Abstract
Global warming not only alters phenology but also nutritional quality and defense compounds in plants, which consequently hinders their defense against herbivorous insects. In this study, the performance of Spodoptera litura was analyzed to observe the effects of high temperatures on chemical-based defense in plants in the context of insect–plant interaction. Results show that high temperature reduced the nutritional value and content of defense compounds in the foliage of yellow cress (Rorippa dubia). These alterations negatively affected the performance of second instar S. litura larvae feeding on plants grown at high temperature. Low quality of the food source is likely the key cause of slow development of larvae. Adaptation of herbivorous insects known as compensatory feeding is projected resulting in more crop losses under global warming. Our data reveal temperature-induced reduction in the content of defensive compounds (in constitutive resistance) along with lower response capability against herbivore attacks (in induced resistance), which indicate a decrease in plant fitness. High temperatures caused by global warming negatively affect crop production and are expected to increase the burden on plant protection practices.
Similar content being viewed by others
References
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190. https://doi.org/10.1007/s11099-013-0021-6
Bale J, Masters GJ, Hodkins ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16. https://doi.org/10.1046/j.1365-2486.2002.00451.x
Bassirirad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytol 147:155–169. https://doi.org/10.1046/j.1469-8137.2000.00682.x
Battisti A (2008) Forests and climate change—lessons from insects. iForest Biogeosci For 1(1):1–5. https://doi.org/10.3832/ifor0210-0010001
Bebber DP, Holmes T, Gurr SJ (2014) The global spread of crop pests and pathogens. Glob Ecol Biogeogr 23:1398–1407. https://doi.org/10.1111/geb.12214
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher-plants. Annu Rev Plant Physiol 31:491–543. https://doi.org/10.1146/annurev.pp.31.060180.002423
Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol 50:1339–1354. https://doi.org/10.1111/j.1744-7909.2008.00751.x
Bidart-Bouzat MG, Mithen R, Berenbaum MR (2005) Elevated CO2 influences herbivory-induced defense responses of Arabidopsis thaliana. Oecologia 145:415–424. https://doi.org/10.1007/s00442-005-0158-5
Bradford MM (1976) A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brody AK, Karban R (1992) Lack of a tradeoff between constitutive and induced defenses among varieties of cotton. Oikos 65:301–306. https://doi.org/10.2307/3545022
Clissold FJ, Coggan N, Simpson SJ (2013) Insect herbivores can choose microclimates to achieve nutritional homeostasis. J Exp Biol 216:2089–2096. https://doi.org/10.1242/jeb.078782
Coggan N, Clissold FJ, Simpson JS (2011) Locusts use dynamic thermoregulatory behavior to optimize nutritional outcomes. Proc R Soc B 278:2745–2752. https://doi.org/10.1098/rspb.2010.2675
Coughlan MP, Moloney AP (1988) Isolation of 1,4-b-d-glucan 4-glucanohydrolases of Talaromyces emersonii. In: Wood WA, Kellogg ST (eds) Methods in enzymology, vol 160. Academic Press, London, p 365
Dhaliwal GS, Jindal V, Dhawan AK (2010) Insect pest problems and crop losses: changing trends. Indian J Ecol 37:1–7
Dong SF, Scagel CF, Cheng LL, Fuchigami LH, Rygiewicz PT (2001) Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth. Tree Physiol 21:541–547. https://doi.org/10.1093/treephys/21.8.541
Evan HD, Paul DN, Jorge AZ, May RB (2012) Climate change: resetting plant–insect interactions. Plant Physiol 160:1677–1685. https://doi.org/10.1104/pp.112.204750
Flato G, Marotzke J, Abiodun B, Braconnot P, Chou SC, Collins WJ, Eyring V (2013) Evaluation of climate models. In: Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Clim Change 5:741–866
Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285
Gupta GP, Rani S, Birah A, Raghuraman M (2005) Improved artificial diet for mass rearing of the tobacco caterpillar, Spodoptera litura (Lepidoptera: Noctuidae). Int J Trop Insect Sci 25:55–58. https://doi.org/10.1079/IJT200551
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extrem 10:4–10. https://doi.org/10.1016/j.wace.2015.08.001
Hermilo S-S, Alina M-C (2016) Chemical plant defense against herbivores (chapter 1). In: Shields VDC (ed) Herbivores. IntechOpen. https://doi.org/10.5772/67346
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or to defend. Quart Rev Biol 67:283–335
