Plant Ecology

, Volume 220, Issue 3, pp 305–320 | Cite as

Changes in defense traits of young leaves in subtropical forests succession

  • Taotao Han
  • Jun Wang
  • Hai RenEmail author
  • Huilin Yi
  • Qianmei Zhang
  • Qinfeng Guo


Plants develop diverse adaptive traits in changeable environments, yet whether plant defense traits change during succession remains unclear. In this study, we investigated the young leaf physical traits (i.e., upright orientation of leaves, trichomes, an enhanced cuticle, and a multilayered epidermis) and leaf color trait (i.e., red pigmentation) of dominant plants in three subtropical forests. These forests included a pioneer forest, a mixed coniferous-broadleaved forest, and a monsoon-evergreen broadleaved forest representing early, middle, and later successional stages, respectively. Our results show that the red color trait in young leaves is related to anti-herbivory defense, and the percentage of species with red young leaves is higher in later than in early succession. Physical defense tends to be weaker for red young leaves than for green young leaves in early and middle successions. In addition, the number of defense traits of young leaves increases with succession. We speculate that young leaves in subtropical forests depend increasingly on multiple defense traits during succession because of the increased biotic stresses and environmental complexity in later succession.


Adaptation Environmental stress Multiple defense Red leaves Successional stage 



This research was supported by the National Natural Science Foundation of China (no. 31570422) and Guangdong Science and Technology Program (no. 2016A030303044). We thank Mr Yiming Fan for field investigation. Thanks are also due to Prof. Bruce Jaffee for English editing and constructive comments and to anonymous reviewers for their valuable comments on an early version of the manuscript.


