Semenov M A, Shcherbak I, Stöckle C, Stratonovitch P, Streck T, Supit I, Tao F, Thorburn P J, Waha K, Wang E, Wallach D, Wolf J, Zhao Z, Zhu Y. Rising temperatures reduce global wheat production. Nature Climate Change, 2015, 5( 2): 143–147

[4] Wang X H, Zhao C, Müller C, Wang C Z, Ciais P, Janssens I, Peñuelas J, Asseng S, Li T, Elliott J, Huang Y, Li L, Piao S L. Emergent constraint on crop yield response to warmer temperature from field experiments. Nature Sustainability, 2020, 3( 11): 908–916

[5] Juroszek P, Von Tiedemann A. Plant pathogens, insect pests and weeds in a changing global climate: a review of approaches, challenges, research gaps, key studies and concepts. Journal of Agricultural Science, 2013, 151( 2): 163–188

[6] Bebber D P. Range-expanding pests and pathogens in a warming world. Annual Review of Phytopathology, 2015, 53( 1): 335–356

[7] Bajwa A A, Farooq M, Al-Sadi A M, Nawaz A, Jabran K, Siddique K H M. Impact of climate change on biology and management of wheat pests. Crop Protection, 2020, 137 : 105304

[8] AndrewN R, Terblanche J S. The response of insects to climate change. In: Salinger J, ed. Climate of Change: Living in a Warmer World. Auckland, New Zealand: David Bateman Ltd., 2013, 38–50

[9] Ma C S, Ma G, Pincebourde S. Survive a warming climate: insect responses to extreme high temperatures. Annual Review of Entomology, 2021, 66( 1): 163–184

[10] Trębicki P, Dáder B, Vassiliadis S, Fereres A. Insect-plant-pathogen interactions as shaped by future climate: effects on biology, distribution, and implications for agriculture. Insect Science, 2017, 24( 6): 975–989

[11] FoodOrganization of the United Nations (FAO). FAOSTAT, FAO Satistics Division. Available at FAO website on December 22, 2020

[12] YadavS S, Redden R J, HatfieldJ L, Lotze-CampenH, HallA E. Crop adaptation to climate change. Chichester, UK: Wiley-Blackwell, 2011, 84–102

[13] Smith S D, Charlet T N, Zitzer S F, Abella S R, Vanier C H, Huxman T E. Long-term response of a Mojave Desert winter annual plant community to a whole-ecosystem atmospheric CO₂ manipulation (FACE). Global Change Biology, 2014, 20( 3): 879–892

[14] Cook R J, Vaseth R J. Limiting effects of the physical and chemical environment In: Cook R J, Vaseth R J, eds. Wheat Health Management. American Phytopathological Society, 1991, 21–39

[15] Porter J R, Gawith M. Temperatures and the growth and development of wheat: a review. European Journal of Agronomy, 1999, 10( 1): 23–36

[16] Cai C, Li G, Di L, Ding Y, Fu L, Guo X, Struik P C, Pan G, Li H, Chen W, Luo W, Yin X. The acclimation of leaf photosynthesis of wheat and rice to seasonal temperature changes in T-FACE environments. Global Change Biology, 2020, 26( 2): 539–556

[17] Nuttall J G, O’Leary G J, Panozzo J F, Walker C K, Barlow K M, Fitzgerald G J. Models of grain quality in wheat—a review. Field Crops Research, 2017, 202 : 136–145

[18] Tao Z Q, Chang X H, Wang D M, Wang Y J, Ma S K, Yang Y S, Zhao G C. Effects of sulfur fertilization and short-term high temperature on wheat grain production and wheat flour proteins. Crop Journal, 2018, 6( 4): 413–425

[19] Erda L, Wei X, Hui J, Yinlong X, Yue L, Liping B, Liyong X. Climate change impacts on crop yield and quality with CO₂ fertilization in China. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2005, 360( 1463): 2149–2154

[20] KimH Y, Horie T, NakagawaH, WadaK. Effects of elevated CO₂ concentration and high temperature on growth and yield of rice: I. The effect on development, dry matter production and some growth characteristics. Nihon Sakumotsu Gakkai Kiji, 1996, 65(4): 634–643 (in Japanese)

