Autotrofe bodemrespiratie in bosecosystemen: hoe belangrijk is intern CO2 transport via sapstroom?

Laura

Agneessens

Nieuw ontdekte interne CO2 flux beïnvloedt autotrofe bodemrespiratie

Ecosysteemrespiratie is, na fotosynthese, de grootste terrestrische koolstofflux in bosecosystemen. Deze flux zorgt voor de vrijstelling van 18 keer meer CO2 dan de wereldwijde verbranding van fossiele brandstoffen. Een goede kennis van de verschillende processen en fluxen in de koolstofcyclus is dus noodzakelijk om de impact en feedback tussen klimaatsverandering en ecosystemen correct te kunnen inschatten. Een belangrijk onderdeel van ecosysteemrespiratie is wortelrespiratie. Onderzoek aan het Laboratorium voor Plantecologie aan de Universiteit Gent toont het belang aan van een nieuw ontdekte interne CO2 flux in bomen. Via deze flux wordt een gedeelte van de CO2 afkomstig van wortelrespiratie via de opwaartse sapstroom bovengronds naar de stam getransporteerd. Deze interne CO2 flux werd tot nog toe niet in rekening gebracht bij bepaling van wortel- en stamrespiratie. Ons onderzoek toonde echter aan dat dit kan leiden tot een onderschatting van wortelrespiratie tot 45%. Tezelfdertijd droeg CO2 afkomstig van wortelrespiratie voor de helft bij aan de CO2 vrijgesteld door de stam, wat aantoont dat in de gangbare praktijk de stamrespiratie sterk overschat wordt.

Bodem CO2 efflux vormt een belangrijke flux in ecosysteemrespiratie en bestaat uit een autotrofe component, de wortelrespiratie, en een heterotrofe component, de respiratie van bodemmicro-organismen. Algemeen wordt aangenomen dat alle CO2 afkomstig van wortelrespiratie volledig via de bodem terugkeert naar de atmosfeer en zo bijdraagt aan bodem CO2 efflux. Een schematisch overzicht van koolstoffluxen rond een boom wordt gegeven in Figuur 1. Recent onderzoek suggereert dat een gedeelte van de CO2 afkomstig van wortelrespiratie de wortels niet verlaat, maar intern oplost in de sapstroom en opwaarts getransporteerd wordt. Een gedeelte van de CO2 afkomstig van wortelrespiratie kan zo bovengronds naar de atmosfeer diffunderen en bijdragen tot stam CO2 efflux. Metingen van CO2 efflux uit stam of bodem worden vaak gebruikt als schatting van de respiratiesnelheid van het beschouwde weefsel. Door oplossing en transport van CO2 in de sapstroom komt de plaats van diffusie niet noodzakelijk overeen met de plaats van respiratie. Door intern transport te verwaarlozen, betekent dit een onderschatting van de respiratiesnelheid van bepaalde weefsels tegenover een overschatting van andere weefsels.

Om het belang van intern CO2 transport te bepalen, werd in een plantage te Zwijnaarde de stam van 7-jarige eiken (Quercus robur L.) geringd. Bij ringen wordt een deel van het stamweefsel verwijderd, waardoor de stroom van fotosynthetische producten van de bladeren naar de wortels wordt onderbroken. Hierdoor zal de wortelrespiratie en dus de totale bodem CO2 efflux afnemen. Indien een gedeelte van de CO2 afkomstig van wortelrespiratie intern blijft, moet er na het ringen echter ook een daling in de interne CO2 concentratie in de stam te zien zijn. Vijf dagen na het ringen werd een afname van zowel de bodem CO2 efflux als de interne CO2 concentratie van respectievelijk 22% en 21% waargenomen. Deze daling waargenomen in de interne CO2 concentratie bevestigt het opwaartse transport van CO2 uit de wortels naar de stam.

Bij eerdere bepalingen van wortelrespiratie werd het intern CO2 transport via de sapstroom niet in kaart gebracht. Uit deze studie bleek het niet in rekening brengen van intern CO2 transport gedurende periodes van hoge sapstroom de wortelrespiratie met 45% te onderschatten. Op een dagelijkse basis bedroeg deze onderschatting 25%. Het opwaarts getransporteerde CO2 kan bovengronds diffunderen en zo foutief worden toegeschreven aan stamrespiratie. Via opstelling van een koolstofmassabalans rond een segment van de stam bleek de bijdrage van CO2 afkomstig van wortelrespiratie aan stam CO2 efflux op een dagelijkse basis 50% te bedragen.

Uit deze studie blijkt aldus dat om de boven- en ondergrondse respiratie en de koolstofcyclus in ecosystemen correct in te schatten, zowel intern CO2 transport als de boven- en ondergrondse CO2 efflux beschouwd moet worden. Een accurate bepaling van boven- en ondergrondse respiratie is namelijk vereist om een grondige kennis van de koolstofkringloop in een bosecosystemen te bekomen. Deze kennis is van essentieel belang voor de correcte inschatting van de koolstofhuishouding in ecosystemen en om de invloed van wijzigende omgevingsfactoren op de interacties tussen bio- en atmosfeer in te schatten.

Bibliografie

Faculteit Bio-ingenieurswetenschappen
Academiejaar 2011-2012
Autotrofe bodemrespiratie in bosecosystemen: hoe
belangrijk is intern CO2 transport via sapstroom?
