Leaf water δ18O reflects water vapour exchange and uptake by C3 and CAM epiphytic bromeliads in Panama
Monica Mejia-Chang A , Casandra Reyes-Garcia A B , Ulli Seibt A C , Jessica Royles A , Moritz T. Meyer A , Glyn D. Jones A , Klaus Winter D , Miquel Arnedo E and Howard Griffiths A FA Physiological Ecology Group, Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.
B Unidad de Recursos Naturales, Centro de Investigación Científica de Yucatán, Calle 43 Num. 130 Churburná de Hidalgo, Mérida, 97200, México.
C Department of Atmospheric and Oceanic Sciences, UCLA, Los Angeles, CA, USA.
D Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Republic of Panama.
E Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Fac. Biologia, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain.
F Corresponding author. Email: hg230@cam.ac.uk
Functional Plant Biology 48(7) 732-742 https://doi.org/10.1071/FP21087
Submitted: 23 March 2021 Accepted: 20 April 2021 Published: 21 May 2021
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
The distributions of CAM and C3 epiphytic bromeliads across an altitudinal gradient in western Panama were identified from carbon isotope (δ13C) signals, and epiphyte water balance was investigated via oxygen isotopes (δ18O) across wet and dry seasons. There were significant seasonal differences in leaf water (δ18Olw), precipitation, stored ‘tank’ water and water vapour. Values of δ18Olw were evaporatively enriched at low altitude in the dry season for the C3 epiphytes, associated with low relative humidity (RH) during the day. Crassulacean acid metabolism (CAM) δ18Olw values were relatively depleted, consistent with water vapour uptake during gas exchange under high RH at night. At high altitude, cloudforest locations, C3 δ18Olw also reflected water vapour uptake by day. A mesocosm experiment with Tillandsia fasciculata (CAM) and Werauhia sanguinolenta (C3) was combined with simulations using a non-steady-state oxygen isotope leaf water model. For both C3 and CAM bromeliads, δ18Olw became progressively depleted under saturating water vapour by day and night, although evaporative enrichment was restored in the C3 W. sanguinolenta under low humidity by day. Source water in the overlapping leaf base ‘tank’ was also modified by evaporative δ18O exchanges. The results demonstrate how stable isotopes in leaf water provide insights for atmospheric water vapour exchanges for both C3 and CAM systems.
Keywords: C3, CAM, Crassulacean acid metabolism, Tillandsia fasciculata, Werauhia sanguinolenta, photosynthetic pathway, gas exchange, epiphyte, oxygen isotopes, altitudinal gradient, mesocosm.
References
Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34, 83–94.| Stable oxygen isotope composition of plant tissue: a review.Crossref | GoogleScholarGoogle Scholar | 32689335PubMed |
Benettin P, Nehemy MF, Cernusak LA, Kahmen A, McDonnell JJ (2021) On the use of leaf water to determine plant water source: A proof of concept. Hydrological Processes 35, e14073
| On the use of leaf water to determine plant water source: A proof of concept.Crossref | GoogleScholarGoogle Scholar |
Benzing DH (1976) Bromeliad trichomes: structure, function, and ecological significance. Selbyana 1, 330–348.
Berry ZC, Emery NC, Gotsch SG, Goldsmith GR (2019) Foliar water uptake: Processes, pathways, and integration into plant water budgets. Plant, Cell & Environment 42, 410–423.
| Foliar water uptake: Processes, pathways, and integration into plant water budgets.Crossref | GoogleScholarGoogle Scholar |
Cavelier J, Solis D, Jaramillo MA (1996) Fog interception in montane forests across the Central Cordillera of Panamá. Journal of Tropical Ecology 12, 357–369.
| Fog interception in montane forests across the Central Cordillera of Panamá.Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Mejia-Chang M, Winter K, Griffiths H (2008) Oxygen isotope composition of CAM and C3 Clusia species: non-steady-state dynamics control leaf water 18O enrichment in succulent leaves. Plant, Cell & Environment 31, 1644–1662.
