Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems
Kathy Steppe A C , An Saveyn A , Mary Anne McGuire B , Raoul Lemeur A and Robert O. Teskey BA Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B-9000 Ghent, Belgium.
B Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA.
C Corresponding author. Email: kathy.steppe@UGent.be
Functional Plant Biology 34(9) 785-792 https://doi.org/10.1071/FP07077
Submitted: 29 March 2007 Accepted: 14 June 2007 Published: 30 August 2007
Abstract
Rates of CO2 efflux of stems and branches are highly variable among and within trees and across stands. Scaling factors have only partially succeeded in accounting for the observed variations. In this study, the resistance to radial CO2 diffusion was quantified for tree stems of an eastern cottonwood (Populus deltoides Bartr. ex Marsh.) clone by direct manipulation of the CO2 concentration ([CO2]) of xylem sap under controlled conditions. Tree-specific linear relationships between rates of stem CO2 efflux (JO) and xylem [CO2] were found. The resistance to radial CO2 diffusion differed 6-fold among the trees and influenced the balance between the amount of CO2 retained in the xylem v. that which diffused to the atmosphere. Therefore, we hypothesised that variability in the resistance to radial CO2 diffusion might be an overlooked cause for the inconsistencies and large variations in woody tissue CO2 efflux. It was found that transition from light to dark conditions caused a rapid increase in JO and xylem [CO2], both in manipulated trees and in an intact tree with no sap manipulation. This resulted in an increased resistance to radial CO2 diffusion during the dark, at least for trees with smaller daytime resistances. Stem diameter changes measured in the intact tree supported the idea that higher actual respiration rates occurred at night owing to higher metabolism in relation to an improved water status and higher turgor pressure.
Additional keywords: carbon dioxide, clone, permeability, sap velocity, stem diameter changes, stem respiration.
Acknowledgements
The authors wish to thank the Research Foundation – Flanders (FWO) for the Postdoctoral Fellow funding granted to the first author and for the travel funding granted to the first and the second author. The authors also wish to thank the Special Research Fund (BOF) of Ghent University for the PhD funding granted to the second author. This project was supported by grants from the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (2003–35100–13783) and the National Science Foundation (0445495) to ROT; and by a grant to ROT and MAM from the Global Forest Foundation.
Alessio G,
Pietrini F,
Brilli F, Loreto F
(2005) Characteristics of CO2 exchange between peach stems and the atmosphere. Functional Plant Biology 32, 787–795.
| Crossref | GoogleScholarGoogle Scholar |
Barbour MM,
Cernusak LA,
Whitehead D,
Griffin KL,
Turnbull MH,
Tissue DT, Farquhar GD
(2005) Nocturnal stomatal conductance and implications for modelling δ18O of leaf-respired CO2 in temperate tree species. Functional Plant Biology 32, 1107–1121.
| Crossref | GoogleScholarGoogle Scholar |
Bowman WP,
Barbour MM,
Turnbull MH,
Tissue DT,
Whitehead D, Griffin KL
(2005) Sap flow rates and sapwood density are critical factors in within- and between-tree variation in CO2 efflux from stems of mature Dacrydium cupressinum trees. New Phytologist 167, 815–828.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bucci SJ,
Scholz FG,
Goldstein G,
Meinzer FC,
Hinojosa JA,
Hoffmann WA, Franco AC
(2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiology 24, 1119–1127.
| PubMed |
Bushong FW
(1907) Composition of gas from cottonwood trees. Transactions of the Kansas Academy of Science 21, 53.
| Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Marshall JD
(2000) Photosynthetic refixation in branches of western white pine. Functional Ecology 14, 300–311.
| Crossref | GoogleScholarGoogle Scholar |
Damesin C,
Ceschia E,
Le Goff N,
Ottorini JM, Dufrene E
(2002) Stem and branch respiration of beech: from tree measurements to estimations at the stand level. New Phytologist 153, 159–172.
| Crossref | GoogleScholarGoogle Scholar |
Daudet FA,
Améglio T,
Cochard H,
Archilla O, Lacointe A
(2005) Experimental analysis of the role of water and carbon in tree stem diameter variations. Journal of Experimental Botany 56, 135–144.
| PubMed |
Eklund L
(1990) Endogenous levels of oxygen, carbon dioxide and ethylene in stems of Norway spruce trees during one growing season. Trees 4, 150–154.
| Crossref |
Eklund L
(1993) Seasonal variations of O2, CO2, and ethylene in oak and maple stems. Canadian Journal of Forest Research 23, 2608–2610.
| Crossref |
Eklund L, Lavigne MB
(1995) Restricted lateral gas movement in Pinus strobus branches. Trees 10, 83–85.
| Crossref |
Gartner BL,
Moore JR, Gardiner BA
(2004) Gas in stems: abundance and potential consequences for tree biomechanics. Tree Physiology 24, 1239–1250.
| PubMed |
Granier A
(1985) A new method of sap flow measurements in tree stems. Annales Des Sciences Forestieres 42, 193–200.
| Crossref | GoogleScholarGoogle Scholar |
Granier A
(1987) Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiology 3, 309–319.
| PubMed |
Groh B,
Hübner C, Lendzian KJ
(2002) Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215, 794–801.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hari P,
Nygren P, Korpilahti E
(1991) Internal circulation of carbon within a tree. Canadian Journal of Forest Research 21, 514–515.
| Crossref |
Hook DD,
Brown CL, Wetmore RH
(1972) Aeration in trees. Botanical Gazette (Chicago, Ill.) 133, 443–454.
| Crossref | GoogleScholarGoogle Scholar |
Klasnja B,
Kopitovic S, Orlovic S
(2003) Variability of some wood properties of eastern cottonwood (Populus deltoides Bartr.) clones. Wood Science and Technology 37, 331–337.
| Crossref | GoogleScholarGoogle Scholar |
Kinerson RS
(1975) Relationships between plant surface area and respiration in loblolly pine. Journal of Applied Ecology 12, 965–971.
| Crossref | GoogleScholarGoogle Scholar |
Lavigne MB, Ryan MG
(1997) Growth and maintenance respiration rates of aspen, black spruce and jack pine stems at northern and southern BOREAS sites. Tree Physiology 17, 543–551.
| PubMed |
Lavigne MB,
Franklin SE, Hunt ER
(1996) Estimating stem maintenance respiration rates of dissimilar balsam fir stands. Tree Physiology 16, 687–695.
| PubMed |
Lendzian KJ
(2006) Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen and carbon dioxide. Journal of Experimental Botany 57, 2535–2546.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Levy PE,
Meir P,
Allen SJ, Jarvis PG
(1999) The effect of aqueous transport of CO2 in xylem sap on gas exchange in woody plants. Tree Physiology 19, 53–58.
| PubMed |
Maier CA
(2001) Stem growth and respiration in loblolly pine plantations differing in soil resource availability. Tree Physiology 21, 1183–1193.
| PubMed |
McGuire MA, Teskey RO
(2002) Microelectrode technique for in situ measurement of carbon dioxide concentrations in xylem sap of trees. Tree Physiology 22, 807–811.
| PubMed |
McGuire MA, Teskey RO
(2004) Estimating stem respiration in trees by a mass balance approach that accounts for internal and external fluxes of CO2. Tree Physiology 24, 571–578.
| PubMed |
McGuire MA,
Cerasoli S, Teskey RO
(2007) CO2 fluxes and respiration of branch segments of sycamore (Platanus occidentalis L.) examined at different sap velocities, branch diameters, and temperatures. Journal of Experimental Botany 58, 2159–2168.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pilarski J
(1994) Diffusion of carbon dioxide through the cork and stomata in lilac. Acta Physiologiae Plantarum 16, 137–140.
Ryan MG
(1990) Growth and maintenance respiration in stems of Pinus contorta and Picea engelmannii. Canadian Journal of Forest Research 20, 48–57.
Ryan MG
(1991) A simple method for estimating gross carbon budgets for vegetation in forest ecosystems. Tree Physiology 9, 255–266.
| PubMed |
Saveyn A,
Steppe K, Lemeur R
(2007) Daytime depression in tree stem CO2 efflux rates: is it caused by low stem turgor pressure? Annals of Botany 99, 477–485.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schönherr J, Ziegler H
(1980) Water permeability of Betula periderm. Planta 147, 345–354.
| Crossref | GoogleScholarGoogle Scholar |
Snyder KA,
Richards JH, Donovan LA
(2003) Night-time conductance in C3 and C4 species: do plants lose water at night? Journal of Experimental Botany 54, 861–865.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sorz J, Hietz P
(2006) Gas diffusion through wood: implications for oxygen supply. Trees 20, 34–41.
| Crossref | GoogleScholarGoogle Scholar |
Sprugel DG
(1990) Components of woody-tissue respiration in young Abies amabilis (Dougl.) Forbes trees. Trees 4, 88–98.
| Crossref |
Steppe K,
De Pauw DJW,
Lemeur R, Vanrolleghem PA
(2006) A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. Tree Physiology 26, 257–273.
| PubMed |
Steppe K, Lemeur R
(2004) An experimental system for analysis of the dynamic sap-flow characteristics in young trees: results of a beech tree. Functional Plant Biology 31, 83–92.
| Crossref | GoogleScholarGoogle Scholar |
Stockfors J, Linder S
(1998) Effect of nitrogen on the seasonal course of growth and maintenance respiration of Norway spruce trees. Tree Physiology 18, 155–166.
| PubMed |
Teskey RO, McGuire MA
(2002) Carbon dioxide transport in xylem causes errors in estimation of rates of respiration in stems and branches of trees. Plant, Cell & Environment 25, 1571–1577.
| Crossref | GoogleScholarGoogle Scholar |
Teskey RO, McGuire MA
(2005) CO2 transported in xylem sap affects CO2 efflux from Liquidambar styraciflua and Platanus occidentalis stems, and contributes to observed wound respiration phenomena. Trees 19, 357–362.
| Crossref | GoogleScholarGoogle Scholar |
Teskey RO, McGuire MA
(2007) Measurement of stem respiration of sycamore (Platanus occidentalis L.) trees involves internal and external fluxes of CO2 and possible transport of CO2 from roots. Plant, Cell & Environment 30, 570–579.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wittmann C,
Pfanz H,
Loreto F,
Centritto M,
Pietrini F, Alessio G
(2006) Stem CO2 release under illumination: corticular photosynthesis, photorespiration or inhibition of mitochondrial respiration? Plant, Cell & Environment 29, 1149–1158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |