, Volume 184, Issue 3, pp 609–621 | Cite as

Xeromorphic traits help to maintain photosynthesis in the perhumid climate of a Taiwanese cloud forest

  • Shyam Pariyar
  • Shih-Chieh Chang
  • Daniel Zinsmeister
  • Haiyang Zhou
  • David A. Grantz
  • Mauricio Hunsche
  • Juergen BurkhardtEmail author
Physiological ecology - original research


Previous flux measurements in the perhumid cloud forest of northeastern Taiwan have shown efficient photosynthesis of the endemic tree species Chamaecyparis obtusa var. formosana even under foggy conditions in which leaf surface moisture would be expected. We hypothesized this to be the result of ‘xeromorphic’ traits of the Chamaecyparis leaves (hydrophobicity, stomatal crypts, stomatal clustering), which could prevent coverage of stomata by precipitation, fog, and condensation, thereby maintaining CO2 uptake. Here we studied the amount, distribution, and composition of moisture accumulated on Chamaecyparis leaf surfaces in situ in the cloud forest. We studied the effect of surface tension on gas penetration to stomata using optical O2 microelectrodes in the laboratory. We captured the dynamics of condensation to the leaf surfaces with an environmental scanning electron microscope (ESEM). In spite of substantial surface hydrophobicity, the mean water film thickness on branchlets under foggy conditions was 80 µm (upper surface) and 40 µm (lower surface). This amount of water could cover stomata and prevent CO2 uptake. This is avoided by the clustered arrangement of stomata within narrow clefts and the presence of Florin rings. These features keep stomatal pores free from water due to surface tension and provide efficient separation of plant and atmosphere in this perhumid environment. Air pollutants, particularly hygroscopic aerosol, may disturb this functionality by enhancing condensation and reducing the surface tension of leaf surface water.


Fog Clustered stomata Gas exchange LMA ESEM Xeromorphism 



This work was supported by Deutscher Akademischer Austauschdienst (DAAD 56186816), Germany, Taiwan Ministry of Science and Technology (MOST: 102-2911-I-259-502) and Deutsche Forschungsgemeinschaft (BU 1099/7-1, 7-2). We thank Knut Wichterich for his help with the ESEM measurements, I-Ling Lai for advice.

Author contribution statement

SP, S-CC, and JB designed the study, SP, S-CC, DZ, and JB performed the field experiments, SP, MH, and JB designed and performed the ESEM studies, SP, DZ, HZ, and JB performed the O2 measurements, SP performed the statistical analysis, and SP, DZ, DAG, and JB performed the lab analysis and wrote the manuscript, with revision by all authors.

Supplementary material

442_2017_3894_MOESM1_ESM.docx (946 kb)
Supplementary material 1 (DOCX 947 kb)

Supplementary material 2 (MPG 2544 kb)

Supplementary material 3 (MPG 7822 kb)

Supplementary material 4 (MPG 1730 kb)

Supplementary material 5 (MPG 1732 kb)

442_2017_3894_MOESM6_ESM.avi (2.2 mb)
Supplementary material 6 (AVI 2204 kb)


  1. Aboal JR, Jimenez MS, Morales D, Gil P (2000) Effects of thinning on throughfall in Canary Islands pine forest—the role of fog. J Hydrol 238(3–4):218–230CrossRefGoogle Scholar
  2. Abramoff MD, Magalhães PJ, Ram SJ (2004) Image processing with image. J. Biophotonics Int 11(7):36–42Google Scholar
  3. Barthlott W, Schimmel T, Wiersch S, Koch K, Brede M, Barczewski M, Walheim S, Weis A, Kaltenmaier A, Leder A, Bohn HF (2010) The salvinia paradox: superhydrophobic surfaces with hydrophilic pins for air retention under water. Adv Mater 22(21):2325–2328CrossRefPubMedGoogle Scholar
  4. Beiderwieden E, Schmidt A, Hsia YJ, Chang SC, Wrzesinsky T, Klemm O (2007) Nutrient input through occult and wet deposition into a subtropical montane cloud forest. Water Air Soil Pollut 186(1–4):273–288CrossRefGoogle Scholar
  5. Berry ZC, Smith WK (2013) Ecophysiological importance of cloud immersion in a relic spruce-fir forest at elevational limits, southern Appalachian Mountains, USA. Oecologia 173(3):637–648CrossRefPubMedGoogle Scholar
  6. Berry ZC, Smith WK (2014) Experimental cloud immersion and foliar water uptake in saplings of Abies fraseri and Picea rubens. Trees-Struct Funct 28(1):115–123CrossRefGoogle Scholar
  7. Berry ZC, Johnson DM, Reinhardt K (2015) Vegetation-zonation patterns across a temperate mountain cloud forest ecotone are not explained by variation in hydraulic functioning or water relations. Tree Physiol 35(9):925–935CrossRefPubMedGoogle Scholar
  8. Brewer CA, Smith WK, Vogelmann TC (1991) Functional interaction between leaf trichomes, leaf wettability and the optical-properties of water droplets. Plant Cell Environ 14(9):955–962CrossRefGoogle Scholar
  9. Brodribb T, Hill RS (1997) Imbricacy and stomatal wax plugs reduce maximum leaf conductance in Southern Hemisphere conifers. Aust J Bot 45(4):657–668CrossRefGoogle Scholar
  10. Bruijnzeel LA, Kappelle M, Miulligan M, Scatena FN (2010) Tropical Monatane Cloud Forests: state of knowledge and sustainability perspectives in a changing world. In: Bruijnzeel LA, Scatena FN, Hamilton LS (eds) Tropical Monatane Cloud Forests: science for conservation and management. Cambridge University Press, Cambridge, pp 691–740Google Scholar
  11. Burgess SSO, Dawson TE (2004) The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant Cell Environ 27(8):1023–1034CrossRefGoogle Scholar
  12. Carpenter RJ, McLoughlin S, Hill RS, McNamara KJ, Jordan GJ (2014) Early evidence of xeromorphy in angiosperms: stomatal encryption in a new Eocene species in Banksia (Proteaceae) from western Australia. Am J Bot 101(9):1486–1497CrossRefPubMedGoogle Scholar
  13. Chang SC, Lai IL, Wu JT (2002) Estimation of fog deposition on epiphytic bryophytes in a subtropical montane forest ecosystem in northeastern Taiwan. Atmos Res 64(1–4):159–167CrossRefGoogle Scholar
  14. Chang SC, Yeh CF, Wu MJ, Hsia YJ, Wu JT (2006) Quantifying fog water deposition by in situ exposure experiments in a mountainous coniferous forest in Taiwan. For Ecol Manage 224(1–2):11–18CrossRefGoogle Scholar
  15. Chang S-C, Tseng K-H, Hsia Y-J, Wang C-P, Wu J-T (2008) Soil respiration in a subtropical montane cloud forest in Taiwan. Agric For Meteorol 148(5):788–798. doi: 10.1016/j.agrformet.2008.01.003 CrossRefGoogle Scholar
  16. Chu HS, Chang SC, Klemm O, Lai CW, Lin YZ, Wu CC, Lin JY, Jiang JY, Chen JQ, Gottgens JF, Hsia YJ (2014) Does canopy wetness matter? Evapotranspiration from a subtropical montane cloud forest in Taiwan. Hydrol Process 28(3):1190–1214CrossRefGoogle Scholar