[21] Peng S, Huang J, Sheehy J E, Laza R C, Visperas R M, Zhong X, Centeno G S, Khush G S, Cassman K G. Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101( 27): 9971–9975

[22] Krishnan P, Ramakrishnan B, Reddy K R, Reddy V R. High-temperature effects on rice growth, yield, and grain quality. Advances in Agronomy, 2011, 111 : 87–206

[23] Liu X F, Zhang Z, Shuai J B, Wang P, Shi W J, Tao F L, Chen Y. Impact of chilling injury and global warming on rice yield in Heilongjiang Province. Journal of Geographical Sciences, 2013, 23( 1): 85–97

[24] Naylor R L, Battisti D S, Vimont D J, Falcon W P, Burke M B. Assessing risks of climate variability and climate change for Indonesian rice agriculture. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104( 19): 7752–7757

[25] Ewert F, Rötter R P, Bindi M, Webber H, Trnka M, Kersebaum K C, Olesen J E, van Ittersum M K, Janssen S, Rivington M, Semenov M A, Wallach D, Porter J R, Stewart D, Verhagen J, Gaiser T, Palosuo T, Tao F, Nendel C, Roggero P P, Bartošová L, Asseng S. Crop modelling for integrated assessment of risk to food production from climate change. Environmental Modelling & Software, 2015, 72 : 287–303

[26] Stöckle C O, Kemanian A R. Can crop models identify critical gaps in genetics, environment, and management interactions. Frontiers in Plant Science, 2020, 11 : 737

[27] Moreno-Delafuente A, Viñuela E, Fereres A, Medina P, Trębicki P. Simultaneous increase in CO₂ and temperature alters wheat growth and aphid performance differently depending on virus infection. Insects, 2020, 11( 8): 459

[28] Zhu L, Hoffmann A A, Li S, Ma C S. Extreme climate shifts pest dominance hierarchy through thermal evolution and transgenerational plasticity. Functional Ecology, 2021, 35( 7): 1524–1537

[29] Ma G, Ma C S. Effect of acclimation on heat-escape temperatures of two aphid species: implications for estimating behavioral response of insects to climate warming. Journal of Insect Physiology, 2012, 58( 3): 303–309

[30] Zhao F, Zhang W, Hoffmann A A, Ma C S. Night warming on hot days produces novel impacts on development, survival and reproduction in a small arthropod. Journal of Animal Ecology, 2014, 83( 4): 769–778

[31] Zhu L, Wang L, Ma C S. Sporadic short temperature events cannot be neglected in predicting impacts of climate change on small insects. Journal of Insect Physiology, 2019, 112 : 48–56

[32] Ma G, Bai C M, Rudolf V H W, Ma C S. Night warming alters mean warming effects on predator–prey interactions by modifying predator demographics and interaction strengths. Functional Ecology, 2021, 35( 9): 2094–2107

[33] Aljaryian R, Kumar L. Changing global risk of invading greenbug Schizaphis graminum under climate change. Crop Protection, 2016, 88 : 137–148

[34] Brabec M, Honěk A, Pekár S, Martinková Z. Population dynamics of aphids on cereals: digging in the time-series data to reveal population regulation caused by temperature. PLoS One, 2014, 9( 9): e106228

[35] Davis T S, Abatzoglou J T, Bosque-Pérez N A, Halbert S E, Pike K, Eigenbrode S D. Differing contributions of density dependence and climate to the population dynamics of three eruptive herbivores. Ecological Entomology, 2014, 39( 5): 566–577

[36] Woli P, Ortiz B V, Buntin D, Flanders K. El Niño-Southern Oscillation (ENSO) effects on Hessian fly (Diptera: Cecidomyiidae) infestation in the southeastern United States. Environmental Entomology, 2014, 43( 6): 1641–1649

[37] Olfert O, Weiss R M, Catton H, Cárcamo H, Meers S. Bioclimatic assessment of abiotic factors affecting relative abundance and distribution of wheat stem sawfly (hymenoptera: Cephidae) in western Canada. Canadian Entomologist, 2019, 151( 1): 16–33

