Research progress of plant chemical defense strategies in response to herbivory

doi:10.17521/cjpe.2024.0230

Abstract

Abstract:

Plants have evolved diverse defense strategies to herbivory over time. Chemical defenses based on plant secondary metabolites play a key role in plants-herbivores interspecific interactions. There is a trade-off between the biosynthesis of secondary metabolites for plants and resource allocation to growth and reproduction. Recently, numerous studies have examined how plant secondary metabolites affect behavior of herbivores as well as plant growth and fitness. However, a comprehensive and in-depth elaboration of the chemical defense strategies of plants is still lacking. We systematically review the factors influencing the synthesis and release of plant secondary metabolites, the chemical defense strategies and their formation mechanisms in response to herbivory. Plant tissues and organs, population and species composition in the community, species identity and feeding intensity of herbivores, soil resource availability, seasons, environmental stresses all can affect the synthesis and release of plant secondary metabolites. Plants respond to herbivory by enhancing the plasticity of chemical defense, regulating the partitioning pattern of photosynthetic products and the trade-offs relationship between growth, reproduction and defense. Many hypotheses have been proposed to explain plant chemical defense strategies, including growth-differentiation balance hypothesis, plant apparency hypothesis, optimal defense theory, carbon/nutrient balance hypothesis, growth rate hypothesis, plant defense syndromes hypothesis, and error management theory. As the intensification of human activities (e.g., livestock grazing) and climate change, researches on plant defense strategies in response to large herbivore feeding, environmental stress and global change should be strengthened in the future with a multidisciplinary perspective, which will be helpful for deeper understanding of the defense processes and mechanisms of plants in response to herbivores.

Key words: plant secondary metabolites, chemical defense strategies, cost of defense, growth-defense trade off, herbivores

PING Xiao-Yan, DU Yi-Qian, LAI Shi-Rong, KONG Meng-Qiao, YU Guo-Jie. Research progress of plant chemical defense strategies in response to herbivory[J]. Chin J Plant Ecol, 2025, 49(5): 667-680.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2024.0230

https://www.plant-ecology.com/EN/Y2025/V49/I5/667

Figures/Tables 1

References 121

[1]	Aartsma Y, Bianchi FJJA, van der Werf W, Poelman EH, Dicke M (2017). Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytologist, 216, 1054-1063. DOI PMID
[2]	Agrawal AA (2011). Current trends in the evolutionary ecology of plant defence. Functional Ecology, 25, 420-432.
[3]	Agrawal AA, Fishbein M (2006). Plant defense syndromes. Ecology, 87, S132-S149. DOI PMID
[4]	Ameye M, Allmann S, Verwaeren J, Smagghe G, Haesaert G, Schuurink RC, Audenaert K (2018). Green leaf volatile production by plants: a meta-analysis. New Phytologist, 220, 666-683. DOI PMID
[5]	Anstett DN, Nunes KA, Baskett C, Kotanen PM (2016). Sources of controversy surrounding latitudinal patterns in herbivory and defense. Trends in Ecology & Evolution, 31, 789-802.
[6]	Avila-Sakar G (2020). Resource allocation and defence against herbivores in wild and model plants//Núñez-Farfán J, Valverde P. Evolutionary Ecology of Plant-Herbivore Interaction. Springer, Cham, Schweiz.
[7]	Baker NR, Zhalnina K, Yuan M, Herman D, Ceja-Navarro JA, Sasse J, Jordan JS, Bowen BP, Wu L, Fossum C, Chew A, Fu Y, Saha M, Zhou J, Pett-Ridge J, Northen TR, Firestone MK (2024). Nutrient and moisture limitations reveal keystone metabolites linking rhizosphere metabolomes and microbiomes. Proceedings of the National Academy of Sciences of the United States of America, 121, e2303439121. DOI: 10.1073/pnas.2303439121.
