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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 (2009) 1764–1767
Contents lists available at ScienceDirect
Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Partitioning of soil respiration into its autotrophic and heterotrophic components by means of tree-girdling in old boreal spruce forest Peter Ho¨gberg a,*, Bhupinderpal-Singh a,b, Mikaell Ottosson Lo¨fvenius a, Anders Nordgren a a b
Department of Forest Ecology and Management, SLU, SE-901 83 Umea˚, Sweden NSW Department of Primary Industries, Forest Science Centre, P.O. Box 100, Beecroft, NSW 2119, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 October 2008 Received in revised form 8 January 2009 Accepted 25 January 2009
Forests accumulate much less carbon than the amount fixed through photosynthesis because of an almost equally large opposing flux of CO2 from the ecosystem. Most of the return flux to the atmosphere is through soil respiration, which has two major sources, one heterotrophic (organisms decomposing organic matter) and one autotrophic (roots, mycorrhizal fungi and other root-associated microbes dependent on recent photosynthate). We used tree-girdling to stop the flow of photosynthate to the belowground system, hence, blocking autotrophic soil activity in a 120-yr-old boreal Picea abies forest. We found that at the end of the summer, two months after girdling, the treatment had reduced soil respiration by up to 53%. This figure adds to a growing body of evidence indicating (t-test, d.f. = 7, p < 0.05) that autotrophic respiration may contribute more to total soil respiration in boreal (mean 53 2%) as compared to temperate forests (mean 44 3%). Our data also suggests that there is a seasonal hysteresis in the response of total soil respiration to changes in temperature. We propose that this reflects seasonality in the tree below-ground carbon allocation. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Boreal forest Carbon balance Soil respiration Tree-girdling
1. Introduction Boreal forests are the second largest forest biome (Chapin et al., 2002) and contain large amounts of soil carbon, especially in the upper organic layer (Schlesinger, 1997). Flux measurements in Europe show that the boreal forests are weaker sinks for atmospheric CO2 per unit area than are forests further south (Valentini et al., 2000), mainly as a result of high soil respiration in relation to net photosynthesis (Janssens et al., 2001). This could potentially reflect a disequilibrium, e.g., that decomposition currently occurs at a higher rate than before because of a warmer climate. Alternatively, it could reflect a natural higher tree belowground C allocation to the activities of mycorrhizal roots in the extremely nutrient-limited northerly forest ecosystems (Ho¨gberg et al., 2003; Ma¨kela¨ et al., 2008). The latter may explain why aboveground primary production and tree below-ground allocation may not show the same response to variations in site temperature, as found in a study of spruce in N. America (Vogel et al., 2008). Testing of these hypotheses critically requires the partitioning of the major components of soil activity, autotrophic and heterotrophic respiration. Here, we define autotrophic soil respiration as that of live roots, their mycorrhizal fungal symbionts
* Corresponding author. E-mail address: [email protected] (P. Ho¨gberg). 0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.01.036
and other closely associated microorganisms dependent on the flux of recent photosynthate (Ho¨gberg and Read, 2006). Heterotrophic activity is the decomposition of more complex compounds of ‘‘higher ecosystem age’’, e.g., litter and soil organic matter. Autotrophic mycorrhizal roots and heterotrophic organisms occur in close proximity. This makes it difficult to separate their respective activities in natural settings, especially since organisms in the rhizosphere may be partly autotrophic and partly heterotrophic, and may vary temporally in this respect. Thus, the concept of an autotroph-heterotroph continuum has been advocated (Ho¨gberg and Read, 2006). There is a range of methods to approach the problem of partitioning soil activity into its major components, each of which has its own advantages and disadvantages (Hanson et al., 2000; Kuzyakov, 2006). In a previous study, we demonstrated that girdling of boreal pine trees on comparatively large plots (30 m by 30 m quadrates) decreased the soil respiration by up to 56% in the central area of the plots during the first summer (Ho¨gberg et al., 2001) and by up to 65% the second summer (Bhupinderpal-Singh et al., 2003). Girdling stops the flow of C sustaining the autotrophic soil component. Ultimately, it kills the roots and then the whole trees and thus increases the supply of substrates for soil heterotrophs. Initially, it leads to an accelerated use of non-structural C, e.g., starch, in the roots (Ho¨gberg et al., 2001; Olsson et al., 2005). Hence, it does not give a realistic estimate of the autotrophic component if the stores of non-structural C are large, as in Eucalyptus (Binkley et al., 2006). The accelerated supply of new substrates and use of non-structural
P. Ho¨gberg et al. / Forest Ecology and Management 257 (2009) 1764–1767
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Table 1 Estimates of the contribution of autotrophic respiration to total soil respiration based on the tree-girdling method. Forest type (age in yrs)
Latitude
Region
% Autotrophic respiration
Ref.