Himanen SJ, Nissinen A, Auriola S, Poppy GM, Stewart CN, Holopainen JK, Nerg AM (2008) Constitutive and herbivore-inducible glucosinolate concentrations in oilseed rape (Brassica napus) leaves are not affected by Bt Cry1Ac insertion but change under elevated atmospheric CO2 and O3. Planta 227:427–437. https://doi.org/10.1007/s00425-007-0629-5
Huang SJ, Han ZJ (2007) Mechanisms for multiple resistances in field populations of common cutworm, Spodoptera litura (Fabricius) in China. Pestic Biochem Physiol 87:14–22. https://doi.org/10.1016/j.pestbp.2006.05.002
Hungaria M, Franco AA (1993) Effects of high temperature on nodulation on nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102. https://doi.org/10.1007/BF00010766
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, et al. (eds) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
IPCC (2013) Working Group I Contribution to the IPCC Fifth Assessment Report. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, et al. (eds) Climate change 2013: the physical sciences basis summary for policymakers. Cambridge University Press, Cambridge
Jadhav DR, Mallikarjuna N, Rathore A, Pokle D (2012) Effect of some flavonoids on survival and development of Helicoverpa armigera (Hübner) and Spodoptera litura (Fab) (Lepidoptera: Noctuidae). Asian J Agric Environ Sci 4:298–307
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant–insect and multitrophic interactions. Plant Physiol 160(4):1719–1727. https://doi.org/10.1104/pp.112.206524
Kingsolver JG, Woods HA (1998) Interactions of temperature and dietary protein concentration in growth and feeding of Manduca sexta caterpillars. Physiol Entomol 23:354–359. https://doi.org/10.1046/j.1365-3032.1998.234105.x
Kuokkanen K, Julkunen-Tiitto R, Keinanen M, Niemela P, Tahvanainen J (2001) The effect of elevated CO2 and temperature on the secondary chemistry of Betula pendula seedlings. Trees (Berlin) 15:378–384. https://doi.org/10.1007/s004680100108
Lafta AM, Lorenzen JH (1995) Effect of high temperature on plant growth and carbohydrate metabolism in potato. Plant physiol 109(2):637–643. https://doi.org/10.1104/pp.109.2.637
Lang CA (1958) Simple micro determination of Kjeldahl nitrogen in biological materials. Anal Chem 30:1692–1694. https://doi.org/10.1021/ac60142a038
Lee TM, Lin YH (1995) Trypsin inhibitor and trypsin-like protease activity in air or submergence-grown rice (Oryza sativa L.) coleoptiles. Plant Sci 106:43–54. https://doi.org/10.1016/0168-9452(95)04058-3
Lee KP, Behmer ST, Simpson SJ, Raubenheimer D (2002) A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). J Insect Physiol 48:655–665. https://doi.org/10.1016/S0022-1910(02)00088-4
Li Q, Eigenbrode SD, Stringham GR, Thiagarajah MR (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419. https://doi.org/10.1023/A:1005535129399
Lindroth RL (1991) Differential toxicity of plant allelochemicals in insects: roles of enzymatic detoxification systems. In: Bernays EA (ed) Insect–plant interactions. CRC Press, Boca Raton, pp 1–33
Luo YQ (2007) Terrestrial carbon-cycling feedback to climate warming. Annu Rev Ecol Evol Syst 38:683–712. https://doi.org/10.1146/annurev.ecolsys.38.091206.095808
Makkar HPS, Becker K, Abel H, Pawelzik E (1997) Nutrient contents, rumen protein degradability and antinutritional factors in some colour- and white-flowering cultivars of Vicia faba beans. J Sci Food Agric 75:511–520. https://doi.org/10.1002/(SICI)1097-0010(199712)75:4%3c511:AID-JSFA907%3e3.0.CO;2-M
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Moreira X, Abdala-Roberts L, Gols R (2018) Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Sci Rep 8:12678. https://doi.org/10.1038/s41598-018-31041-0
Pan J, Lin S, Woodbury NW (2012) Bacteriochlorophyll excited-state quenching pathways in bacterial reaction centers with the primary donor oxidized. J Phys Chem B 116:2014–2022. https://doi.org/10.1021/jp212441b
Parkinson JA, Allen SE (1975) A wet oxidation process suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11. https://doi.org/10.1080/00103627509366539
Pereira FMV, Rosa E, Fahey JW, Stephenson KK, Carvalho R, Aires A (2002) Influence of temperature and ontogeny on the levels of glucosinolates in broccoli (Brassica oleracea var. italica) sprouts and their effect on the induction of mammalian phase 2 enzymes. J Agric Food Chem 50:6239–6244. https://doi.org/10.1021/jf020309x
Price PW (1997) Insect ecology. Wiley, New York
Pureswaran DS, Roques A, Battisti A (2018) Forest insects and climate change. Curr For Rep 4:35–50. https://doi.org/10.1007/s40725-018-0075-6