[38] Olfert O, Weiss R M, Elliott R H. Bioclimatic approach to assessing the potential impact of climate change on wheat midge (Diptera: Cecidomyiidae) in North America. Canadian Entomologist, 2016, 148( 1): 52–67

[39] Jacques J, Sampaio F, dos Santos H T, Marchioro C A. Climate change and voltinism of Mythimna sequax: the location and choice of phenological models matter. Agricultural and Forest Entomology, 2019, 21( 4): 431–444

[40] Ouyang F, Hui C, Men X Y, Zhang Y S, Fan L P, Shi P J, Zhao Z H, Ge F. Early eclosion of overwintering cotton bollworm moths from warming temperatures accentuates yield loss in wheat. Agriculture, Ecosystems & Environment, 2016, 217 : 89–98

[41] Yang L, Huang L F, Wang W L, Chen E H, Chen H S, Jiang J J. Effects of temperature on growth and development of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Environmental Entomology, 2021, 50( 1): 1–11

[42] Horgan F G, Arida A, Ardestani G, Almazan M L P. Temperature-dependent oviposition and nymph performance reveal distinct thermal niches of coexisting planthoppers with similar thresholds for development. PLoS One, 2020, 15( 6): e0235506

[43] Piyaphongkul J, Pritchard J, Bale J. Can tropical insects stand the heat? A case study with the brown planthopper Nilaparvata lugens (Stål). PLoS One, 2012, 7( 1): e29409

[44] Ge L Q, Wu J C, Sun Y C, Ouyang F, Ge F. Effects of triazophos on biochemical substances of transgenic Bt rice and its nontarget pest Nilaparvata lugens Stål under elevated CO₂. Pesticide Biochemistry and Physiology, 2013, 107( 2): 188–199

[45] Wang C, Fei M, Meng L, Harvey J A, Li B. Effects of elevated CO₂ and temperature on survival and wing dimorphism of two species of rice planthoppers (Hemiptera: Delphacidae) under interaction. Pest Management Science, 2020, 76( 6): 2087–2094

[46] Gu L L, Li M Z, Wang G R, Liu X D. Multigenerational heat acclimation increases thermal tolerance and expression levels of Hsp70 and Hsp90 in the rice leaf folder larvae. Journal of Thermal Biology, 2019, 81 : 103–109

[47] Bodlah M A, Gu L L, Wang G R, Liu X D. Rice leaf folder larvae alter their shelter-building behavior and shelter structure in response to heat stress. Journal of Economic Entomology, 2019, 112( 1): 149–155

[48] Bodlah M A, Gu L L, Tan Y, Liu X D. Behavioural adaptation of the rice leaf folder Cnaphalocrocis medinalis to short-term heat stress. Journal of Insect Physiology, 2017, 100 : 28–34

[49] Lee H, Kang W S, Ahn M I, Cho K, Lee J H. Predicting temporal shifts in the spring occurrence of overwintered Scotinophara lurida (Hemiptera: Pentatomidae) and rice phenology in Korea with climate change. International Journal of Biometeorology, 2016, 60( 1): 53–61

[50] Lu M X, Cao S S, Liu Z X, Wang X, Du Y Z. Heat tolerance of developmental and seasonal stages of Chilo suppressalis. Entomologia Experimentalis et Applicata, 2014, 152( 2): 91–99

[51] Veres A, Wyckhuys K A G, Kiss J, Tóth F, Burgio G, Pons X, Avilla C, Vidal S, Razinger J, Bazok R, Matyjaszczyk E, Milosavljević I, Le X V, Zhou W, Zhu Z R, Tarno H, Hadi B, Lundgren J, Bonmatin J M, van Lexmond M B, Aebi A, Rauf A, Furlan L. An update of the Worldwide Integrated Assessment (WIA) on systemic pesticides. Part 4: Alternatives in major cropping systems. Environmental Science and Pollution Research International, 2020, 27( 24): 29867–29899

[52] ChengX B. The simulation of population dynamics of Sitobion avenae and Rhopalosiphum padi. Dissertation for the Master’s Degree. Beijing: Chinese Academey of Agricultural Science, 2018 (in Chinese)

