Stomatal pore size and density in mangrove leaves and artificial leaves: effects on leaf water isotopic enrichment during transpiration
Leonel da Silveira Lobo Sternberg A B and Lynn M. Manganiello A
+ Author Affiliations
- Author Affiliations
A Department of Biology, University of Miami, 1301 Memorial Drive, Coral Gables, FL 33146, USA.
B Corresponding author. Email: leo@bio.miami.edu
Functional Plant Biology 41(6) 648-658 https://doi.org/10.1071/FP13235
Submitted: 6 August 2013 Accepted: 20 December 2013 Published: 29 January 2014
Abstract
We tested the hypothesis that the previously observed low isotopic enrichment of mangrove leaf water is caused by larger stomatal pores and lower densities compared with freshwater plants. First, we measured and compared pore size and density in mangroves, transitional and freshwater species in South Florida. We pooled this data with other reports encompassing 14 mangrove species and 134 freshwater species and tested for differences in pore size and density between mangroves and freshwater plants. Second, we built artificial leaves having different pore size and density and determined whether there were isotopic differences in their water after transpiration. Both the local survey and pooled data showed that mangrove leaves have significantly larger stomatal pores with lower densities compared with freshwater plants. Isotope enrichment of water from artificial leaves having larger less dense pores was lower than those having smaller and denser pores. Stomatal pore size and density has an effect on leaf water isotopic enrichment amongst other factors. Pore size and density probably affects key components of the Peclet ratio such as the distance advective flow of water must travel to the evaporative surface and the cross-sectional area of advective flow. These components, in turn, affect leaf water isotopic enrichment. Results from the artificial leaf experiment also mimic a recent finding that effective path length scales to the inverse of transpiration in real leaves. The implications of these findings further our understanding of leaf water isotope ratios and are important in applications of stable isotopes in the study of paleoclimate and atmospheric processes.
Additional keywords: hydrogen isotope ratios, leaf water, oxygen isotope ratios, paleoclimate, stomatal density, stomatal size.
References
Allison GB, Gat JR, Leaney FWJ (1985) The relationship between deuterium and oxygen-18 delta values in leaf water. Chemical Geology 58, 145–156.| The relationship between deuterium and oxygen-18 delta values in leaf water.Crossref | GoogleScholarGoogle Scholar |
Barbieri G, Vallone S, Orsini F, Paradiso R, De Pascale S, Negre-Zakharov F, Maggio A (2012) Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.). Journal of Plant Physiology 169, 1737–1746.
| Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtV2msrzO&md5=b766ee3ef726b6b22b5eb169fc5e8f36CAS | 22840325PubMed |
Barbour MM, Farquhar GD (2004) Do pathways of water movement and leaf anatomical dimensions allow development of gradients in H2 18O between veins and the sites of evaporation within leaves? Plant, Cell & Environment 27, 107–121.
| Do pathways of water movement and leaf anatomical dimensions allow development of gradients in H2 18O between veins and the sites of evaporation within leaves?Crossref | GoogleScholarGoogle Scholar |
Beerling DJ (1999) The influence of vegetation activity on the Dole effect and its implications for changes in biospheric productivity in the mid-Holocene. Proceedings of the Royal Society of London. Series B, Biological Sciences 266, 627–632.
| The influence of vegetation activity on the Dole effect and its implications for changes in biospheric productivity in the mid-Holocene.Crossref | GoogleScholarGoogle Scholar |
Beerling DJ, Royer DL (2002) Reading a CO2 signal from fossil stomata. New Phytologist 153, 387–397.
| Reading a CO2 signal from fossil stomata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Wgt78%3D&md5=39ca6fe4d2ad2e697ba66a6807542f58CAS |
Bongers F, Popma J (1990) Leaf characteristics of the tropical rain-forest flora of Los-Tuxtlas, Mexico. Botanical Gazette 151, 354–365.
| Leaf characteristics of the tropical rain-forest flora of Los-Tuxtlas, Mexico.Crossref | GoogleScholarGoogle Scholar |
Camargo MAB, Marenco RA (2011) Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia. Acta Amazonica 41, 205–212.
| Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia.Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Kahmen A (2013) The multifaceted relationship between leaf water 18O enrichment and transpiration rate. Plant, Cell & Environment 36, 1239–1241.