Boreal pine (45–55)
648N
N. Sweden
54 65 (2nd year)
Boreal spruce (40) Fertilized boreal spruce (40) Boreal spruce (120) Temperate spruce (35) Temperate spruce (40–50) Temperate beech (40–50) Temperate chestnut (57) Montane pine Temperate pine (19) Subtrop. Eucalyptus (6.5)
648N 648N 648N 508N 488N 488N 468N 408N 358N 128S
N. Sweden N. Sweden N. Sweden Germany Germany Germany Switzerland Colorado N. Carolina S. Brazil
60 40 53 48 38 50 36 44 50 24
Ho¨gberg et al. (2001), Bhupinderpal-Singh et al. (2003) Olsson et al. (2005) Olsson et al. (2005) This study Subke et al. (2004) Andersen et al. (2005) Andersen et al. (2005) Frey et al. (2006) Scott-Denton et al. (2006) Johnsen et al. (2007) Binkley et al. (2006)
The contribution varies seasonally, and the effect of girdling is delayed as stored non-structural carbohydrates (mainly starch) are used at an accelerated rate after girdling. Hence, we show data for the maximal contribution during the season of girdling, except for the first site, where data also for the second year are available. Plot sizes vary, and as an exception Andersen et al. studied the response to girdling around single trees, but did a careful spatial gradient analysis of the response to the treatment.
root C both lead to an underestimation of the calculated autotrophic fraction of total soil activity, especially directly after the girdling (Ho¨gberg et al., 2001). Mesocosm studies are undoubtedly more precise (Kuzyakov, 2006), but their results cannot be extrapolated to the field. Given the great importance of the partitioning between autotrophic and heterotrophic soil respiration, there is a considerable need for estimates across a wide range of systems. Since a largescale replicated tree-girdling experiment was first used explicitly for this purpose (Ho¨gberg et al., 2001), there has been a number of studies using this and similar approaches (Table 1), but this number is still small in view of the wide range of climates and soils and vast areas covered by forests. Here, we present data from a tree-girdling experiment in a northern boreal forest, which is considerably older than the ones previously studied in boreal forests by the use of this method. We also summarize the published findings of studies using tree-girdling in a preliminary attempt to find a potential difference between boreal and temperate forest biomes in the partitioning of soil respiratory components. 2. Materials and methods The site is a 120-year-old Norway spruce-dominated (Picea abies (L.) Karst.) forest at Storskogberget (648000 N, 208350 E, 75 m a.s.l.) in northern Sweden (Go¨ttlicher et al., 2008). The terrain is irregular with a microtopographic variation of a few meters, and with lowlying wetter patches with Spaghnum mosses. The soil is a podzolised glacial till. It has an upper organic layer of 10–15 cm, with a C:N ratio of 32 2 (n = 6) and a pH in water of 4.1 0.2 (n = 3, mean S.E.). The annual mean temperature is around 2.9 8C, with monthly means of 8.7 and 15.5 8C in January and July, respectively. The mean annual precipitation is around 660 mm (average for 1961–1990 at Umea˚ airport, c. 25 km S of the site). The time of snow cover is variable, but is typically from October–November to late April. In 2002, the year of this study, the mean temperature for June–July was 2 8C above the average, and August and September were drier than the long-term average. There were around 1100 trees ha1. P. abies dominates the lower terrain, but on higher ground the contribution of Pinus sylvestris L. becomes significant. Other tree species are Betula spp. and Populus tremula L. The understory vegetation is dominated by Vaccinium myrtillus L. In early June 2002, six circular plots with a radius of 15 m (707 m2) were laid out. Three of these were randomly selected to be girdled, i.e. the bark of every living tree in these plots was removed down to the phloem along a 0.3 m section around the circumference. In the centre of each plot soil respiration was measured in three permanent circular sub-plots (0.0464 m2). In these sub-plots gas samples were collected at 3–8 min intervals for
