Large-scale stem-girdling experiment reduced soil respiration for five consecutive years. Timing and magnitude of soil respiration declines are better explained by changes in leaf area rather than in soil microclimate.
Soil respiration (Rs) represents the largest flux of carbon (C) from forests to the atmosphere, but the long-term influence of phloem-disrupting disturbance on Rs is poorly understood, limiting robust forecasts of ecosystem C balance. Using a decade of observations from the Forest accelerated succession experiment (FASET), we examined relationships among Rs, soil temperature, soil moisture, and leaf area index (LAI) following the stem girdling-induced mortality of 40% of all canopy trees within a 39-ha area. Mean annual Rs declined by about 20% relative to the control two years after disturbance, but recovered to near pre-disturbance values within five years; this reduction correlated with LAI losses and lower Rs temperature sensitivity (i.e., Q10), with the latter counteracting soil warming caused by partial canopy defoliation. These observations are consistent with progressive reductions in belowground labile C causing reductions in Rs. We conclude that the effects of stem girdling on Rs (1) were not immediate, occurring two years after the treatment, (2) were primarily influenced by biotic rather than soil microclimate changes, and (3) persisted for nearly a decade but were temporally dynamic, underscoring the value of long-term experiments.
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Amiro BD, Barr AG, Barr JG, Black TA et al (2010) Ecosystem carbon dioxide fluxes after disturbance in forests of North America. J Geophys Res Biogeosci. https://doi.org/10.1029/2010JG001390
Bhupinderpal-Singh NA, Ottosson-Löfvenius M, Högberg MN, Mellander PE, Högberg 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. https://doi.org/10.1046/j.1365-3040.2003.01053.x
Binkley D, Stape JL, Takahashi EN, Ryan MG (2006) Tree-girdling to separate root and heterotrophic respiration in two Eucalyptus stands in Brazil. Oecologia 148:447–454. https://doi.org/10.1007/s00442-006-0383-6
Bond-Lamberty B, Fisk JP, Holm JA, Bailey VL, Bohrer G, Gough CM (2015) Moderate forest disturbance as a stringent test for gap and big-leaf models. Biogeosciences 12:513–526. https://doi.org/10.5194/bg-12-513-2015
Bond-Lamberty B, Bailey VL, Chen M, Gough CM, Vargas R (2018) Globally rising soil heterotrophic respiration over recent decades. Nature 560:80–83. https://doi.org/10.1038/s41586-018-0358-x
Borkhuu B, Peckham SD, Ewers BE, Norton U, Pendall E (2015) Does soil respiration decline following bark beetle induced forest mortality? Evidence from a lodgepole pine forest. Agric for Meteorol 214–215:201–207. https://doi.org/10.1016/j.agrformet.2015.08.258
Chen D, Zhang Y, Lin Y, Zhu W, Fu S (2009) Changes in belowground carbon in Acacia crassicarpa and Eucalyptus urophylla plantations after tree girdling. Plant Soil 326:123. https://doi.org/10.1007/s11104-009-9986-0
Concilio A, Ma S, Ryu SR, North M, Chen J (2006) Soil respiration response to experimental disturbances over 3 years. For Ecol Manage 228:82–90. https://doi.org/10.1016/j.foreco.2006.02.029
Curtis PS, Vogel CS, Gough CM, Schmid HP, Su HB, Bovard BD (2005) Respiratory carbon losses and the carbon-use efficiency of a northern hardwood forest, 1999–2003. New Phytol 167:437–455. https://doi.org/10.1111/j.1469-8137.2005.01438.x
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. https://doi.org/10.1038/nature04514
Edwards NT, Ross-Todd BM (1979) Effects of stem girdling on biogeochemical cycles within a mixed deciduous forest in eastern Tennessee. 1. Soil solution chemistry, soil respiration, litterfall and root biomass studies. Oecologia 40:247–257. https://doi.org/10.1007/BF00345323
Fahey RT, Atkins JW, Campbell JL, Rustad LE, Duffy M, Driscoll CT et al (2020) Effects of an experimental ice storm on forest canopy structure. Can J for Res 50:136–145. https://doi.org/10.1139/cjfr-2019-0276
Goetz SJ, Bond-Lamberty B, Law BE, Hickle JA, Huang C, Houghton RA, McNulty S et al (2012) Observations and assessment of forest carbon dynamics following disturbance in North America. J Geophys Res Biogeosci 117:G02022. https://doi.org/10.1029/2011JG001733
Gough CM, Flower CE, Vogel CS, Dragoni D, Curtis PS (2009) Whole-ecosystem labile carbon production in a north temperate deciduous forest. Agric for Meteorol 149:1531–1540. https://doi.org/10.1016/j.agrformet.2009.04.006
Gough CM, Hardiman BS, Nave LE, Bohrer G, Maurer KD, Vogel CS, Nadelhoffer KJ (2013) Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest. Ecol Appl 23:1202–1215. https://doi.org/10.1890/12-1554.1
Gough CM, Atkins JW, Bond-Lamberty B, Agee EA, Dorheim KR, Fahey RT et al (2021a) Forest structural complexity and biomass predict first-year carbon cycling responses to disturbance. Ecosystems 24:699–712. https://doi.org/10.1007/s10021-020-00544-1
Gough CM, Bohrer G, Hardiman BS, Nave LE, Vogel CS, Atkins JW, Bond-Lamberty B et al (2021b) Disturbance-accelerated succession increases the production of a temperate forest. Ecol Appl 31:e02417. https://doi.org/10.1002/eap.2417
Harmon ME, Bond-Lamberty B, Vargas R, Tang J (2011) Heterotrophic respiration in disturbed forests: a review with examples from North America. J Geophys Res Biogeosci. https://doi.org/10.1029/2010JG001495
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN et al (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792. https://doi.org/10.1038/35081058
Hu T, Sun L, Hu H, Weise DR, Guo F (2017) Soil respiration of the dahurian larch (Larix gmelinii) forest and the response to fire disturbance in Da Xing’an Mountains. China Sci Rep 7:2967. https://doi.org/10.1038/s41598-017-03325-4
Hursh A, Ballantyne A, Cooper L, Maneta M, Kimball J, Watts J (2017) The sensitivity of soil respiration to soil temperature, moisture, and carbon supply at the global scale. Glob Chang Biol 23:2090–2103. https://doi.org/10.1111/gcb.13489
Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL et al (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990. https://doi.org/10.1038/nature06777
Levy-Varon JH, Schuster WSF, Griffin KL (2012) The autotrophic contribution to soil respiration in a northern temperate deciduous forest and its response to stand disturbance. Oecologia 169:211–220. https://doi.org/10.1007/s00442-011-2182-y
Li W, Ciais P, Wang Y, Yin Y, Peng S, Zhu Z, Bastos A et al (2018) Recent changes in global photosynthesis and terrestrial ecosystem respiration constrained from multiple observations. Geophys Res Lett. https://doi.org/10.1002/2017GL076622
Lindauer M, Schmid HP, Grote R, Mauder M, Steinbrecher R, Wolpert B (2014) Net ecosystem exchange over a non-cleared wind-throw-disturbed upland spruce forest—measurements and simulations. Agric for Meteorol 197:219–234. https://doi.org/10.1016/j.agrformet.2014.07.005
Lindroth A, Lagergren F, Aurela M, Bjarnadottir B, Christensen T, Dellwik E, Grelle A et al (2008) Leaf area index is the principal scaling parameter for both gross photosynthesis and ecosystem respiration of Northern deciduous and coniferous forests. Tellus B Chem Phys Meteorol 60:129–142. https://doi.org/10.1111/j.1600-0889.2007.00330.x
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. https://doi.org/10.1111/j.1469-8137.2009.03063.x
Mathes KM, Ju Y, Kleinke C, Oldfield C, Bohrer G, Bond-Lamberty B, Vogel CS, Dorheim K, Gough CM (2022) A multidimensional stability framework enhances interpretation and comparison of carbon cycling response to disturbance. Ecosphere 12:e03800. https://doi.org/10.1002/ecs2.3800
Matteucci M, Gruening C, Goded Ballarin I, Seufert G, Cescatti A (2015) Components, drivers and temporal dynamics of ecosystem respiration in a Mediterranean pine forest. Soil Biol Biochem 88:224–235. https://doi.org/10.1016/j.soilbio.2015.05.017
McDowell NG, Allen CD, Anderson-Teixeira K, Aukema BH, Bond-Lamberty B (2020) Pervasive shifts in forest dynamics in a changing world. Science 368:6494. https://doi.org/10.1126/science.aaz9463
Moore DJP, Trahan NA, Wilkes P, Quaife T, Stephens BB, Elder K et al (2013) Persistent reduced ecosystem respiration after insect disturbance in high elevation forests. Ecol Lett 16:731–737. https://doi.org/10.1111/ele.12097
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373. https://doi.org/10.1073/pnas.1006463107
Pan Y, Birdsey RA, Fang J, Houghton RA, Kauppi PE, Kurz WA, Phillips OL et al (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993. https://doi.org/10.1126/science.1201609
Pellegrini AFA, Caprio AC, Georgiou K, Finnegan C, Hobbie SE, Hatten JA, Jackson RB (2021) Low-intensity frequent fires in coniferous forests transform soil organic matter in ways that may offset ecosystem carbon losses. Glob Chang Biol 27:3810–3823. https://doi.org/10.1111/gcb.15648
Reichstein M, Rey A, Freibauer A, Tenhunen J, Valentini R, Banza J et al (2003) Modeling temporal and large-scale spatial variability of soil respiration from soil water availability, temperature and vegetation productivity indices. Global Biogeochem Cycles 17:4. https://doi.org/10.1029/2003gb002035
Ribeiro-Kumara C, Köster E, Aaltonen H, Köster K (2020) How do forest fires affect soil greenhouse gas emissions in upland boreal forests? A Review Environ Res 184:109328. https://doi.org/10.1016/j.envres.2020.109328
Seidl R, Thom D, Kautz M, Martin-Benito D, Peltoniemi M, Vacchiano G et al (2017) Forest disturbances under climate change. Nat Clim Chang 7:395–402. https://doi.org/10.1038/nclimate3303
Speckman HN, Frank JM, Bradford JB, Miles BL, Massman WJ et al (2014) Forest ecosystem respiration estimated from eddy covariance and chamber measurements under high turbulence and substantial tree mortality from bark beetles. Glob Chang Biol 21:708–721. https://doi.org/10.1111/gcb.12731
Vargas R, Allen MF (2008) Diel patterns of soil respiration in a tropical forest after Hurricane Wilma. J Geophys Res 113:G03021. https://doi.org/10.1029/2007JG000620
Weed AS, Ayres MP, Hicke JA (2013) Consequences of climate change for biotic disturbances in North American forests. Ecol Monogr 83:441–470. https://doi.org/10.1890/13-0160.1
Wolkovich EM, Regetz J, O’Connor MI (2012) Advances in global change research require open science by individual researchers. Glob Chang Biol 18:2102–2110. https://doi.org/10.1111/j.1365-2486.2012.02693.x
Xu M, Shang H (2016) Contribution of soil respiration to the global carbon equation. J Plant Physiol 203:16–28. https://doi.org/10.1016/j.jplph.2016.08.007
Yang Y, Hillebrand H, Lagisz M, Cleasby I, Nakagawa S (2022) Low statistical power and overestimated anthropogenic impacts, exacerbated by publication bias, dominate field studies in global change biology. Glob Chang Biol 28:969–989. https://doi.org/10.1111/gcb.15972
This work was supported by the National Science Foundation Division of Environmental Biology, Award 1655095 and by the Department of Energy AmeriFlux Core Site support to US-UMB and US-UMd sites. We thank the University of Michigan Biological Station for hosting and supporting our work.
This work was supported by the National Science Foundation Division of Environmental Biology, Award 1655095 and by the Department of Energy AmeriFlux Core Site support to US-UMB and US-UMd sites.
The authors declare that there are no personal, professional or financial relationships that could potentially be construed as a conflict of interest.
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Clippard, E.A., Haruna, S.I., Curtis, P.S. et al. Decadal forest soil respiration following stem girdling. Trees 36, 1943–1949 (2022). https://doi.org/10.1007/s00468-022-02340-x