[53] Avila G A, Davidson M, van Helden M, Fagan L. The potential distribution of the Russian wheat aphid (Diuraphis noxia): an updated distribution model including irrigation improves model fit for predicting potential spread. Bulletin of Entomological Research, 2019, 109( 1): 90–101

[54] EigenbrodeS D, MacfadyenS. The impact of climate change on wheat insect pests: current knowledge and future trends. In: Langridge, P, eds. Achieving sustainable cultivation of wheat, volume 1: breeding, quality traits, pests and diseases. Cambridge: Burleigh Dodds Science Publishing, 2017, 545–567

[55] Wu Y Q, Gong Z J, Bebber D P, Miao J, Zhao Z H, Jiang Y Y, Xiao S H, Zhang G Y, Yu D Z, Fang J C, Lu X M, Lei C L, Ding J Q, Wang Q, Jiang Y L, Li T, Lian H M, Li H L, Duan Y, Huang J R, Jing D L, He Y Z, Zhang Z, Zhang Y H, Chen J L, Qiao H B, Huang W J. Phenological matching drives wheat pest range shift under climate change. bioRxiv, 2019, 614743

[56] Ma C S, Ma G, Zhao F. Impact of global warming on cereal aphids. Chinese Journal of Applied Entomology, 2014, 51( 6): 1435–1443

[57] Ma G, Rudolf V H W, Ma C S. Extreme temperature events alter demographic rates, relative fitness, and community structure. Global Change Biology, 2015, 21( 5): 1794–1808

[58] MaG, Hoffmann A A, MaC S. Daily temperature extremes play an important role in predicting thermal effects. Journal of Experimental Biology, 2015, 218(Pt 14): 2289–2296

[59] Ma C S, Wang L, Zhang W, Rudolf V H W. Resolving biological impacts of multiple heat waves: interaction of hot and recovery days. Oikos, 2018, 127( 4): 622–633

[60] Zhao F, Hoffmann A A, Xing K, Ma C S. Life stages of an aphid living under similar thermal conditions differ in thermal performance. Journal of Insect Physiology, 2017, 99 : 1–7

[61] Zhao F, Xing K, Hoffmann A A, Ma C S. The importance of timing of heat events for predicting the dynamics of aphid pest populations. Pest Management Science, 2019, 75( 7): 1866–1874

[62] Ma G, Hoffmann A A, Ma C S. Are extreme high temperatures at low or high latitudes more likely to inhibit the population growth of a globally distributed aphid. Journal of Thermal Biology, 2021, 98 : 102936

[63] Zvereva E L, Kozlov M V. Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Global Change Biology, 2006, 12( 1): 27–41

[64] Xing G M, Zhang J, Liu J, Zhang X Y, Wang G X, Wang Y F. Impacts of atmospheric CO₂ concentrations and soil water on the population dynamics, fecundity and development of the bird cherry-oat aphid Rhopalosiphum padi. Phytoparasitica, 2003, 31( 5): 449–514

[65] Shi B K, Hu C X, Huang J L, Hou M L. Modeling the influence of temperature on development, survival and oviposition of the brown planthopper, Nilaparvata lugens. Acta Ecologica Sinica, 2014, 34( 20): 5868–5874

[66] Guru-Pirasanna-Pandi G, Chander S, Pal M, Soumia P S. Impact of elevated CO₂ on Oryza sativa phenology and brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae) population. Current Science, 2018, 114( 8): 1767–1777

[67] Hu C X, Wei G S, Hou M L. Influences of future climate warming on overwintering boundary of the brown planthopper. Plant Protection, 2013, 39( 6): 21–25

[68] Morimoto N, Imura O, Kiura T. Potential effects of global warming on the occurrence of Japanese pest insects. Applied Entomology and Zoology, 1998, 33( 1): 147–155

[69] Yamamura K, Yokozawa M, Nishimori M, Ueda Y, Yokosuka T. How to analyze long-term insect population dynamics under climate change: 50-year data of three insect pests in paddy fields. Population Ecology, 2006, 48( 1): 31–48