12–20 min from opaque temporary 6 l headspaces (Ho¨gberg and Ekblad, 1996), eight times between early June and early October during 2002. The gas samples were transferred to 12 ml Exetainer vials and analysed on a gas purification module coupled on-line to an isotope ratio mass spectrometer (Ho¨gberg and Ekblad, 1996). We report the mean soil respiration rates ( S.E.) for girdled and non-girdled plots. Autotrophic respiration was calculated as the respiration on the control plots minus the respiration on the girdled plots. We monitored soil (at 10–15 cm depth) temperature in 5 plots and air temperature through the experiment. 3. Results and discussion The foliage of the spruce trees, the dominant tree species, remained green through the first summer of this experiment, but considerable defoliation occurred the second year after girdling. Hence, we use respiration data for the first summer only. Inventories of ectomycorrhizal sporocarps in August, c. 70 days after girdling, showed that the treatment had stopped effectively the flux of photosynthate to the tree belowground system in the central area of the plots; there were no ectomycorrhizal fungal sporocarps in the central 240 m2 of girdled plots (Go¨ttlicher et al., 2008). We assume, based on previous studies (Ho¨gberg et al., 2001; Olsson et al., 2005; Giesler et al., 2007) that one immediate response to girdling is an accelerated use of stored non-structural carbohydrates in roots and mycorrhizal fungi. Thus, estimates of autotrophic respiration during the first half of the summer are not reliable. This argument is supported by the relatively constant relation between the autotrophic and heterotrophic components through the second year, including data from early summer, in the previous experiment with pine, in which the foliage remained green for almost three years (Bhupinderpal-Singh et al., 2003). Based on these arguments, we derive our partitioning from data later in the summer in this case. In August, the calculated autotrophic respiration was slightly higher than the heterotrophic respiration (the respiration on girdled plots) at around 53% (52.8% on 12 August, 52.5% on 23 August) of total soil respiration (Fig. 1). Later in the season, heterotrophic respiration was higher than autotrophic respiration, most likely as a result of rapidly diminishing rates of photosynthesis this time of the year. Since there was very little variation in soil respiration rates within treatments (Fig. 1), there was no evidence that the microtopographic position had any influence on the partitioning of soil respiratory components. We would like to emphasize, once again, that the estimate of 53% autotrophic respiration is conservative. First, there may still be an accelerated use of sugars and starch in the roots of girdled trees. Second, there should also be an accelerated mortality of fine roots
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P. Ho¨gberg et al. / Forest Ecology and Management 257 (2009) 1764–1767
Fig. 1. Soil respiration (a), and air and soil temperatures (b, diurnal means) at Storskogberget through the summer of 2002. Symbols in (a) filled circles, control plots; open circles, girdled plots; filled triangles, calculated autotrophic respiration. Lines in (b) solid line, soil temperature; dotted line, air temperature.
and mycorrhizal fungal mycelium (Ho¨gberg and Ho¨gberg, 2002). Third, we did not stop the below-ground C flux in understory plants. All three work in the same direction, i.e. they lead to underestimation of the calculated fractional contribution of the autotrophic component. The fact that it is still estimated at around 50% is clear evidence of the importance of the direct below-ground flux of recent
photosynthate for soil activity in this type of forest. How does this figure compare with previous estimates? Estimates based on a wider range of methods, time scales and across biomes vary as widely as between 10 and 90% (Hanson et al., 2000). Not surprisingly, the studies based on tree-girdling in boreal and temperate forests vary much less (Table 1). The mean for unfertilized boreal forests (n = 3, using data only from the 1st season) is 56 2% as compared to 44 3% in temperate forests (n = 6). At present, the sample is too small to provide a basis for more advanced interpretation. We excluded an early tree-girdling experiment (Edwards and Ross-Todd, 1979), which did not explicitly address the partitioning between autotrophic and heterotrophic components, used comparatively small plots and had no replicates. Addition of nutrients can lead to decreased plant below-ground allocation. It apparently had a negative effect on the fractional contribution of autotrophic respiration in an experiment in boreal forest (Olsson et al., 2005), but the slightly lower (t-test, d.f. = 7, p < 0.05) autotrophic respiration in temperate as compared to in boreal forests cannot, at present, be ascribed to a higher availability of nutrients. Another