[8]	Baldwin IT (1998). Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the United States of America, 95, 8113-8118. DOI PMID
[9]	Ballaré CL, Austin AT (2019). Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates. Journal of Experimental Botany, 70, 3425-3434. DOI PMID
[10]	Ballhorn DJ, Godschalx AL, Smart SM, Kautz S, Schädler M (2014). Chemical defense lowers plant competitiveness. Oecologia, 176, 811-824. DOI PMID
[11]	Bouwmeester H, Schuurink RC, Bleeker PM, Schiestl F (2019). The role of volatiles in plant communication. The Plant Journal, 100, 892-907. DOI PMID
[12]	Bryant JP, Chapin III FS, Klein DR (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 40, 357-368.
[13]	Cipollini D, Walters D, Voelckel C (2014). Costs of resistance in plants: from theory to evidence//Singh IK, Singh A. Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology. Springer, Singapore. 263-307.
[14]	Coley PD, Barone JA (1996). Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27, 305-335.
[15]	Coley PD, Bryant JP, Chapin III FS (1985). Resource availability and plant antiherbivore defense. Science, 230, 895-899. DOI PMID
[16]	Cornelissen T, Stiling P (2005). Sex-biased herbivory: a meta-analysis of the effects of gender on plant-herbivore interactions. Oikos, 111, 488-500.
[17]	Courtney SP (1985). Apparency in coevolving relationships. Oikos, 44, 91-98.
[18]	Coverdale TC, Goheen JR, Palmer TM, Pringle RM (2018). Good neighbors make good defenses: associational refuges reduce defense investment in African savanna plants. Ecology, 99, 1724-1736. DOI PMID
[19]	Croy JR, Pratt JD, Mooney KA (2022). Latitudinal resource gradient shapes multivariate defense strategies in a long-lived shrub. Ecology, 103, e3830. DOI: 10.1002/ecy.3830. PMID
[20]	de Vries J, Evers JB, Poelman EH (2017). Dynamic plant-plant-herbivore interactions govern plant growth-defence integration. Trends in Plant Science, 22, 329-337. DOI PMID
[21]	Defossez E, Pellissier L, Rasmann S (2018). The unfolding of plant growth form-defence syndromes along elevation gradients. Ecology Letters, 21, 609-618. DOI PMID
[22]	Divekar PA, Narayana S, Divekar BA, Kumar R, Gadratagi BG, Ray A, Singh AK, Rani V, Singh V, Singh AK, Kumar A, Singh RP, Meena RS, Behera TK (2022). Plant secondary metabolites as defense tools against herbivores for sustainable crop protection. International Journal of Molecular Sciences, 23, 2690. DOI: 10.3390/ijms23052690.
[23]	Dixon RA, Dickinson AJ (2024). A century of studying plant secondary metabolism—From “what?” to “where, how, and why?”. Plant Physiology, 195, 48-66.
[24]	Endara MJ, Coley PD (2011). The resource availability hypothesis revisited: a meta-analysis. Functional Ecology, 25, 389-398.
[25]	Erb M (2018). Plant defenses against herbivory: closing the fitness gap. Trends in Plant Science, 23, 187-194. DOI PMID
[26]	Erb M, Kliebenstein DJ (2020). Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiology, 184, 39-52. DOI PMID
[27]	Feeny P (1976). Plant apparency and chemical defense// Wallace JW, Mansell RL. Biochemical Interaction Between Plants and Insects. Springer, New York. 1-40.
[28]	Fernández de Bobadilla M, Vitiello A, Erb M, Poelman EH (2022). Plant defense strategies against attack by multiple herbivores. Trends in Plant Science, 27, 528-535. DOI PMID
[29]	Ferrieri AP, Agtuca B, Appel HM, Ferrieri RA, Schultz JC (2013). Temporal changes in allocation and partitioning of new carbon as ⁽¹¹⁾C elicited by simulated herbivory suggest that roots shape aboveground responses in Arabidopsis. Plant Physiology, 161, 692-704. DOI PMID
[30]	Fornoni J (2011). Ecological and evolutionary implications of plant tolerance to herbivory. Functional Ecology, 25, 399-407.
[31]	Fraenkel GS (1959). The raison d'ĕtre of secondary plant substances; these odd chemicals arose as a means of protecting plants from insects and now guide insects to food. Science, 129, 1466-1470. DOI PMID
[32]	Gao C, Zhang XL, Xiu AJ, Huang L, Zhao HM, Wang K, Tong QQ (2019). Spatiotemporal distribution of biogenic volatile organic compounds emissions in China. Acta Scientiae Circumstantiae, 39, 4140-4151.