  17. Colmer TD, Pedersen O (2008) Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O-2 exchange. N Phytol 177(4):918–926CrossRefGoogle Scholar
  18. Compton RH (1911) Xerophyly in the Coniferae and microphylly. N Phytol 10:100–105CrossRefGoogle Scholar
  19. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51(4):335–380CrossRefGoogle Scholar
  20. Cray JA, Russell JT, Timson DJ, Singhal RS, Hallsworth JE (2013) A universal measure of chaotropicity and kosmotropicity. Environ Microbiol 15(1):287–296CrossRefPubMedGoogle Scholar
  21. Dawson TE (1998) Fog in the California redwood forest: ecosystem inputs and use by plants. Oecologia 117(4):476–485CrossRefPubMedGoogle Scholar
  22. Deegan RD, Bakajin O, Dupont TF, Nagel SR, Witten TA (2000) Contact line deposits in an evaporating drop. Phys Rev E 62(1):756–765CrossRefGoogle Scholar
  23. Dörken VM, Parsons RF (2016) Morpho-anatomical studies on the change in the foliage of two imbricate-leaved New Zealand podocarps: Dacrycarpus dacrydioides and Dacrydium cupressinum. Plant Syst Evol 302(1):41–54CrossRefGoogle Scholar
  24. Dow GJ, Berry JA, Bergmann DC (2014) The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. N Phytol 201(4):1205–1217CrossRefGoogle Scholar
  25. Dutcher CS, Wexler AS, Clegg SL (2010) Surface tensions of inorganic multicomponent aqueous electrolyte solutions and melts. J Phys Chem A 114(46):12216–12230CrossRefPubMedGoogle Scholar
  26. Eiden R, Burkhardt J, Burkhardt O (1994) Atmospheric aerosol particles and their role in the formation of dew on the surface of plant leaves. J Aerosol Sci 25(2):367–376CrossRefGoogle Scholar
  27. Eller CB, Lima AL, Oliveira RS (2013) Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). N Phytol 199(1):151–162CrossRefGoogle Scholar
  28. Eller CB, Lima AL, Oliveira RS (2016) Cloud forest trees with higher foliar water uptake capacity and anisohydric behavior are more vulnerable to drought and climate change. N Phytol. doi: 10.1111/nph.13952 Google Scholar
  29. El-Madany TS, Walk JB, Deventer MJ, Degefie DT, Chang SC, Juang JY, Griessbaum F, Klemm O (2016) Canopy–atmosphere interactions under foggy condition: size-resolved fog droplet fluxes and their implications. J Geophys Res-Biogeosci 121(3):796–808CrossRefGoogle Scholar
  30. Emery NC (2016) Foliar uptake of fog in coastal California shrub species. Oecologia 182(3):731–742CrossRefPubMedGoogle Scholar
  31. Feild TS, Zwieniecki MA, Donoghue MJ, Holbrook NM (1998) Stomatal plugs of Drimys winteri (Winteraceae) protect leaves from mist but not drought. Proc Natl Acad Sci USA 95(24):14256–14259CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fiorin L, Brodribb TJ, Anfodillo T (2016) Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves. N Phytol 209(1):216–227CrossRefGoogle Scholar
  33. Florin R (1931) Untersuchungen zur Stammesgeschichte der Coniferales und Cordaitales. KungligaSvenska Vetenskapsakademiens Handlingar 10:1–588Google Scholar
  34. Haworth M, McElwain J (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeogr Palaeoclimatol Palaeoecol 262(1–2):79–90CrossRefGoogle Scholar
  35. Herzog M, Pedersen O (2014) Partial versus complete submergence: snorkelling aids root aeration in Rumex palustris but not in R. acetosa. Plant Cell Environ 37(10):2381–2390PubMedGoogle Scholar
  36. Holder CD (2007) Leaf water repellency as an adaptation to tropical montane cloud forest environments. Biotropica 39(6):767–770CrossRefGoogle Scholar