driver of respiratory activity of great interest is temperature (Davidson et al., 2006). A problem is that the effect of another major driver, the supply of substrate, photosynthate, may co-vary strongly with temperature because both are driven by solar radiation. Many studies have reported strong correlations between soil temperature and total soil respiratory activity. We concentrate on total soil respiratory activity here, because the components of respiration are not well separated for much of the observation period, as discussed above. Since we assumed that below-ground C allocation has a strong seasonality (Hansen et al., 1997; Ho¨gberg et al., 2001), with greatest allocation in late summer, we plotted soil respiratory activity vs. temperature in a way that enabled tracking the changes in respiration over time (Fig. 2). There are undoubtedly correlations between soil respiration and air and soil temperatures (Fig. 2). However, the loops in these relations provide evidence of a seasonal hysteresis, as found elsewhere in seasonal climates (Curiel Yuste et al., 2004; Richardson et al., 2006), similar respiration rates were observed over a difference in temperature of 4 8C (Fig. 2). Thus, in this boreal forest, season, and not just temperature per se, appears important. Our observations show that autotrophic respiration can account for at least 53% of total soil respiration in this boreal forest. They add to the small set of data available from other studies using tree-girdling, which seem to indicate that the fractional contribution of autotrophic activity may be greater in boreal than in temperate forests. Boreal forests are strongly seasonal. Our data suggest that the seasonality in soil respiration cannot be explained by temperature alone. We propose that it could also be attributed to seasonal variation in below-ground C allocation. Acknowledgments We would like to thank the company Holmen Skog AB, especially Dr. Ola Ka˚re´n, for the permit to conduct this experiment on their property. The study was supported by grants from the Swedish Science Council (VR) and the EU (project FORCAST). References
Fig. 2. Soil respiration plotted vs. soil (solid lines and arrows) and air (dotted lines and arrows) temperatures (diurnal means). The arrows describe the course of change starting early in the summer: S denotes starting points (5/6 = 5 June) and E end points (4/10 = 4 October).
Andersen, C.P., Nikolov, I., Nikolova, P., Matyssek, R., Ha¨berle, K.-H., 2005. Estimating ‘‘autotrophic’’ belowground respiration in spruce and beech forests: decreases following girdling. Eur. J. For. Res. 124, 155–163. Bhupinderpal-Singh, Nordgren, A., Ottosson-Lo¨fvenius, M., Ho¨gberg, M.N., Mellander, P.E., Ho¨gberg, P., 2003. Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant Cell Environ. 26, 1287–1296.
P. Ho¨gberg et al. / Forest Ecology and Management 257 (2009) 1764–1767 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, 447–454. Chapin III, F.S., Matson, P.A., Mooney, H.A., 2002. Principles of Terrestrial Ecosystem Ecology. Springer Verlag, New York. Curiel Yuste, J., Janssens, I.A., Carrara, A., Ceulemans, R., 2004. Annual Q10 of soil respiration reflects plant phonological patterns as well as temperature sensitivity. Glob. Change Biol. 10, 161–169. Davidson, E.A., Janssens, I.A., Luo, Y., 2006. On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Glob. Change Biol. 12, 154–164. Edwards, N.T., Ross-Todd, B.M., 1979. The effects of stem girdling on biogeochemical cycles within a mixed deciduous forest in eastern Tennessee. I. Soil solution chemistry, soil respiration, litterfall and root biomass studies. Oecologia 40, 247–257. Frey, B., Hagedorn, F., Giudici, T., 2006. Effect of girdling on soil respiration and root composition in a sweet chestnut forest. For. Ecol. Manage. 225, 271–277. Giesler, R., Ho¨gberg, M.N., Strobel, B.W., Richter, A., Nordgren, A., Ho¨gberg, P., 2007. Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate. Biogeochemistry 84, 1–12. Go¨ttlicher, S.G., Taylor, A.F.S., Grip, H., Betson, N.R., Valinger, E., Ho¨gberg, M.N., Ho¨gberg, P., 2008. The lateral spread of tree root systems in boreal forests: Estimates based on 15N uptake and distribution of sporocarps of ectomycorrhizal fungi. For. Ecol. Manage. 255, 75–81. Hansen, J., Tu¨rk, R., Vogg, G., Heim, R., Beck, E., 1997. Conifer carbohydrate physiology: updating classical views. In: Rennenberg, H., Eschrich, W., Ziegler, H. (Eds.), Trees–Contributions to Modern Tree Physiology. Backhuys, Leiden, pp. 97–108. Hanson, P.J., Edwards, N.T., Garten, C.T., Andrews, J.A., 2000. Separating root and microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48, 115–146. Ho¨gberg, M.N., Ho¨gberg, P., 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 154, 791–795. Ho¨gberg, M.N., Ba˚a˚th, E., Nordgren, A., Arnebrant, K., Ho¨gberg, P., 2003. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and