	[ 高超, 张学磊, 修艾军, 黄凌, 赵红梅, 王堃, 童清清 (2019). 中国生物源挥发性有机物(BVOCs)时空排放特征研究. 环境科学学报, 39, 4140-4151.]
[33]	Gelambi M, Morales ME, Whitehead SR (2024). Interactions between nutrients and fruit secondary metabolites shape bat foraging behavior and protein absorption. Ecosphere, 15, e4843. DOI: 10.1002/ecs2.4843.
[34]	Gershenzon J, Ullah C (2022). Plants protect themselves from herbivores by optimizing the distribution of chemical defenses. Proceedings of the National Academy of Sciences of the United States of America, 119, e2120277119. DOI: 10.1073/pnas.2120277119.
[35]	Gols R, van Dam NM, Reichelt M, Gershenzon J, Raaijmakers CE, Bullock JM, Harvey JA (2018). Seasonal and herbivore-induced dynamics of foliar glucosinolates in wild cabbage (Brassica oleracea). Chemoecology, 28, 77-89.
[36]	Gomes AF, Almeida MP, Leite MF, Schwaiger S, Stuppner H, Halabalaki M, Amaral JG, David JM (2019). Seasonal variation in the chemical composition of two chemotypes of Lippia alba. Food Chemistry, 273, 186-193.
[37]	Hahn PG, Maron JL (2016). A framework for predicting intraspecific variation in plant defense. Trends in Ecology & Evolution, 31, 646-656.
[38]	Halliday FW, Cappelli SL, Laine AL (2023). Multiple dimensions of biodiversity mediate effects of temperature on invertebrate herbivory in a montane grassland. Oikos, e10028. DOI: 10.1111/oik.10028.
[39]	Hattas D, Scogings PF, Julkunen-Tiitto R (2017). Does the growth differentiation balance hypothesis explain allocation to secondary metabolites in Combretum apiculatum, an African savanna woody species? Journal of Chemical Ecology, 43, 153-163.
[40]	He ZH, Webster S, He SY (2022). Growth-defense trade-offs in plants. Current Biology, 32, R634-R639.
[41]	Heiser S, Amsler CD, Brothers CJ, Amsler MO, Shilling AJ, Bozarth L, Davis CB, McClintock JB, Baker BJ (2022). Who cares more about chemical defenses-the macroalgal producer or its main grazer? Journal of Chemical Ecology, 48, 416-430.
[42]	Herms DA, Mattson WJ (1992). The dilemma of plants: to grow or defend. The Quarterly Review of Biology, 67, 283-335.
[43]	Hervé MR, Erb M (2019). Distinct defense strategies allow different grassland species to cope with root herbivore attack. Oecologia, 191, 127-139. DOI PMID
[44]	Holmes KD, Agrawal AA (2021). Induced resistance mitigates the effect of plant neighbors on susceptibility to herbivores. Ecosphere, 12, e03334. DOI: 10.1002/ecs2.3334.
[45]	Holopainen JK, Gershenzon J (2010). Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15, 176-184. DOI PMID
[46]	Howard MM, Kalske A, Kessler A (2018). Eco-evolutionary processes affecting plant-herbivore interactions during early community succession. Oecologia, 187, 547-559. DOI PMID
[47]	Howe GA, Jander G (2008). Plant immunity to insect herbivores. Annual Review of Plant Biology, 59, 41-66. PMID
[48]	Hu LF, Wu ZW, Robert CAM, Ouyang X, Züst T, Mestrot A, Xu JM, Erb M (2021). Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth. Proceedings of the National Academy of Sciences of the United States of America, 118, e2109602118. DOI: 10.1073/pnas.2109602118.
[49]	Huang BR, Wang Y, Su LY, Zhang CL, Cheng DW, Sun J, He SY (2018). Pilot programs for national park system in China: Progress, problems and recommendations. Bulletin of Chinese Academy of Sciences, 33, 76-85.
	[ 黄宝荣, 王毅, 苏利阳, 张丛林, 程多威, 孙晶, 何思源 (2018). 我国国家公园体制试点的进展、问题与对策建议. 中国科学院院刊, 33, 76-85.]