| The multifaceted relationship between leaf water 18O enrichment and transpiration rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOnt7o%3D&md5=f4698ecce9f37d697987cdf8c36e6d29CAS |
Clark ID, Fritz P (1997) ‘Environmental isotopes in hydrology.’ (Lewis Publishers: New York)
Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytologist 179, 964–974.
| Flooding tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqurzM&md5=d0509897b19ff327c63c479151577511CAS | 18482227PubMed |
Craig H, Gordon LI (1965) Deuterium and oxygen-18 variations in the ocean and marine atmosphere. In ‘Proceedings of the conference on stable isotopes in oceanographic studies and paleotemperatures’. (Ed. E Tongiorgi) pp. 9–130. (Laboratory of Geology and Nuclear Science: Piza)
Cuntz M, Ogee J, Farquhar GD, Peylin P, Cernusak LA (2007) Modelling advection and diffusion of water isotopologues in leaves. Plant, Cell & Environment 30, 892–909.
| Modelling advection and diffusion of water isotopologues in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslGksr0%3D&md5=aad22f0e7c16eb93efbb4b1c1129d5a8CAS |
Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16, 436–468.
| Stable isotopes in precipitation.Crossref | GoogleScholarGoogle Scholar |
Doria G, Royer DL, Wolfe AP, Fox A, Westgate JA, Beerling DJ (2011) Declining atmospheric CO2 during the late middle Eocene climate transition. American Journal of Science 311, 63–75.
| Declining atmospheric CO2 during the late middle Eocene climate transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVGluro%3D&md5=f22714bc25744eb6d365c8333aecea5aCAS |
Ellsworth PZ, Williams DG (2007) Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant and Soil 291, 93–107.
| Hydrogen isotope fractionation during water uptake by woody xerophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFygur4%3D&md5=aa640d27fe4626f862dd06571dfc3286CAS |
Ellsworth PV, Ellsworth PZ, Anderson WT, Sternberg LSL (2013) The role of effective leaf mixing length in the relationship between the δ18O of stem cellulose and source water across a salinity gradient. Plant, Cell & Environment 36, 138–148.
| The role of effective leaf mixing length in the relationship between the δ18O of stem cellulose and source water across a salinity gradient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2lsr3O&md5=619705f0162744dc46bf80b66f761935CAS |
Farquhar GD, Cernusak LA (2005) On the isotopic composition of leaf water in the non-steady state. Functional Plant Biology 32, 293–303.
| On the isotopic composition of leaf water in the non-steady state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFyktr4%3D&md5=de68c0aeedd08a338c6b96e6cbf53f7cCAS |
Farquhar GD, Ball MC, von Caemmerer S, Roksandic Z (1982) Effect of salinity and humidity on δ13C value of halophytes- evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 52, 121–124.
| Effect of salinity and humidity on δ13C value of halophytes- evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Lloyd J, Taylor JA, Flanagan LB, Syvertsen JP, Hubick KT, Wong SC, Ehleringer JR (1993) Vegetation effects on the isotope composition of oxygen in atmospheric CO2. Nature 363, 439–443.
| Vegetation effects on the isotope composition of oxygen in atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktlWrt7s%3D&md5=12e4fe34266525ec61b4385ff5e38447CAS |
Ferrio JP, Pou A, Florez-Sarasa I, Gessler A, Kodama N, Flexas J, Ribas-Carbo M (2012) The Peclet effect on leaf water enrichment correlates with leaf hydraulic conductance and mesophyll conductance for CO2. Plant, Cell & Environment 35, 611–625.
| The Peclet effect on leaf water enrichment correlates with leaf hydraulic conductance and mesophyll conductance for CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktV2nsrk%3D&md5=0640919cdb43ff1cbb14434fde37211cCAS |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=5be89aeb6924a58f5526ed228831987eCAS | 18565144PubMed |
Flowers TJ, Troke PF, Yeo AR (1977) Mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology and Plant Molecular Biology 28, 89–121.
| Mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXksFSisb8%3D&md5=491f50236353de214a72a475c627bad9CAS |
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 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=6419ad3cc05fd039f1c3a0f286092430CAS | 19506250PubMed |
Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143, 78–87.
