Changes in oak (Quercus robur) photosynthesis after winter moth (Operophtera brumata) herbivory are not explained by changes in chemical or structural leaf traits

Autoři: Kristiina Visakorpi aff001;  Terhi Riutta aff002;  Yadvinder Malhi aff002;  Juha-Pekka Salminen aff004;  Norma Salinas aff002;  Sofia Gripenberg aff006
Působiště autorů: Department of Zoology, University of Oxford, Oxford, England, United Kingdom aff001;  Environmental Change Institute, School of Geography and the Environment, University of Oxford, Oxford, England, United Kingdom aff002;  Department of Life Sciences, Silwood Park Campus, Imperial College London, Ascot, England, United Kingdom aff003;  Natural Chemistry Research Group, Department of Chemistry, University of Turku, FI Turku, Finland aff004;  Seccion Química, Pontificia Universidad Católica del Peru, Lima, Peru aff005;  School of Biological Sciences, University of Reading, Reading, England, United Kingdom aff006
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0228157


Insect herbivores have the potential to change both physical and chemical traits of their host plant. Although the impacts of herbivores on their hosts have been widely studied, experiments assessing changes in multiple leaf traits or functions simultaneously are still rare. We experimentally tested whether herbivory by winter moth (Operophtera brumata) caterpillars and mechanical leaf wounding changed leaf mass per area, leaf area, leaf carbon and nitrogen content, and the concentrations of 27 polyphenol compounds on oak (Quercus robur) leaves. To investigate how potential changes in the studied traits affect leaf functioning, we related the traits to the rates of leaf photosynthesis and respiration. Overall, we did not detect any clear effects of herbivory or mechanical leaf damage on the chemical or physical leaf traits, despite clear effect of herbivory on photosynthesis. Rather, the trait variation was primarily driven by variation between individual trees. Only leaf nitrogen content and a subset of the studied polyphenol compounds correlated with photosynthesis and leaf respiration. Our results suggest that in our study system, abiotic conditions related to the growth location, variation between tree individuals, and seasonal trends in plant physiology are more important than herbivory in determining the distribution and composition of leaf chemical and structural traits.

Klíčová slova:

Herbivory – Leaves – Oaks – Photosynthesis – Plant biochemistry – Plant defenses – Trees – Plant respiration


1. Roskov Y, Abucay L, Orrell T, Nicholson D, Bailly N, Kirk PM, et al., editors. Species 2000 & ITIS Catalogue of Life, 2018 Annual Checklist. Species 2000: Naturalis, Leiden, the Netherlands; 2018. Available:

2. Forister ML, Novotny V, Panorska AK, Baje L, Basset Y, Butterill PT, et al. The global distribution of diet breadth in insect herbivores. Proceedings of the National Academy of Sciences. 2015;112: 442–447. doi: 10.1073/pnas.1423042112 25548168

3. Karban R, Baldwin IT. Induced responses to herbivory. Chicago: University of Chicago Press; 1997.

4. Nykänen H, Koricheva J. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos. 2004;104: 247–268.

5. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment. 2010;33: 1597–1613. doi: 10.1111/j.1365-3040.2010.02167.x 20444224

6. Nabity PD, Zavala JA, DeLucia EH. Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata. Journal of Experimental Botany. 2013;64: 685–694. doi: 10.1093/jxb/ers364 23264519

7. Coley PD. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia. 1988;74: 531–536. doi: 10.1007/BF00380050 28311759

8. Zhang Y, Turner JG. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. Weigel D, editor. PLoS ONE. 2008;3: e3699. doi: 10.1371/journal.pone.0003699 19002244

9. Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. The Quarterly Review of Biology. 1992;67: 283–335.

10. Züst T, Agrawal AA. Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology. 2017;68: 513–534. doi: 10.1146/annurev-arplant-042916-040856 28142282

11. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM, Froehlich JE, et al. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nature Communications. 2016;7: 12570. doi: 10.1038/ncomms12570 27573094

12. Visakorpi K, Gripenberg S, Malhi Y, Bolas C, Oliveras I, Harris N, et al. Small-scale indirect plant responses to insect herbivory could have major impacts on canopy photosynthesis and isoprene emission. New Phytologist. 2018;220. doi: 10.1111/nph.15338 30047151

13. Chapman SK, Hart SC, Cobb NS, Whitham TG, Koch GW. Insect herbivory increases litter quality and decompostion: an extension of the acceleration hypothesis. Ecology. 2003;84: 2867–2876. doi: 10.1890/02-0046

14. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters. 2008;11: 1065–1071. doi: 10.1111/j.1461-0248.2008.01219.x 18627410

15. Chomel M, Guittonny-Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, et al. Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. Journal of Ecology. 2016;104: 1527–1541. doi: 10.1111/1365-2745.12644

16. Schultz JC, Baldwin IT. Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science. 1982;217: 149–151. doi: 10.1126/science.217.4555.149 17770257

17. Nykänen H, Koricheva J. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos. 2004;104: 247–268.

18. Rossiter M, Schultz JC, Baldwin IT. Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology. 1988;69: 267–277. doi: 10.2307/1943182

19. Kaitaniemi P, Ruohomäki K, Ossipov V, Haukioja E, Pihlaja K. Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia. 1998;116: 182–190. doi: 10.1007/s004420050578 28308525

20. Tuomi J, Niemela P, Rousi M, Siren S, Vuorisalo T. Induced accumulation of foliage phenols in mountain birch: branch response to defoliation? The American Naturalist. 1988;132: 602–608. doi: 10.1086/284875

21. Havko N, Major I, Jewell J, Attaran E, Browse J, Howe G. Control of carbon assimilation and partitioning by jasmonate: an accounting of growth–defense tradeoffs. Plants. 2016;5: 7. doi: 10.3390/plants5010007 27135227

22. Lambers H, Chapin FS, Pons TL. Plant physiological ecology. New York, NY, U.S.A: Springer; 1998.

23. Evans JR. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia. 1989;78: 9–19. doi: 10.1007/BF00377192 28311896

24. Haukioja E, Ossipov V, Lempa K. Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomologia Experimentalis et Applicata. 2002;104: 125–136. doi: 10.1046/j.1570-7458.2002.00999.x

25. Salminen J-P, Karonen M. Chemical ecology of tannins and other phenolics: we need a change in approach: Chemical ecology of tannins. Functional Ecology. 2011;25: 325–338. doi: 10.1111/j.1365-2435.2010.01826.x

26. Feeny P. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by Winter moth caterpillars. Ecology. 1970;51: 565–581. doi: 10.2307/1934037

27. Salminen J-P, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P. Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. Journal of Chemical Ecology. 2004;30: 1693–1711. doi: 10.1023/b:joec.0000042396.40756.b7 15586669

28. Roslin T, Salminen J-P. Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos. 2008;117: 1560–1568. doi: 10.1111/j.0030-1299.2008.16725.x

29. Elderd BD, Rehill BJ, Haynes KJ, Dwyer G. Induced plant defenses, host-pathogen interactions, and forest insect outbreaks. Proceedings of the National Academy of Sciences. 2013;110: 14978–14983. doi: 10.1073/pnas.1300759110 23966566

30. Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen J-P. Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition. Oecologia. 2009;159: 777–788. doi: 10.1007/s00442-008-1268-7 19148684

31. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, van Loon JJA, Dicke M. Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. Journal of Experimental Botany. 2014;65: 2203–2217. doi: 10.1093/jxb/eru096 24619996

32. Ohse B, Hammerbacher A, Seele C, Meldau S, Reichelt M, Ortmann S, et al. Salivary cues: simulated roe deer browsing induces systemic changes in phytohormones and defence chemistry in wild-grown maple and beech saplings. Functional Ecology. 2017;31: 340–349. doi: 10.1111/1365-2435.12717

33. Faeth SH. Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology. 1986;67: 479–494. doi: 10.2307/1938591

34. Roth S, Lindroth RL, Volin JohnC, Kruger EricL. Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance. Global Change Biology. 1998;4: 419–430. doi: 10.1046/j.1365-2486.1998.00164.x

35. Ayres MP, Clausen TP, MacLean SF, Redman AM, Reichardt PB. Diversity of structure and antiherbivore activity in condensed tannins. Ecology. 1997;78: 1696–1712. doi: 10.1890/0012-9658(1997)078[1696:DOSAAA]2.0.CO;2

36. Osier TL, Hwang S-Y, Lindroth RL. Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecological Entomology. 2000;25: 197–207. doi: 10.1046/j.1365-2311.2000.00245.x

37. Barbehenn RV, Constabel P. Tannins in plant–herbivore interactions. Phytochemistry. 2011;72: 1551–1565. doi: 10.1016/j.phytochem.2011.01.040 21354580

38. Engström MT, Arvola J, Nenonen S, Virtanen VTJ, Leppä MM, Tähtinen P, et al. Structural features of hydrolyzable tannins determine their ability to form insoluble complexes with bovine serum albumin. J Agric Food Chem. 2019;67: 6798–6808. doi: 10.1021/acs.jafc.9b02188 31134805

39. Moilanen J, Salminen J-P. Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology. 2008;18: 73–83. doi: 10.1007/s00049-007-0395-7

40. Hunter MD. Interactions within herbivore communities mediated by the host plant: the keystone herbivore concept. In: Hunter MD, Ohgushi T, Price PW, editors. Effects of resource distribution on animal–plant interactions. San Diego, California, USA: Academin Press, Inc.; 1992. pp. 287–325.

41. Crawley MJ. The R book. Chichester, England: Wiley; 2007. Available:

42. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018. Available: URL

43. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package. 2017. Available:

44. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67. doi: 10.18637/jss.v067.i01

45. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. nlme: linear and nonlinear mixed effects models. 2017. Available:

46. Josse J, Husson F. missMDA: a package for handling missing values in multivariate data analysis. Journal of Statistical Software. 2016;70. doi: 10.18637/jss.v070.i08

47. Wang Y, Naumann U, Wright S, Eddelbuettel D, Warton D. mvabund: statistical methods for analysing multivariate abundance data. 2017. Available:

48. Warton DI, Wright ST, Wang Y. Distance-based multivariate analyses confound location and dispersion effects: Mean-variance confounding in multivariate analysis. Methods in Ecology and Evolution. 2012;3: 89–101. doi: 10.1111/j.2041-210X.2011.00127.x

49. Warton DI, Blanchet FG, O’Hara RB, Ovaskainen O, Taskinen S, Walker SC, et al. So many variables: joint modeling in community ecology. Trends in Ecology & Evolution. 2015;30: 766–779. doi: 10.1016/j.tree.2015.09.007 26519235

50. Wang Y, Naumann U, Wright ST, Warton DI. mvabund—an R package for model-based analysis of multivariate abundance data: The mvabund R package. Methods in Ecology and Evolution. 2012;3: 471–474. doi: 10.1111/j.2041-210X.2012.00190.x

51. Oksanen J. Multivariate analysis of ecological communities in R: vegan tutorial. 2015. Available:

52. Lempa K, Agrawal AA, Salminen J-P, Turunen T, Ossipov V, Ossipova S, et al. Rapid herbivore-induced changes in mountain birch phenolics and nutritive compounds and their effects on performance of the major defoliator, Epirrita autumnata. Journal of Chemical Ecology. 2004;30: 303–321. doi: 10.1023/b:joec.0000017979.94420.78 15112726

53. Beyaert I, Kopke D, Stiller J, Hammerbacher A, Yoneya K, Schmidt A, et al. Can insect egg deposition “warn” a plant of future feeding damage by herbivorous larvae? Proceedings of the Royal Society B: Biological Sciences. 2012;279: 101–108. doi: 10.1098/rspb.2011.0468 21561977

54. Stamp NE, Osier TL. Response of five insect herbivores to multiple allelochemicals under fluctuating temperatures. Entomologia Experimentalis et Applicata. 1998;88: 81–96. doi: 10.1046/j.1570-7458.1998.00349.x

55. Barbehenn RV, Kochmanski J. Searching for synergism: effects of combinations of phenolic compounds and other toxins on oxidative stress in Lymantria dispar caterpillars. Chemoecology. 2013;23: 219–231. doi: 10.1007/s00049-013-0136-z

56. Pascacio-Villafán C, Lapointe S, Williams T, Sivinski J, Niedz R, Aluja M. Mixture-amount design and response surface modeling to assess the effects of flavonoids and phenolic acids on developmental performance of Anastrepha ludens. Journal of Chemical Ecology. 2014;40: 297–306. doi: 10.1007/s10886-014-0404-6 24619732

57. Nelson AC, Kursar TA. Interactions among plant defense compounds: a method for analysis. Chemoecology. 1999;9: 81–92. doi: 10.1007/s000490050037

58. Steppuhn A, Baldwin IT. Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecology Letters. 2007;10: 499–511. doi: 10.1111/j.1461-0248.2007.01045.x 17498149

59. Smilanich AM, Fincher RM, Dyer LA. 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. 2016;210: 1044–1057. doi: 10.1111/nph.13875 26889654

60. Després L, David J-P, Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology & Evolution. 2007;22: 298–307. doi: 10.1016/j.tree.2007.02.010 17324485

61. Schultz JC, Nothnagle PJ, Baldwin IT. Seasonal and individual variation in leaf quality of two northern hardwoods tree species. American Journal of Botany. 1982;69: 753. doi: 10.2307/2442965