Laura Agneessens
Promotor: Prof. dr. ir. Kathy Steppe
Tutor: ir. Jasper Bloemen
Masterproef voorgedragen tot het behalen van de graad van
Master in de bio-ingenieurswetenschappen: Milieutechnologie
ii
Bibliograﬁe
Adachi, M., Ishida, A., Bunyavejchewin, S., Okuda, T., & Koizumi, H. (2009). Spatial and
temporal variation in soil respiration in a seasonally dry tropical forest, thailand. Journal of
Tropical Ecology, 25, 531–539.
Amiro, B. D. & Ewing, L. L. (1992). Physiological conditions and uptake of inorganic C14 by
plant-roots. Environmental and Experimental Botany, 32 (3), 203–211.
Amthor, J. S. (2000). The McCree-de Wit-penning de Vries-Thornley respiration paradigms: 30
years later. Annals of Botany, 86 (1), 1–20.
Amundson, R. G. & Davidson, E. A. (1990). Carbon-dioxide and nitrogenous gases in the soil
atmosphere. Journal of Geochemical Exploration, 38 (1-2), 13–41.
Arteca, R. N. & Poovaiah, B. W. (1982). Absorption of CO2 -C14 by potato roots and its subsequent
translocation. Journal of the American Society for Horticultural Science, 107 (3), 398–401.
Aschan, G. & Pfanz, H. (2003). Non-foliar photosynthesis - a strategy of additional carbon
acquisition. Flora, 198 (2), 81–97.
Atjay, G., Ketner, P., & Duvigneaud, P. (1979). Terrestrial primary production and photomass,
(pp. 129–182.). Chichester: Wiley.
Atkin, O., Bruhn, D., & Tjoelker, M. (2005). Response of Plant Respiration to Changes in
Temperature: Mechanisms and Consequences of Variations in Q10 Values and Acclimation,
chapter 7. Dordrecht: Springer.
Atkins, C. A. & Smith, P. M. C. (2007). Translocation in legumes: Assimilates, nutrients, and
signaling molecules. Plant Physiology, 144 (2), 550–561.
Aubrey, D. P., Boyles, J. G., Krysinsky, L. S., & Teskey, R. O. (2011). Spatial and temporal
patterns of xylem sap ph derived from stems and twigs of Populus deltoides L. Environmental
and Experimental Botany, 71 (3), 376–381.
Aubrey, D. P. & Teskey, R. O. (2009). Root-derived CO2 eﬄux via xylem stream rivals soil CO2
eﬄux. New Phytologist, 184 (1), 35–40.
Baath, E. & Wallander, H. (2003). Soil and rhizosphere microorganisms have the same Q10 for
respiration in a model system. Global Change Biology, 9 (12), 1788–1791.
Baldocchi, D. (2008). Breathing of the terrestrial biosphere: lessons learned from a global network
of carbon dioxide ﬂux measurement systems. Australian Journal of Botany, 56 (1), 1–26.
iii
Bibliograﬁe
Bekku, Y. S., Sakata, T., Nakano, T., & Koizumi, H. (2009). Midday depression in root respiration
of Quercus crispula and Chamaecyparis obtusa: its implication for estimating carbon cycling
in forest ecosystems. Ecological Research, 24 (4), 865–871.
Bekku, Y. S., Sakata, T., Tanaka, T., & Nakano, T. (2011). Midday depression of tree root
respiration in relation to leaf transpiration. Ecological Research, 26 (4), 791–799.
Bhupinderpal, S., Nordgren, A., Lofvenius, M. O., Hogberg, M. N., Mellander, P. E., & Hogberg,
P. (2003). Tree root and soil heterotrophic respiration as revealed by girdling of boreal scots
pine forest: extending observations beyond the ﬁrst year. Plant Cel l and Environment, 26 (8),
1287–1296.
Binkley, D., Stape, J. L., Takahashi, E. N., & Ryan, M. G. (2006). Tree-girdling to separate root
and heterotrophic respiration in two Eucalyptus stands in brazil. Oecologia, 148 (3), 447–454.
Bird, J. A., Herman, D. J., & Firestone, M. K. (2011). Rhizosphere priming of soil organic matter
by bacterial groups in a grassland soil. Soil Biology & Biochemistry, 43 (4), 718–725.
Bonkowski, M. (2004). Protozoa and plant growth: the microbial loop in soil revisited. New
Phytologist, 162 (3), 617–631.
Boone, R. D., Nadelhoﬀer, K. J., Canary, J. D., & Kaye, J. P. (1998). Roots exert a strong
inﬂuence on the temperature sensitivity of soil respiration. Nature, 396 (6711), 570–572.
Borken, W., Savage, K., Davidson, E. A., & Trumbore, S. E. (2006). Eﬀects of experimental
drought on soil respiration and radiocarbon eﬄux from a temperate forest soil. Global Change
Biology, 12 (2), 177–193.
Boutton, T. W., Archer, S. R., Midwood, A. J., Zitzer, S. F., & Bol, R. (1998). delta C13 values
of soil organic carbon and their use in documenting vegetation change in a subtropical savanna
ecosystem. Geoderma, 82 (1-3), 5–41.
Bowman, W. P., Barbour, M. M., Turnbull, M. H., Tissue, D. T., Whitehead, D., & Griﬃn, K. L.
(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 (3), 815–828.
Buckley, T. N. (2005). The control of stomata by water balance. New Phytologist, 168 (2), 275–291.
Butler, J. (1991). Carbon dioxide equilibria and their applications. Lewis Publishers.