| The mechanical diversity of stomata and its significance in gas-exchange control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1OgsQ%3D%3D&md5=df05204553c3afcc37b09d6ae0ab1b56CAS | 17114276PubMed |
Hartard B, Cuntz M, Maguas C, Lakatos M (2009) Water isotopes in desiccating lichens. Planta 231, 179–193.
| Water isotopes in desiccating lichens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsValu7bM&md5=bc5aadaf700237a78a6fbcb1a974d4eaCAS | 19888598PubMed |
Helliker BR, Griffiths H (2007) Toward a plant-based proxy for the isotope ratio of atmospheric water vapor. Global Change Biology 13, 723–733.
| Toward a plant-based proxy for the isotope ratio of atmospheric water vapor.Crossref | GoogleScholarGoogle Scholar |
Jahren AH, Sternberg L (2002) Eocene meridional weather patterns reflected in the oxygen isotopes of Arctic fossil wood. GSA Today 12, 4–9.
| Eocene meridional weather patterns reflected in the oxygen isotopes of Arctic fossil wood.Crossref | GoogleScholarGoogle Scholar |
Kahmen A, Simonin K, Tu K, Goldsmith GR, Dawson TE (2009) The influence of species and growing conditions on the 18O enrichment of leaf water and its impact on ‘effective path length’. New Phytologist 184, 619–630.
| The influence of species and growing conditions on the 18O enrichment of leaf water and its impact on ‘effective path length’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVOgs7jJ&md5=6da0f1876a7bc78f02db6b4b06a45997CAS | 19761496PubMed |
Karan DM, Macey RI (1980) The permeability of the human red-cell to deuterium oxide (heavy-water). Journal of Cellular Physiology 104, 209–214.
| The permeability of the human red-cell to deuterium oxide (heavy-water).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2FgslWgsw%3D%3D&md5=3b9f8ec4f7aa1acb488a47fba8b412d2CAS | 7410489PubMed |
Krauss KW, Ball MC (2013) On the halophytic nature of mangroves. Trees – Structure and Function 27, 7–11.
| On the halophytic nature of mangroves.Crossref | GoogleScholarGoogle Scholar |
Li Y, Li Z, Lin P, Soc IC (2009) The study on the leaf anatomy of some mangrove species of CHINA. In ‘Proceedings of the 2009 International Conference on Environmental Science and Information Application Technology, Vol. III’. pp. 47–51. (Ieee Computer Society: Los Alamitos, CA, USA)
Lin G, Sternberg LdSL (1995) Hydrogen isotopic fractionation by plant roots during water uptake in coastal wetland plants. In ‘Perspective on carbon and water relations from stable isotopes’. (Eds J Ehleringer, G Farquhar, A Hall) pp. 497–510. (Academic Press: New York)
Manning AC, Nisbet EG, Keeling RF, Liss PS (2011) Greenhouse gases in the earth system: setting the agenda to 2030. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences 369, 1885–1890.
| Greenhouse gases in the earth system: setting the agenda to 2030.Crossref | GoogleScholarGoogle Scholar | 21502164PubMed |
Nemiah Ladd SN, Sachs JP (2012) Inverse relationship between salinity and n-alkane δD values in the mangrove Avicennia marina. Organic Geochemistry 48, 25–36.
| Inverse relationship between salinity and n-alkane δD values in the mangrove Avicennia marina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xot1Cisrs%3D&md5=cc9a5221fbc63a4b08533a2ebe87e0afCAS |
Orsini F, Alnayef M, Bona S, Maggio A, Gianquinto G (2012) Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity. Environmental and Experimental Botany 81, 1–10.
| Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1GgtLY%3D&md5=0dac69a0d61feabcd05d4a01334980f8CAS |
Price RM, Swart PK, Willoughby HE (2008) Seasonal and spatial variation in the stable isotopic composition (δ18O and δD) of precipitation in south Florida. Journal of Hydrology 358, 193–205.
| Seasonal and spatial variation in the stable isotopic composition (δ18O and δD) of precipitation in south Florida.Crossref | GoogleScholarGoogle Scholar |
Richter SL, Johnson AH, Dranoff MM, LePage BA, Williams CJ (2008) Oxygen isotope ratios in fossil wood cellulose: isotopic composition of Eocene- to Holocene-aged cellulose. Geochimica et Cosmochimica Acta 72, 2744–2753.
