Abstract
Key message
Besides stem temperature, seasonality and vertical gradient in stem diameter growth strongly affect both seasonal and vertical variations in stem CO 2 efflux.
Abstract
Stem CO2 efflux (E s) is known to vary seasonally and vertically along tree stems. We measured E s at various heights in a 50-year-old hinoki cypress [Chamaecyparis obtusa (Sieb. et Zucc) Endl.] stand over 2 consecutive years in Central Japan. Effects of stem temperature (T s), daily stem diameter increment (D i), and difference in vapor pressure deficit between nighttime and daytime (VPDdiff) on seasonal variation in daily E s were examined by a generalized linear model (GLM). Daily E s exhibited a substantial seasonal variation, which was mostly affected by T s and D i. Any effect of VPDdiff, which was assumed to be an index of daily sap flow rate, was not detected. The GLM prediction of daily E s from the combination of T s and D i showed good agreement with the observed seasonal trend in daily E s. These results suggest that, in addition to stem temperature as the important environmental factor, stem radial growth is a significant phenological factor influencing seasonal variation in E s. Additionally, the intercept of GLM, which indicates the basal daily efflux that is independent of T s and D i, was closely related to the annual diameter increment. Furthermore, a strong relationship was found between annual E s and annual diameter increment. These findings suggest that variation in stem diameter growth along stems is considerably responsible for the observed vertical variation in E s. Therefore, stem radial growth can affect both seasonal and spatial variations in stem CO2 efflux.
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Acosta M, Pavelka M, Pokorný R, Janouš D, Marek MV (2008) Seasonal variation in CO2 efflux of stems and branches of Norway spruce trees. Ann Bot 101:469–477
Adu-Bredu S, Yokota T, Hagihara A (1996) Carbon balance of the aerial parts of a young hinoki cypress (Chamaecyparis obtusa) stand. Tree Physiol 16:239–245
Adu-Bredu S, Yokota T, Hagihara A (1997) Long-term respiratory cost of maintenance and growth of field-grown young hinoki cypress (Chamaecyparis obtusa). Ann Bot 80:753–758
Aiba S-I, Kohyama T (1996) Tree species stratification in relation to allometry and demography in a warm-temperate rain forest. J Ecol 84:207–218
Amthor JS (1984) The role of maintenance respiration in plant growth. Plant Cell Environ 7:561–569
Amthor JS (1989) Respiration and crop productivity. Springer, New York
Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Ann Bot 86:1–20
Araki MG (2006) Vertical variations of stem temperature and relationships between stem and air temperatures in Chamaecyparis obtusa trees. Kyushu J For Res 59:85–86 (in Japanese)
Araki MG, Utsugi H, Kajimoto T, Han Q, Kawasaki T, Chiba Y (2010) Estimation of whole-stem respiration, incorporating vertical and seasonal variations in stem CO2 efflux rate, of Chamaecyparis obtusa trees. J For Res 15:115–122
Atkin OK, Bruhn D, Tjoelker MG (2005) Response of plant respiration to changes in temperature: mechanisms and consequences of variations in Q10 values and acclimation. In: Lambers H, Ribas-Carbo M (eds) plant respiration. Springer, Dordrecht, pp 95–135
Aubrey DP, Teskey RO (2009) Root-derived CO2 efflux via xylem stream rivals soil CO2 efflux. New Phytol 184:35–40
Bloemen J, McGuire MA, Aubrey DP, Teskey RO, Steppe K (2013) Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees. New Phytol 197:555–565
Bloemen J, Agneessens L, Van Meulebroek L, Aubrey DP, McGuire MA, Teskey RO, Steppe K (2014) Stem girdling affects the quantity of CO2 transported in xylem as well as CO2 efflux from soil. New Phytol 201:897–907
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 Phytol 167:815–828
Bowman WP, Turnbull MH, Tissue DT, Whitehead D, Griffin KL (2008) Sapwood temperature gradients between lower stems and the crown do not influence estimates of stand-level stem CO2 efflux. Tree Physiol 28:1553–1559
Brito P, Morales D, Wieser G, Jiménez MS (2010) Spatial and seasonal variations in stem CO2 efflux of Pinus canariensis at their upper distribution limit. Trees 24:523–531
Carey EV, DeLucia EH, Ball JT (1996) Stem maintenance and construction respiration in Pinus ponderosa grown in different concentrations of atmospheric CO2. Tree Physiol 16:125–130
Carey EV, Callaway RM, DeLucia EH (1997) Stem respiration of ponderosa pines grown in contrasting climates: implications for global climate change. Oecologia 111:19–25
Cavaleri MA, Oberbauer SF, Ryan MG (2006) Wood CO2 efflux in a primary tropical rain forest. Glob Chang Biol 12:2442–2458
Ceschia É, Damesin C, Lebaube S, Pontailler JY, Dufrêne É (2002) Spatial and seasonal variations in stem respiration of beech trees (Fagus sylvatica). Ann For Sci 59:801–812
Chambers JQ, Tribuzy ES, Toledo LC, Crispim BF, Higuchi N, Santos J, Araújo AC, Kruijt B, Nobre AD, Trumbore SE (2004) Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency. Ecol Appl 14(4 Suppl.):S72–S88
Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-plus. Wiley, London
Damesin C (2003) Respiration and photosynthesis characteristics of current-year stems of Fagus sylvatica: from the seasonal pattern to an annual balance. New Phytol 158:465–475
Damesin C, Ceschia E, Le Goff N, Ottorini JM, Dufrêne E (2002) Stem and branch respiration of beech: from tree measurements to estimations at the stand level. New Phytol 153:159–172
Dannoura M, Maillard P, Fresneau C, Plain C, Berveiller D, Gerant D, Chipeaux C, Bosc A, Ngao J, Damesin C, Loustau D, Epron D (2011) In situ assessment of the velocity of carbon transfer by tracing 13C in trunk CO2 efflux after pulse labelling: variations among tree species and seasons. New Phytol 190:181–192
Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees 19:402–408
Edwards NT, Tschaplinski TJ, Norby RJ (2002) Stem respiration increases in CO2-enriched sweetgum trees. New Phytol 155:239–248
Etzold S, Zweifel R, Ruehr NK, Eugster W, Buchmann N (2013) Long-term stem CO2 concentration measurements in Norway spruce in relation to biotic and abiotic factors. New Phytol 197:1173–1184
Forest soil division (1976) Classification of forest soil in Japan (1975). Bull Gov Forest Exp Stn 280:1–28 (in Japanese, with English summary)
Fujiwara T, Yamashita K, Kuroda K (2007) Basic densities as a parameter for estimating the amount of carbon removal by forests and their variation. Bull FFPRI 6:215–226
Fukatsu E, Takahashi M, Fujisawa Y, Kurinobu S (2006) The effects of several traits on family variation of carbon contents in stem of hinoki cypress (Cupressus obtusa). Bull Kantou Jpn For Soc 57:143–145 (in Japanese)
Gartner BL, Moore JR, Gardiner BA (2004) Gas in stems: abundance and potential consequences for tree biomechanics. Tree Physiol 24:1239–1250
Gruber A, Wieser G, Oberhuber W (2009) Intra-annual dynamics of stem CO2 efflux in relation to cambial activity and xylem development in Pinus cembra. Tree Physiol 29:641–649
Hagihara A, Hozumi K (1981) Respiration consumption by woody organs in a Chamaecyparis obtusa plantation. J Jpn For Soc 63:156–164
Hagihara A, Hozumi K (1983) Studies on the primary production in a Chamaecyparis obtusa plantation. J Jpn For Soc 65:357–365
Hölttä T, Kolari P (2009) Interpretation of stem CO2 efflux measurements. Tree Physiol 29:1447–1456
Japan Meteorology Agency (2013) Climate statistics. http://www.data.jma.go.jp/obd/stats/etrn/index.php
Kakubari Y (1988) Diurnal and seasonal fluctuations in the bark respiration of standing Fagus sylvatica trees at Solling, West Germany. J Jpn For Soc 70:64–70
Katayama A, Kume T, Komatsu H, Saitoh TM, Ohashi M, Nakagawa M, Suzuki M, Otsuki K, Kumagai T (2013) Carbon allocation in a Bornean tropical rainforest without dry seasons. J Plant Res 126:505–515
Katayama A, Kume T, Komatsu H, Ohashi M, Matsumoto K, Ichihashi R, Kumagai T, Otsuki K (2014) Vertical variations in wood CO2 efflux for live emergent trees in a Bornean tropical rainforest. Tree Physiol 34:503–512
Kira T, Shidei T (1967) Primary production and turnover of organic matter in different forest ecosystems of the Western Pacific. Jap J Ecol 17:70–87
Kozlowski TT, Kramer PJ, Pallardy SG (1991) The physiological ecology of woody plants. Academic Press, San Diego
Kramer PJ, Kozlowski TT (1979) Physiology of woody plants. Academic Press, New York
Landsberg JJ, Gower ST (1997) Applications of physiological ecology to forest management. Academic Press, San Diego
Lavigne MB (1996) Comparing stem respiration and growth of jack pine provenances from northern and southern locations. Tree Physiol 16:847–852
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 Physiol 17:543–551
Lavigne MB, Little CHA, Riding RT (2004) Changes in stem respiration rate during cambial reactivation can be used to refine estimates of growth and maintenance respiration. New Phytol 162:81–93
Lendzian KJ (2006) Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. J Exp Bot 57:2535–2546
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 Physiol 19:53–58
Maier CA (2001) Stem growth and respiration in loblolly pine plantations differing in soil resource availability. Tree Physiol 21:1183–1193
Maier CA, Clinton BD (2006) Relationship between stem CO2 efflux, stem sap velocity and xylem CO2 concentration in young loblolly pine trees. Plant Cell Environ 29:1471–1483
Maier CA, Johnsen KH, Clinton BD, Ludovici KH (2010) Relationships between stem CO2 efflux, substrate supply, and growth in young loblolly pine trees. New Phytol 185:502–513
McCree KJ (1974) Equations for the rate of dark respiration of white clover and grain sorghum, as functions of dry weight, photosynthetic rate, and temperature. Crop Sci 14:509–514
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 Physiol 24:571–578
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. J Exp Bot 58:2159–2168
Meir P, Grace J (2002) Scaling relationships for woody tissue respiration in two tropical rain forests. Plant Cell Environ 25:963–973
Mori S, Hagihara A (1988) Respiration in stems of hinoki (Chamaecyparis obtusa) trees. J Jpn For Soc 70:187–481
Negisi K (1979) Bark respiration rate in stem segments detached from young Pinus densiflora trees in relation to velocity of artificial sap flow. J Jpn For Soc 61:88–93
Ninomiya I, Hozumi K (1983) Respiration of forest trees (II) Measurament of nighttime respiration in a Chamaecyparis obtusa plantation. J Jpn For Soc 65:193–200
Ogawa K (2006) Stem respiration is influenced by pruning and girdling in Pinus sylvestris. Scand J Forest Res 21:293–298
Ogawa H, Kira T (1977) Methods of estimating forest biomass. In: Shidei T, Kira T (eds) Primary productivity of Japanese forests, JIBP Synthesis, vol 16. University of Tokyo Press, Tokyo, pp 15–25
Oohata S, Shidei T (1972) Seasonal changes in respiratory rate of stems and their growth. Bull Kyoto Univ For 43:63–72
Oohata S, Yamakura T, Saito H, Shidei T (1971) A study on the vertical distribution of respiratory activity of a 40-year-old stand of Chamaecyparis obtusa. Bull Kyoto Univ For 42:103–116
Paembonan SA, Hagihara A, Hozumi K (1991) Long-term measurement of CO2 release from the aboveground parts of a hinoki forest tree in relation to air temperature. Tree Physiol 8:399–405
Paembonan SA, Hagihara A, Hozumi K (1992) Long-term respiration in relation to growth and maintenance processes of the aboveground parts of a hinoki forest tree. Tree Physiol 10:101–110
Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften 89:147–162
Pruyn ML, Gartner BL, Harmon ME (2002a) Respiratory potential in sapwood of old versus young ponderosa pine trees in the Pacific Northwest. Tree Physiol 22:105–116
Pruyn ML, Gartner BL, Harmon ME (2002b) Within-stem variation of respiration in Pseudotsuga menziesii (Douglas-fir) trees. New Phytol 154:359–372
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rossi S, Deslauriers A, Morin H (2003) Application of the Gompertz equation for the study of xylem cell development. Dendrochronologia 21:33–39
Ryan MG (1990) Growth and maintenance respiration in stems of Pinus contorta and Picea engelmannii. Can J For Res 20:48–57
Ryan MG, Waring RH (1992) Maintenance respiration and stand development in a subalpine lodgepole pine forest. Ecology 73:2100–2108
Ryan MG, Gower ST, Hubbard RM, Waring RH, Gholz HL, Cropper WP, Running SW (1995) Woody tissue maintenance respiration of four conifers in contrasting climates. Oecologia 101:133–140
Ryan MG, Hubbard RM, Pongratic S, Raison RJ, McMurtrie RE (1996) Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status. Tree Physiol 16:333–343
Ryan MG, Lavigne MB, Gower ST (1997) Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate. J Geophys Res-Atmos 102:28871–28883
Sakai Y, Ugawa S, Ishizuka S, Takahashi M, Takenaka C (2012) Wood density and carbon and nitrogen concentrations in deadwood of Chamaecyparis obtusa and Cryptomeria japonica. Soil Sci Plant Nutr 58:526–537
Saveyn A, Steppe K, Lemeur R (2007) Drought and the diurnal patterns of stem CO2 efflux and xylem CO2 concentration in young oak (Quercus robur). Tree Physiol 27:365–374
Saveyn A, Steppe K, Lemeur R (2008a) Report on non-temperature related variations in CO2 efflux rates from young tree stems in the dormant season. Trees 22:165–174
Saveyn A, Steppe K, McGuire MA, Lemeur R, Teskey RO (2008b) Stem respiration and carbon dioxide efflux of young Populus deltoides trees in relation to temperature and xylem carbon dioxide concentration. Oecologia 154:637–649
Sorz J, Hietz P (2006) Gas diffusion through wood: implications for oxygen supply. Trees 20:34–41
Sprugel DG (1990) Components of woody-tissue respiration in young Abies amabilis (Dougl.) Forbes trees. Trees 4:88–98
Sprugel DG, Benecke U (1991) Measuring woody-tissue respiration and photosynthesis. In: Lassoie JP, Hinckley TM (eds) Techniques and approaches in forest tree ecophysiology. CRC Press, Boca Raton, pp 329–355
Sprugel DG, Ryan MG, Brooks JR, Vogt KA, Martin TA (1995) Respiration from the organ level to the stand. In: Smith WK, Hinckley TM (eds) Resource physiology of conifers: aquisition, allocation and utilization. Academic Press, San Diego, pp 255–299
Steppe K, Saveyn A, McGuire MA, Lemeur R, Teskey RO (2007) Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems. Funct Plant Biol 34:785–792
Stockfors J (2000) Temperature variations and distribution of living cells within tree stems: implications for stem respiration modelling and scale-up. Tree Physiol 20:1057–1062
Stockfors J, Linder S (1998) Effect of nitrogen on the seasonal course of growth and maintenance respiration in stems of Norway spruce trees. Tree Physiol 18:155–166
Tarvainen L, Räntfors M, Wallin G (2014) Vertical gradients and seasonal variation in stem CO2 efflux within a Norway spruce stand. Tree Physiol 34:488–502
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 Environ 25:1571–1577
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
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 Environ 30:570–579
Teskey RO, Saveyn A, Steppe K, McGuire MA (2008) Origin, fate and significance of CO2 in tree stems. New Phytol 177:17–32
Trumbore SE, Angert A, Kunert N, Muhr J, Chambers JQ (2013) What’s the flux? Unraveling how CO2 fluxes from trees reflect underlying physiological processes. New Phytol 197:353–355
Ubierna N, Kumar AS, Cernusak LA, Pangle RE, Gag PJ, Marshall JD (2009) Storage and transpiration have negligible effects on d13C of stem CO2 efflux in large conifer trees. Tree Physiol 29:1563–1574
Utsugi H (1999) Angle distribution of foliage in indivisual Chamaecyparis obtusa canopies and effect of angle on diffuse light penetration. Trees 14:1–9
Utsugi H, Araki M, Kawasaki T, Ishizuka M (2006) Vertical distributions of leaf area and inclination angle, and their relationship in a 46-year-old Chamaecyparis obtusa stand. For Ecol Manag 225:104–112
Vose JM, Ryan MG (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Glob Change Biol 8:182–193
Waring RH, Schlesinger WH (1985) Forest ecosystems concepts and management. Academic Press, San Diego
Wertin TM, Teskey RO (2008) Close coupling of whole-plant respiration to net photosynthesis and carbohydrates. Tree Physiol 28:1831–1840
Wieser G, Bahn M (2004) Seasonal and spatial variation of woody tissue respiration in a Pinus cembra tree at the alpine timberline in the central Austrian Alps. Trees 18:576–580
Wieser G, Gruber A, Bahn M, Catalá E, Carrillo E, Jiménez MS, Morales D (2009) Respiratory fluxes in a Canary Islands pine forest. Tree Physiol 29:457–466
Wittmann C, Pfanz H (2007) Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees. J Exp Bot 58:4293–4306
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 Environ 29:1149–1158
Yoda K, Shinozaki K, Ogawa H, Hozumi K, Kira T (1965) Estimation of the total amount of respiration in woody organs of trees and forest communities. J Biol Osaka City Univ 16:15–26
Yokota T, Hagihara A (1998) Changes in the relationship between tree size and aboveground respiration in field-grown hinoki cypress (Chamaecyparis obtusa) trees over three years. Tree Physiol 18:37–43
Yokota T, Ogawa K, Hagihara A (1994) Dependence of the aboveground respiration of hinoki cypress (Chamaecyparis obtusa) on tree size. Tree Physiol 14:467–479
Zha TS, Kellomäki S, Wang KY, Ryyppö A, Niinistö S (2004) Seasonal and annual stem respiration of Scots pine trees under boreal conditions. Ann Bot 94:889–896
Zha TS, Kellomäki S, Wang KY, Ryyppö A (2005) Respiratory response of Scots pine stems to 5 years of exposure to elevated CO2 concentration and temperature. Tree Physiol 25:49–56
Author contribution statement
MG Araki: Data collection, data analysis, manuscript writing. T Kajimoto: manuscript reviewing. Q Han: Data collection, manuscript reviewing. T Kawasaki: Data collection. H Utsugi: Design of the study, data collection. K Gyokusen: Conception of data analysis. Y Chiba: Conception and design of the study.
Acknowledgments
The authors thank the two anonymous reviewers for valuable and helpful comments on a previous version of the manuscript. We also thank Dr. Daisuke Kabeya, Department of Plant Ecology, Forestry and Forest Products Research Institute, for advice on statistical analysis. This study was supported by research grants #199903 and #201104 of Forestry and Forest Products Research Institute.
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The authors declare that they have no conflict of interest.
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Araki, M.G., Kajimoto, T., Han, Q. et al. Effect of stem radial growth on seasonal and spatial variations in stem CO2 efflux of Chamaecyparis obtusa . Trees 29, 499–514 (2015). https://doi.org/10.1007/s00468-014-1127-6
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DOI: https://doi.org/10.1007/s00468-014-1127-6