Carbone, M. S. & Vargas, R. (2008). Automated soil respiration measurements: new information,
opportunities and challenges. New Phytologist, 177 (2), 295–297.
iv
Bibliograﬁe
Cerasoli, S., McGuire, M. A., Faria, J., Mourato, M., Schmidt, M., Pereira, J. S., Chaves, M. M.,
& Teskey, R. O. (2009). CO2 eﬄux, CO2 concentration and photosynthetic reﬁxation in stems
of Eucalyptus globulus (labill.). Journal of Experimental Botany, 60 (1), 99–105.
Cernusak, L. A. & Marshall, J. D. (2000). Photosynthetic reﬁxation in branches of western white
Pine. Functional Ecology, 14 (3), 300–311.
Ceschia, E., Damesin, C., Lebaube, S., Pontailler, J. Y., & Dufrene, E. (2002). Spatial and seasonal
variations in stem respiration of beech trees (Fagus sylvatica). Annals of Forest Science, 59 (8),
801–812.
Cheng, W. (2009). Rhizosphere priming eﬀect: Its functional relationships with microbial turn-
over, evapotranspiration, and C-N budgets. Soil Biology & Biochemistry, 41 (9), 1795–1801.
Cheng, Y. H., Arakawa, O., Kasai, M., & Sawada, S. (2008). Analysis of reduced photosynthesis
in the apple leaf under sink-limited conditions due to girdling. Journal of the Japanese Society
for Horticultural Science, 77 (2), 115–121.
Colmer, T. D. (2003). Long-distance transport of gases in plants: a perspective on internal aeration
and radial oxygen loss from roots. Plant Cel l and Environment, 26 (1), 17–36.
Conant, R. T., Ryan, M. G., Agren, G. I., Birge, H. E., Davidson, E. A., Eliasson, P. E., Evans,
S. E., Frey, S. D., Giardina, C. P., Hopkins, F. M., Hyvonen, R., Kirschbaum, M. U. F., Lavallee,
J. M., Leifeld, J., Parton, W. J., Steinweg, J. M., Wallenstein, M. D., Wetterstedt, J. A. M., &
Bradford, M. A. (2011). Temperature and soil organic matter decomposition rates - synthesis
of current knowledge and a way forward. Global Change Biology, 17 (11), 3392–3404.
Conen, F. & Smith, K. A. (2000). An explanation of linear increases in gas concentration under
closed chambers used to measure gas exchange between soil and the atmosphere. European
Journal of Soil Science, 51 (1), 111–117.
Couteaux, M. M., Mousseau, M., Celerier, M. L., & Bottner, P. (1991). Increased atmospheric
CO2 and litter quality - decomposition of sweet chestnut leaf litter with animal food webs of
diﬀerent complexities. Oikos, 61 (1), 54–64.
Crill, P. M., Keller, M., Weitz, A., Grauel, B., & Veldkamp, E. (2000). Intensive ﬁeld measurements
of nitrous oxide emissions from a tropical agricultural soil. Global Biogeochemical Cycles, 14 (1),
85–95.
Cutler, D., Botha, C., & Stevenson, D. (2008). Plant Anatomy: an applied approach. Blackwell
Publishing.
v
Bibliograﬁe
Dalsgaard, L., Mikkelsen, T. N., & Bastrup-Birk, A. (2011). Sap ﬂow for beech (Fagus sylvatica l.)
in a natural and a managed forest-eﬀect of spatial heterogeneity. Journal of Plant Ecology-Uk,
4 (1-2), 23–35.
Damesin, C., Ceschia, E., Le Goﬀ, N., Ottorini, J. M., & Dufrene, E. (2002). Stem and branch
respiration of beech: from tree measurements to estimations at the stand level. New Phytologist,
153 (1), 159–172.
Daudet, F. A., Ameglio, 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 (409), 135–144.
Davidson, E., Belk, E., & Boone, R. (1998). Soil water content and temperature as independent
or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global
Change Biology, 4 (2), 217–227.
Davidson, E. & Janssens, I. A. (2006). Temperature sensitivity of soil carbon decomposition and
feedbacks to climate change. Nature, 440 (7081), 165–173.
Davidson, E., Richardson, A., Savage, K., & Hollinger, D. (2006). A distinct seasonal pattern of
the ratio of soil respiration to total ecosystem respiration in a spruce-dominated forest. Global
Change Biology, 12 (2), 230–239.
Davidson, E., Savage, K., Verchot, L., & Navarro, R. (2002). Minimizing artifacts and biases in
chamber-based measurements of soil respiration. Agricultural and Forest Meteorology, 113 (1-4),
21–37. 6.
De Schepper, V., Steppe, K., Van Labeke, M.-C., & Lemeur, R. (2010). Detailed analysis of double
girdling eﬀects on stem diameter variations and sap ﬂow in young oak trees. Environmental
and Experimental Botany, 68 (2), 149–156.
De Vries, F. W. T. & Penning (1975). The cost of maintenance processes in plant cells. Annals
of Botany, 39 (1), 77–92.
Domec, J. C. & Pruyn, M. L. (2008). Bole girdling aﬀects metabolic properties and root, trunk
and branch hydraulics of young ponderosa pine trees. Tree Physiology, 28 (10), 1493–1504.
Enoch, H. Z. & Olesen, J. M. (1993). Plant-response to irrigation with water enriched with
carbon-dioxide. New Phytologist, 125 (2), 249–258.
Fahn, A. (1982). Plant Anatomy: Third Edition. Pergamon Press.
vi
Bibliograﬁe
Fang, C., Smith, P., Moncrieﬀ, J. B., & Smith, J. U. (2005). Similar response of labile and resistant
soil organic matter pools to changes in temperature. Nature, 433 (7021), 57–59.
