Abstract
Tree species interact with soil biota to impact soil organic carbon (C) pools, but it is unclear how this interaction is shaped by various ecological factors. We used multiple regression to describe how ~100 variables were related to soil organic C pools in a common garden experiment with 14 temperate tree species. Potential predictor variables included: (i) the abundance, chemical composition, and decomposition rates of leaf litter and fine roots, (ii) species richness and abundance of bacteria, fungi, and invertebrate animals in soil, and (iii) measures of soil acidity and texture. The amount of organic C in the organic horizon and upper 20 cm of mineral soil (i.e. the combined C pool) was strongly negatively correlated with earthworm abundance and strongly positively correlated with the abundance of aluminum, iron, and protons in mineral soils. After accounting for these factors, we identified additional correlations with soil biota and with litter traits. Rates of leaf litter decomposition, measured as litter mass loss, were negatively correlated with size of the combined soil organic C pool. Somewhat paradoxically, the combined soil organic C pool was also negatively related to the ratio of recalcitrant compounds to nitrogen in leaf litter. These apparent effects of litter traits probably arose because two independent components of litter “quality” were controlling different aspects of decomposition. Leaf litter mass loss rates were positively related with leaf litter calcium concentrations, reflecting greater utilization and depolymerization of calcium-rich leaf litter by earthworms and other soil biota, which presumably led to greater proportional losses of litter C as CO2 or dissolved organic C. The fraction of depolymerized and metabolized litter that is ultimately lost as CO2 is an inverse function of microbial C use efficiency, which increases with litter nutrient concentrations but decreases with concentrations of recalcitrant compounds (e.g. lignin); thus, high ratios of recalcitrant compounds to nitrogen in leaf litter likely caused a greater fraction of depolymerized litter to be lost as CO2. Existing conceptual models of soil C stabilization need to reconcile the effects of litter quality on these two potentially counteracting factors: rates of litter depolymerization and microbial C use efficiency.
References
Berg B, Davey MP, De Marco A et al (2010) Factors influencing limit values for pine needle litter decomposition: a synthesis for boreal and temperate pine forest systems. Biogeochemistry 100:57–73. doi:10.1007/s10533-009-9404-y
Bring J (1994) How to standardize regression coefficients. Am Stat 48:209–213. doi:10.2307/2684719
Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198. doi:10.1016/S1164-5563(00)01062-1
Cornwell WK, Cornelissen JHC, Amatangelo K et al (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071. doi:10.1111/j.1461-0248.2008.01219.x
Cotrufo MF, Wallenstein MD, Boot CM et al (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Change Biol 19:988–995. doi:10.1111/gcb.12113
Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50:463–477. doi:10.1016/j.pedobi.2006.09.001
Dauer JE, Chorover J, Chadwick OA et al (2007) Controls over leaf and litter calcium concentrations among temperate trees. Biogeochemistry 86:175–187. doi:10.1007/s10533-007-9153-8
De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531. doi:10.1111/j.1461-0248.2008.01164.x
De Vries FT, Thébault E, Liiri M et al (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci 110:14296–14301. doi:10.1073/pnas.1305198110
Dickie IA, Kałucka I, Stasińska M, Oleksyn J (2010) Plant host drives fungal phenology. Fungal Ecol 3:311–315. doi:10.1016/j.funeco.2009.12.002
Don A, Steinberg B, Schöning I et al (2008) Organic carbon sequestration in earthworm burrows. Soil Biol Biochem 40:1803–1812. doi:10.1016/j.soilbio.2008.03.003
Dornbush ME, Isenhart TM, Raich JW (2002) Quantifying fine-root decomposition: an alternative to buried litterbags. Ecology 83:2985–2990. doi:10.2307/3071834
Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman and Hall, London
Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486
Finzi AC, Van Breemen N, Canham CD (1998) Canopy tree-soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–446. doi:10.2307/2641083
Garbelotto M, Pautasso M (2012) Impacts of exotic forest pathogens on Mediterranean ecosystems: four case studies. Eur J Plant Pathol 133:101–116. doi:10.1007/s10658-011-9928-6
Gessner MO, Swan CM, Dang CK et al (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380. doi:10.1016/j.tree.2010.01.010
Goebel M, Hobbie SE, Bulaj B et al (2010) Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure. Ecol Monogr 81:89–102. doi:10.1890/09-2390.1
Goodenough AE, Hart AG, Stafford R (2012) Regression with empirical variable selection: description of a new method and application to ecological datasets. PLoS ONE 7:e34338. doi:10.1371/journal.pone.0034338
Hobbie SE, Reich PB, Oleksyn J et al (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297
Hobbie SE, Ogdahl M, Chorover J et al (2007) Tree species effects on soil organic matter dynamics: the role of soil cation composition. Ecosystems 10:999–1018. doi:10.1007/s10021-007-9073-4
Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513. doi:10.1007/s00442-009-1479-6
Iverson LR, Prasad AM, Matthews SN, Peters M (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios. For Ecol Manag 254:390–406. doi:10.1016/j.foreco.2007.07.023
Keiblinger KM, Hall EK, Wanek W et al (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440. doi:10.1111/j.1574-6941.2010.00912.x
Koranda M, Kaiser C, Fuchslueger L et al (2014) Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability. FEMS Microbiol Ecol 87:142–152. doi:10.1111/1574-6941.12214
Leckie SE (2005) Methods of microbial community profiling and their application to forest soils. For Ecol Manag 220:88–106. doi:10.1016/j.foreco.2005.08.007
Lovett GM, Canham CD, Arthur MA et al (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405
Lumley T (2009) Leaps: regression subset selection. R package version 2.9. http://CRAN.R-project.org/package=leaps
Lützow MV, Kögel-Knabner I, Ekschmitt K et al (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445. doi:10.1111/j.1365-2389.2006.00809.x
Manzoni S, Taylor P, Richter A et al (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91. doi:10.1111/j.1469-8137.2012.04225.x
Mueller KE, Eissenstat DM, Hobbie SE et al (2012) Tree species effects on coupled cycles of carbon, nitrogen, and acidity in mineral soils at a common garden experiment. Biogeochemistry 111:601–614. doi:10.1007/s10533-011-9695-7
Osler GHR, Sommerkorn M (2007) Toward a complete soil C and N cycle: incorporating the soil fauna. Ecology 88:1611–1621. doi:10.1890/06-1357.1
Paquette A, Messier C (2009) The role of plantations in managing the world’s forests in the Anthropocene. Front Ecol Environ 8:27–34. doi:10.1890/080116
Plaza C, Courtier-Murias D, Fernández JM et al (2013) Physical, chemical, and biochemical mechanisms of soil organic matter stabilization under conservation tillage systems: a central role for microbes and microbial by-products in C sequestration. Soil Biol Biochem 57:124–134. doi:10.1016/j.soilbio.2012.07.026
Prescott CE (2005) Do rates of litter decomposition tell us anything we really need to know? For Ecol Manag 220:66–74. doi:10.1016/j.foreco.2005.08.005
Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149. doi:10.1007/s10533-010-9439-0
Prescott CE, Vesterdal L (2013) Tree species effects on soils in temperate and boreal forests: Emerging themes and research needs. For Ecol Manag 309:1–3. doi:10.1016/j.foreco.2013.06.042
Rasse DP, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. doi:10.1007/s11104-004-0907-y
Reich PB, Oleksyn J, Modrzynski J et al (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818. doi:10.1111/j.1461-0248.2005.00779.x
Rubino M, Lubritto C, D’Onofrio A et al (2007) An isotopic method for testing the influence of leaf litter quality on carbon fluxes during decomposition. Oecologia 154:155–166. doi:10.1007/s00442-007-0815-y
Rubino M, Dungait JAJ, Evershed RP et al (2010) Carbon input belowground is the major C flux contributing to leaf litter mass loss: Evidences from a 13C labelled-leaf litter experiment. Soil Biol Biochem 42:1009–1016. doi:10.1016/j.soilbio.2010.02.018
Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. doi:10.1038/nature10386
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. doi:10.2136/sssaj2004.0347
Skorupski M (2010) Influence of selected tree species on forest ecosystem biodiversity for the example of Mesostigmata mites in a common-garden experiment. Rozprawy Naukowe 408. Wydawnictwo Uniwersytetu Przyrodniczego w Poznaniu, pp. 1–106
Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. doi:10.1016/j.soilbio.2010.05.007
Trocha LK, Kałucka I, Stasińska M et al (2012) Ectomycorrhizal fungal communities of native and non-native Pinus and Quercus species in a common garden of 35-year-old trees. Mycorrhiza 22:121–134. doi:10.1007/s00572-011-0387-x
Vesterdal L, Schmidt IK, Callesen I et al (2008) Carbon and nitrogen in forest floor and mineral soil under six common European tree species. For Ecol Manag 255:35–48. doi:10.1016/j.foreco.2007.08.015
Vesterdal L, Clarke N, Sigurdsson BD, Gundersen P (2013) Do tree species influence soil carbon stocks in temperate and boreal forests? For Ecol Manag 309:4–18. doi:10.1016/j.foreco.2013.01.017
Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875
Wilcox C, Domínguez J, Parmelee R, McCartney D (2002) Soil carbon and nitrogen dynamics in Lumbricus terrestris. L. middens in four arable, a pasture, and a forest ecosystems. Biol Fertil Soils 36:26–34. doi:10.1007/s00374-002-0497-x
Withington JM, Reich PB, Oleksyn J, Eissenstat DM (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–397
Acknowledgments
We acknowledge support from the U.S. National Science Foundation (NSF; DEB-0816935, DEB-0128958, OISE-0754731) and the State Committee for Scientific Research (in Poland; PBZ-KBN 087/P04/2003).
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Mueller, K.E., Hobbie, S.E., Chorover, J. et al. Effects of litter traits, soil biota, and soil chemistry on soil carbon stocks at a common garden with 14 tree species. Biogeochemistry 123, 313–327 (2015). https://doi.org/10.1007/s10533-015-0083-6
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DOI: https://doi.org/10.1007/s10533-015-0083-6