[70] Matsukura K, Sanada-Morimura S, Fujii T, Matsumura M. Potential risks of poaceous plants as infectious sources of rice black-streaked dwarf virus transmitted by the small brown planthopper, Laodelphax striatellus. Plant Disease, 2019, 103( 6): 1244–1248

[71] Horgan F G, Arida A, Ardestani G, Almazan M L P. Positive and negative interspecific interactions between coexisting rice planthoppers neutralise the effects of elevated temperatures. Functional Ecology, 2021, 35( 1): 181–192

[72] Wójtowicz A, Wójtowicz M, Sigvald R, Czernecki B, Ratajkiewicz H, Łacka A, Zacharczuk M, Pasternak M. Assessment of the impact of climate change on the latency period of leaf rust on triticale in Poland. Acta Agriculturæ Scandinavica. Section B: Soil and Plant Science, 2020, 70( 3): 195–207

[73] Caubel J, Launay M, Ripoche D, Gouache D, Buis S, Huard F, Huber L, Brun F, Bancal M O. Climate change effects on leaf rust of wheat: implementing a coupled crop-disease model in a French regional application. European Journal of Agronomy, 2017, 90 : 53–66

[74] Lyon B, Broders K. Impact of climate change and race evolution on the epidemiology and ecology of stripe rust in central and eastern USA and Canada. Canadian Journal of Plant Pathology, 2017, 39( 4): 385–392

[75] Xu X, Ma L, Hu X. Overwintering of wheat stripe rust under field conditions in the northwestern regions of China. Plant Disease, 2019, 103( 4): 638–644

[76] Rodriguez-Algaba J, Sørensen C K, Labouriau R, Justesen A F, Hovmøller M S. Susceptibility of winter wheat and triticale to yellow rust influenced by complex interactions between vernalisation, temperature, plant growth stage and pathogen race. Agronomy, 2020, 10( 1): 13

[77] Chen F, Duan G H, Li D L, Zhan J. Host resistance and temperature-dependent evolution of aggressiveness in the plant pathogen Zymoseptoria tritici. Frontiers in Microbiology, 2017, 8 : 1217

[78] Tang X, Cao X, Xu X, Jiang Y, Luo Y, Ma Z, Fan J, Zhou Y. Effects of climate change on epidemics of powdery mildew in winter wheat in China. Plant Disease, 2017, 101( 10): 1753–1760

[79] Matić S, Cucu M A, Garibaldi A, Gullino M L. Combined effect of CO₂ and temperature on wheat powdery mildew development. Plant Pathology Journal, 2018, 34( 4): 316–326

[80] Shang S, Shang Z T, Yu J, Zhang X H, Wu J, Jiang D. Impacts of climate change on Fusarium head blight in winter wheat. Fresenius Environmental Bulletin, 2018, 27( 6): 3906–3913

[81] Song Y, Linderholm H W, Wang C, Tian J, Huo Z, Gao P, Song Y, Guo A. The influence of excess precipitation on winter wheat under climate change in China from 1961 to 2017. Science of the Total Environment, 2019, 690 : 189–196

[82] Wakelin S A, Gomez-Gallego M, Jones E, Smaill S, Lear G, Lambie S. Climate change induced drought impacts on plant diseases in New Zealand. Australasian Plant Pathology, 2018, 47( 1): 101–114

[83] Liu C, Van der Fels-Klerx H J. Quantitative modeling of climate change impacts on mycotoxins in cereals: a review. Toxins, 2021, 13( 4): 276

[84] Dorneles K R, Refatti J P, Pazdiora P C, de Avila L A, Deuner S, Dallagnol L J. Biochemical defenses of rice against Bipolaris oryzae increase with high atmospheric concentration of CO₂. Physiological and Molecular Plant Pathology, 2020, 110 : 101484

[85] Kim K H, Cho J, Lee Y H, Lee W S. Predicting potential epidemics of rice leaf blast and sheath blight in South Korea under the RCP 4.5 and RCP 8.5 climate change scenarios using a rice disease epidemiology model, EPIRICE. Agricultural and Forest Meteorology, 2015, 203 : 191–207