Fenn, K. M., Malhi, Y., & Morecroft, M. D. (2010). Soil CO2 eﬄux in a temperate deciduous forest:
Environmental drivers and component contributions. Soil Biology & Biochemistry, 42 (10),
1685–1693.
Fisher, F. M. & Gosz, J. R. (1986). Eﬀects of trenching on soil processes and properties in a
new-mexico mixed-conifer forest. Biology and Fertility of Soils, 2 (1), 35–42.
Flores, H. E., Vivanco, J. M., & Loyola-Vargas, V. M. (1999). ‘Radicle’ biochemistry: the biology
of root-speciﬁc metabolism. Trends in Plant Science, 4 (6), 220–226.
Ford, C. R., Wurzburger, N., Hendrick, R. L., & Teskey, R. O. (2007). Soil DIC uptake and
ﬁxation in pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal
fungi. Tree Physiology, 27 (3), 375–383.
Frey, B., Hagedorn, F., & Giudici, F. (2006). Eﬀect of girdling on soil respiration and root
composition in a sweet chestnut forest. Forest Ecology and Management, 225 (1-3), 271–277.
Gansert, D. & Burgdorf, M. (2005). Eﬀects of xylem sap ﬂow on carbon dioxide eﬄux from stems
of birch (Betula pendula Roth). Flora, 200 (5), 444–455.
Gartner, B. L., Moore, J. R., & Gardiner, B. A. (2004). Gas in stems: abundance and potential
consequences for tree biomechanics. Tree Physiology, 24 (11), 1239–1250.
Gillman, M.; Hails, R. (1997). An Introduction to Ecological Model ling: Putting Practice Into
Theory. Oxford: Blackwell Science.
Goulden, M. L., Munger, J. W., Fan, S. M., Daube, B. C., & Wofsy, S. C. (1996). Exchange
of carbon dioxide by a deciduous forest: Response to interannual climate variability. Science,
271 (5255), 1576–1578.
Greenway, H., Armstrong, W., & Colmer, T. D. (2006). Conditions leading to high CO2 ( 5 kpa)
in waterlogged-ﬂooded soils and possible eﬀects on root growth and metabolism. Annals of
Botany, 98 (1), 9–32.
Gregory, P. J. (2006). Roots, rhizosphere and soil: the route to a better understanding of soil
science? European Journal of Soil Science, 57 (1), 2–12.
Grossiord, C., M. L. & Epron, D. (2012). Transpiration alters the contribution of autotrophic and
heterotrophic components of soil CO2 eﬄux. New Phytologist.
vii
Bibliograﬁe
Hanson, P. J., Edwards, N. T., Garten, C. T., & Andrews, J. A. (2000). Separating root and soil
microbial contributions to soil respiration: A review of methods and observations. Biogeoche-
mistry, 48 (1), 115–146.
Hari, P., Nygren, P., & Korpilahti, E. (1991). Internal circulation of carbon within a tree. Canadian
Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 21 (4), 514–515.
Heath, J., Ayres, E., Possell, M., Bardgett, R. D., Black, H. I. J., Grant, H., Ineson, P., &
Kerstiens, G. (2005). Rising atmospheric CO2 reduces sequestration of root-derived soil carbon.
Science, 309 (5741), 1711–1713.
Heinemeyer, A., Di Bene, C., Lloyd, A. R., Tortorella, D., Baxter, R., Huntley, B., Gelsomino, A.,
& Ineson, P. (2011). Soil respiration: implications of the plant-soil continuum and respiration
chamber collar-insertion depth on measurement and modelling of soil CO2 eﬄux rates in three
ecosystems. European Journal of Soil Science, 62 (1), 82–94.
Hogberg, P., Bhupinderpal, S., Lofvenius, M. O., & Nordgren, A. (2009). Partitioning of soil
respiration into its autotrophic and heterotrophic components by means of tree-girdling in old
boreal spruce forest. Forest Ecology and Management, 257 (8), 1764–1767.
Hogberg, P., Nordgren, A., Buchmann, N., Taylor, A. F. S., Ekblad, A., Hogberg, M. N., Nyberg,
G., Ottosson-Lofvenius, M., & Read, D. J. (2001). Large-scale forest girdling shows that current
photosynthesis drives soil respiration. Nature, 411 (6839), 789–792.
Horwath, W. R., Pregitzer, K. S., & Paul, E. A. (1994). CO14 allocation in tree soil systems. Tree
Physiology, 14 (10), 1163–1176.
Hutsch, B. W., Augustin, J., & Merbach, W. (2002). Plant rhizodeposition - an important
source for carbon turnover in soils. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur
Pﬂanzenernahrung Und Bodenkunde, 165 (4), 397–407.
Huxman, T. E., Snyder, K. A., Tissue, D., Leﬄer, A. J., Ogle, K., Pockman, W. T., Sandquist,
D. R., Potts, D. L., & Schwinning, S. (2004). Precipitation pulses and carbon ﬂuxes in semiarid
and arid ecosystems. Oecologia, 141 (2), 254–268.
Insam, H. (1990). Are the soil microbial biomass and basal respiration governed by the climatic
regime. Soil Biology & Biochemistry, 22 (4), 525–532.