Reda FA, Bakr RFA, Elaziz MFA, Awad MH, El-Halim HME (2013) The activity of some detoxification enzymes in Spodoptera littoralis (Boisd.) larvae (Lepidoptera–Noctuidae) treated with two different insect growth regulators. Egypt Acad J Biol Sci 5:19–27. https://doi.org/10.21608/eajbsc.2013.16092
Rennenberg H, Loreto F, Polle A, Brilli F, Fares S, Beniwal RS, Gessler A (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571. https://doi.org/10.1055/s-2006-924084
Rodriguez-Saona C, Chalmers JA, Raj S, Thaler JS (2005) Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577. https://doi.org/10.1007/s00442-005-0006-7
Rose R, Rose CL, Omi SK, Forry KR, Durall DM, Bigg WL (1991) Starch determination by perchloric acid vs. enzymes: evaluating the accuracy and precision of six colorimetric methods. J Agric Food Chem 39:2–11. https://doi.org/10.1021/jf00001a001
Rufty TW, Raper CD, Jackson WA (1981) Nitrogen assimilation, root growth and whole plant responses of soybean to root temperature and to carbon dioxide and light in the aerial environment. New Phytol 88:607–619. https://doi.org/10.1111/j.1469-8137.1981.tb01736.x
Ryan CA, Gregory P, Tingey W (1982) Phenolic oxidase activities in glandular trichomes of Solanum berthaultii. Phytochemistry 21:1885–1887. https://doi.org/10.1016/0031-9422(82)83008-2
Sadasivam S, Thayumanavan B (2003) Molecular host plant resistance to pests. Marcel Dekker, New York, p 479
Siddhuraju P, Becker K (2003) Studies on antioxidant activities of mucuna seed (Mucuna pruriens var. utilis) extracts and certain non-protein amino/imino acids through in vitro models. J Sci Food Agric 83:1517–1524. https://doi.org/10.1002/jsfa.1587
Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, Dordrecht, p 423
Smriti S, Rubaljot K, Singh SS, Ramesh A (2018) Impact of elevated temperature and carbon dioxide on insect performance indices of Spodoptera litura Fabricius. J Entomol Res 42:315–324. https://doi.org/10.5958/0974-4576.2018.00053.1
Stout MJ, Workman KV, Bostock RM, Duffey S (1997) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81. https://doi.org/10.1007/s004420050355
Underwood N, Anderson K, Inouye BD (2005) Induced vs. constitutive resistance and the spatial distribution of insect herbivores among plants. Ecology 86:594–602. https://doi.org/10.1890/03-0290
Veteli TO, Kuokkanen K, Julkunen-Tiitto R, Roininen H, Tahvanainen J (2002) Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry. Glob Change Biol 8:1240–1252. https://doi.org/10.1046/j.1365-2486.2002.00553.x
Vu JCV, Gesh RW, Pennanen AH, Allen LH Jr, Boote KJ, Bowes G (2001) Soybean photosynthesis, Rubisco, and carbohydrate enzyme function at supraoptimal temperatures in elevated CO2. J Plant Physiol 158:295–307. https://doi.org/10.1078/0176-1617-00290
War AR, Paulraj MG, Ahamad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
Wood TM, Bhat KM (1988) Methods for measuring cellulase activities. In: Wood WA, Kellogg ST (eds) Methods in enzymology, vol 160. Academic Press, Inc., London, pp 87–112
Xia J, Zhao YH, Wang WK, He YH (2015) Elevated temperature altered photosynthetic products in wheat seedlings and organic compounds and biological activity in rhizopshere soil under cadmium stress. Sci Rep. https://doi.org/10.1038/srep14426
Yang Y, Joern A (1994) Influence of diet quality, developmental stage, and temperature on food residence time in the grasshopper Melanoplus differentialis. Physiol Zool 67:598–616
Yang LY, Yang SL, Li JY (2018) Effects of different growth temperatures on growth, development, and plastid pigments metabolism of tobacco (Nicotiana tabacum L.) plants. Bot Stud 59(5):1–13. https://doi.org/10.1186/s40529-018-0221-2
Zhang YF, Wan GJ, Liu B, Zhang XG, Xing GN, Chen FJ (2017) Elevated CO2 and temperature alter development and food utilization of Spodoptera litura fed on resistant soybean. J Apply Entomol 142:250–262. https://doi.org/10.1111/jen.12463
Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a meta-analysis. Glob Change Biol 12:27–41. https://doi.org/10.1111/j.1365-2486.2005.01086.x
Acknowledgements
The study was supported by grant from Ministry of Science and Technology (MOST), Taiwan (Grant No. 105-2313-B-005-003-MY3). We also thank Dr. Melissa Andrews from Wallace Academic Editing for editing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Heikki Hokkanen.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pham, T.A., Hwang, SY. High temperatures reduce nutrients and defense compounds against generalist Spodoptera litura F. in Rorippa dubia. Arthropod-Plant Interactions 14, 333–344 (2020). https://doi.org/10.1007/s11829-020-09750-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-020-09750-z