[86] Duku C, Sparks A H, Zwart S J. Spatial modelling of rice yield losses in Tanzania due to bacterial leaf blight and leaf blast in a changing climate. Climatic Change, 2016, 135( 3−4): 569–583

[87] Gória M M, Ghini R, Bettiol W. Elevated atmospheric CO₂ concentration increases rice blast severity. Tropical Plant Pathology, 2013, 38( 3): 253–257

[88] Viswanath K, Sinha P, Naresh Kumar S, Sharma T, Saxena S, Panjwani S, Pathak H, Shukla S M. Simulation of leaf blast infection in tropical rice agro-ecology under climate change scenario. Climatic Change, 2017, 142( 1–2): 155–167

[89] Yoshida R, Onodera Y, Tojo T, Yamazaki T, Kanno H, Takayabu I, Suzuki-Parker A. An application of a physical vegetation model to estimate climate change impacts on rice leaf wetness. Journal of Applied Meteorology and Climatology, 2015, 54( 7): 1482–1495

[90] Matić S, Garibaldi A, Gullino M L. Combined and single effects of elevated CO₂ and temperatures on rice bakanae disease under controlled conditions in phytotrons. Plant Pathology, 2021, 70( 4): 815–826

[91] Luo Y, Tebeest D O, Teng P S, Fabellar N G. Simulation studies on risk analysis of rice leaf blast epidemics associated with global climate change in several Asian countries. Journal of Biogeography, 1995, 22( 4/5): 673–678

[92] Kobayashi T, Ishiguro K, Nakajima T, Kim H Y, Okada M, Kobayashi K. Effects of elevated atmospheric CO₂ concentration on the infection of rice blast and sheath blight. Phytopathology, 2006, 96( 4): 425–431

[93] Gregory P J, Johnson S N, Newton A C, Ingram J S I. Integrating pests and pathogens into the climate change/food security debate. Journal of Experimental Botany, 2009, 60( 10): 2827–2838

[94] Bezemer T M, Jones T H. Plant-insect herbivore interactions in elevated atmospheric CO₂ : quantitative analyses and guild effects. Oikos, 1998, 82( 2): 212–222

[95] Rodríguez-Castañeda G, MacVean C, Cardona C, Hof A R. What limits the distribution of Liriomyza huidobrensis and its congener Liriomyza sativae in their native niche: when temperature and competition affect species’ distribution range in Guatemala. Journal of Insect Science, 2017, 17( 4): 88

[96] Asalf B, Ficke A, Klingen I. Interaction between the bird cherry-oat aphid (Rhopalosiphum padi) and stagonospora nodorum blotch (parastagonospora nodorum) on wheat. Insects, 2021, 12( 1): 35

[97] Stenberg J A. A conceptual framework for integrated pest management. Trends in Plant Science, 2017, 22( 9): 759–769

[98] Karlsson Green K, Stenberg J A, Lankinen Å. Making sense of Integrated Pest Management (IPM) in the light of evolution. Evolutionary Applications, 2020, 13( 8): 1791–1805

[99] Hof A R, Dymond C C, Mladenoff D J. Climate change mitigation through adaptation: the effectiveness of forest diversification by novel tree planting regimes. Ecosphere, 2017, 8( 11): e01981

[100] Verheyen J, Stoks R. Current and future daily temperature fluctuations make a pesticide more toxic: contrasting effects on life history and physiology. Environmental Pollution, 2019, 248 : 209–218

Acknowledgements

We thank the Joint PhD Talent Cultivation Program between Wageningen University and Research and Graduate School of Chinese Academy of Agricultural Sciences (MOE11NL1A20151701N), and all the people who assisted in this program. This work was supported by the Agricultural Science and Technology Innovation Program of CAAS, “Research on national food security strategy of China in the new era” (CAAS-ZDRW202012), research grants from the National Natural Science Foundation of China (31620103914 and 31772156), the National Key R & D Program of China (2018YFD0201400), the Chinese Academy of Agricultural Sciences (Y2017LM10).

Compliance with ethics guidelines

Bing-Xin Wang, Anouschka R. Hof, and Chun-Sen Ma declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any study with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2021. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)