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saprotrophs–a hypothesis based on field observations in boreal forests. New Phytol. 160, 225–238. Ho¨gberg, P., Ekblad, A., 1996. Substrate-induced respiration measured in situ in a C3-plant ecosystem using additions of C4-sucrose. Soil Biol. Biochem. 28, 1131–1138. Ho¨gberg, P., et al., 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792. Ho¨gberg, P., Read, D.J., 2006. Towards a more plant physiological perspective on soil ecology. Trends Ecol. Evol. 21, 548–554. Janssens, I.A., et al., 2001. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Glob. Change Biol. 7, 269–278. Johnsen, K., Maier, C., Sanchez, F., Anderson, P., Butnor, J., Waring, R., Linder, S., 2007. Physiological girdling of trees via phloem chilling: proof of concept. Pl. Cell. Environ. 30, 128–134. Kuzyakov, Y., 2006. Sources of soil CO2 efflux from soil and review of partitioning methods. Soil Biol. Biochem. 38, 425–448. Ma¨kela¨, A., Valentine, H.T., Helmisaari, H.-S., 2008. Optimal co-allocation of carbon and nitrogen in a forest stand at steady-state. New Phytol. 180, 114–123. Olsson, P., Linder, S., Giesler, R., Ho¨gberg, P., 2005. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob. Change Biol. 11, 1745–1753. Richardson, A.D., et al., 2006. Comparing simple respiration models for eddy flux and dynamic chamber data. Agric. For. Meteor. 141, 219–234. Schlesinger, W.H., 1997. Biogeochemistry, 2nd ed. Academic Press, San Diego. Scott-Denton, L.E., Rosenstiel, T.N., Monson, R.K., 2006. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob. Change Biol. 12, 205–216. Subke, J.A., et al., 2004. Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139, 551–559. Valentini, R., et al., 2000. Respiration as the main determinant of the carbon balance in European forests. Nature 404, 861–865. ´ Connell, Vogel, J.G., Bond-Lamberty, B.P., Schuur, E.A.G., Gower, S.T., Mack, M.C., O K.E.B., Valentine, D.W., Ruess, R.W., 2008. Carbon allocation in boreal black spruce forests across regions varying in soil temperature and precipitation. Glob. Change Biol. 14, 1503–1516.
Contents lists available at ScienceDirect
Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Partitioning of soil respiration into its autotrophic and heterotrophic components by means of tree-girdling in old boreal spruce forest Peter Ho¨gberg a,*, Bhupinderpal-Singh a,b, Mikaell Ottosson Lo¨fvenius a, Anders Nordgren a a b
Department of Forest Ecology and Management, SLU, SE-901 83 Umea˚, Sweden NSW Department of Primary Industries, Forest Science Centre, P.O. Box 100, Beecroft, NSW 2119, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 October 2008 Received in revised form 8 January 2009 Accepted 25 January 2009
Forests accumulate much less carbon than the amount fixed through photosynthesis because of an almost equally large opposing flux of CO2 from the ecosystem. Most of the return flux to the atmosphere is through soil respiration, which has two major sources, one heterotrophic (organisms decomposing organic matter) and one autotrophic (roots, mycorrhizal fungi and other root-associated microbes dependent on recent photosynthate). We used tree-girdling to stop the flow of photosynthate to the belowground system, hence, blocking autotrophic soil activity in a 120-yr-old boreal Picea abies forest. We found that at the end of the summer, two months after girdling, the treatment had reduced soil respiration by up to 53%. This figure adds to a growing body of evidence indicating (t-test, d.f. = 7, p < 0.05) that autotrophic respiration may contribute more to total soil respiration in boreal (mean 53 2%) as compared to temperate forests (mean 44 3%). Our data also suggests that there is a seasonal hysteresis in the response of total soil respiration to changes in temperature. We propose that this reflects seasonality in the tree below-ground carbon allocation. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Boreal forest Carbon balance Soil respiration Tree-girdling