Irvine, J., Law, B. E., & Kurpius, M. R. (2005). Coupling of canopy gas exchange with root and
rhizosphere respiration in a semi-arid forest. Biogeochemistry, 73 (1), 271–282.
viii
Bibliograﬁe
Janssens, I., Lankreijer, H., Matteucci, G., Kowalski, A., Buchmann, N., Epron, D., Pilegaard, K.,
Kutsch, W., Longdoz, B., Grunwald, T., Montagnani, L., Dore, S. abd Rebmann, C., Moors,
E. J., Grelle, A., Rannik, U., Ceulemans, R., & Valentini, R. (2001). Productivity overshadows
temperature in determining soil and ecosystem respiration across European forests. Global
Change Biology, 7 (3), 269–278.
Jassal, R., Black, A., Novak, M., Morgenstern, K., Nesic, Z., & Gaumont-Guay, D. (2005). Rela-
tionship between soil CO2 concentrations and forest-ﬂoor CO2 eﬄuxes. Agricultural and Forest
Meteorology, 130 (3-4), 176–192.
Jones, H., G. (1992). Plants and Microclimate: A Quantitative Approach to Environmental Plant
Physiology. Cambridge University Press.
Jordan, M. O. & Habib, R. (1996). Mobilizable carbon reserves in young peach trees as evidenced
by trunk girdling experiments. Journal of Experimental Botany, 47 (294), 79–87.
Karberg, N. J., Pregitzer, K. S., King, J. S., Friend, A. L., & Wood, J. R. (2005). Soil carbon
dioxide partial pressure and dissolved inorganic carbonate chemistry under elevated carbon
dioxide and ozone. Oecologia, 142 (2), 296–306.
Kharouk, V. I., Middleton, E. M., Spencer, S. L., Rock, B. N., & Williams, D. L. (1995). Aspen
bark photosynthesis and its signiﬁcance to remote-sensing and carbon budget estimates in the
boreal ecosystem. Water Air and Soil Pol lution, 82 (1-2), 483–497.
Knohl, A., Schulze, E. D., Kolle, O., & Buchmann, N. (2003). Large carbon uptake by an unma-
naged 250-year-old deciduous forest in central germany. Agricultural and Forest Meteorology,
118 (3-4), 151–167.
Knorr, W., Prentice, I. C., House, J. I., & Holland, E. A. (2005). Long-term sensitivity of soil
carbon turnover to warming. Nature, 433 (7023), 298–301.
Kramer, P. & Boyer, J. (1995). Water Relations of Plants and Soils. San Diego: Academic Press,
Inc.
Kuhn, C. & Grof, C. P. L. (2010). Sucrose transporters of higher plants. Current Opinion in
Plant Biology, 13 (3), 288–298.
Kunert, N., Schwendenmann, L., & Holscher, D. (2010). Seasonal dynamics of tree sap ﬂux and
water use in nine species in Panamanian forest plantations. Agricultural and Forest Meteorology,
150 (3), 411–419.
Kuzyakov, Y. (2002). Review: Factors aﬀecting rhizosphere priming eﬀects. Journal of Plant
Nutrition and Soil, 165 (4), 382–396.
ix
Bibliograﬁe
Kuzyakov, Y. (2006). Sources of CO2 eﬄux from soil and review of partitioning methods. Soil
Biology & Biochemistry, 38 (3), 425–448.
Kuzyakov, Y. & Gavrichkova, O. (2010). Review: Time lag between photosynthesis and carbon
dioxide eﬄux from soil: a review of mechanisms and controls. Global Change Biology, 16 (12),
3386–3406.
Kuzyakov, Y. & Larionova, A. (2006). Contribution of rhizomicrobial and root respiration to the
CO2 emission from soil (a review). Eurasian Soil Science, 39 (7), 753–764.
Law, B. E., Ryan, M. G., & Anthoni, P. M. (1999). Seasonal and annual respiration of a ponderosa
pine ecosystem. Global Change Biology, 5 (2), 169–182.
Lawlor, D. (2001). Photosynthesis. Third edition. (Third Edition ed.). Oxford: BIOS Scientiﬁc
Publishers Ltd.
Lee, M., Nakane, K., Nakatsubo, T., & Koizumi, H. (2003). Seasonal changes in the contribution
of root respiration to total soil respiration in a cool-temperate deciduous forest. Plant and Soil,
255 (1), 311–318.
Lee, X., Wu, H., Sigler, J., Oishi, C., & Siccama, T. (2004). Rapid and transient response of soil
respiration to rain. Global Change Biology, 10 (6), 1017–1026.
Levy, P. E., Meir, P., Allen, S. J., & Jarvis, P. G. (1999). The eﬀect of aqueous transport of CO2
in xylem sap on gas exchange in woody plants. Tree Physiology, 19 (1), 53–58.
Li, C. Y., Weiss, D., & Goldschmidt, E. E. (2003). Girdling aﬀects carbohydrate-related gene
expression in leaves, bark and roots of alternate-bearing citrus trees. Annals of Botany, 92 (1),
137–143.
Litton, C. M., Raich, J. W., & Ryan, M. G. (2007). Carbon allocation in forest ecosystems. Global
Change Biology, 13 (10), 2089–2109.
Liu, Q., Edwards, N. T., Post, W. M., Gu, L., Ledford, J., & Lenhart, S. (2006). Temperature-
independent diel variation in soil respiration observed from a temperate deciduous forest. Global
Change Biology, 12 (11), 2136–2145.
Livingston, G. & Hutchinson, G. (1995). Enclosure-based measurement of trace gas exchange:
applications and sources of error. Cambridge: Blackwell Science.
Lloyd, J. & Taylor, J. A. (1994). On the temperature dependence of soil respiration. Functional
Ecology, 8, 315–323.
x
Bibliograﬁe
Longdoz, B., Yernaux, M., & Aubinet, M. (2000). Soil CO2 eﬄux measurements in a mixed forest:
impact of chamber disturbances, spatial variability and seasonal evolution. Global Change
Biology, 6 (8), 907–917.
