Chinese Science Bulletin

, Volume 59, Issue 3, pp 310–319 | Cite as

Evolution of stomatal and trichome density of the Quercus delavayi complex since the late Miocene

  • Qian Hu
  • Yaowu XingEmail author
  • Jinjin Hu
  • Yongjiang Huang
  • Hongjie Ma
  • Zhekun ZhouEmail author
Article Evolution


A fossil oak species, Quercus tenuipilosa Q. Hu et Z.K. Zhou, is reported from the upper Pliocene Ciying Formation in Kunming, Yunnan Province, southwestern China. The establishment of this species is based on detailed morphologic and cuticular investigations. The fossil leaves are elliptic, with serrate margins on the apical half. The primary venation is pinnate, and the major secondary venation is craspedodromous. The tertiary veins are opposite or alternate-opposite percurrent with two branches. The stomata are anomocytic, occurring only on the abaxial epidermis. The trichome bases are unicellular or multicellular. The new fossil species shows the closest affinity with the extant Q. delavayi and the late Miocene Q. praedelavayi Y.W. Xing et Z.K. Zhou from the Xiaolongtan Formation of the Yunnan Province. All three species share similar leaf morphology, but differ with respect to trichome base and stomatal densities. Q. tenuipilosa, Q. praedelavayi, and Q. delavayi can be considered to constitute the Q. delavayi complex. Since the late Miocene, a gradual reduction in trichome base density has occurred in this complex. This trend is the opposite of that of precipitation, indicating that increased trichome density is not an adaptation to dry environments. The stomatal density (SD) of the Q. delavayi complex was the highest during the late Miocene, declined in the late Pliocene, and then increased during the present epoch. These values show an inverse relationship with atmospheric CO2 concentrations, suggesting that the SD of the Q. delavayi complex may be a useful proxy for reconstruction of paleo-CO2 concentrations.


Quercus delavayi complex Quercus tenuipilosa Morphology evolution Neogene CO2 concentration 



We thank Dr. Frédéric M.B. Jacques for naming the new species, Mr. Guy Atchison for English phrasing, and Dr. Tao Su and Mr. Haobo Wang for their constructive suggestions and help during the field work. This work was supported by the National Basic Research Program of China (2012CB821901), the National Natural Science Foundation of China (41030212) to Zhekun Zhou.