1. Introduction Boreal forests are the second largest forest biome (Chapin et al., 2002) and contain large amounts of soil carbon, especially in the upper organic layer (Schlesinger, 1997). Flux measurements in Europe show that the boreal forests are weaker sinks for atmospheric CO2 per unit area than are forests further south (Valentini et al., 2000), mainly as a result of high soil respiration in relation to net photosynthesis (Janssens et al., 2001). This could potentially reflect a disequilibrium, e.g., that decomposition currently occurs at a higher rate than before because of a warmer climate. Alternatively, it could reflect a natural higher tree belowground C allocation to the activities of mycorrhizal roots in the extremely nutrient-limited northerly forest ecosystems (Ho¨gberg et al., 2003; Ma¨kela¨ et al., 2008). The latter may explain why aboveground primary production and tree below-ground allocation may not show the same response to variations in site temperature, as found in a study of spruce in N. America (Vogel et al., 2008). Testing of these hypotheses critically requires the partitioning of the major components of soil activity, autotrophic and heterotrophic respiration. Here, we define autotrophic soil respiration as that of live roots, their mycorrhizal fungal symbionts
* Corresponding author. E-mail address: [email protected] (P. Ho¨gberg). 0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.01.036
and other closely associated microorganisms dependent on the flux of recent photosynthate (Ho¨gberg and Read, 2006). Heterotrophic activity is the decomposition of more complex compounds of ‘‘higher ecosystem age’’, e.g., litter and soil organic matter. Autotrophic mycorrhizal roots and heterotrophic organisms occur in close proximity. This makes it difficult to separate their respective activities in natural settings, especially since organisms in the rhizosphere may be partly autotrophic and partly heterotrophic, and may vary temporally in this respect. Thus, the concept of an autotroph-heterotroph continuum has been advocated (Ho¨gberg and Read, 2006). There is a range of methods to approach the problem of partitioning soil activity into its major components, each of which has its own advantages and disadvantages (Hanson et al., 2000; Kuzyakov, 2006). In a previous study, we demonstrated that girdling of boreal pine trees on comparatively large plots (30 m by 30 m quadrates) decreased the soil respiration by up to 56% in the central area of the plots during the first summer (Ho¨gberg et al., 2001) and by up to 65% the second summer (Bhupinderpal-Singh et al., 2003). Girdling stops the flow of C sustaining the autotrophic soil component. Ultimately, it kills the roots and then the whole trees and thus increases the supply of substrates for soil heterotrophs. Initially, it leads to an accelerated use of non-structural C, e.g., starch, in the roots (Ho¨gberg et al., 2001; Olsson et al., 2005). Hence, it does not give a realistic estimate of the autotrophic component if the stores of non-structural C are large, as in Eucalyptus (Binkley et al., 2006). The accelerated supply of new substrates and use of non-structural
P. Ho¨gberg et al. / Forest Ecology and Management 257 (2009) 1764–1767
1765
Table 1 Estimates of the contribution of autotrophic respiration to total soil respiration based on the tree-girdling method. Forest type (age in yrs)
Latitude
Region
% Autotrophic respiration
Ref.
Boreal pine (45–55)
648N
N. Sweden
54 65 (2nd year)
Boreal spruce (40) Fertilized boreal spruce (40) Boreal spruce (120) Temperate spruce (35) Temperate spruce (40–50) Temperate beech (40–50) Temperate chestnut (57) Montane pine Temperate pine (19) Subtrop. Eucalyptus (6.5)
648N 648N 648N 508N 488N 488N 468N 408N 358N 128S
N. Sweden N. Sweden N. Sweden Germany Germany Germany Switzerland Colorado N. Carolina S. Brazil
60 40 53 48 38 50 36 44 50 24
Ho¨gberg et al. (2001), Bhupinderpal-Singh et al. (2003) Olsson et al. (2005) Olsson et al. (2005) This study Subke et al. (2004) Andersen et al. (2005) Andersen et al. (2005) Frey et al. (2006) Scott-Denton et al. (2006) Johnsen et al. (2007) Binkley et al. (2006)
The contribution varies seasonally, and the effect of girdling is delayed as stored non-structural carbohydrates (mainly starch) are used at an accelerated rate after girdling. Hence, we show data for the maximal contribution during the season of girdling, except for the first site, where data also for the second year are available. Plot sizes vary, and as an exception Andersen et al. studied the response to girdling around single trees, but did a careful spatial gradient analysis of the response to the treatment.