  1. Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432CrossRefGoogle Scholar
  2. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:132–149CrossRefGoogle Scholar
  3. Archetti M, Döring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG, Thomas H (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173CrossRefGoogle Scholar
  4. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488CrossRefGoogle Scholar
  5. Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: Characterizing general patterns using meta-analysis. Am Nat 175:481–493CrossRefGoogle Scholar
  6. Bennett RN, Wallsgrove RM (2006) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633CrossRefGoogle Scholar
  7. Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259CrossRefGoogle Scholar
  8. Chassot C, Nawrath C, Métraux JP (2008) The cuticle: Not only a barrier for plant defence: A novel defence syndrome in plants with cuticular defects. Plant Signal Behav 3:142–144CrossRefGoogle Scholar
  9. Chen YZ, Huang SQ (2013) Red young leaves have less mechanical defence than green young leaves. Oikos 122:1035–1041CrossRefGoogle Scholar
  10. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Systemat 27:305–335CrossRefGoogle Scholar
  11. Dalin P, Björkman C (2003) Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia 134:112–118CrossRefGoogle Scholar
  12. Davidson DW (1993) The effects of herbivory and granivory on terrestrial plant succession. Oikos 68:23–35CrossRefGoogle Scholar
  13. Eichenberg D, Purschke O, Ristok C, Wessjohann L, Bruelheide H (2015) Trade-offs between physical and chemical carbon-based leaf defence: of intraspecific variation and trait evolution. J Ecol 103:1667–1679CrossRefGoogle Scholar
  14. Erickson AA, Bell SS, Dawes CJ (2004) Does mangrove leaf chemistry help explain crab herbivory patterns? Biotropica 36:333–343Google Scholar
  15. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol 57:761–780CrossRefGoogle Scholar
  16. Guo Q (2003) Temporal species richness-biomass relationships along successional gradients. J Veg Sci 14:121–128CrossRefGoogle Scholar
  17. Gutschick VP (1999) Biotic and abiotic consequences of differences in leaf structure. New Phytol 143:3–18CrossRefGoogle Scholar
  18. Gutterman Y, Chauser-Volfson E (2000) The distribution of the phenolic metabolites barbaloin, aloeresin and aloenin as a peripheral defense strategy in the succulent leaf parts of aloe arborescens. Biochem Syst Ecol 28:825–838CrossRefGoogle Scholar
  19. Hakes AS, Cronin JT (2011) Environmental heterogeneity and spatiotemporal variability in plant defense traits. Oikos 120:452–462CrossRefGoogle Scholar
  20. Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol 8:157–178CrossRefGoogle Scholar
  21. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272CrossRefGoogle Scholar
  22. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  23. Iii FSC, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92CrossRefGoogle Scholar
  24. Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176CrossRefGoogle Scholar
  25. Kirkwood RC (1999) Recent developments in our understanding of the plant cuticle as a barrier to the foliar uptake of pesticides. J Pestic Sci 55:69–77CrossRefGoogle Scholar
  26. Kursar TA, Coley PD (1992) Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24:256–262CrossRefGoogle Scholar
  27. Lamont BB, Groom PK, Cowling RM (2002) High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentrations. Funct Ecol 16:403–412CrossRefGoogle Scholar
  28. Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17CrossRefGoogle Scholar
  29. Lee DW, Gould KS (2002) Anthocyanins in leaves and other vegetative organs: An introduction. Adv Bot Res 37:1–16CrossRefGoogle Scholar
  30. Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15CrossRefGoogle Scholar
  31. Liu J, Yan HF, Newmaster SG, Pei N, Ragupathy S, Ge XJ (2015) The use of DNA barcoding as a tool for the conservation biogeography of subtropical forests in China. Divers Distrib 21:188–199CrossRefGoogle Scholar
  32. Manetas Y, Drinia A, Petropoulou Y (2002) High contents of anthocyanins in young leaves are correlated with low pools of xanthophyll cycle components and low risk of photoinhibition. Photosynthetica 40:349–354CrossRefGoogle Scholar
  33. Manetas Y (2003) The importance of being hairy: The adverse effects of hair removal on stem photosynthesis of verbascum speciosum are due to solar UV-B radiation. New Phytol 158:503–508CrossRefGoogle Scholar
  34. Martin JT (2003) Role of cuticle in the defense against plant disease. Annu Rev Phytopathol 2:81–100CrossRefGoogle Scholar
  35. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  36. Moles AT, Bonser SP, Poore AG, Wallis IR, Foley WJ (2011) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25:380–388CrossRefGoogle Scholar
  37. Peng SL (1996) Community dynamics of lower subtropical forests. Science Press, BeijingGoogle Scholar
  38. Peng SL, Ren H (1998) The energy ecology study in sub-tropical forest ecosystem. China Meteorological Press, BeijingGoogle Scholar
  39. Pritsch C, Muehlbauer GJ, Bushnell WR, Somers DA, Vance CP (2000) Fungal development and induction of defense response genes during early infection of wheat spikes by fusarium graminearum. Mol Plant Microbe In 13:159–169CrossRefGoogle Scholar
  40. Raevel V, Violle C, Munoz F (2012) Mechanisms of ecological succession: Insights from plant functional strategies. Oikos 121:1761–1770CrossRefGoogle Scholar
  41. Sangoi L, Gracietti M, Rampazzo C, Bianchetti P (2002) Response of brazilian maize hybrids from different eras to changes in plant density. Field Crop Res 79:39–51CrossRefGoogle Scholar
  42. Schaefer HM, Wilkinson DM (2004) Red leaves, insects and coevolution: a red herring? Trends Ecol Evol 19:616–618CrossRefGoogle Scholar
  43. Serrano M, Coluccia F, Torres M, L'Haridon F, Métraux JP (2014) The cuticle and plant defense to pathogens. Front Plant Sci 5:274CrossRefGoogle Scholar
  44. Tattini M, Landi M, Brunetti C, Giordano C, Remorini D, Gould KS, Guidi L (2014) Epidermal coumaroyl anthocyanins protect sweet basil against excess light stress: multiple consequences of light attenuation. Physiol Plant 152:585–598CrossRefGoogle Scholar
  45. Wagner GJ (1991) Secreting glandular trichomes: More than just hairs. Plant Physiol 96:675–679CrossRefGoogle Scholar
  46. Woodman RL, Fernandes GW (1991) Differential mechanical defense : herbivory, evapotranspiration, and leaf-hairs. Oikos 60:11–19CrossRefGoogle Scholar
  47. Wu F, Yu Y, Sun J, Zhang J, Wang J, Tang G, Wang Y (2016) Characteristics, source apportionment and reactivity of ambient volatile organic compounds at Dinghu mountain in Guangdong Province, China. Sci Total Environ 548:347–359CrossRefGoogle Scholar
  48. Zhou G, Guan L, Wei X, Zhang D, Zhang Q, Yan J, Wen D, Liu J, Liu S, Huang Z (2007) Litterfall production along successional and altitudinal gradients of subtropical monsoon evergreen broadleaved forests in Guangdong, China. Plant Ecol 188:77–89CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Taotao Han
    • 1
    • 2
  • Jun Wang
    • 1
  • Hai Ren
    • 1
    Email author
  • Huilin Yi
    • 1
  • Qianmei Zhang
    • 1
  • Qinfeng Guo
    • 3
  1. 1.Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Eastern Forest Environmental Threat Assessment CenterUSDA Forest ServiceResearch Triangle ParkUSA

Personalised recommendations