| Oxygen isotope ratios in fossil wood cellulose: isotopic composition of Eocene- to Holocene-aged cellulose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVektrk%3D&md5=762cee2d914a68abd379f4d91036c878CAS |
Romero IC, Feakins SJ (2011) Spatial gradients in plant leaf wax D/H across a coastal salt marsh in southern California. Organic Geochemistry 42, 618–629.
| Spatial gradients in plant leaf wax D/H across a coastal salt marsh in southern California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFyntLw%3D&md5=903da9ab86b0bca3e02c94759b55329eCAS |
Rundgren M, Beerling D (2003) Fossil leaves: effective bioindicators of ancient CO2 levels? Geochemistry Geophysics Geosystems 4, 1058
| Fossil leaves: effective bioindicators of ancient CO2 levels?Crossref | GoogleScholarGoogle Scholar |
Scholander PF (1968) How mangroves desalinate seawater. Physiologia Plantarum 21, 251–261.
| How mangroves desalinate seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXhtVamtb8%3D&md5=db385d1c3722a82af5e24ccbe850d551CAS |
Scholander PF, Hemmingsen E, Garey W, Hammel HT (1962) Salt balance in mangroves. Plant Physiology 37, 722–729.
| Salt balance in mangroves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXjsVyjug%3D%3D&md5=f9717d20ced391217712ffa90c06117aCAS | 16655719PubMed |
Seshavatharam V, Srivalli M (1989) Systematic leaf anatomy of some Indian mangroves. Proceedings of the Indian Academy of Sciences-Plant Sciences 99, 557–565.
Song X, Barbour MM, Farquhar GD, Vann DR, Helliker BR (2013) Transpiration rate relates to within- and across-species variations in effective path length in a leaf water model of oxygen isotope enrichment. Plant, Cell & Environment 36, 1338–1351.
| Transpiration rate relates to within- and across-species variations in effective path length in a leaf water model of oxygen isotope enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOntrc%3D&md5=c8f1b429f81ef8d111bd13d047fcd089CAS |
Sternberg L, Swart PK (1987) Utilization of freshwater and ocean water by costal plants of Southern Florida. Ecology 68, 1898–1905.
| Utilization of freshwater and ocean water by costal plants of Southern Florida.Crossref | GoogleScholarGoogle Scholar |
Verheyden A, Helle G, Schleser GH, Dehairs F, Beeckman H, Koedam N (2004) Annual cyclicity in high-resolution stable carbon and oxygen isotope ratios in the wood of the mangrove tree Rhizophora mucronata. Plant, Cell & Environment 27, 1525–1536.
| Annual cyclicity in high-resolution stable carbon and oxygen isotope ratios in the wood of the mangrove tree Rhizophora mucronata.Crossref | GoogleScholarGoogle Scholar |
Wang XF, Yakir D, Avishai M (1998) Non-climatic variations in the oxygen isotopic compositions of plants. Global Change Biology 4, 835–849.
| Non-climatic variations in the oxygen isotopic compositions of plants.Crossref | GoogleScholarGoogle Scholar |
Winter K, Holtum JAM (2005) The effects of salinity, crassulacean acid metabolism and plant age on the carbon isotope composition of Mesembryanthemum crystallinum L., a halophytic C3-CAM species. Planta 222, 201–209.
| The effects of salinity, crassulacean acid metabolism and plant age on the carbon isotope composition of Mesembryanthemum crystallinum L., a halophytic C3-CAM species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVektr3F&md5=a03b2ccdc899510bb8a38e73cbf38dcaCAS | 15968514PubMed |
Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytologist 131, 311–327.
| The influence of CO2 concentration on stomatal density.Crossref | GoogleScholarGoogle Scholar |
Zhang JL, Cao KF (2009) Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Functional Ecology 23, 658–667.
| Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species.Crossref | GoogleScholarGoogle Scholar |
Zhang JL, Poorter L, Cao KF (2012) Productive leaf functional traits of Chinese savanna species. Plant Ecology 213, 1449–1460.
| Productive leaf functional traits of Chinese savanna species.Crossref | GoogleScholarGoogle Scholar |