root C both lead to an underestimation of the calculated autotrophic fraction of total soil activity, especially directly after the girdling (Ho¨gberg et al., 2001). Mesocosm studies are undoubtedly more precise (Kuzyakov, 2006), but their results cannot be extrapolated to the field. Given the great importance of the partitioning between autotrophic and heterotrophic soil respiration, there is a considerable need for estimates across a wide range of systems. Since a largescale replicated tree-girdling experiment was first used explicitly for this purpose (Ho¨gberg et al., 2001), there has been a number of studies using this and similar approaches (Table 1), but this number is still small in view of the wide range of climates and soils and vast areas covered by forests. Here, we present data from a tree-girdling experiment in a northern boreal forest, which is considerably older than the ones previously studied in boreal forests by the use of this method. We also summarize the published findings of studies using tree-girdling in a preliminary attempt to find a potential difference between boreal and temperate forest biomes in the partitioning of soil respiratory components. 2. Materials and methods The site is a 120-year-old Norway spruce-dominated (Picea abies (L.) Karst.) forest at Storskogberget (648000 N, 208350 E, 75 m a.s.l.) in northern Sweden (Go¨ttlicher et al., 2008). The terrain is irregular with a microtopographic variation of a few meters, and with lowlying wetter patches with Spaghnum mosses. The soil is a podzolised glacial till. It has an upper organic layer of 10–15 cm, with a C:N ratio of 32 2 (n = 6) and a pH in water of 4.1 0.2 (n = 3, mean S.E.). The annual mean temperature is around 2.9 8C, with monthly means of 8.7 and 15.5 8C in January and July, respectively. The mean annual precipitation is around 660 mm (average for 1961–1990 at Umea˚ airport, c. 25 km S of the site). The time of snow cover is variable, but is typically from October–November to late April. In 2002, the year of this study, the mean temperature for June–July was 2 8C above the average, and August and September were drier than the long-term average. There were around 1100 trees ha1. P. abies dominates the lower terrain, but on higher ground the contribution of Pinus sylvestris L. becomes significant. Other tree species are Betula spp. and Populus tremula L. The understory vegetation is dominated by Vaccinium myrtillus L. In early June 2002, six circular plots with a radius of 15 m (707 m2) were laid out. Three of these were randomly selected to be girdled, i.e. the bark of every living tree in these plots was removed down to the phloem along a 0.3 m section around the circumference. In the centre of each plot soil respiration was measured in three permanent circular sub-plots (0.0464 m2). In these sub-plots gas samples were collected at 3–8 min intervals for
12–20 min from opaque temporary 6 l headspaces (Ho¨gberg and Ekblad, 1996), eight times between early June and early October during 2002. The gas samples were transferred to 12 ml Exetainer vials and analysed on a gas purification module coupled on-line to an isotope ratio mass spectrometer (Ho¨gberg and Ekblad, 1996). We report the mean soil respiration rates ( S.E.) for girdled and non-girdled plots. Autotrophic respiration was calculated as the respiration on the control plots minus the respiration on the girdled plots. We monitored soil (at 10–15 cm depth) temperature in 5 plots and air temperature through the experiment. 3. Results and discussion The foliage of the spruce trees, the dominant tree species, remained green through the first summer of this experiment, but considerable defoliation occurred the second year after girdling. Hence, we use respiration data for the first summer only. Inventories of ectomycorrhizal sporocarps in August, c. 70 days after girdling, showed that the treatment had stopped effectively the flux of photosynthate to the tree belowground system in the central area of the plots; there were no ectomycorrhizal fungal sporocarps in the central 240 m2 of girdled plots (Go¨ttlicher et al., 2008). We assume, based on previous studies (Ho¨gberg et al., 2001; Olsson et al., 2005; Giesler et al., 2007) that one immediate response to girdling is an accelerated use of stored non-structural carbohydrates in roots and mycorrhizal fungi. Thus, estimates of autotrophic respiration during the first half of the summer are not reliable. This argument is supported by the relatively constant relation between the autotrophic and heterotrophic components through the second year, including data from early summer, in the previous experiment with pine, in which the foliage remained green for almost three years (Bhupinderpal-Singh et al., 2003). Based on these arguments, we derive our partitioning from data later in the summer in this case. In August, the calculated autotrophic respiration was slightly higher than the heterotrophic respiration (the respiration on girdled plots) at around 53% (52.8% on 12 August, 52.5% on 23 August) of total soil respiration (Fig. 1). Later in the season, heterotrophic respiration was higher than autotrophic respiration, most likely as a result of rapidly diminishing rates of photosynthesis this time of the year. Since there was very little variation in soil respiration rates within treatments (Fig. 1), there was no evidence that the microtopographic position had any influence on the partitioning of soil respiratory components. We would like to emphasize, once again, that the estimate of 53% autotrophic respiration is conservative. First, there may still be an accelerated use of sugars and starch in the roots of girdled trees. Second, there should also be an accelerated mortality of fine roots
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Fig. 1. Soil respiration (a), and air and soil temperatures (b, diurnal means) at Storskogberget through the summer of 2002. Symbols in (a) filled circles, control plots; open circles, girdled plots; filled triangles, calculated autotrophic respiration. Lines in (b) solid line, soil temperature; dotted line, air temperature.