| Oxygen isotope composition of CAM and C3 Clusia species: non-steady-state dynamics control leaf water 18O enrichment in succulent leaves.Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Barbour MM, Arndt SK, Cheesman AW, English NB, Feild TS, Helliker BR, Holloway-Phillips MM, Holtum JAM, Kahmen A, McInerney FA, Munksgaard NC, Simonin KA, Song X, Stuart-Williams H, West JB, Farquhar GD (2016) Stable isotopes in leaf water of terrestrial plants. Plant, Cell & Environment 39, 1087–1102.
| Stable isotopes in leaf water of terrestrial plants.Crossref | GoogleScholarGoogle Scholar |
Crayn DM, Winter K, Schulte K, Smith JAC (2015) Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society 178, 169–221.
| Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species.Crossref | GoogleScholarGoogle Scholar |
Dawson TE, Goldsmith GR (2018) The value of wet leaves. New Phytologist 219, 1156–1169.
| The value of wet leaves.Crossref | GoogleScholarGoogle Scholar |
Dawson TE, Burgess SSO, Tu KP, Oliveira RS, Santiago LS, Fisher JB, Simonin KA, Ambrose AR (2007) Nighttime transpiration in woody plants from contrasting ecosystems. Tree Physiology 27, 561–575.
| Nighttime transpiration in woody plants from contrasting ecosystems.Crossref | GoogleScholarGoogle Scholar | 17241998PubMed |
Dubbert M, Kübert A, Werner C (2017) Impact of leaf traits on temporal dynamics of transpired oxygen isotope signatures and its impact on atmospheric vapor. Frontiers in Plant Science 8, 5
| Impact of leaf traits on temporal dynamics of transpired oxygen isotope signatures and its impact on atmospheric vapor.Crossref | GoogleScholarGoogle Scholar | 28149303PubMed |
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 | 32689132PubMed |
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Carbon isotope discrimination and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Henry BK, Styles JM (1997) A rapid on-line technique for determination of oxygen isotope composition of nitrogen-containing organic matter and water. Rapid Communications in Mass Spectrometry 11, 1554–1560.
| A rapid on-line technique for determination of oxygen isotope composition of nitrogen-containing organic matter and water.Crossref | GoogleScholarGoogle Scholar |
Gómez González DC, Quiel CR, Zotz G, Bader MY (2017) Species richness and biomass of epiphytic vegetation in a tropical montane forest in western Panama. Tropical Conservation Science 10, 1–17.
| Species richness and biomass of epiphytic vegetation in a tropical montane forest in western Panama.Crossref | GoogleScholarGoogle Scholar |
Griffiths H, Smith JAC (1983) Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and the occurrence of CAM. Oecologia 60, 176–184.
| Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and the occurrence of CAM.Crossref | GoogleScholarGoogle Scholar | 28310484PubMed |
Griffiths H, Lüttge U, Stimmel KH, Crook CE, Griffiths NM, Smith JAC (1986) Comparative ecophysiology of CAM and C3 bromeliads. III: Environmental influences on CO2 assimilation and transpiration. Plant, Cell & Environment 9, 385–393.
| Comparative ecophysiology of CAM and C3 bromeliads. III: Environmental influences on CO2 assimilation and transpiration.Crossref | GoogleScholarGoogle Scholar |
Harwood KG, Gillon JS, Griffiths H, Broadmeadow MSJ (1998) Diurnal variation of Δ13CO2, ΔC18O16O and evaporative site enrichment of δH218O in Piper aduncum under field conditions in Trinidad. Plant, Cell & Environment 21, 269–283.
| Diurnal variation of Δ13CO2, ΔC18O16O and evaporative site enrichment of δH218O in Piper aduncum under field conditions in Trinidad.Crossref | GoogleScholarGoogle Scholar |
Helliker BR (2011) On the controls of leaf-water oxygen isotope ratios in the atmospheric Crassulacean acid metabolism epiphyte Tillandsia usneoides. Plant Physiology 155, 2096–2107.
