Contrasting altitudinal trends in leaf anatomy between three dominant species in an alpine meadow
Mengying Zhong A C , Xinqing Shao A D , Ruixin Wu B , Xiaoting Wei A , Richard S. P. van Logtestijn C and Johannes H. C. Cornelissen CA Grassland Science Department, College of Animal Science and Technology, China Agricultural University,No. 2 Yuanmingyuan West Road, Haidian District, 100193 Beijing, China.
B Dryland Farming Institute, Hebei Academy of Agricultural and Forestry Sciences, Taocheng District, 053000 Hebei, China.
C Department of Systems Ecology, Institute of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
D Corresponding author. Email: shaoxinqing@163.com
Australian Journal of Botany 66(5) 448-458 https://doi.org/10.1071/BT17247
Submitted: 14 December 2017 Accepted: 4 September 2018 Published: 19 September 2018
Abstract
Variation in leaf anatomical traits underpins the adaptations and phenotypic responses of plant species to their different natural environments. Temperature is a primary driver of plant trait variation along altitudinal gradients. However, other environmental drivers may also play important roles, and the interactions between drivers may have different effects on leaf anatomy for different species of the same larger clade. Such interactions might be especially important along shorter altitudinal (i.e. temperature) gradients. We predicted, therefore, that different monocot species could show idiosyncratic responses of leaf anatomical traits to a short altitudinal gradient. Moreover, for a species in which vegetative growth and reproduction are separated in time, its anatomical responses to altitude may differ and trade-offs between leaf and flowering stem anatomy may occur. To test these hypotheses, we examined leaf anatomy and δ13C signature (a possible indicator of anatomy-related water use efficiency or indicator of response to a decrease in CO2 concentration with altitude) of three dominant and widely distributed monocot species (Scirpus distigmaticus, Elymus nutans, Carex moorcroftii) from seven elevations in an alpine meadow on the Qinghai-Tibetan Plateau. In addition, we examined the flowering stem anatomy of S. distigmaticus, across a short altitudinal gradient (four elevations) in the same region. Leaf anatomical traits (e.g. epidermal cell area, epidermal cell thickness, cuticular layer thickness, xylem transect area, phloem transect area) varied with altitude, but the patterns varied substantially among species and among anatomical traits within species. Additionally, for S. distigmaticus, (allometric) coordination between leaves and flowering stems was apparent for xylem transect area and phloem transect area. Trade-offs between leaf and flowering stem traits were also found for epidermal cell area, epidermal cell thickness and mesophyll cell area. Leaves were more responsive to altitude in their anatomical traits than flowering stems in S. distigmaticus, perhaps reflecting their relatively short period of stem development during a climatically relatively favourable season compared with that for leaves, which already start growing earlier in the year. Further research is needed on the interactive effects of environmental variables, as well as vegetative versus reproductive phenology both across and within suites of species to better understand and upscale plant anatomical responses to climate warming in alpine environments.
Additional keywords: altitude, climate, functional traits, flowering stem anatomy, leaf anatomy, monocotyledons, mountain, stable carbon isotopes.
References
Castro-Díez P, Puyravaud JP, Cornelissen JHC (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124, 476–486.| Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types.Crossref | GoogleScholarGoogle Scholar |
Chapin FS, Bret‐Harte MS, Hobbie SE, Zhong H (1996) Plant functional types as predictors of transient responses of arctic vegetation to global change. Journal of Vegetation Science 7, 347–358.
| Plant functional types as predictors of transient responses of arctic vegetation to global change.Crossref | GoogleScholarGoogle Scholar |
Cresswell JE (1998) Stabilizing selection and the structural variability of flowers within species. Annals of Botany 81, 463–473.
| Stabilizing selection and the structural variability of flowers within species.Crossref | GoogleScholarGoogle Scholar |
Diaz HF, Grosjean M, Graumlich L (2003) Climate variability and change in high elevation regions: past, present and future. Climatic Change 59, 1–4.
| Climate variability and change in high elevation regions: past, present and future.Crossref | GoogleScholarGoogle Scholar |
Duncan RP (2013) Leaf morphology shift is not linked to climate change. Biology Letters 9, 1–2.
Farquhar G, O’Leary M, Berry J (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
| On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Fisher JB, Goldstein G, Jones TJ, Cordell S (2007) Wood vessel diameter is related to elevation and genotype in the Hawaiian tree Metrosideros polymorpha (Myrtaceae). American Journal of Botany 94, 709–715.
| Wood vessel diameter is related to elevation and genotype in the Hawaiian tree Metrosideros polymorpha (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Frei ER, Ghazoul J, Matter P, Heggli M, Pluess AR (2014) Plant population differentiation and climate change: responses of grassland species along an elevational gradient. Global Change Biology 20, 441–455.
| Plant population differentiation and climate change: responses of grassland species along an elevational gradient.Crossref | GoogleScholarGoogle Scholar |
Gratani L, Crescente MF, D’Amato V, Ricotta C, Frattaroli AR, Puglielli G (2014) Leaf traits variation in Sesleria nitida growing at different altitudes in the Central Apennines. Photosynthetica 52, 386–396.
| Leaf traits variation in Sesleria nitida growing at different altitudes in the Central Apennines.Crossref | GoogleScholarGoogle Scholar |
Guan ZJ, Zhang SB, Guan KY, Li SY, Hu H (2011) Leaf anatomical structures of Paphiopedilum and Cypripedium and their adaptive significance. Journal of Plant Research 124, 289–298.
| Leaf anatomical structures of Paphiopedilum and Cypripedium and their adaptive significance.Crossref | GoogleScholarGoogle Scholar |
Guerin GR, Wen H, Lowe AJ (2012) Leaf morphology shift linked to climate change. Biology Letters 8, 882–886.
| Leaf morphology shift linked to climate change.Crossref | GoogleScholarGoogle Scholar |
Hengxiao G, McMillin JD, Wagner MR, Zhou J, Zhou Z, Xu X (1999) Altitudinal variation in foliar chemistry and anatomy of yunnan pine, Pinus yunnanensis, and pine sawfly (Hym., Diprionidae) performance. Journal of Applied Entomology-Zeitschrift Fur Angewandte Entomologie 123, 465–471.
Hoffmann AA, Griffin PC, Macraild RD (2009) Morphological variation and floral abnormalities in a trigger plant across a narrow altitudinal gradient. Austral Ecology 34, 780–792.
| Morphological variation and floral abnormalities in a trigger plant across a narrow altitudinal gradient.Crossref | GoogleScholarGoogle Scholar |
Hölscher D, Schmitt S, Kupfer K (2002) Growth and leaf traits of four broad‐leaved tree species along a hillside gradient. Forstwissenschaftliches Centralblatt 121, 229–239.
| Growth and leaf traits of four broad‐leaved tree species along a hillside gradient.Crossref | GoogleScholarGoogle Scholar |
Hovenden MJ, Vander Schoor JK (2006) The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii. New Phytologist 169, 291–297.
| The response of leaf morphology to irradiance depends on altitude of origin in Nothofagus cunninghamii.Crossref | GoogleScholarGoogle Scholar |
Hovenden MJ, Newton PC, Wills KE (2014) Seasonal not annual rainfall determines grassland biomass response to carbon dioxide. Nature 511, 583–586.
| Seasonal not annual rainfall determines grassland biomass response to carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123, 32–40.
| Altitude trends in conifer leaf morphology and stable carbon isotope composition.Crossref | GoogleScholarGoogle Scholar |
IPCC (2013) The physical science basis. In ‘Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change’. (Cambridge University Press: New York)
Körner C (2003) ‘Alpine plant life: functional plant ecology of high mountain ecosystems.’ (2nd edn) (Springer: Berlin)
Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74, 623–632.
| A global survey of carbon isotope discrimination in plants from high altitude.Crossref | GoogleScholarGoogle Scholar |
Körner C, Farquhar GD, Wong SC (1991) Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88, 30–40.
| Carbon isotope discrimination by plants follows latitudinal and altitudinal trends.Crossref | GoogleScholarGoogle Scholar |
Kuster VC, de Castro SAB, Vale FHA (2016) Photosynthetic and anatomical responses of three plant species at two altitudinal levels in the Neotropical savannah. Australian Journal of Botany 64, 696–703.
| Photosynthetic and anatomical responses of three plant species at two altitudinal levels in the Neotropical savannah.Crossref | GoogleScholarGoogle Scholar |
Li GY, Yang DM, Sun SC (2008) Allometric relationships between lamina area, lamina mass and petiole mass of 93 temperate woody species vary with leaf habit, leaf form and altitude. Functional Ecology 22, 557–564.
| Allometric relationships between lamina area, lamina mass and petiole mass of 93 temperate woody species vary with leaf habit, leaf form and altitude.Crossref | GoogleScholarGoogle Scholar |
Li FY, Newton PCD, Lieffering M (2014) Testing simulations of intra- and inter-annual variation in the plant production response to elevated CO2 against measurements from an 11-year FACE experiment on grazed pasture. Global Change Biology 20, 228–239.