and mycorrhizal fungal mycelium (Ho¨gberg and Ho¨gberg, 2002). Third, we did not stop the below-ground C flux in understory plants. All three work in the same direction, i.e. they lead to underestimation of the calculated fractional contribution of the autotrophic component. The fact that it is still estimated at around 50% is clear evidence of the importance of the direct below-ground flux of recent
photosynthate for soil activity in this type of forest. How does this figure compare with previous estimates? Estimates based on a wider range of methods, time scales and across biomes vary as widely as between 10 and 90% (Hanson et al., 2000). Not surprisingly, the studies based on tree-girdling in boreal and temperate forests vary much less (Table 1). The mean for unfertilized boreal forests (n = 3, using data only from the 1st season) is 56 2% as compared to 44 3% in temperate forests (n = 6). At present, the sample is too small to provide a basis for more advanced interpretation. We excluded an early tree-girdling experiment (Edwards and Ross-Todd, 1979), which did not explicitly address the partitioning between autotrophic and heterotrophic components, used comparatively small plots and had no replicates. Addition of nutrients can lead to decreased plant below-ground allocation. It apparently had a negative effect on the fractional contribution of autotrophic respiration in an experiment in boreal forest (Olsson et al., 2005), but the slightly lower (t-test, d.f. = 7, p < 0.05) autotrophic respiration in temperate as compared to in boreal forests cannot, at present, be ascribed to a higher availability of nutrients. Another driver of respiratory activity of great interest is temperature (Davidson et al., 2006). A problem is that the effect of another major driver, the supply of substrate, photosynthate, may co-vary strongly with temperature because both are driven by solar radiation. Many studies have reported strong correlations between soil temperature and total soil respiratory activity. We concentrate on total soil respiratory activity here, because the components of respiration are not well separated for much of the observation period, as discussed above. Since we assumed that below-ground C allocation has a strong seasonality (Hansen et al., 1997; Ho¨gberg et al., 2001), with greatest allocation in late summer, we plotted soil respiratory activity vs. temperature in a way that enabled tracking the changes in respiration over time (Fig. 2). There are undoubtedly correlations between soil respiration and air and soil temperatures (Fig. 2). However, the loops in these relations provide evidence of a seasonal hysteresis, as found elsewhere in seasonal climates (Curiel Yuste et al., 2004; Richardson et al., 2006), similar respiration rates were observed over a difference in temperature of 4 8C (Fig. 2). Thus, in this boreal forest, season, and not just temperature per se, appears important. Our observations show that autotrophic respiration can account for at least 53% of total soil respiration in this boreal forest. They add to the small set of data available from other studies using tree-girdling, which seem to indicate that the fractional contribution of autotrophic activity may be greater in boreal than in temperate forests. Boreal forests are strongly seasonal. Our data suggest that the seasonality in soil respiration cannot be explained by temperature alone. We propose that it could also be attributed to seasonal variation in below-ground C allocation. Acknowledgments We would like to thank the company Holmen Skog AB, especially Dr. Ola Ka˚re´n, for the permit to conduct this experiment on their property. The study was supported by grants from the Swedish Science Council (VR) and the EU (project FORCAST). References
Fig. 2. Soil respiration plotted vs. soil (solid lines and arrows) and air (dotted lines and arrows) temperatures (diurnal means). The arrows describe the course of change starting early in the summer: S denotes starting points (5/6 = 5 June) and E end points (4/10 = 4 October).
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