Lund, C. P., Riley, W. J., Pierce, L. L., & Field, C. B. (1999). The eﬀects of chamber pressurization
on soil-surface CO2 ﬂux and the implications for NEE measurements under elevated CO2. Global
Change Biology, 5 (3), 269–281.
Luyssaert, S., Ciais, P., Piao, S. L., Schulze, E. D., Jung, M., Zaehle, S., Schelhaas, M. J.,
Reichstein, M., Churkina, G., Papale, D., Abril, G., Beer, C., Grace, J., Loustau, D., Matteucci,
G., Magnani, F., Nabuurs, G. J., Verbeeck, H., Sulkava, M., van der Werf, G. R., Janssens,
I. A., & Team, C.-I. S. (2010). The european carbon balance. part 3: forests. Global Change
Biology, 16 (5), 1429–1450.
Maier, C. A. & Clinton, B. D. (2006). Relationship between stem CO2 eﬄux, stem sap velocity
and xylem CO2 concentration in young loblolly pine trees. Plant Cel l and Environment, 29 (8),
1471–1483.
Maier, C. A., Johnsen, K. H., Clinton, B. D., & Ludovici, K. H. (2010). Relationships between
stem CO(2) eﬄux, substrate supply, and growth in young loblolly pine trees. New Phytol,
185 (2), 502–13.
Martin, T. A., Teskey, R. O., & Dougherty, P. M. (1994). Movement of respiratory CO2 in stems
of loblolly-pine (Pinus-taeda l) seedlings. Tree Physiology, 14 (5), 481–495.
McDowell, N. G., Balster, N. J., & Marshall, J. D. (2001). Belowground carbon allocation of rocky
mountain douglas-ﬁr. Canadian Journal of Forest Research-Revue Canadienne De Recherche
Forestiere, 31 (8), 1425–1436.
McGuire, M. A. & Teskey, R. O. (2002). Microelectrode technique for in situ measurement of
carbon dioxide concentrations in xylem sap of trees. Tree Physiology, 22 (11), 807–811.
McGuire, M. A. & Teskey, R. O. (2004). Estimating stem respiration in trees by a mass balance
approach that accounts for internal and external ﬂuxes of CO2 . Tree Physiology, 24 (5), 571–578.
Moyano, F. E., Kutsch, W. L., & Rebmann, C. (2008). Soil respiration ﬂuxes in relation to
photosynthetic activity in broad-leaf and needle-leaf forest stands. Agricultural and Forest
Meteorology, 148 (1), 135–143.
Murakami, P. F., Schaberg, P. G., & Shane, J. B. (2008). Stem girdling manipulates leaf sugar
concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiology,
28 (10), 1467–1473.
xi
Bibliograﬁe
Murray, P., Ostle, N., Kenny, C., & Grant, H. (2004). Eﬀect of defoliation on patterns of carbon
exudation from Agrostis capillaris. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur
Pﬂanzenernahrung Und Bodenkunde, 167 (4), 487–493.
Nardi, S., Concheri, G., Pizzeghello, D., Sturaro, A., Rella, R., & Parvoli, G. (2000). Soil organic
matter mobilization by root exudates. Chemosphere, 41 (5).
Nasr, Z., Woo, S. Y., Zineddine, M., Khaldi, A., & Rejeb, M. N. (2011). Sap ﬂow estimates of
Quercus suber according to climatic conditions in north Tunisia. African Journal of Agricultural
Research, 6 (20), 4705–4710.
Nobel, P. (1999). Physicochemical and environmental plant physiology. Academic Press.
Norby, R. J., Ledford, J., Reilly, C. D., Miller, N. E., & O’Neill, E. G. (2004). Fine-root production
dominates response of a deciduous forest to atmospheric CO2 enrichment. Proceedings of the
National Academy of Sciences of the United States of America, 101 (26), 9689–9693.
O’Brien, J. J., Oberbauer, S. F., & Clark, D. B. (2004). Whole tree xylem sap ﬂow responses to
multiple environmental variables in a wet tropical forest. Plant Cel l and Environment, 27 (5),
551–567.
Olsson, P., Linder, S., Giesler, R., & Hogberg, P. (2005). Fertilization of boreal forest reduces
both autotrophic and heterotrophic soil respiration. Global Change Biology, 11 (10), 1745–1753.
Perry, T. (1982). The ecology of tree roots and the practical signiﬁcance thereof. Journal of
Arboriculture, 9, 197–211.
Pfanz, H., Aschan, G., Langenfeld-Heyser, R., Wittmann, C., & Loose, M. (2002). Ecology and
ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften, 89 (4),
147–162.
Pregitzer, K. S., King, J. A., Burton, A. J., & Brown, S. E. (2000). Responses of tree ﬁne roots
to temperature. New Phytologist, 147 (1), 105–115.
Prentice, I., Farquhar, G., Fasham, M., Goulden, M., Heimann, M., Jaramillo, V., Kheshgi, H.,
Le Quere, C., Scholes, R., & Wallace, D. (2001). The carbon cycle atmospheric carbon dioxide,
chapter 3. Cambridge: Cambridge University Press.
Pumpanen, J., Ilvesniemi, H., Peramaki, M., & Hari, P. (2003). Seasonal patterns of soil CO2 eﬄux
and soil air CO2 concentration in a scots pine forest: comparison of two chamber techniques.