| Testing simulations of intra- and inter-annual variation in the plant production response to elevated CO2 against measurements from an 11-year FACE experiment on grazed pasture.Crossref | GoogleScholarGoogle Scholar |
Luo ZH, Jiang ZG, Tang SH (2015) Impacts of climate change on distributions and diversity of ungulates on the Tibetan Plateau. Ecological Applications 25, 24–38.
| Impacts of climate change on distributions and diversity of ungulates on the Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |
Marshall JD, Zhang J (1994) Carbon isotope discrimination and water-use efficiency in native plants of the north-central Rockies. Ecology 75, 1887–1895.
| Carbon isotope discrimination and water-use efficiency in native plants of the north-central Rockies.Crossref | GoogleScholarGoogle Scholar |
Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences 1206, 35–55.
| Global change and the evolution of phenotypic plasticity in plants.Crossref | GoogleScholarGoogle Scholar |
Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
| Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Nogués-Bravo D, Araújo MB, Errea MP, Martínez-Rica JP (2007) Exposure of global mountain systems to climate warming during the 21st Century. Global Environmental Change 17, 420–428.
| Exposure of global mountain systems to climate warming during the 21st Century.Crossref | GoogleScholarGoogle Scholar |
Pérez-Harguindeguy N, Diaz S, et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Shope PF (1927) Stem and leaf structure of aspen at different altitudes in Colorado. American Journal of Botany 14, 116–119.
| Stem and leaf structure of aspen at different altitudes in Colorado.Crossref | GoogleScholarGoogle Scholar |
Soudzilovskaia NA, Elumeeva TG, Onipchenko VG, Shidakov II, Salpagarova FS, Khubiev AB, Tekeev DK, Cornelissen JHC (2013) Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proceedings of the National Academy of Sciences of the United States of America 110, 18180–18184.
| Functional traits predict relationship between plant abundance dynamic and long-term climate warming.Crossref | GoogleScholarGoogle Scholar |
Thompson LG (2000) Ice core evidence for climate change in the tropics: implications for our future. Quaternary Science Reviews 19, 19–35.
| Ice core evidence for climate change in the tropics: implications for our future.Crossref | GoogleScholarGoogle Scholar |
Van de Water P, Leavitt S, Betancourt J (2002) Leaf δ13C variability with elevation, slope aspect, and precipitation in the southwest United States. Oecologia 132, 332–343.
| Leaf δ13C variability with elevation, slope aspect, and precipitation in the southwest United States.Crossref | GoogleScholarGoogle Scholar |
Vendramini F, Díaz S, Gurvich DE, Wilson PJ, Thompson K, Hodgson JG (2002) Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytologist 154, 147–157.
| Leaf traits as indicators of resource-use strategy in floras with succulent species.Crossref | GoogleScholarGoogle Scholar |
Violle C, Garnier E, Lecoeur J, Roumet C, Podeur C, Blanchard A, Navas ML (2009) Competition, traits and resource depletion in plant communities. Oecologia 160, 747–755.
| Competition, traits and resource depletion in plant communities.Crossref | GoogleScholarGoogle Scholar |
Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends in Ecology & Evolution 27, 244–252.
| The return of the variance: intraspecific variability in community ecology.Crossref | GoogleScholarGoogle Scholar |
Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84, 362–370.
| Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance?Crossref | GoogleScholarGoogle Scholar |
White PS (1983a) Corner’s rules in eastern deciduous trees: allometry and its implications for the adaptive architecture of trees. Bulletin of the Torrey Botanical Club 110, 203–212.
| Corner’s rules in eastern deciduous trees: allometry and its implications for the adaptive architecture of trees.Crossref | GoogleScholarGoogle Scholar |
White PS (1983b) Evidence that temperate east North-American evergreen woody-plants follow corners rules. New Phytologist 95, 139–145.
| Evidence that temperate east North-American evergreen woody-plants follow corners rules.Crossref | GoogleScholarGoogle Scholar |
Wu YB, Zhang J, Deng YC, Wu J, Wang SP, Tang YH, Cui XY (2014) Effects of warming on root diameter, distribution, and longevity in an alpine meadow. Plant Ecology 215, 1057–1066.
| Effects of warming on root diameter, distribution, and longevity in an alpine meadow.Crossref | GoogleScholarGoogle Scholar |
Zhong M, Wang J, Liu K, Wu R, Liu Y, Wei X, Pan D, Shao X (2014) Leaf morphology shift of three dominant species along altitudinal gradient in an alpine meadow of the Qinghai-Tibetan Plateau. Polish Journal of Ecology 62, 639–648.
| Leaf morphology shift of three dominant species along altitudinal gradient in an alpine meadow of the Qinghai-Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |
