Temperature influences stomatal density and maximum potential water loss through stomata of Dodonaea viscosa subsp. angustissima along a latitude gradient in southern Australia
Kathryn E. Hill A C , Greg R. Guerin A , Robert S. Hill A B and Jennifer R. Watling A
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, The University of Adelaide, SA 5005, Australia.
B South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
C Corresponding author. Email: kathryn.hill@adelaide.edu.au
Australian Journal of Botany 62(8) 657-665 https://doi.org/10.1071/BT14204
Submitted: 20 August 2014 Accepted: 11 December 2014 Published: 26 March 2015
Abstract
It is well known that physical leaf traits influence leaf functions, and that these traits vary across environmental gradients. Stomata can influence leaf function, with changes in density and size affecting potential water loss, CO2 uptake, and also leaf cooling. Plasticity in stomatal traits occurs in response to environmental factors; however, identifying which factors have the greatest influence is often difficult. We investigated variation in leaf size, stomatal density and size, and potential water loss from open stomata (gwmax), in the Australian native shrub Dodonaea viscosa subsp. angustissima, across a range of environmental factors including temperature, rainfall and CO2. We used herbarium specimens collected across a latitudinal gradient, and also sampled along an elevation gradient in southern Australia. There were significant relationships between mean summer maximum temperature and stomatal density, and gwmax. We found no significant relationships between rainfall or CO2 and the leaf traits we studied. Increased stomatal density at warmer locations may result in an increase in the potential for transpiration, as a means for evaporative cooling. Alternatively, it may enable increased CO2 and nutrient uptake during the short, winter-growing season.
References
Aslantaş R, Karakurt H (2009) The effects of altitude on stomata number and some vegetative growth parameters of some apple cultivars. Research Journal of Agriculture and Biological Sciences 5, 853–857.Bates D, Maechler M, Bolker B, Walker S (2014) ‘lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-5.’ Available at http://CRAN.R-project.org/package=lme4 [accessed January 2014]
Beerling D, Chaloner W (1993) The impact of atmospheric CO2 and temperature change on stomatal density: observations from Quercus robur lammas leaves. Annals of Botany 71, 231–235.
| The impact of atmospheric CO2 and temperature change on stomatal density: observations from Quercus robur lammas leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXisFWmurc%3D&md5=7ac2078f29d5681d35f32042701fc8bbCAS |
Brodribb T, Hill RS (1997) Imbricacy and stomatal wax plugs reduce maximum leaf conductance in southern hemisphere conifers. Australian Journal of Botany 45, 657–668.
| Imbricacy and stomatal wax plugs reduce maximum leaf conductance in southern hemisphere conifers.Crossref | GoogleScholarGoogle Scholar |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2014) 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 | 1:CAS:528:DC%2BC3sXhvVyjurfN&md5=12debb0bb4560ccd0892fef41ccc7980CAS |
Drake PL, Froend RH, Franks PJ (2013) Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. Journal of Experimental Botany 64, 495–505.
| Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVGltg%3D%3D&md5=dbbe4fad2a454e55f16867d3b7f0ab31CAS | 23264516PubMed |
Eensalu E, Kupper P, Sellin A, Rahi M, Sober A, Kull O (2008) Do stomata operate at the same relative opening range along a canopy profile of Betula pendula? Functional Plant Biology 35, 103–110.
| Do stomata operate at the same relative opening range along a canopy profile of Betula pendula? Crossref | GoogleScholarGoogle Scholar |
Ferris R, Nijs I, Behaeghe T, Impens I (1996) Elevated CO2 and temperature have different effects on leaf anatomy of perennial ryegrass in spring and summer. Annals of Botany 78, 489–497.
| Elevated CO2 and temperature have different effects on leaf anatomy of perennial ryegrass in spring and summer.Crossref | GoogleScholarGoogle Scholar |
Franks P, Beerling D (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, USA 106, 10343–10347.
| Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1Giurg%3D&md5=d50bcd2b019cab2d8554e4b252624d2dCAS |
Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell & Environment 32, 1737–1748.
| Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Frey B, Scheidegger C, GunthardtGoerg MS, Matyssek R (1996) The effects of ozone and nutrient supply on stomatal response in birch (Betula pendula) leaves as determined by digital as image-analysis and X-ray microanalysis. New Phytologist 132, 135–143.
| The effects of ozone and nutrient supply on stomatal response in birch (Betula pendula) leaves as determined by digital as image-analysis and X-ray microanalysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsV2rsL8%3D&md5=3afbbb58cd02833eea626d896ab7b756CAS |
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 | 22764114PubMed |
Harrington MG, Gadek PA (2009) A species well travelled: the Dodonaea viscosa (Sapindaceae) complex based on phylogenetic analyses of nuclear ribosomal ITS and ETSf sequences. Journal of Biogeography 36, 2313–2323.
| A species well travelled: the Dodonaea viscosa (Sapindaceae) complex based on phylogenetic analyses of nuclear ribosomal ITS and ETSf sequences.Crossref | GoogleScholarGoogle Scholar |
Hijmans R, Cameron S, Parra J, Jones P, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
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 LLR, Kurschner WM, McElwain JC (2007) Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry. Paleoaltimetry: Geochemical and Thermodynamic Approaches 66, 215–241.