[50]	Huang JB, Hammerbacher A, Weinhold A, Reichelt M, Gleixner G, Behrendt T, van Dam NM, Sala AN, Gershenzon J, Trumbore S, Hartmann H (2019). Eyes on the future-evidence for trade-offs between growth, storage and defense in Norway spruce. New Phytologist, 222, 144-158.
[51]	Huang W, Siemann E, Wheeler GS, Zou JW, Carrillo J, Ding JQ (2010). Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. Journal of Ecology, 98, 1157-1167.
[52]	Hunziker P, Lambertz SK, Weber K, Crocoll C, Halkier BA, Schulz A (2021). Herbivore feeding preference corroborates optimal defense theory for specialized metabolites within plants. Proceedings of the National Academy of Sciences of the United States of America, 118, e2111977118. DOI: 10.1073/pnas.2111977118.
[53]	Iason GR, Dicke M, Hartley SE (2012). The Ecology of Plant Secondary Metabolites: from Genes to Global Processes. Cambridge University Press, Cambridge, UK.
[54]	Isah T (2019). Stress and defense responses in plant secondary metabolites production. Biological Research, 52, 39. DOI: 10.1186/s40659-019-0246-3. PMID
[55]	Jamieson MA, Burkle LA, Manson JS, Runyon JB, Trowbridge AM, Zientek J (2017). Global change effects on plant-insect interactions: the role of phytochemistry. Current Opinion in Insect Science, 23, 70-80. DOI PMID
[56]	Johnson DDP, Blumstein DT, Fowler JH, Haselton MG (2013). The evolution of error: error management, cognitive constraints, and adaptive decision-making biases. Trends in Ecology & Evolution, 28, 474-481.
[57]	Johnson MTJ (2011). Evolutionary ecology of plant defences against herbivores. Functional Ecology, 25, 305-311.
[58]	Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J, Schimmel BCJ, Villarroel CA, Ataide LMS, Dermauw W, Glas JJ, Egas M, Janssen A, van Leeuwen T, Schuurink RC, Sabelis MW, Alba JM (2015). Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Annals of Botany, 115, 1015-1051. DOI PMID
[59]	Karasov TL, Chae E, Herman JJ, Bergelson J (2017). Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell, 29, 666-680. DOI PMID
[60]	Kergunteuil A, Descombes P, Glauser G, Pellissier L, Rasmann S (2018). Plant physical and chemical defence variation along elevation gradients: a functional trait-based approach. Oecologia, 187, 561-571. DOI PMID
[61]	Kessler A, Baldwin IT (2001). Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291, 2141-2144. DOI PMID
[62]	Kharel B, Rusalepp L, Bhattarai B, Kaasik A, Kupper P, Lutter R, Mänd P, Rohula-Okunev G, Rosenvald K, Tullus A (2023). Effects of air humidity and soil moisture on secondary metabolites in the leaves and roots of Betula pendula of different competitive status. Oecologia, 202, 193-210.
[63]	Koricheva J (2002). Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology, 83, 176-190.
[64]	Kurokawa H, Kitahashi Y, Koike T, Lai J, Nakashizuka T (2004). Allocation to defense or growth in dipterocarp forest seedlings in Borneo. Oecologia, 140, 261-270. PMID
[65]	Lazzarin M, Meisenburg M, Meijer D, van Ieperen W, Marcelis LFM, Kappers IF, van der Krol AR, van Loon JJA, Dicke M (2021). LEDs make it resilient: effects on plant growth and defense. Trends in Plant Science, 26, 496-508. DOI PMID
[66]	Le Bot J, Bénard C, Robin C, Bourgaud F, Adamowicz S (2009). The ‘trade-off’ between synthesis of primary and secondary compounds in young tomato leaves is altered by nitrate nutrition: experimental evidence and model consistency. Journal of Experimental Botany, 60, 4301-4314.
