Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Rapid rebound of soil respiration following partial stand disturbance by tree girdling in a temperate deciduous forest

Abstract

Forests serve an essential role in climate change mitigation by removing CO2 from the atmosphere. Within a forest, disturbance events can greatly impact C cycling and subsequently influence the exchange of CO2 between forests and the atmosphere. This connection makes understanding the forest C cycle response to disturbance imperative for climate change research. The goal of this study was to examine the temporal response of soil respiration after differing levels of stand disturbance for 3 years at the Black Rock Forest (southeastern NY, USA; oaks comprise 67 % of the stand). Tree girdling was used to mimic pathogen attack and create the following treatments: control, girdling all non-oaks (NOG), girdling half of the oak trees (O50), and girdling all the oaks (OG). Soil respiratory rates on OG plots declined for 2 years following girdling before attaining a full rebound of belowground activity in the third year. Soil respiration on NOG and O50 were statistically similar to the control for the duration of the study although a trend for a stronger decline in respiration on O50 relative to NOG occurred in the first 2 years. Respiratory responses among the various treatments were not proportional to the degree of disturbance and varied over time. The short-lived respiratory response on O50 and OG suggests that belowground activity is resilient to disturbance; however, sources of the recovered respiratory flux on these plots are likely different than they were pre-treatment. The differential taxon response between oaks and non-oaks suggests that after a defoliation or girdling event, the temporal response of the soil respiratory flux may be related to the C allocation pattern of the affected plant group.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Amiro BD, Barr AG, Barr JG, Black TA, Bracho R, Brown M, Chen J, Clark KL, Davis KJ, Desai AR, Dore S, Engel V, Fuentes JD, Goldstein AH, Goulden ML, Kolb TE, Lavigne MB, Law BE, Margolis HA, Martin T, McCaughey JH, Misson L, Montes-Helu M, Noormets A, Randerson JT, Starr G, Xiao J (2010) Ecosystem carbon dioxide fluxes after disturbance in forests of North America. J Geophys Res 115:G00K02

  2. Andersen CP, Nikolov I, Nikolova P, Matyssek R, Häberle K-H (2005) Estimating “autotrophic” belowground respiration in spruce and beech forests: decreases following girdling. Eur J For Res 124:155–163. doi:10.1007/s10342-005-0072-8

  3. Ayres MP, Lombardero MJ (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262:263–286

  4. Baldocchi D (2008) Breathing of the terrestrial biosphere: lessons learned from a global network of carbon dioxide flux measurement systems. Aust J Bot 56:1–26

  5. Berryman E, Marshall JD, Rahn T, Litvak M, Butnor J (2013) Decreased carbon limitation of litter respiration in a mortality-affected piñon–juniper woodland. Biogeosciences 10:1625–1634

  6. Bhupinderpal-Singh, Nordgren A, Ottosson Lofvenius M, Hogberg MN, Mellander PE, 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 Cell Environ 26:1287–1296. doi:10.1046/j.1365-3040.2003.01053.x

  7. 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. doi:10.1007/s00442-006-0383-6

  8. Bormann FJ, Likens GE (1994) Pattern and process in a forested ecosystem: disturbance, development, and the steady state based on the Hubbard Brook ecosystem study. Springer, Berlin

  9. Brenneman BB, Fredreick DJ, Gardner WE, Schoenhofen LH, Marsh PL (1978) Biomass of species and stands of West Virginia hardwoods. In: Pope PE (ed) Proceedings of Central Hardwoods Forest Conference II, Purdue University. Purdue University, West Lafayette, IN, pp 159–178

  10. Brown M, Black TA, Nesic Z, Foord VN, Spittlehouse DL, Fredeen AL, Grant NJ, Burton PJ, Trofymow JA (2010) Impact of mountain pine beetle on the net ecosystem production of lodgepole pine stands in British Columbia. Agric For Meteorol 150:254–264

  11. Chakraborty S (2013) Migrate or evolve: options for plant pathogens under climate change. Global Change Biol 19:1985–2000

  12. Chen D, Zhang Y, Lin Y, Zhu W, Fu S (2010) Changes in belowground carbon in Acacia crassicarpa and Eucalyptus urophylla plantations after tree girdling. Plant Soil 326:123–135

  13. Clark KL, Skowronski N, Hom J (2010) Invasive insects impact forest carbon dynamics. Global Change Biol 16:88–101. doi:10.1111/j.1365-2486.2009.01983.x

  14. Claus A, George E (2005) Effect of stand age on fine-root biomass and biomass distribution in three European forest chronosequences. Can J For Res 35:1617–1625

  15. Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Wotton BM (2001) Climate change and forest disturbances. Bioscience 51:723–734

  16. DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant–insect interactions. Plant Physiol 160:1677–1685

  17. Detto M, Bohrer G, Goedhart Nietz J, Maurer K, Vogel CS, Gough CM, Curtis PS (2013) Multivariate conditional granger causality analysis for lagged response of soil respiration in a temperate forest. Entropy 15:4266–4284

  18. Ekberg A, Buchmann N, Gleixner G (2007) Rhizospheric influence on soil respiration and decomposition in a temperate Norway spruce stand. Soil Biol Biochem 39:2103–2110

  19. Falxa-Raymond N, Patterson AE, Schuster SF, Griffin KG (2012) Oak loss increases foliar nitrogen, δ15N and growth rates of Betula lenta in a north-eastern deciduous forest. Tree Physiol 9:1092–1101

  20. Forrester JA, Mlandenoff DJ, Gower ST (2013) Experimental manipulation of forest structure: near-term effects on gap and stand scale C dynamics. Ecosystems. doi:10.1007/s10021-013-9695-7

  21. Frey B, Hagedorn F, Giudici F (2006) Effect of girdling on soil respiration and root composition in a sweet chestnut forest. For Ecol Manage 225:271–277. doi:10.1016/j.foreco.2006.01.003

  22. Goetz SJ, Bond-Lamberty B, Law BE, Hicke JA, Huang C, Houghton RA, McNulty S, O’Halloran T, Harmon M, Meddens JH, Pfeifer EM, Mildrexler D, Kasischke ES (2012) Observations and assessment of forest carbon recovery following disturbance in North America. J Geophys Res 117:G02022. doi:10.1029/2011JG001733

  23. Gough CM, Hardiman BS, Nave LE, Bohrer G, Maurer KD, Vogel CS, Nadelhoffer KJ, Curtis PS (2013) Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest. Ecol Appl 23:1202–1215

  24. Goulden ML, McMillan AMS, Winston GC, Rocha AV, Manies KL, Harden JW, Bond-Lamberty BP (2011) Patterns of NPP, GPP, respiration, and NEP during boreal forest succession. Global Change Biol 17:855–871

  25. Hancock JE, Arthur MA, Weathers KC, Lovett GM (2008) Carbon cycling along a gradient of beech bark disease impact in the Catskill Mountains, New York. Can J For Res 38:1267–1274

  26. Harrington R, Flemming RA, Woiwod IP (2001) Climate change impacts on insect management and conservation in temperate regions: can they be predicted? Agric For Entomol 3:233–240

  27. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

  28. Hicke JA, Allen CD, Desai AR, Dietz MC, Hall RJ, Hogg EH, Kashian DM, Moore D, Raffa KF, Sturrock RN, Vogelmann J (2011) Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Global Change Biol 18:7–34

  29. Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Princeton University Press, Princeton

  30. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekbald A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

  31. Jactel H, Petit J, Desprez-Loustau M-L, Delzon S, Piou D, Battisti A, Koricheva J (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Global Change Biol 18:267–276

  32. Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol 160:1719–1727

  33. Kurz WA, Stinson G, Rampley GJ, Dymond CC, Neilson ET (2008) Risk of natural disturbances makes future contribution of Canada’s forests to the global carbon cycle highly uncertain. Proc Natl Acad Sci USA 105:551–1555

  34. Law BE, Sun OJ, Campbell J, Tuyl SV, Thornton PE (2003) Changes in carbon storage and fluxes in a chronosequence of ponderosa pine. Global Change Biol 9:510–524

  35. Levy-Varon JH, Schuster WSF, Griffin KL (2012) The autotrophic contribution to soil respiration in a northern temperate deciduous forest and its response to disturbance. Oecologia 169:211–220

  36. Liu S, Bond-Lamberty B, Hicke JA, Vargas R, Zhao S, Chen J, Edburg SL, Hu Y, Liu J, McGuire DA, Xiao J, Keane R, Yuan W, Tang J, Luo Y, Potter C, Oeding J (2011) Simulating the impacts of disturbances on forest carbon cycling in North America: processes, data, models, and challenges. J Geophys Res 116:1–22

  37. Logan J, Régnière J, Powell JA (2003) Assessing the impacts of global warming on forest pest dynamics. Front Ecol Environ 1:130–137

  38. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405

  39. Monteith DB (1979) Whole-tree weight tables for New York. AFRI research report 40. State University of New York, Syracuse

  40. Moore DJP, Trahan NA, Wilkes P, Quaife T, Stephens BB, Elder K, Desai AR, Negron J, Monson RK (2013) Persistent reduced ecosystem respiration after insect disturbance in high elevation forests. Ecol Lett 16:731–737

  41. Morehouse K, Johns T, Kaye J, Kaye A (2008) Carbon and nitrogen cycling immediately following bark beetle outbreaks in southwestern ponderosa pine forests. For Ecol Manage 255:2698–2708

  42. Nave LE, Gough CM, Maurer KD, Bohrer G, Hardiman BS, Le Moine J, Munoz AB, Nadelhoffer KJ, Sparks JP, Strahm BD, Vogel CS, Curtis PS (2011) Disturbance and the resilience of coupled carbon and nitrogen cycling in a north temperate forest. J Geophys Res 116:G04016

  43. Noel ARA (1970) The girdled tree. Bot Rev 36:162–195

  44. Nuckolls AE, Wurzburger N, Ford CR, Hendrick RL, Vose JM, Kloeppel BD (2009) Hemlock declines rapidly with hemlock woolly adelgid infestation: impacts on the carbon cycle of southern Appalachian forests. Ecosystems 12:179–190

  45. Orwig DA, Barker Plotkin AA, Davidson EA, Lux H, Savage KE, Ellison AM (2013) Foundation species loss affects vegetation structure more than ecosystem function in a northeastern USA forest. Peer J 1:e41. doi:10.7717/peerj.41

  46. Overpeck JT, Rind D, Goldberg R (1990) Climate-induced changes in forest disturbance and vegetation. Nature 343:51–53

  47. Pautasso M, Doring TF, Barbelotto M, Pellis L, Jeger MJ (2012) Impacts of climate change on plant diseases-opinions and trends. Eur J Plant Pathol 133:295–313

  48. Peltzer DA, Allen RB, Lovett GM, Whitehead D, Wardle DA (2010) Effects of biological invasions on forest carbon sequestration. Global Change Biol 16:732–746

  49. Pfeifer EM, Hicke JA, Meddens AJH (2011) Observations and modeling of aboveground tree carbon stocks and fluxes following a bark beetle outbreak in the western United States. Global Change Biol 17:339–350

  50. Pregitzer KS, Euskirchen ES (2004) Carbon cycling and storage in world forests: biome patterns related to forest age. Global Change Biol 10:2052–2077

  51. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL http://www.r-project.org/

  52. Rhoades CC, McCutchan JH, Cooper LA, Clow D, Detmer TM, Briggs JS, Stednixk JD, Veblen TT, Ertz RM, Likens GE, Lewis WM (2013) Biogeochemistry of beetle-killed forests: explaining a weak nitrate response. Proc Natl Acad Sci USA 110:1756–1760

  53. Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Global Change Biol 12:205–216

  54. Seidl R, Rammer W, Jager D, Lexer MJ (2008) Impact of bark beetle (Ips typographus L.) disturbance on timber production and carbon sequestration in different management strategies under climate change. For Ecol Manage 256:209–220

  55. Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Official Soil Series Descriptions [Online WWW]. Available URL: http://soils.usda.gov/technical/classification/osd/index.html. Accessed 10 July 2010. USDA-NRCS, Lincoln, NE

  56. Uhl C, Jordan CF (1984) Succession and nutrient dynamics following forest cutting and burning in Amazonia. Ecology 65:1476–1490

  57. Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221

Download references

Acknowledgments

We are grateful to the Ernst C. Stiefel Foundation, the Black Rock Forest Consortium and the Chevron Student Initiative Fund for providing funding for this research. We thank the entire Black Rock Forest staff for logistical support and help with data collection. We also thank Dr. David Madigan and Louis Mittel for statistical consulting, and Dr. Gary Lovett and anonymous reviewers for their insightful feedback.

Author information

Correspondence to Jennifer H. Levy-Varon.

Additional information

Communicated by Evan DeLucia.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1068 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Levy-Varon, J.H., Schuster, W.S.F. & Griffin, K.L. Rapid rebound of soil respiration following partial stand disturbance by tree girdling in a temperate deciduous forest. Oecologia 174, 1415–1424 (2014). https://doi.org/10.1007/s00442-013-2844-z

Download citation

Keywords

  • Soil respiration
  • Autotrophic respiration
  • Forest disturbance
  • Tree girdling
  • Pathogen attack