| On the controls of leaf-water oxygen isotope ratios in the atmospheric Crassulacean acid metabolism epiphyte Tillandsia usneoides.Crossref | GoogleScholarGoogle Scholar | 21300917PubMed |
Helliker BR (2014) Reconstructing the δ18O of atmospheric water vapour via the CAM epiphyte Tillandsia usneoides: seasonal controls on δ18O in the field and large-scale reconstruction of δ18Oa. Plant, Cell & Environment 37, 541–556.
| Reconstructing the δ18O of atmospheric water vapour via the CAM epiphyte Tillandsia usneoides: seasonal controls on δ18O in the field and large-scale reconstruction of δ18Oa.Crossref | GoogleScholarGoogle Scholar |
Helliker BR, Ehleringer JR (2000) Establishing a grassland signature in veins: O18 in the leaf water of C3 and C4 grasses. Proceedings of the National Academy of Sciences of the United States of America 97, 7894–7898.
| Establishing a grassland signature in veins: O18 in the leaf water of C3 and C4 grasses.Crossref | GoogleScholarGoogle Scholar | 10884421PubMed |
Helliker BR, Griffiths H (2007) Towards a plant-based proxy for the isotope ratio of atmospheric water vapor. Global Change Biology 13, 723–733.
| Towards a plant-based proxy for the isotope ratio of atmospheric water vapor.Crossref | GoogleScholarGoogle Scholar |
Helliker BR, Roden JS, Cook C, Ehleringer JR (2002) A rapid and precise method for sampling and determining the oxygen isotope ratio of atmospheric water vapor. Rapid Communications in Mass Spectrometry 16, 929–932.
| A rapid and precise method for sampling and determining the oxygen isotope ratio of atmospheric water vapor.Crossref | GoogleScholarGoogle Scholar | 11968123PubMed |
Horwath AB, Royles J, Tito R, Gudiño JA, Salazar Allen N, Farfan-Rios W, Rapp JM, Silman MR, Malhi Y, Swamy V, Latorre Farfan JP, Griffiths H (2019) Bryophyte stable isotope composition, diversity and biomass define tropical montane cloud forest extent. Proceedings of the Royal Society B: Biological Sciences 286, 20182284
| Bryophyte stable isotope composition, diversity and biomass define tropical montane cloud forest extent.Crossref | GoogleScholarGoogle Scholar | 30963945PubMed |
Lai CT, Ometto JPHB, Berry JA, Martinelli LA, Domingues TF, Ehleringer JR (2008) Life form-specific variations in leaf water oxygen-18 enrichment in Amazonia vegetation. Oecologia 157, 197–210.
| Life form-specific variations in leaf water oxygen-18 enrichment in Amazonia vegetation.Crossref | GoogleScholarGoogle Scholar | 18543002PubMed |
Lange OL, Medina E (1979) Stomata of the CAM plant Tillandsia recurvata respond directly to humidity. Oecologia 40, 357–363.
| Stomata of the CAM plant Tillandsia recurvata respond directly to humidity.Crossref | GoogleScholarGoogle Scholar | 28309618PubMed |
Lehmann MM, Goldsmith GR, Mirande-Ney C, Weigt RB, Schönbeck L, Kahmen A, Gessler A, Siegwolf RTW, Saurer M (2020) The 18O-signal transfer from water vapour to leaf water and assimilates varies among plant species and growth forms. Plant, Cell & Environment 43, 510–523.
| The 18O-signal transfer from water vapour to leaf water and assimilates varies among plant species and growth forms.Crossref | GoogleScholarGoogle Scholar |
Leroy C, Gril E, Ouali LS, Coste S, Gérard B, Maillard P, Mercier H, Stahl C (2019) Water and nutrient uptake capacity of leaf-absorbing trichomes vs. roots in epiphytic tank bromeliads. Environmental and Experimental Botany 163, 112–123.
| Water and nutrient uptake capacity of leaf-absorbing trichomes vs. roots in epiphytic tank bromeliads.Crossref | GoogleScholarGoogle Scholar |
Males J (2016) Think tank: water relations of Bromeliaceae in their evolutionary context. Botanical Journal of the Linnaean Society 181, 415–440.
| Think tank: water relations of Bromeliaceae in their evolutionary context.Crossref | GoogleScholarGoogle Scholar |
Males J, Griffiths H (2018) Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae. Plant, Cell & Environment 41, 64–78.
| Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
North GB, Lynch FH, Maharaj FDR, Phillips CA, Woodside WT (2013) Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water. Frontiers in Plant Science 4, 78
| Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water.Crossref | GoogleScholarGoogle Scholar | 23596446PubMed |
Ogée J, Cuntz M, Peylin P, Bariac T (2007) Non-steady-state, non-uniform transpiration rate and leaf anatomy effects on the progressive stable isotope enrichment of leaf water along monocot leaves. Plant, Cell & Environment 30, 367–387.
| Non-steady-state, non-uniform transpiration rate and leaf anatomy effects on the progressive stable isotope enrichment of leaf water along monocot leaves.Crossref | GoogleScholarGoogle Scholar |
Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29, 379–414.
| Crassulacean acid metabolism: a curiosity in context.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Maxwell K, Griffiths H, Winter K (2001) Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. American Journal of Botany 88, 1371–1389.
| Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 21669669PubMed |
Pierce S, Winter K, Griffiths H (2002a) Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytologist 156, 75–83.
| Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Winter K, Griffiths H (2002b) The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae. Plant, Cell & Environment 25, 1181–1189.
| The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2018) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing, Vienna, Austria). Available at https://www.R-project.org/
Reyes-García C, Mejia-Chang M, Jones G, Griffiths H (2008) Water vapour isotopic exchange by epiphytic bromeliads in tropical dry forests reflects niche differentiation and climatic signals. Plant, Cell & Environment 31, 828–841.
| Water vapour isotopic exchange by epiphytic bromeliads in tropical dry forests reflects niche differentiation and climatic signals.Crossref | GoogleScholarGoogle Scholar |
Seibt U, Wingate L, Berry JA, Lloyd J (2006) Non-steady state effects in diurnal 18O discrimination by Picea sitchensis branches in the field. Plant, Cell & Environment 29, 928–939.
| Non-steady state effects in diurnal 18O discrimination by Picea sitchensis branches in the field.Crossref | GoogleScholarGoogle Scholar |
Seibt U, Wingate L, Berry JA (2007) Nocturnal stomatal conductance effects on the δ18O signatures of foliage gas exchange observed in two forest ecosystems. Tree Physiology 27, 585–595.
| Nocturnal stomatal conductance effects on the δ18O signatures of foliage gas exchange observed in two forest ecosystems.Crossref | GoogleScholarGoogle Scholar | 17242000PubMed |
Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155, 441–454.
| Carbon isotopes and water use efficiency: sense and sensitivity.Crossref | GoogleScholarGoogle Scholar | 18224341PubMed |
Sternberg L, Pinzon MC, Anderson WT, Jahren AH (2006) Variation in oxygen isotope fractionation during cellulose synthesis: intramolecular and biosynthetic effects. Plant, Cell & Environment 29, 1881–1889.
| Variation in oxygen isotope fractionation during cellulose synthesis: intramolecular and biosynthetic effects.Crossref | GoogleScholarGoogle Scholar |
Williams CB, Murray JG, Glunk A, Dawson TE, Nadkarni NM, Gotsch SG (2020) Vascular epiphytes show low physiological resistance and high recovery capacity to episodic, short-term drought in Monteverde, Costa Rica. Functional Ecology 34, 1537–1550.
| Vascular epiphytes show low physiological resistance and high recovery capacity to episodic, short-term drought in Monteverde, Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Andrade JL (1998) Water relations of two co-occurring epiphytic bromeliads. Journal of Plant Physiology 152, 545–554.
| Water relations of two co-occurring epiphytic bromeliads.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany 83, 183–192.
| How much water is in the tank? Model calculations for two epiphytic bromeliads.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Laube S, Schmidt G (2005) Long-term population dynamics of the epiphytic bromeliad, Werauhia sanguinolenta. Ecography 28, 806–814.
| Long-term population dynamics of the epiphytic bromeliad, Werauhia sanguinolenta.Crossref | GoogleScholarGoogle Scholar |