Weak co-ordination between vein and stomatal densities in 105 angiosperm tree species along altitudinal gradients in Southwest China
Wan-Li Zhao A B , Ya-Jun Chen B , Timothy J. Brodribb C and Kun-Fang Cao D E
+ Author Affiliations
- Author Affiliations
A School of Life Sciences, University of Science and Technology of China, Hefei, Anhui Province, 230 026, China.
B Key Laboratory of Tropical Forest Ecology, XishuangbannaTropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan Province, 666 303, China.
C School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.
D Plant Ecophysiology and Evolution Group, State Key Laboratory for Conservation and Utilisation of Subtropical Agro-Bioresources, and College of Forestry, Guangxi University, Nanning, Guangxi, 530 004, China.
E Corresponding author. Email: kunfangcao@gxu.edu.cn
Functional Plant Biology 43(12) 1126-1133 https://doi.org/10.1071/FP16012
Submitted: 12 January 2016 Accepted: 29 July 2016 Published: 31 August 2016
Abstract
Leaf-level water balance, as revealed by a correlation between stomatal density (SD) and vein density (VD), has been reported in some plants. However, the generality of this correlation and how it may be affected by altitude changes are unclear. Here, we investigated whether this balance is maintained across tree species of diverse families along a large altitudinal gradient. We measured leaf area (LA), SD, stomata length (SL), and VD in 105 angiosperm species across two altitudinal ranges, 800–1400 m above sea level (a.s.l.) in tropical montane forests (TMF) and 2000–2600 m a.s.l. in subtropical montane forests (SMF) in Yunnan, South-west China. The average SD was independent of altitude in both regions. Similarly, the average VD within either SMF or TMF was also not significantly different. However, overall, TMF had significantly larger VD and LA but smaller SL than SMF. Vein density was positively correlated with SD across SMF species, with a weaker correlation for TMF species and all species combined. Stomatal length was negatively correlated with SD and VD across all species. Our results extend the leaf water balance theory to diverse angiosperm tree species, and indicate decoupled adaptation of SD and VD in these species along a large altitudinal gradient.
Additional keywords: minor vein density, stomata density, subtropical forests, tropical forests.
References
Blonder B, Enquist BJ (2014) Inferring climate from angiosperm leaf venation networks. New Phytologist 204, 116–126.| Inferring climate from angiosperm leaf venation networks.Crossref | GoogleScholarGoogle Scholar | 24725225PubMed |
Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. Plant Physiology 150, 1083–1092.
| Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleiu74%3D&md5=83c1acbb4c9c4c81b3ec15cef208cb5aCAS | 19363093PubMed |
Boyce CK (2009) Seeing the forest with the leaves – clues to canopy placement from leaf fossil size and venation characteristics. Geobiology 7, 192–199.
| Seeing the forest with the leaves – clues to canopy placement from leaf fossil size and venation characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3ltV2nsw%3D%3D&md5=ed1093d7eafb330547640b927100990eCAS | 19207570PubMed |
Bresson CC, Vitasse Y, Kremer A, Delzon S (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiology 31, 1164–1174.
| To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1ymsrs%3D&md5=78d6cf86a872f47dc66c208d9ab4b0dcCAS | 21908436PubMed |
Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175–183.
| Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification.Crossref | GoogleScholarGoogle Scholar | 19968696PubMed |
Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192, 437–448.
| Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees.Crossref | GoogleScholarGoogle Scholar | 21679190PubMed |
Brodribb TJ, Holbrook NM, Gutierrez MV (2002) Hydraulic and photosynthetic coordination in seasonally dry tropical forest trees. Plant, Cell & Environment 25, 1435–1444.
| Hydraulic and photosynthetic coordination in seasonally dry tropical forest trees.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=52674169ae1dca1c088306428cad4fedCAS | 17556506PubMed |
Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit co-ordinated leaf evolution. New Phytologist 199, 559–570.
| Unified changes in cell size permit co-ordinated leaf evolution.Crossref | GoogleScholarGoogle Scholar | 23647069PubMed |
Cao M, Zhang JH, Feng ZL, Deng JW, Deng XB (1996) Tree species composition of a seasonal rain forest in Xishuangbanna, Southwest China. Tropical Ecology 37, 183–192.
Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
| Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2013) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant, Cell & Environment 37, 124–131.
| Acclimation to humidity modifies the link between leaf size and the density of veins and stomata.Crossref | GoogleScholarGoogle Scholar |
Cheng JG, Wang XF, Fan LZ, Yang XP, Yang PW (2009) Variations of Yunnan climatic zones in recent 50 years. Progress in Geography 28, 18–24.
Ding LZ, Chen YJ, Zhang JL (2014) Leaf traits and their associations among liana species in tropical rainforest. Plant Science Journal 32, 362–370. [In Chinese]
Fanourakis D, Carvalho SM, Almeida DP, Heuvelink E (2011) Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning. Physiologia Plantarum 142, 274–286.
| Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1Cmsrc%3D&md5=841b4d7c3b05a5eafefde68019d7a287CAS | 21457269PubMed |
Fukami T, Wardle DA (2005) Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proceedings of the Royal Society of London B: Biological Sciences 272, 2105–2115.
| Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients.Crossref | GoogleScholarGoogle Scholar |
Grytnes JA, Vetaas OR (2002) Species richness and altitude: a comparison between null models and interpolated plant species richness along the Himalayan altitudinal gradient, Nepal. American Naturalist 159, 294–304.
| Species richness and altitude: a comparison between null models and interpolated plant species richness along the Himalayan altitudinal gradient, Nepal.Crossref | GoogleScholarGoogle Scholar | 18707381PubMed |
Gupta B (1961a) Correlation of tissues in leaves 1. Absolute vein-islet numbers and absolute veinlet termination numbers. Annals of Botany 25, 65–70.
Gupta B (1961b) Correlation of tissues in leaves 2. Absolute stomatal numbers. Annals of Botany 25, 71–77.
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
| The role of stomata in sensing and driving environmental change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsV2isLw%3D&md5=6106f4f30e8835ea45381b408dd74101CAS | 12931178PubMed |
Holland N, Richardson AD (2009) Stomatal length correlates with elevation of growth in four temperate species. Journal of Sustainable Forestry 28, 63–73.
| Stomatal length correlates with elevation of growth in four temperate species.Crossref | GoogleScholarGoogle Scholar |
Hovenden MJ, Vander Schoor JK, Osanai Y (2012) Relative humidity has dramatic impacts on leaf morphology but little effect on stomatal index or density in Nothofagus cunninghamii. (Nothofagaceae). Australian Journal of Botany 60, 700–706.
| Relative humidity has dramatic impacts on leaf morphology but little effect on stomatal index or density in Nothofagus cunninghamii. (Nothofagaceae).Crossref | GoogleScholarGoogle Scholar |
Hu J, Yang QY, Huang W, Zhang SB, Hu H (2014) Effects of temperature on leaf hydraulic architecture of tobacco plants. Planta 240, 489–496.
| Effects of temperature on leaf hydraulic architecture of tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVejsb8%3D&md5=295032226574b95341663882a0fcdeb0CAS | 24915747PubMed |
Körner C (2007) The use of ‘altitude’ in ecological research. Trends in Ecology & Evolution 22, 569–574.
| The use of ‘altitude’ in ecological research.Crossref | GoogleScholarGoogle Scholar |
Kouwenberg LL, Kürschner WM, McElwain JC (2007) Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry. Reviews in Mineralogy and Geochemistry 66, 215–241.
| Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaksLfK&md5=23202182e28ef8f501139353190139a8CAS |
Li D, Tang JW, Luo CK, Li JS, Liu ZA (2006) The community characteristics of monsoon evergreen broad-leaved forest in Xishuangbanna. Journal of Mountain Science 24, 257–267. [In Chinese]
Medek DE, Evans JR, Schortemeyer M, Ball MC (2011) Effects of growth temperature on photosynthetic gas exchange characteristics and hydraulic anatomy in leaves of two cold-climate Poa species. Functional Plant Biology 38, 54–62.
| Effects of growth temperature on photosynthetic gas exchange characteristics and hydraulic anatomy in leaves of two cold-climate Poa species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFynurvP&md5=c85121585bf44687a97dcfe800a65534CAS |
Niklas KJ (1999) A mechanical perspective on foliage leaf form and function. New Phytologist 143, 19–31.
| A mechanical perspective on foliage leaf form and function.Crossref | GoogleScholarGoogle Scholar |
Pyykkö M (1979) Morphology and anatomy of leaves from some woody plants in a humid tropical forest of Venezuelan Guayana. Acta Botanica Fennica 112, 1–41.
Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ (2014) Convergent effects of elevation on functional leaf traits within and among species. Functional Ecology 28, 37–45.
| Convergent effects of elevation on functional leaf traits within and among species.Crossref | GoogleScholarGoogle Scholar |
Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ (2010) Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest. American Journal of Botany 97, 1109–1120.
| Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest.Crossref | GoogleScholarGoogle Scholar | 21616863PubMed |
Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983–1000.
| Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future.Crossref | GoogleScholarGoogle Scholar | 23600478PubMed |
Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM (2008) Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proceedings of the National Academy of Sciences of the United States of America 105, 1567–1572.
| Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvFCitLY%3D&md5=67e61fd1fed669ac0ee58be7bc0b3204CAS | 18227511PubMed |
Schoettle AW, Rochelle S (2000) Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations. American Journal of Botany 87, 1797–1806.
| Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MngtlSjsQ%3D%3D&md5=b48bbb12a5d236f9e31943d6d35e0c1dCAS | 11118417PubMed |
Sun M, Yang SJ, Zhang JL, Bartlett M, Zhang SB (2014) Correlated evolution in traits influencing leaf water balance in Dendrobium (Orchidaceae). Plant Ecology 215, 1255–1267.
| Correlated evolution in traits influencing leaf water balance in Dendrobium (Orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Sun M, Su T, Zhang SB, Li SF, Anberree-Lebreton J, Zhou ZK (2016) Variations in leaf morphological traits of Quercus guyavifolia (Fagaceae) were mainly influenced by water and ultraviolet irradiation at high elevations on the Qinghai–Tibet plateau, China. International Journal of Agriculture and Biology 18, 266–273.
| Variations in leaf morphological traits of Quercus guyavifolia (Fagaceae) were mainly influenced by water and ultraviolet irradiation at high elevations on the Qinghai–Tibet plateau, China.Crossref | GoogleScholarGoogle Scholar |
Torre S, Fjeld T, Gislerød HR, Moe R (2003) Leaf anatomy and stomatal morphology of greenhouse roses grown at moderate or high air humidity. Journal of the American Society for Horticultural Science 128, 598–602.
Uhl D, Mosbrugger V (1999) Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography, Palaeoclimatology, Palaeoecology 149, 15–26.
| Leaf venation density as a climate and environmental proxy: a critical review and new data.Crossref | GoogleScholarGoogle Scholar |
Wang R, Yu G, He N, Wang Q, Xia F, Zhao N, Xu Z, Ge J (2014) Elevation-related variation in leaf stomatal traits as a function of plant functional type: evidence from Changbai Mountain, China. PLoS One 9, e115395
| Elevation-related variation in leaf stomatal traits as a function of plant functional type: evidence from Changbai Mountain, China.Crossref | GoogleScholarGoogle Scholar | 25517967PubMed |
Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiology 32, 1066–1081.
| Sunflecks in trees and forests: from photosynthetic physiology to global change biology.Crossref | GoogleScholarGoogle Scholar | 22887371PubMed |
Woodward F (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327, 617–618.
| Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels.Crossref | GoogleScholarGoogle Scholar |
Yang GP, Zheng Z, Zhang YP, Liu YH, Gong HD, Lu ZY (2010) The community ecological characteristics of mid-montane moist evergreen broad-leaved forest in Ailao Mountain. Journal of Northeast Forestry University 38, 16–19. [In Chinese]
Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF, Hu H (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS One 7, e40080
| Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVaitrc%3D&md5=b58812e9365f358f8b97b84c0987c4ccCAS | 22768224PubMed |
Zhang YJ, Yang QY, Lee DW, Goldstein G, Cao KF (2013) Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests. Oecologia 173, 721–730.
| Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests.Crossref | GoogleScholarGoogle Scholar | 23636462PubMed |
Zhang Y, Yang SJ, Sun M, Cao KF (2014) Stomatal traits are evolutionarily associated with vein density in basal angiosperms. Plant Science Journal 32, 320–328. [In Chinese]
Zhang SB, Dai Y, Hao GY, Li JW, Fu XW, Zhang JL (2015) Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species. Frontiers in Plant Science 6, 260
| Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species.Crossref | GoogleScholarGoogle Scholar | 25954289PubMed |
Zhou YM, Schaub M, Shi LX, Guo ZL, Fan AA, Yan CF, Wang XJ, Wang CG, Han SJ, Li MH (2012) Non-linear response of stomata in Pinus koraiensis to tree age and elevation. Trees 26, 1389–1396.
| Non-linear response of stomata in Pinus koraiensis to tree age and elevation.Crossref | GoogleScholarGoogle Scholar |
Zhu H (2008) The tropical flora of Southern Yunnan, china, and its biogeographic affinities. Annals of the Missouri Botanical Garden 95, 661–680.
| The tropical flora of Southern Yunnan, china, and its biogeographic affinities.Crossref | GoogleScholarGoogle Scholar |
Zhu YH, Kang HZ, Xie Q, Wang Z, Yin S, Liu CJ (2012) Pattern of leaf vein density and climate relationship of Quercus variabilis populations remains unchanged with environmental changes. Trees 26, 597–607.
| Pattern of leaf vein density and climate relationship of Quercus variabilis populations remains unchanged with environmental changes.Crossref | GoogleScholarGoogle Scholar |