[67]	Leong JV, Mezzomo P, Kozel P, Volfová T, de Lima Ferreira P, Seifert CL, Butterill PT, Freiberga I, Michálek J, Matos-Maraví P, Weinhold A, Engström MT, Salminen JP, Segar ST, Sedio BE, Volf M (2024). Effects of individual traits vs. trait syndromes on assemblages of various herbivore guilds associated with central European Salix. Oecologia, 205, 725-737. DOI PMID
[68]	Lerdau M, Litvak M, Monson R (1994). Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis. Trends in Ecology & Evolution, 9, 58-61.
[69]	Loomis WE (1932). Growth-differentiation balance vs. carbohydrate-nitrogen ratio. Proceedings of the American Society for Horticultural Science, 29, 240-245.
[70]	Li Y, Gong JR, Liu M, Hou XY, Ding Y, Yang B, Zhang ZH, Wang B, Zhu CC (2020). Defense strategies of dominant plants under different grazing intensity in the typical temperate steppe of Nei Mongol, China. Chinese Journal of Plant Ecology, 44, 642-653.
	[ 李颖, 龚吉蕊, 刘敏, 侯向阳, 丁勇, 杨波, 张子荷, 王彪, 朱趁趁 (2020). 不同放牧强度下内蒙古温带典型草原优势种植物防御策略. 植物生态学报, 44, 642-653.] DOI
[71]	Malhotra B, Kumar P, Bisht NC (2023). Defense versus growth trade-offs: insights from glucosinolates and their catabolites. Plant, Cell & Environment, 46, 2964-2984.
[72]	Masto NM, Blake-Bradshaw AG, Highway CJ, Keever AC, Feddersen JC, Hagy HM, Cohen BS (2024). Human access constrains optimal foraging and habitat availability in an avian generalist. Ecological Applications, 34, e2952. DOI: 10.1002/eap.2952.
[73]	McKey D (1979). The distribution of secondary compounds within plants//Rosenthal GA, Janzen DH. Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York. 55-133.
[74]	Mertens D, Fernández de Bobadilla M, Rusman Q, Bloem J, Douma JC, Poelman EH (2021). Plant defence to sequential attack is adapted to prevalent herbivores. Nature Plants, 7, 1347-1353. DOI PMID
[75]	Metlen KL, Aschehoug ET, Callaway RM (2009). Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant, Cell & Environment, 32, 641-653.
[76]	Monson RK, Trowbridge AM, Lindroth RL, Lerdau MT (2022). Coordinated resource allocation to plant growth- defense tradeoffs. New Phytologist, 233, 1051-1066.
[77]	Moore BD, Andrew RL, Külheim C, Foley WJ (2014). Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist, 201, 733-750. DOI PMID
[78]	Moore BD, Foley WJ (2005). Tree use by koalas in a chemically complex landscape. Nature, 435, 488-490.
[79]	Mosa KA, Ali MA, Ramamoorthy K, Ismail A (2022). Exploring the relationship between plant secondary metabolites and macronutrient homeostasis//Kumar V, Sivastava AK, Suprasanna P. Plant Nutrition and Food Security in the Era of Climate Change. Academic Press, Oxford, UK. 119-146.
[80]	Neilson EH, Goodger JQD, Woodrow IE, Møller BL (2013). Plant chemical defense: at what cost? Trends in Plant Science, 18, 250-258. DOI PMID
[81]	Ninkovic V, Rensing M, Dahlin I, Markovic D (2019). Who is my neighbor? Volatile cues in plant interactions. Plant Signaling & Behavior, 14, 1634993. DOI: 10.1080/15592324.2019.1634993.
[82]	Niveyro SL, Mortensen AG, Fomsgaard IS, Salvo A (2013). Differences among five amaranth varieties (Amaranthus spp.) regarding secondary metabolites and foliar herbivory by chewing insects in the field. Arthropod-Plant Interactions, 7, 235-245.
[83]	Noctor G, Mhamdi A (2017). Climate change, CO₂, and defense: the metabolic, redox, and signaling perspectives. Trends in Plant Science, 22, 857-870.
[84]	Ohnmeiss TE, Baldwin IT (2000). Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology, 81, 1765-1783.
[85]	Orrock JL, Sih A, Ferrari MCO, Karban R, Preisser EL, Sheriff MJ, Thaler JS (2015). Error management in plant allocation to herbivore defense. Trends in Ecology & Evolution, 30, 441-445.