Global Change Biology, 9 (3), 371–382.
xii
Bibliograﬁe
Pumpanen, J., Kolari, P., Ilvesniemi, H., Minkkinen, K., Vesala, T., Niinisto, S., Lohila, A.,
Larmola, T., Morero, M., Pihlatie, M., Janssens, I., Yuste, J. C., Grunzweig, J. M., Reth, S.,
Subke, J. A., Savage, K., Kutsch, W., Ostreng, G., Ziegler, W., Anthoni, P., Lindroth, A., &
Hari, P. (2004). Comparison of diﬀerent chamber techniques for measuring soil CO2 eﬄux.
Agricultural and Forest Meteorology, 123 (3-4), 159–176.
Qi, J., Marshall, J., & Mattson, K. (1994). High soil carbon-dioxide concentrations inhibit root
respiration of douglas-ﬁr. New Phytologist, 128 (3), 435–442.
Qi, Y. & Xu, M. (2001). Separating the eﬀects of moisture and temperature on soil CO2 eﬄux in
a coniferous forest in the sierra nevada mountains. Plant and Soil, 237 (1), 15–23.
Raich, J. W. & Schlesinger, W. H. (1992). The global carbon-dioxide ﬂux in soil respiration and
its relationship to vegetation and climate. Tel lus Series B-Chemical and Physical Meteorology,
44 (2), 81–99.
Rasse, D. P., Rumpel, C., & Dignac, M. F. (2005). Is soil carbon mostly root carbon? Mechanisms
for a speciﬁc stabilisation. Plant and Soil, 269 (1-2), 341–356.
Regier, N., Streb, S., Zeeman, S. C., & Frey, B. (2010). Seasonal changes in starch and sugar
content of poplar (Populus deltoides x nigra cv. Dorskamp) and the impact of stem girdling on
carbohydrate allocation to roots. Tree Physiology, 30 (8), 979–987.
Ryan, M. G. (1990). Growth and maintenance respiration in stems of Pinus-contorta and Picea-
engelmannii. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere,
20 (1), 48–57.
Ryan, M. G. & Law, B. E. (2005). Interpreting, measuring, and modeling soil respiration. Bioge-
ochemistry, 73 (1), 3–27.
Savage, K. & Davidson, E. (2003). A comparison of manual and automated systems for soil CO2
ﬂux measurements: trade-oﬀs between spatial and temporal resolution. Journal of Experimental
Botany, 54 (384), 891–899.
Savage, K., Davidson, E., & Richardson, A. (2008). A conceptual and practical approach to data
quality and analysis procedures for high-frequency soil respiration measurements. Functional
Ecology, 22 (6), 1000–1007.
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 (3), 477–485.
xiii
Bibliograﬁe
Saveyn, A., Steppe, K., & Lemeur, R. (2008). Report on non-temperature related variations in
CO2 eﬄux rates from young tree stems in the dormant season. Trees-Structure and Function,
22 (2), 165–174.
Saveyn, A., Steppe, K., Ubierna, N., & Dawson, T. E. (2010). Woody tissue photosynthesis
and its contribution to trunk growth and bud development in young plants. Plant Cel l and
Environment, 33 (11), 1949–1958.
Saxton, K. E. & Rawls, W. J. (2006). Soil water characteristic estimates by texture and organic
matter for hydrologic solutions. Soil Science Society of America Journal, 70 (5), 1569–1578.
Schimel, D. S., Braswell, B. H., Holland, E. A., McKeown, R., Ojima, D. S., Painter, T. H.,
Parton, W. J., & Townsend, A. R. (1994). Climatic, edaphic, and biotic controls over storage
and turnover of carbon in soils. Global Biogeochemical Cycles, 8 (3), 279–293.
Schmidt, J., Batic, F., & Pfanz, H. (2000). Photosynthetic performance of leaves and twigs of
evergreen holly (Ilex aquifolium L.). Phyton-Annales Rei Botanicae, 40 (1), 179–190.
Schuur, E. A. G. & Trumbore, S. E. (2006). Partitioning sources of soil respiration in boreal black
spruce forest using radiocarbon. Global Change Biology, 12 (2), 165–176.
Selsted, M. B., van der Linden, L., Ibrom, A., Michelsen, A., Larsen, K. S., Pedersen, J. K.,
Mikkelsen, T. N., Pilegaard, K., Beier, C., & Ambus, P. (2012). Soil respiration is stimulated
by elevated CO2 and reduced by summer drought: three years of measurements in a multifactor
ecosystem manipulation experiment in a temperate heathland (CLIMAITE). Global Change
Biology, 18 (4), 1216–1230.
Sorz, J. & Hietz, P. (2006). Gas diﬀusion through wood: implications for oxygen supply. Trees-
Structure and Function, 20 (1), 34–41.
Sperry, J. S. (2003). Evolution of water transport and xylem structure. International Journal of
Plant Sciences, 164 (3), S115–S127.
Sprugel, D., Ryan, M., Brooks, J., Vogt, K., & Martin, T. (1995). Respiration from organ level
to the stand. San Diego, CA, USA: Academic Press.
Steppe, K., De Pauw, D. J. W., Doody, T. M., & Teskey, R. O. (2010). A comparison of sap
ﬂux density using thermal dissipation, heat pulse velocity and heat ﬁeld deformation methods.
Agricultural and Forest Meteorology, 150 (7-8), 1046–1056.
Steppe, K., Saveyn, A., McGuire, M. A., Lemeur, R., & Teskey, R. O. (2007). Resistance to radial
CO2 diﬀusion contributes to between-tree variation in CO2 eﬄux of Populus deltoides stems.
Functional Plant Biology, 34 (9), 785–792.
xiv
Bibliograﬁe
Stoyan, H., De-Polli, H., Bohm, S., Robertson, G. P., & Paul, E. A. (2000). Spatial heterogeneity
of soil respiration and related properties at the plant scale. Plant and Soil, 222 (1-2), 203–214.
Stumm, W. & Morgan, J. (1996). Aquatic Chemistry: Chemical Equilibria and Rates in Natural
Waters. Third Edition. New York: John Wiley & Sons, Inc.
Subke, J. A., Hahn, V., Battipaglia, G., Linder, S., Buchmann, N., & Cotrufo, M. F. (2004).
Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia,
139 (4), 551–559.
Subke, J. A., Inglima, I., & Cotrufo, M. F. (2006). Trends and methodological impacts in soil
CO2 eﬄux partitioning. Global Change Biology, 12 (9), 1813–1813.
Subke, J.-A., Voke, N. R., Leronni, V., Garnett, M. H., & Ineson, P. (2011). Dynamics and
pathways of autotrophic and heterotrophic soil CO2 eﬄux revealed by forest girdling. Journal
of Ecology, 99 (1), 186–193.
Sulzman, E. W., Brant, J. B., Bowden, R. D., & La jtha, K. (2005). Contribution of aboveground
litter, belowground litter, and rhizosphere respiration to total soil CO2 eﬄux in an old growth
coniferous forest. Biogeochemistry, 73 (1), 231–256.
Taiz, L. & Zeiger, E. (2006). Plant Physiology: Fourth Edition. Sinauer Associates, Inc.
Teskey, R. O. & McGuire, M. A. (2002). Carbon dioxide transport in xylem causes errors in
estimation of rates of respiration in stems and branches of trees. Plant Cel l and Environment,
25 (11), 1571–1577.
Teskey, R. O. & McGuire, M. A. (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 Cel l and Environment, 30 (5), 570–579.
Teskey, R. O., Saveyn, A., Steppe, K., & McGuire, M. A. (2008). Origin, fate and signiﬁcance of
CO2 in tree stems. New Phytologist, 177 (1), 17–32.
Thornton, B., Paterson, E., Midwood, A. J., Sim, A., & Pratt, S. M. (2004). Contribution
of current carbon assimilation in supplying root exudates of Lolium perenne measured using
steady-state C13 labelling. Physiologia Plantarum, 120 (3), 434–441.
Trumbore, S. (2006). Carbon respired by terrestrial ecosystems - recent progress and challenges.
Global Change Biology, 12 (2), 141–153.
Valentini, R. (2003). Fluxes of Carbon, Water and Energy of European Forests. Berlin: Springer.
xv
Vande Walle, I., Samson, R., Looman, B., Verheyen, K., & Lemeur, R. (2007). Temporal variation
and high-resolution spatial heterogeneity in soil CO2 eﬄux in a short-rotation tree plantation.
Tree Physiology, 27 (6), 837–848.
Verstraeten, W. W., Veroustraete, F., & Feyen, J. (2008). Assessment of evapotranspiration and
soil moisture content across diﬀerent scales of observation. Sensors, 8 (1), 70–117.
Vose, J. M. & Ryan, M. G. (2002). Seasonal respiration of foliage, ﬁne roots, and woody tissues
in relation to growth, tissue N, and photosynthesis. Global Change Biology, 8 (2), 182–193.
Walker, T. S., Bais, H. P., Grotewold, E., & Vivanco, J. M. (2003). Root exudation and rhizosphere
biology. Plant Physiology, 132 (1), 44–51.
Wang, C. K. & Yang, J. Y. (2007). Rhizospheric and heterotrophic components of soil respiration
in six chinese temperate forests. Global Change Biology, 13 (1), 123–131.
Wang, K. Y., Kellomaki, S., Zha, T. S., & Peltola, H. (2005). Annual and seasonal variation of sap
ﬂow and conductance of pine trees grown in elevated carbon dioxide and temperature. Journal
of Experimental Botany, 56 (409), 155–165.
Wertin, T. M., McGuire, M. A., & Teskey, R. O. (2010). The inﬂuence of elevated temperature,
elevated atmospheric CO(2) concentration and water stress on net photosynthesis of loblolly
pine (pinus taeda l.) at northern, central and southern sites in its native range. Global Change
Biology, 16 (7), 2089–2103.
Winston, G. C., Sundquist, E. T., Stephens, B. B., & Trumbore, S. E. (1997). Winter CO2 ﬂuxes
in a boreal forest. Journal of Geophysical Research-Atmospheres, 102 (D24), 28795–28804.
Wu, J., Brookes, P. C., & Jenkinson, D. S. (1993). Formation and destruction of microbial biomass
during the decomposition of glucose and ryegrass in soil. Soil Biology & Biochemistry, 25 (10),
1435–1441.
Xu, X. L., Kuzyakov, Y., Wanek, W., & Richter, A. (2008). Root-derived respiration and non-
structural carbon of rice seedlings. European Journal of Soil Biology, 44 (1), 22–29.
Yavitt, J. B., Fahey, T. J., & Simmons, J. A. (1995). Methane and carbon-dioxide dynamics in a
northern hardwood ecosystem. Soil Science Society of America Journal, 59 (3), 796–804.
Zak, D. R., Pregitzer, K. S., King, J. S., & Holmes, W. E. (2000). Elevated atmospheric CO2,
ﬁne roots and the response of soil microorganisms: a review and hypothesis. New Phytologist,
147 (1), 201–222.