62. Hwang S-Y, Lindroth RL. Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia. 1997;111: 99–108. doi: 10.1007/s004420050213 28307511

63. Kazakou E, Violle C, Roumet C, Navas M-L, Vile D, Kattge J, et al. Are trait-based species rankings consistent across data sets and spatial scales? Journal of Vegetation Science. 2014;25: 235–247. doi: 10.1111/jvs.12066

64. Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, et al. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters. 2015;18: 1406–1419. doi: 10.1111/ele.12508 26415616

65. Roslin T, Gripenberg S, Salminen J-P, Karonen M, B. O’Hara R, Pihlaja K, et al. Seeing the trees for the leaves—oaks as mosaics for a host-specific moth. Oikos. 2006;113: 106–120. doi: 10.1111/j.0030-1299.2006.14460.x

66. Top SM, Preston CM, Dukes JS, Tharayil N. Climate influences the content and chemical composition of foliar tannins in green and senesced tissues of Quercus rubra. Frontiers in Plant Science. 2017;8. doi: 10.3389/fpls.2017.00423 28559896

67. Hunter MD, Schultz JC. Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology. 1995;76: 1226–1232. doi: 10.2307/1940929

68. Fischbach RJ, Kossmann B, Panten H, Steinbrecher R, Heller W, Seidlitz HK, et al. Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant, Cell and Environment. 1999;22: 27–37. doi: 10.1046/j.1365-3040.1999.00390.x

69. Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M. Functional roles of flavonoids in photoprotection: New evidence, lessons from the past. Plant Physiology and Biochemistry. 2013;72: 35–45. doi: 10.1016/j.plaphy.2013.03.014 23583204

70. Bennett RN, Wallsgrove RM. Secondary metabolites in plant defence mechanisms. New Phytologist. 1994;127: 617–633. doi: 10.1111/j.1469-8137.1994.tb02968.x

71. Kang Z-W, Liu F-H, Tan X-L, Zhang Z-F, Zhu J-Y, Tian H-G, et al. Infection of powdery mildew reduces the fitness of grain aphids (Sitobion avenae) through restricted nutrition and induced defense response in wheat. Frontiers in Plant Science. 2018;9. doi: 10.3389/fpls.2018.00778 29967627

72. Li F-R, Peng S-L, Chen B-M, Hou Y-P. A meta-analysis of the responses of woody and herbaceous plants to elevated ultraviolet-B radiation. Acta Oecologica. 2010;36: 1–9. doi: 10.1016/j.actao.2009.09.002

73. Lankau RA, Kliebenstein DJ. Competition, herbivory and genetics interact to determine the accumulation and fitness consequences of a defence metabolite. Journal of Ecology. 2009;97: 78–88. doi: 10.1111/j.1365-2745.2008.01448.x

74. Lim PO, Kim HJ, Gil Nam H. Leaf senescence. Annual Review of Plant Biology. 2007;58: 115–136. doi: 10.1146/annurev.arplant.57.032905.105316 17177638

75. Nabity PD, Zavala JA, DeLucia EH. Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Annals of Botany. 2009;103: 655–663. doi: 10.1093/aob/mcn127 18660492

76. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, et al. Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences. 2002;99: 1088–1091. doi: 10.1073/pnas.022647099 11792866

77. Koricheva J, Larsson S, Haukioja E, Keinänen M, Keinanen M. Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos. 1998;83: 212. doi: 10.2307/3546833

78. Schwachtje J, Baldwin IT. Why does herbivore attack reconfigure primary metabolism? Plant Physiology. 2008;146: 845–851. doi: 10.1104/pp.107.112490 18316639

79. Edwards PJ, Wratten SD, Greenwood S. Palatability of British trees to insects: constitutive and induced defences. Oecologia. 1986;69: 316–319. doi: 10.1007/BF00377640 28311377

80. Kliebenstein DJ. False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology. Physiological and Molecular Plant Pathology. 2016;95: 55–59. doi: 10.1016/j.pmpp.2016.02.004

81. Koricheva J. Meta-analysis of sources of variation in fitness costs of plant antiherbviore defenses. Ecology. 2002;83: 176–190. doi: 10.1890/0012-9658(2002)083[0176:MAOSOV]2.0.CO;2

82. van der Mejden E, Wijn M, Verkaar HJ. Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos. 1988;51: 355–363.

83. Anten NPR, Ackerly DD. Canopy-level photosynthetic compensation after defoliation in a tropical understorey palm. Functional Ecology. 2001;15.

Článek vyšel v časopise


2020 Číslo 1