Lammertsma EI, de Boer HJ, Dekker SC, Dilcher DL, Lotter AF, Wagner-Cremer F (2011) Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation. Proceedings of the National Academy of Sciences, USA 108, 4035–4040.
| Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1WqtLo%3D&md5=39c51666c591f5c11b23fd80224d87d5CAS |
Limin Y, Mei H, Guangsheng Z, Jiandong L (2007) The changes in water-use efficiency and stoma density of Leymus chinensis along northeast China transect. Acta Ecologica Sinica 27, 16–23.
| The changes in water-use efficiency and stoma density of Leymus chinensis along northeast China transect.Crossref | GoogleScholarGoogle Scholar |
McDonald PG, Fonseca CR, Overton JM, Westoby M (2003) Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades? Functional Ecology 17, 50–57.
| Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades?Crossref | GoogleScholarGoogle Scholar |
Meier IC, Leuschner C (2008) Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11, 655–669.
| Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOntL7K&md5=b5a2d732927c5ae174022acca8e8b66aCAS |
Miller-Rushing AJ, Primack RB, Templer PH, Rathbone S, Mukunda S (2009) Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees. American Journal of Botany 96, 1779–1786.
| Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlanu7vJ&md5=4c1a9157ee1cfff4ef46206ad15a06aaCAS | 21622298PubMed |
Mishio M (1992) Adaptations to drought in five woody species co-occurring on shallow-soil ridges. Functional Plant Biology 19, 539–553.
Mott KA, Gibson AC, O’Leary JW (1982) The adaptive significance of amphistomatic leaves. Plant, Cell & Environment 5, 455–460.
| The adaptive significance of amphistomatic leaves.Crossref | GoogleScholarGoogle Scholar |
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed‐effects models. Methods in Ecology and Evolution 4, 133–142.
| A general and simple method for obtaining R 2 from generalized linear mixed‐effects models.Crossref | GoogleScholarGoogle Scholar |
Nobel PS (2009) Chapter 7. Temperature and energy budgets. In ‘Physicochemical and environmental plant physiology’. 4th edn. pp. 318–363. (Academic Press: San Diego, CA)
Pääkkönen E, Vahala J, Pohjolai M, Holopainen T, Kärenlampi L (1998) Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress. Plant, Cell & Environment 21, 671–684.
| Physiological, stomatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress.Crossref | GoogleScholarGoogle Scholar |
Pandey R, Chacko PM, Choudhary ML, Prasad KV, Pal M (2007) Higher than optimum temperature under CO2 enrichment influences stomata anatomical characters in rose (Rosa hybrida). Scientia Horticulturae 113, 74–81.
| Higher than optimum temperature under CO2 enrichment influences stomata anatomical characters in rose (Rosa hybrida).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1SjsL4%3D&md5=ee4a5d260885857fba88eb1edd76e04eCAS |
Schoettle AW, Rochelle SG (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=87fab817d9e60994e98154333cb67828CAS | 11118417PubMed |
Shtein I, Meir S, Riov J, Philosoph-Hadas S (2011) Interconnection of seasonal temperature, vascular traits, leaf anatomy and hydraulic performance in cut Dodonaea ‘Dana’ branches. Postharvest Biology and Technology 61, 184–192.
| Interconnection of seasonal temperature, vascular traits, leaf anatomy and hydraulic performance in cut Dodonaea ‘Dana’ branches.Crossref | GoogleScholarGoogle Scholar |
Tans P, Keeling R (2013) ‘Mauna Loa CO2 monthly mean data.’ (NOAA/ESRL and Scripps Institution of Oceanography). Available at ftp://aftp.cmdl.noaa.gov/products/trends/co2/co2_mm_mlo.txt. [Verified 18 January 2013]
West J (1984) A revision of Dodonaea Miller (Sapindaceae) in Australia. Australian Systematic Botany 7, 1–194.
Woodward FI (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 |
Xu F, Guo W, Xu W, Wei Y, Wang R (2009) Leaf morphology correlates with water and light availability: what consequences for simple and compound leaves? Progress in Natural Science 19, 1789–1798.
| Leaf morphology correlates with water and light availability: what consequences for simple and compound leaves?Crossref | GoogleScholarGoogle Scholar |
Yates MJ, Anthony Verboom G, Rebelo AG, Cramer MD (2010) Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region. Functional Ecology 24, 485–492.
| Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region.Crossref | GoogleScholarGoogle Scholar |