  37. Ishibashi M, Terashima I (1995) Effects of continuous leaf wetness on photosynthesis—adverse aspects of rainfall. Plant Cell Environ 18(4):431–438CrossRefGoogle Scholar
  38. Klemm O, Chang SC, Hsia Y (2006) Energy fluxes at a subtropical mountain cloud forest. For Ecol Manag 224(1–2):5–10CrossRefGoogle Scholar
  39. Lai IL, Scharr H, Chavarria-Krauser A, Kusters R, Wu JT, Chou CH, Schurr U, Walter A (2005) Leaf growth dynamics of two congener gymnosperm tree species reflect the heterogeneity of light intensities given in their natural ecological niche. Plant Cell Environ 28(12):1496–1505CrossRefGoogle Scholar
  40. Lai IL, Chang SC, Lin PH, Chou CH, Wu JT (2006) Climatic characteristics of the subtropical mountainous cloud forest at the Yuanyang lake long-term ecological research site. Taiwan. Taiwania 51(4):317–329Google Scholar
  41. Lai IL, Schroeder WH, Wu JT, Kuo-Huang LL, Mohl C, Chou CH (2007) Can fog contribute to the nutrition of Chamaecyparis obtusa var. formosana? Uptake of a fog solute tracer into foliage and transport to roots. Tree Physiol 27(7):1001–1009CrossRefPubMedGoogle Scholar
  42. Lakatos M, Obregon A, Büdel B, Bendix J (2012) Midday dew—an overlooked factor enhancing photosynthetic activity of corticolous epiphytes in a wet tropical rain forest. N Phytol 194(1):245–253CrossRefGoogle Scholar
  43. Lauridsen T, Glavina K, Colmer TD, Winkel A, Irvine S, Lefmann K, Feidenhans’l R, Pedersen O (2014) Visualisation by high resolution synchrotron X-ray phase contrast micro-tomography of gas films on submerged superhydrophobic leaves. J Struct Biol 188(1):61–70CrossRefPubMedGoogle Scholar
  44. Letts MG, Mulligan M (2005) The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest. J Trop Ecol 21:549–557CrossRefGoogle Scholar
  45. Li CF, Chytry M, Zeleny D, Chen MY, Chen TY, Chiou CR, Hsia YJ, Liu HY, Yang SZ, Yeh CL, Wang JC, Yu CF, Lai YJ, Chao WC, Hsieh CF (2013) Classification of Taiwan forest vegetation. Appl Veg Sci 16(4):698–719CrossRefGoogle Scholar
  46. Limm EB, Simonin KA, Bothman AG, Dawson TE (2009) Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161(3):449–459CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lin C-S, Lin Y-H, Wu J-T (2012) Biodiversity of the epiphyllous algae in a Chamaecyparis forest of northern Taiwan. Bot Stud 53(4):489–499Google Scholar
  48. Lin CY, Chua YJ, Sheng YF, Hsu HH, Cheng CT, Lin YY (2015) Altitudinal and latitudinal dependence of future warming in Taiwan simulated by WRF nested with ECHAM5/MPIOM. Int J Climatol 35(8):1800–1809CrossRefGoogle Scholar
  49. Marzol-Jaen MV (2010) Historical backgrounds of fog water collection studies in the Canary islands. In: Bruijnzeel LA, Scatena FN, Hamilton LS (eds) Tropical Monatane Cloud Forests: science for conservation and management. Cambridge University Press, Cambridge, pp 352–358Google Scholar
  50. Matos IS, Rosado BHP (2016) Retain or repel? Droplet volume does matter when measuring leaf wetness traits. Ann Bot 117(6):1045–1052CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mildenberger K, Beiderwieden E, Hsia YJ, Klemm O (2009) CO2 and water vapor fluxes above a subtropical mountain cloud forest—the effect of light conditions and fog. Agric For Meteorol 149(10):1730–1736CrossRefGoogle Scholar
  52. Oladele FA (1983) Scanning electron microscope study of stomatal-complex configuration in Cupressaceae. Can J Bot-Rev Canadienne De Botanique 61(4):1232–1240Google Scholar
  53. Pegram LM, Record MT (2007) Hofmeister salt effects on surface tension arise from partitioning of anions and cations between bulk water and the air-water interface. J Phys Chem B 111(19):5411–5417CrossRefPubMedGoogle Scholar
  54. Quere D (2008) Wetting and roughness. Annual review of materials research, Annual Reviews. Palo Alto, Santa Clara, pp 71–99Google Scholar
  55. Raskin I, Kende H (1983) How does deep-water rice solve its aeration problem. Plant Physiol 72(2):447–454CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rennert RJ (1903) The phyllodes of Oxypolis filiformis, a swamp xerophyte. Bull Torrey Bot Club 30(7):403–411CrossRefGoogle Scholar
  57. Rosado BHP, Oliveira RS, Aidar MPM (2010) Is leaf water repellency related to vapor pressure deficit and crown exposure in tropical forests? Acta Oecol-Int J Ecol 36(6):645–649CrossRefGoogle Scholar
  58. Roth-Nebelsick A, Fernandez V, Peguero-Pina JJ, Sancho-Knapik D, Gil-Pelegrin E (2013) Stomatal encryption by epicuticular waxes as a plastic trait modifying gas exchange in a Mediterranean evergreen species (Quercus coccifera L.). Plant Cell Environ 36(3):579–589CrossRefPubMedGoogle Scholar
  59. Sack L, Scoffoni C, PrometheusWiki contributors (2011) Minimum epidermal conductance (gmin, a.k.a. cuticular conductance),,+a.k.a.+cuticular+conductance) (Accessed April 2, 2017)
  60. Shields LM (1950) Leaf xeromorphy as related to physiological and structural influences. Bot Rev 16(8):399–447CrossRefGoogle Scholar
  61. Shiu CJ, Liu SC, Chen JP (2009) Diurnally asymmetric trends of temperature, humidity, and precipitation in Taiwan. J Clim 22(21):5635–5649CrossRefGoogle Scholar
  62. Simon S, Klemm O, El-Madany T, Walk J, Amelung K, Lin PH, Chang SC, Lin NH, Engling G, Hsu SC, Wey TH, Wang YN, Lee YC (2016) Chemical composition of fog water at four sites in Taiwan. Aerosol Air Qual Res 16(3):618–631CrossRefGoogle Scholar
  63. Still CJ, Foster PN, Schneider SH (1999) Simulating the effects of climate change on tropical montane cloud forests. Nature 398(6728):608–610CrossRefGoogle Scholar
  64. Stopes MC (1907) The “xerophytic” character of the gymnosperms. Is it an “ecological” adaptation? N Phytol 6(2):46–50CrossRefGoogle Scholar
  65. Voesenek L, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. N Phytol 206(1):57–73CrossRefGoogle Scholar
  66. Weathers KC (1999) The importance of cloud and fog in the maintenance of ecosystems. Trends Ecol Evol 14(6):214–215CrossRefPubMedGoogle Scholar
  67. Zhang D, Christian T (2013) Chamaecyparis obtusa var. formosana. In: The IUCN red list of threatened species 2013: e.T34076A2843748. doi: 10.2305/IUCN.UK.2013-1.RLTS.T34076A2843748.en
  68. Zobel BD, Lin DB, Liu VT (1978) Stomatal distribution on leaves of three species of Chamaecyparis. Taiwania 23:1–6Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institute of Crop Science and Resource ConservationUniversity of BonnBonnGermany
  2. 2.Department of Natural Resources and Environmental StudiesNational Dong Hwa UniversityHualienTaiwan
  3. 3.Key Laboratory of Agricultural Information Acquisition Technology, Ministry of Agriculture, College of Information and Electrical EngineeringChina Agricultural UniversityBeijingChina
  4. 4.Department of Botany and Plant Sciences, Kearney Agricultural CenterUniversity of California at RiversideParlierUSA

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