  1. 1.
    Axsmith BJ, Jacobs BF (2005) The conifer Frenelopsis ramosissima (Cheirolepidiaceae) in the lower cretaceous of texas: systematic, biogeographical, and paleoecological implications. Int J Plant Sci 166:327–337CrossRefGoogle Scholar
  2. 2.
    Kunzmann L, Mohr BA, Bernardes-de-Oliveira ME et al (2006) Gymnosperms from the early Cretaceous Crato Formation (Brazil). II. Cheirolepidiaceae. Foss Rec 9:213–222CrossRefGoogle Scholar
  3. 3.
    Stace CA (1965) Cuticular studies as an aid to plant taxonomy. Bull Brit Mus (Nat Hist) Bot 4:3–78Google Scholar
  4. 4.
    Beerling DJ, Chaloner WG (1993) The impact of atmospheric CO2 and temperature changes on stomatal density: observation from Quercus robur lammas leaves. Ann Bot 71:231–235CrossRefGoogle Scholar
  5. 5.
    McElwain JC, Chaloner WG (1996) The fossil cuticle as a skeletal record of environmental change. Palaios 11:376–388CrossRefGoogle Scholar
  6. 6.
    Sun BN, Yan DF, Xie SP et al (2009) General discussion on cuticles of fossil plants in China. Acta Palaeontol Sin 3:347–356Google Scholar
  7. 7.
    Beerling D, Woodward F (1995) Stomatal responses of variegated leaves to CO2 enrichment. Ann Bot 75:507–511CrossRefGoogle Scholar
  8. 8.
    Kouwenberg LL, Kürschner WM, McElwain JC (2007) Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry. Rev Miner Geochem 66:215–241CrossRefGoogle Scholar
  9. 9.
    Zhou ZK, Hu JJ, Su T, et al (2011) Changes in stomatal frequency in two oaks along an elevation gradients in the Himalayas. In: Proceedings of the XVIII international botanical congress, MelbourneGoogle Scholar
  10. 10.
    Hu JJ, Zhou ZK (2012) The relationship between stomatal frequency and atmospheric pCO2 of Quercus pannosa and its application to paleoelevation reconstruction. Jpn J Palynol 58:91–92Google Scholar
  11. 11.
    Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347CrossRefGoogle Scholar
  12. 12.
    Hsu Y, Jen H (1976) The classification and distribution of Fagaceae of Yunnan Province (II). Acta Phytotax Sin 14:84–85Google Scholar
  13. 13.
    Zhou ZK (1993) Geographical distribution of Quercus from China. J Grad School Acad Sin 10:95–102Google Scholar
  14. 14.
    Huang C, Zhang Y, Bartholomew B (1999) Fagaceae. Flora China 4:314–400Google Scholar
  15. 15.
    Luo Y, Zhou ZK (2001) Phytogeography of Quercus subg Cyclobalanopsis. Acta Bot Yunnan 23:1–16Google Scholar
  16. 16.
    The Writing Group of Cenozoic Plants of China (1978) Cenozoic plants from China. Science Press, BeijingGoogle Scholar
  17. 17.
    Zhou ZK (1993) The fossil history of Quercus. Acta Bot Yunnan 15:21–33Google Scholar
  18. 18.
    Ge HR, Li DY (1999) Cenozoic coal-bearing basins and coal-forming regularity in West Yunnan. Yunnan Science and Technology Press, Kunming, pp 20–85Google Scholar
  19. 19.
    Xing YW, Hu JJ, Jacques FMB et al (2013) A new Quercus species from the Upper Miocene of southwestern China and its ecological significance. Rev Palaeobot Palynol 193:99–109CrossRefGoogle Scholar
  20. 20.
    Wen WW (2011) Nine fossil plants of Fagaeeae from the Pliocene in Baoshan, Yunnan and paleoenvironmental analysis. Master’s Thesis, Lanzhou University, LanzhouGoogle Scholar
  21. 21.
    Geological Bureau of Yunnan. Geological survey of Qujing area, 1:200000 sheet. 1978Google Scholar
  22. 22.
    Compiling Group of Regional Stratigraphic Scale of Yunnan (1978) Regional stratigraphic scale of southwest China: Yunnan Province. Geological Publishing House, BeijingGoogle Scholar
  23. 23.
    Bureau of Geology (1990) Regional geology of Yunnan province (in Chinese). Geological Publishing House, BeijingGoogle Scholar
  24. 24.
    Jiang CS, Zhou RQ, Hu YX (2003) Features of geological structure for Kunming basin. J Seismol Res 1:009Google Scholar
  25. 25.
    Ye MN (1981) On the preparation methods of fossil cuticle. In: proceedings of the selected papers of the 12th annual conference of the palaeontogical society of China. Science Press, BeijingGoogle Scholar
  26. 26.
    Leng Q (2000) An effective method of observing fine venation from compressed angiosperm fossil leaves. Acta Palaeontol Sin 39:158–159Google Scholar
  27. 27.
    Ma QW, Zhang XS, Li FL (2005) Methods of maceration and microscopical analysis on cuticle. Bull Bot Res 25:307–310Google Scholar
  28. 28.
    Hickey LJ, Wolfe JA (1975) The bases of angiosperm phylogeny: vegetative morphology. Ann Mo Bot Garden 62:538–589CrossRefGoogle Scholar
  29. 29.
    Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338Google Scholar
  30. 30.
    Anderson MJ (2003) PCO: A fortran computer program for principal coordinate analysis. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  31. 31.
    Kovach WL (1998) MVSP: a multivariate statistical package for windows, ver. 3.0. Kovach Computing Services, Pentraeth, Wales. ver.3.0Google Scholar
  32. 32.
    Dilcher DL (1974) Approaches to the identification of angiosperm leaf remains. Bot Rev 40:1–157CrossRefGoogle Scholar
  33. 33.
    Luo Y, Zhou ZK (2002) Leaf architecture in Quercus subgenus Cyclobalanopsis (Fagaceae) from China. Bot J Linn Soc 140:283–295CrossRefGoogle Scholar
  34. 34.
    Ellis B, Daly DC, Hickey LJ et al (2009) Manual of leaf architecture. Cornell University Press, IthacaGoogle Scholar
  35. 35.
    Jones JH (1986) Evolution of the fagaceae: the implications of foliar features. Ann Mo Bot Garden 73:228–275CrossRefGoogle Scholar
  36. 36.
    Deng M (2007) Anatomy, taxonomy, distribution, and phylogeny of Quercus subgenus Cyclobalanopsis (Oersted) Schneid. (Fagaceae). Doctor Thesis, Chinese Academy of Sciences, KunmingGoogle Scholar
  37. 37.
    Jia H, Sun BN, Li XC et al (2009) Microstructures of one species of Quercus from the Neogene in eastern Zhejiang and its palaeo-environmental indication. Earth Sci Front 16:79–90Google Scholar
  38. 38.
    Wuenscher JE (1970) The effect of leaf hairs of verbascum thapsus on leaf energy exchange. New Phytol 69:65–73CrossRefGoogle Scholar
  39. 39.
    Aronne G, De Micco V (2001) Seasonal dimorphism in the mediterranean Cistus incanus L. subsp. incanus Ann Bot 87:789–794CrossRefGoogle Scholar
  40. 40.
    Wu JY (2009) The Pliocene Tuantian flora of Tengchong, Yunnan province and its paleoenvironmental analysis. Doctor Thesis, Lanzhou University, Lanzhou, p 1–119Google Scholar
  41. 41.
    Haworth M, McElwain J (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeogr Palaeoclimatol Palaeoecol 262:79–90CrossRefGoogle Scholar
  42. 42.
    McGuire R, Agrawal A (2005) Trade-offs between the shade-avoidance response and plant resistance to herbivores? Tests with mutant cucumis sativus. Funct Ecol 19:1025–1031CrossRefGoogle Scholar
  43. 43.
    Hardin JW (1979) Patterns of variation in foliar trichomes of eastern North American Quercus. Am J Bot 66:576–585CrossRefGoogle Scholar
  44. 44.
    Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15CrossRefGoogle Scholar
  45. 45.
    Xia K, Su T, Liu Y-SC et al (2009) Quantitative climate reconstructions of the Late Miocene Xiaolongtan megaflora from Yunnan, southwest China. Palaeogeogr Palaeoclimatol Palaeoecol 276:80–86CrossRefGoogle Scholar
  46. 46.
    Jacques F, Guo SX, Su T et al (2011) Quantitative reconstruction of the late Miocene monsoon climates of southwest China: a case study of the Lincang flora from Yunnan Province. Palaeogeogr Palaeoclimatol Palaeoecol 304:318–327CrossRefGoogle Scholar
  47. 47.
    Xu JX (2002) Palynology, paleovegetation and paleoclimate of Neogene, central-western Yunnan, China. Doctor Thesis, Chinese Academy of Sciences, BeijingGoogle Scholar
  48. 48.
    Xing YW, Utescher T, Jacques FMB et al (2012) Paleoclimatic estimation reveals a weak winter monsoon in southwestern China during the late Miocene: evidence from plant macrofossils. Palaeogeogr Palaeoclimatol Palaeoecol 358–360:19–26CrossRefGoogle Scholar
  49. 49.
    Li WY, Wu XF (1978) A palynological investigation on the late tertiary and early quarternary and its significance in the paleo-geographical study in central Yunnan. Acta Geograph Sin 33:142–155Google Scholar
  50. 50.
    Su T (2010) On the establishment of the leaf physiognomy-climate model and a study of the late Pliocene Yangjie flora, southwest China. Doctor Thesis, Graduate School of the Chinese Academy of Science, BeijingGoogle Scholar
  51. 51.
    Huang YJ (2012) The late Pliocene Fudong flora from lanping, Yunnan, and the Neogene climates in Hengduan mountains. Doctor Thesis, Graduate School of the Chinese Academy of Science, BeijingGoogle Scholar
  52. 52.
    Ehleringer JR (1988) Changes in leaf characteristics of species along elevational gradients in the Wasatch Front, Utah. Am J Bot 75:680–689CrossRefGoogle Scholar
  53. 53.
    Haworth M, Heath J, McElwain JC (2010) Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers. Ann Bot 105:411–418CrossRefGoogle Scholar
  54. 54.
    Woodward F (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618CrossRefGoogle Scholar
  55. 55.
    Woodward F, Kelly C (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327CrossRefGoogle Scholar
  56. 56.
    Royer D (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114:1–28CrossRefGoogle Scholar
  57. 57.
    Beerling DJ, Royer DL (2011) Convergent cenozoic CO2 history. Nat Geosci 4:418–420CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Key Laboratory of Biogeography and Biodiversity, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  2. 2.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglaChina
  3. 3.Faculty of Land Resource EngineeringKunming University of Science and TechnologyKunmingChina
  4. 4.Institute of Systematic BotanyUniversity of ZürichZürichSwitzerland
  5. 5.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations