Abstract
A recent unprecedented epidemic of beetle-induced tree mortality has occurred in the lodgepole pine forests of Western North America. Here, we present the results of studies in two subalpine forests in the Rocky Mountains, one that experienced natural pine beetle disturbance and one that experienced simulated disturbance imposed through bole girdling. We assessed changes to soil microclimate and biogeochemical pools in plots representing different post-disturbance chronosequences. High plot tree mortality, whether due to girdling or beetle infestation, caused similar alterations in soil nutrient pools. During the first 4 years after disturbance, sharp declines were observed in the soil dissolved organic carbon (DOC) concentration (45–51 %), microbial biomass carbon concentration (33–39 %), dissolved organic nitrogen (DON) concentration (31–42 %), and inorganic phosphorus (PO4 3−) concentration (53–55 %). Five to six years after disturbance, concentrations of DOC, DON, and PO4 3− recovered to 71–140 % of those measured in undisturbed plots. Recovery was coincident with observed increases in litter depth and the sublitter, soil O-horizon. During the 4 years following disturbance, soil ammonium, but not nitrate, increased to 2–3 times the levels measured in undisturbed plots. Microbial biomass N increased in plots where increased ammonium was available. Our results show that previously observed declines in soil respiration following beetle-induced disturbance are accompanied by losses in key soil nutrients. Recovery of the soil nutrient pool occurs only after several years following disturbance, and is correlated with progressive mineralization of dead tree litter.
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Allen C, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears D, Hogg E, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Jong-Hwan L, Allard G, Running S, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684. doi:10.1016/j.foreco.2009.09.001
Amman GD (1972) Mountain pine beetle brood production in relation to thickness of lodgepole pine phloem. J Econ Entomol 65:138–140
Anderegg W, Kane J, Anderegg L (2013) Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim Change 3:30–36
Bigler C, Veblen T (2011) Changes in litter and dead wood loads following tree death beneath subalpine conifer species in northern Colorado. Can J Forest Res 41:331–340. doi:10.1139/X10-217
Bonan G (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. doi:10.1126/science.1155121
Breshears D et al (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci USA 102:15144–15148. doi:10.1073/pnas.0505734102
Bright B, Hicke J, Meddens A (2013) Effects of bark beetle-caused tree mortality on biogeochemical and biogeophysical MODIS products. J Geophys Res Biogeosciences 118:974–982. doi:10.1002/jgrg.20078
Brookes P, Landman A, Pruden G, Jenkinson D (1985) Chloroform fumigation and the release of soil-nitrogen—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi:10.1016/0038-0717(85)90144-0
Clow D, Rhoades C, Briggs J, Caldwell M, Lewis W (2011) Responses of soil and water chemistry to mountain pine beetle induced tree mortality in Grand County, Colorado, USA. Appl Geochem 26:S174–S178. doi:10.1016/j.apgeochem.2011.03.096
Collins B, Rhoades C, Underhill J, Hubbard R (2010) Post-harvest seedling recruitment following mountain pine beetle infestation of Colorado lodgepole pine stands: a comparison using historic survey records. Can J Forest Res 40:2452–2456. doi:10.1139/X10-172
Dakora F, Phillips D (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. doi:10.1023/A:1020809400075
Dale V, Joyce L, McNulty S, Neilson R, Ayres M, Flannigan M, Hanson P, Irland L, Lugo A, Petersen C, Simberloff D, Swanson F, Stocks B, Wotton B (2001) Climate change and forest disturbances. Bioscience 51:723–734. doi:10.1641/0006-3568(2001)051[0723:CCAFD]2.0.CO;2
D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209
De Schepper V, Steppe K, Van Labeke M, Lemeur R (2010) Detailed analysis of double girdling effects on stem diameter variations and sap flow in young oak trees. Environ Exp Bot 68:149–156. doi:10.1016/j.envexpbot.2009.11.012
Doane T, Horwath W (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722. doi:10.1081/AL-120024647
Domec J, Pruyn M (2008) Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. Tree Physiol 28:1493–1504
Edburg S, Hicke J, Brooks P, Pendall E, Ewers B, Norton U, Gochis D, Gutmann E, Meddens A (2012) Cascading impacts of bark beetle-caused tree mortality on coupled biogeophysical and biogeochemical processes. Front Ecol Environ 10:416–424. doi:10.1890/110173
Fahey T (1983) Nutrient dynamics of above-ground detritus in lodgepole pine (Pinus contorta ssp. latifolia) ecosystems, Southeastern Wyoming. Ecol Monogr 53:51–72. doi:10.2307/1942587
Fahey T, Knight D (1986) Lodgepole pine ecosystems. Bioscience 36:610–616. doi:10.2307/1310196
Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837. doi:10.1890/0012-9658(2003)084[0827:HRCTFO]2.0.CO;2
Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA), version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs. User manual and program documentation. Simon Fraser University/Institute of Ecosystem Studies, Burnaby/Millbrook
Griffin J, Turner M (2012) Changes to the N cycle following bark beetle outbreaks in two contrasting conifer forest types. Oecologia 170:551–565. doi:10.1007/s00442-012-2323-y
Griffin J, Turner M, Simard M (2011) Nitrogen cycling following mountain pine beetle disturbance in lodgepole pine forests of Greater Yellowstone. Forest Ecol Manag 261:1077–1089. doi:10.1016/j.foreco.2010.12.031
Harmon M, Franklin J, Swanson F, Sollins P, Gregory S, Lattin J, Anderson N, Cline S, Aumen N, Sedell J, Lienkaemper G, Cromak K, Cummins K (1986) Ecology of coarse woody debris in temperate ecosystems. Adv Ecol Res 15:133–302. doi:10.1016/S0065-2504(08)60121-X
Hicke J, Allen C, Desai A, Dietze M, Hall R, Hogg E, Kashian D, Moore D, Raffa K, Sturrock R, Vogelmann J (2012) Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Global Change Biol 18:7–34. doi:10.1111/j.1365-2486.2011.02543.x
Högberg M, Högberg 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. doi:10.1046/j.1469-8137.2002.00417.x
Högberg P, Read D (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554. doi:10.1016/j.tree.2006.06.004
Högberg P, Nordgren A, Buchmann N, Taylor A, Ekblad A, Högberg M, Nyberg G, Ottosson-Löfvenius M, Read D (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792
Hubbard R, Rhoades C, Elder K, Negron J (2013) Changes in transpiration and foliage growth in lodgepole pine trees following mountain pine beetle attack and mechanical girdling. Forest Ecol Manag 289:312–317. doi:10.1016/j.foreco.2012.09.028
Huber C (2005) Long lasting nitrate leaching after bark beetle attack in the highlands of the Bavarian Forest National Park. J Environ Qual 34:1772–1779. doi:10.2134/jeq2004.0210
Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A (2010) Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol 187:843–858. doi:10.1111/j.1469-8137.2010.03321.x
Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange C, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–1051
Kaňa J, Tahovská K, Kopáček J (2012) Response of soil chemistry to forest dieback after bark beetle infestation. Biogeochemistry 113:1–3. doi:10.1007/s10533-012-9765-5
Keville M, Reed S, Cleveland C (2013) Nitrogen cycling responses to mountain pine beetle disturbance in a high elevation whitebark pine ecosystem. Plos One 8:e65004. doi:10.1371/journal.pone.0065004
Klutsch J, Negrón J, Costello S, Rhoades C, West D, Popp J, Caissie R (2009) Stand characteristics and downed woody debris accumulations associated with a mountain pine beetle (Dendroctonus ponderosae Hopkins) outbreak in Colorado. Forest Ecol Manag 258:641–649. doi:10.1016/j.foreco.2009.04.034
Knight D, Yavitt J, Joyce G (1991) Water and nitrogen outflow from lodgepole pine forest after two levels of tree mortality. Forest Ecol Manag 46:215–225. doi:10.1016/0378-1127(91)90233-L
Man G (2012) Major forest insect and disease conditions in the United States: 2011. USDA Forest Service, Wahington, DC, pp 41
Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis—model and research methods. Soil Biol Biochem 43:883–894. doi:10.1016/j.soilbio.2011.01.005
McDowell N, Beerling D, Breshears D, Fisher R, Raffa K, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532. doi:10.1016/j.tree.2011.06.003
Mikkelson KM, Bearup LA, Maxwell RM, Stednick JD, McCray JE, Sharp JO (2013) Bark beetle infestation impacts on nutrient cycling, water quality and interdependent hydrological effects. Biogeochemistry 115:1–21
Moore J, McCann K, Setala H, De Ruiter P (2003) Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857. doi:10.1890/0012-9658(2003)084[0846:TIBDPI]2.0.CO;2
Moore D, Trahan N, Wilkes P, Quaife T, Stephens B, Elder K, Desai A, Negrón J, Monson R (2013) Persistent reduced ecosystem respiration after insect disturbance in high elevation forests. Ecol Lett 16:731–737. doi:10.1111/ele.12097
Morehouse K, Johns T, Kaye J, Kaye A (2008) Carbon and nitrogen cycling immediately following bark beetle outbreaks in southwestern ponderosa pine forests. Forest Ecol Manag 255:2698–2708. doi:10.1016/j.foreco.2008.01.050
Piirainen S, Finer L, Mannerkoski H, Starr M (2007) Carbon, nitrogen and phosphorus leaching after site preparation at a boreal forest clear-cut area. Forest Ecol Manag 243:10–18. doi:10.1016/j.foreco.2007.01.053
Pugh E, Gordon E (2013) A conceptual model of water yield effects from beetle-induced tree death in snow-dominated lodgepole pine forests. Hydrol Process 27:2048–2060. doi:10.1002/hyp.9312
Raffa KF, Berryman AA (1983) The role of host resistance in the colonization behavior and ecology of bark beetles. Ecol Monogr 53:27–49
Raffa K, Aukema B, Bentz B, Carroll A, Hicke J, Turner M, Romme W (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58:501–517. doi:10.1641/B580607
Rhine E, Sims G, Mulvaney R, Pratt E (1998) Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Sci Soc Am J 62:473–480
Rhoades C, McCutchan J, Cooper L, Clow D, Detmer T, Briggs J, Stednick J, Veblen T, Ertz R, Likens G, Lewis W (2013) Biogeochemistry of beetle-killed forests: explaining a weak nitrate response. Proc Nat Acad Sci USA 110:1756–1760. doi:10.1073/pnas.1221029110
Schimel J, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. doi:10.1890/03-8002
Scott-Denton L, Sparks K, Monson R (2003) Spatial and temporal controls of soil respiration rate in a high-elevation, subalpine forest. Soil Biol Biochem 35:525–534. doi:10.1016/S0038-0717(03)00007-5
Scott-Denton L, Rosenstiel T, Monson R (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Global Change Biol 12:205–216. doi:10.1111/j.1365-2486.2005.01064.x
Stark J, Hart S (1997) High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385:61–64. doi:10.1038/385061a0
Turner M, Smithwick E, Metzger K, Tinker D, Romme W (2007) Inorganic nitrogen availability after severe stand-replacing fire in the Greater Yellowstone ecosystem. Proc Natl Acad Sci USA 104:4782–4789. doi:10.1073/pnas.0700180104
van Mantgem P, Stephenson N, Byrne J, Daniels L, Franklin J, Fulé P, Harmon M, Larson A, Smith J, Taylor A, Veblen T (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524. doi:10.1126/science.1165000
Vance E, Brookes P, Jenkinson D (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707. doi:10.1016/0038-0717(87)90052-6
Vitousek P, Gosz J, Grier C, Melillo J, Reiners W, Todd R (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474. doi:10.1126/science.204.4392.469
Weintraub M, Scott-Denton L, Schmidt S, Monson R (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338. doi:10.1007/s00442-007-0804-1
Wilkes P (2009) A new remote sensing model to quantify the influence of the mountain pine beetle on GPP in subalpine forests. MSc thesis. King’s College, London
Xiong Y, D’Atri J, Fu S, Xia H, Seastedt T (2011) Rapid soil organic matter loss from forest dieback in a subalpine coniferous ecosystem. Soil Biol Biochem 43:2450–2456. doi:10.1016/j.soilbio.2011.08.013
Yamaoka Y, Swanson RH, Hiratsuka Y (1990) Inoculation of lodgepole pine with four blue-stain fungi associated with mountain pine-beetle, monitored by a heat pulse velocity (hpv) instrument. Can J Forest Res 20:31–36. doi:10.1139/x90-005
Zeller B, Liu J, Buchmann N, Richter A (2008) Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol Biochem 40:1155–1166. doi:10.1016/j.soilbio.2007.12.009
Acknowledgments
This study was funded by the Climate and Environmental Sciences Division of the Office of Biological and Environmental Research at the US Department of Energy through grant award ER65077 to the University of Colorado, Boulder. The authors declare they have no conflict of interest. The experiments in this study comply with the current laws of the USA where the experiments were performed. The authors would like to thank K. Hartfield for mapping the USFS aerial survey data; J. Negron for helping with site establishment; M. Weintraub and R. Alexander for their assistance with the methodology; and three anonymous reviewers for comments that improved the manuscript.
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Trahan, N.A., Dynes, E.L., Pugh, E. et al. Changes in soil biogeochemistry following disturbance by girdling and mountain pine beetles in subalpine forests. Oecologia 177, 981–995 (2015). https://doi.org/10.1007/s00442-015-3227-4
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DOI: https://doi.org/10.1007/s00442-015-3227-4