[86]	Pant P, Pandey S, Dall’Acqua S (2021). The influence of environmental conditions on secondary metabolites in medicinal plants: a literature review. Chemistry & Biodiversity, 18, e2100345. DOI: 10.1002/cbdv.202100345.
[87]	Peters K, Treutler H, Döll S, Kindt ASD, Hankemeier T, Neumann S (2019). Chemical diversity and classification of secondary metabolites in nine bryophyte species. Metabolites, 9, 222. DOI: 10.3390/metabo9100222.
[88]	Prinsloo G, Nogemane N (2018). The effects of season and water availability on chemical composition, secondary metabolites and biological activity in plants. Phytochemistry Reviews, 17, 889-902.
[89]	Qaderi MM, Martel AB, Strugnell CA (2023). Environmental factors regulate plant secondary metabolites. Plants, 12, 447. DOI: 10.3390/plants12030447.
[90]	Qu KR, Cheng YX, Gao KR, Ren WB, Fry EL, Yin JJ, Liu YL (2022). Growth-defense trade-offs induced by long-term overgrazing could act as a stress memory. Frontiers in Plant Science, 13, 917354. DOI: 10.3389/fpls.2022.917354.
[91]	Raman A (2019). Endophytic epichloë (Clavicipitaceae) association with Lolium perenne and Lolium arundinaceum (Poaceae) resulting in health problems for the livestock and horses in temperate Australian pastures: assay of secondary metabolites and antioxidant activity. Plant Physiology Reports, 24, 474-486.
[92]	Rhoades DF, Cates RG (1976). Toward a general theory of plant antiherbivore chemistry//Wallace JW, Mansell RL. Biochemical Interaction Between Plants and Insects. Springer, Boston. 168-213.
[93]	Sánchez-Sánchez H, Morquecho-Contreras A (2017). Chemical plant defense against herbivores//Shields DC. Herbivores. Intechopen, London.
[94]	Sato Y, Ito K, Kudoh H (2017). Optimal foraging by herbivores maintains polymorphism in defence in a natural plant population. Functional Ecology, 31, 2233-2243.
[95]	Schuman MC, Baldwin IT (2016). The layers of plant responses to insect herbivores. Annual Review of Entomology, 61, 373-394. DOI PMID
[96]	Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006). SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proceedings of the National Academy of Sciences of the United States of America, 103, 12935-12940. DOI PMID
[97]	Seixas BU, Al-Shawaf L (2023). Error management theory and the evolution of cognitive bias//Shackelford TK. Encyclopedia of Sexual Psychology and Behavior. Springer, Cham. 1-5.
[98]	Silva JO, Espírito-Santo MM, Morais HC (2015). Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest. Basic and Applied Ecology, 16, 210-219.
[99]	Smilanich AM, Fincher RM, Dyer LA (2016). Does plant apparency matter? Thirty years of data provide limited support but reveal clear patterns of the effects of plant chemistry on herbivores. New Phytologist, 210, 1044-1057. DOI PMID
[100]	Stamp N (2003). Out of the quagmire of plant defense hypotheses. The Quarterly Review of Biology, 78, 23-55.
[101]	Stamp N (2004). Can the growth-differentiation balance hypothesis be tested rigorously? Oikos, 107, 439-448.
[102]	Stewart AJ, Chapman W, Jenkins GI, Graham I, Martin T, Crozier A (2001). The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment, 24, 1189-1197.
[103]	Strauss SY, Agrawal AA (1999). The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution, 14, 179-185.
[104]	Sun YM, Alseekh S, Fernie AR (2023). Plant secondary metabolic responses to global climate change: a meta-analysis in medicinal and aromatic plants. Global Change Biology, 29, 477-504.
[105]	Sun YM, Guo JJ, Li YR, Luo GW, Li L, Yuan HY, Mur LAJ, Guo SW (2020). Negative effects of the simulated nitrogen deposition on plant phenolic metabolism: a meta-analysis. Science of the Total Environment, 719, 137442. DOI: 10.1016/j.scitotenv.2020.137442.
[106]	Thon FM, Müller C, Wittmann MJ (2024). The evolution of chemodiversity in plants—From verbal to quantitative models. Ecology Letters, 27, e14365. DOI: 10.1111/ele.14365.
[107]	Thouvenot L, Gauzens B, Haury J, Thiébaut G (2019). Response of macrophyte traits to herbivory and neighboring species: integration of the functional trait framework in the context of ecological invasions. Frontiers in Plant Science, 9, 1981. DOI: 10.3389/fpls.2018.01981.
[108]	van Velzen E, Etienne RS (2015). The importance of ecological costs for the evolution of plant defense against herbivory. Journal of Theoretical Biology, 372, 89-99. DOI PMID
[109]	Wan JL, Yi JH, Tao ZB, Ren ZK, Otieno EO, Tian BL, Ding JQ, Siemann E, Erb M, Huang W (2022). Species-specific plant-mediated effects between herbivores converge at high damage intensity. Ecology, 103, e3647. DOI: 10.1002/ecy.3647.
[110]	Wang DL, Wang L (2011). Interactions between herbivores and plant diversity. Acta Agrestia Sinica, 19(4), 165-170.
	[ 王德利, 王岭 (2011). 草食动物与草地植物多样性的互作关系研究进展. 草地学报, 19(4), 165-170.]
[111]	Wang DL (2004). Progress in the coadaptation and coevolution between plants and herbivores. Acta Ecologica Sinica, 24, 2461-2468.
	[ 王德利 (2004). 植物与草食动物之间的协同适应及进化. 生态学报, 24, 2461-2468.]
[112]	Wang SP (2004). Grazing resistance of rangeland plants. Chinese Journal of Applied Ecology, 15, 517-522.
	[ 汪诗平 (2004). 草原植物的放牧抗性. 应用生态学报, 15, 517-522.]
[113]	Wang SX, Xu ZR, Qiao T, Zhang B, Wei ZQ, Yang MX (2023). Intensity of competition for forage between livestock and wild herbivores based on grassland carrying capacity. Progress in Geography, 42, 2186-2197. DOI
	[ 王守兴, 徐增让, 乔添, 张彪, 魏子谦, 杨明新 (2023). 基于草地承载力的畜兽冲突强度研究. 地理科学进展, 42, 2186-2197.] DOI
[114]	War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012). Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior, 7, 1306-1320.
[115]	Xiao L (2018). Responses of Invasive Plant Secondary Metabolites to Herbivory and Environmental Factors. PhD dissertation, Wuhan Botanical Garden of Chinese Academy of Sciences, Wuhan.
	[ 肖轹 (2018). 入侵植物次生代谢策略对植食性昆虫和环境因子的响应. 博士学位论文, 中国科学院武汉植物园, 武汉.]
[116]	Xiao L, Huang W, Carrillo J, Ding JQ, Siemann E (2024). Interactive effects of soils, local environmental conditions and herbivores on secondary chemicals in tallow tree. Journal of Plant Ecology, 17, rtae062. DOI: 10.1093/jpe/rtae062.
[117]	Yin WD, Zhou LF, Yang KW, Fang JY, Biere A, Callaway RM, Wu MK, Yu HW, Shi Y, Ding JQ (2023). Rapid evolutionary trade-offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant. Ecology Letters, 26, 942-954. DOI PMID
[118]	Zhang ZH, Gong JR, Shi JY, Li XB, Song LY, Zhang WY, Li Y, Zhang SQ, Dong JJ, Liu YY (2022). Multiple herbivory pressures lead to different carbon assimilation and allocation strategies: evidence from a perennial grass in a typical steppe in Northern China. Agriculture, Ecosystems & Environment, 326, 107776. DOI: 10.1016/j.agee.2021.107776.
[119]	Zhong ZW, Li XF, Wang DL (2021). Research progresses of plant-herbivore interactions. Chinese Journal of Plant Ecology, 45, 1036-1048.
	[ 钟志伟, 李晓菲, 王德利 (2021). 植物-植食性动物相互关系研究进展. 植物生态学报, 45, 1036-1048.] DOI
[120]	Züst T, Agrawal AA (2017). Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology, 68, 513-534. DOI PMID
[121]	Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012). Natural enemies drive geographic variation in plant defenses. Science, 338, 116-119. DOI PMID