Abstract
Aims
Litter decomposition is a complex process closely linked to terrestrial ecosystem dynamics. We examined how forest succession from Scots pine (Pinus sylvestris L.) to Pyrenean oak (Quercus pyrenaica Willd.) driven by global-change may influence litter decomposition in a Mediterranean ecotone forest.
Methods
We performed a reciprocal experiment using litterbags in pure Scots pine and Pyrenean oak forests to assess the litter decomposition process of pine (needles), oak (leaves) and a 1:1 mixture of needles and leaves over a two-year period.
Results
Home-field advantage was only found in the oak leaves, while needle decomposition rates were similar in both forests. There were synergistic effects of mixing litter that mainly increased the decomposition of needle litter. The litter mixing and the forest environment gained influence as drivers of litter decomposition over time by shaping the functional assembly of microbial communities and determining decomposition conditions. We found a staggered functional adjustment of the microbial community assembly driven by the litter type at early stages, followed by the convergence of colonizing microbial communities towards soil microbes and soil organic matter characteristics.
Conclusions
There were specific interlinks between the litter identity and stoichiometry, the aboveground phyllosphere communities and the forest environment (through soil microclimate and soil microbial communities) affecting the cycling of C and N. These ecological feedbacks are of special interest under the current changes in climate and forestry management that may foster the secondary succession of the forest.
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Data availability
Primary data of this study is openly available on Figshare: https://doi.org/10.6084/m9.figshare.19130213.v1 (Fernández-Alonso et al. 2022).
References
Álvarez S, Ortiz C, Díaz-Pinés E, Rubio A (2014) Influence of tree species composition, thinning intensity and climate change on carbon sequestration in Mediterranean mountain forests: a case study using the CO2Fix model. Mitig Adapt Strateg Glob Chang. https://doi.org/10.1007/s11027-014-9565-4
Aneja MK, Sharma S, Fleischmann F et al (2006) Microbial colonization of beech and spruce litter - influence of decomposition site and plant litter species on the diversity of microbial community. Microb Ecol 52:127–135. https://doi.org/10.1007/s00248-006-9006-3
Austin AT, Méndez MS, Ballaré CL (2016) Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems. Proc Natl Acad Sci 113:4392–4397. https://doi.org/10.1073/pnas.1516157113
Austin AT, Vivanco L (2006) Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature 442:555–558. https://doi.org/10.1038/nature05038
Austin AT, Vivanco L, González-Arzac A, Pérez LI (2014) There’s no place like home? An exploration of the mechanisms behind plant litter-decomposer affinity in terrestrial ecosystems. New Phytol 204:307–314. https://doi.org/10.1111/nph.12959
Ayres E, Steltzer H, Simmons BL et al (2009) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem 41:606–610. https://doi.org/10.1016/j.soilbio.2008.12.022
Bach EM, Baer SG, Meyer CK, Six J (2010) Soil texture affects soil microbial and structural recovery during grassland restoration. Soil Biol Biochem 42:2182–2191. https://doi.org/10.1016/j.soilbio.2010.08.014
Barba J, Lloret F, CurielYuste J (2015) Effects of drought-induced forest die-off on litter decomposition. Plant Soil 402:1–11. https://doi.org/10.1007/s11104-015-2762-4
Bärlocher F (2005) Leaching. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: A practical guide. Springer, The Netherlands, pp 33–36
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67. https://doi.org/10.18637/jss.v067.i01
Bélanger N, Collin A, Ricard-Piché J et al (2019) Microsite conditions influence leaf litter decomposition in sugar maple bioclimatic domain of Quebec. Biogeochemistry 145:107–126. https://doi.org/10.1007/s10533-019-00594-1
Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manage 133:13–22. https://doi.org/10.1016/S0378-1127(99)00294-7
Berger TW, Berger P (2012) Greater accumulation of litter in spruce (Picea abies) compared to beech (Fagus sylvatica) stands is not a consequence of the inherent recalcitrance of needles. Plant Soil 358:349–369. https://doi.org/10.1007/s11104-012-1165-z
Berger TW, Berger P (2014) Does mixing of beech (Fagus sylvatica) and spruce (Picea abies) litter hasten decomposition? Plant Soil 377:217–234. https://doi.org/10.1007/s11104-013-2001-9
Bonanomi G, Incerti G, Antignani V et al (2010) Decomposition and nutrient dynamics in mixed litter of Mediterranean species. Plant Soil 331:481–496. https://doi.org/10.1007/s11104-009-0269-6
Bradford MA, Berg B, Maynard DS et al (2016) Understanding the dominant controls on litter decomposition. J Ecol 104:229–238. https://doi.org/10.1111/1365-2745.12507
Brandford M, Tordoff G, Eggers T et al (2002) Microbiota, fauna, and mesh size interations in litter decomposition. Oikos 99:317–323
Breshears DD, Nyhan JW, Heil CE, Wilcox BP (1998) Effects of woody plants on microclimate in a semiarid woodland: soil temperature and evaporation in canopy and intercanopy patches. Int J Plant Sci 159:1010–1017. https://doi.org/10.1086/314083
Canellas I, Montero González G, Martínez García F (2000) Silviculture and dynamics of Pinus sylvestris L. stands in Spain. Investig Agrar Sist y Recur for 9:233–254
Cleveland CC, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252. https://doi.org/10.1007/s10533-007-9132-0
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. https://doi.org/10.1111/j.1461-0248.2008.01219.x
Creamer CA, de Menezes AB, Krull ES et al (2015) Microbial community structure mediates response of soil C decomposition to litter addition and warming. Soil Biol Biochem 80:175–188. https://doi.org/10.1016/j.soilbio.2014.10.008
CurielYuste J, Janssens IA, Carrara A, Ceulemans R (2004) Annual Q10 of soil respiration reflects plant phenological patterns as well as temperature sensitivity. Glob Chang Biol 10:161–169. https://doi.org/10.1111/j.1529-8817.2003.00727.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
de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:1–16. https://doi.org/10.3389/fmicb.2013.00265
DeGrood SH, Claassen VP, Scow KM (2005) Microbial community composition on native and drastically disturbed serpentine soils. Soil Biol Biochem 37:1427–1435. https://doi.org/10.1016/j.soilbio.2004.12.013
Díaz-Pinés E, Rubio A, Van Miegroet H et al (2011) Does tree species composition control soil organic carbon pools in Mediterranean mountain forests? For Ecol Manage 262:1895–1904. https://doi.org/10.1016/j.foreco.2011.02.004
Díaz-Pinés E, Schindlbacher A, Godino M et al (2014) Effects of tree species composition on the CO2 and N2O efflux of a Mediterranean mountain forest soil. Plant Soil 384:243–257. https://doi.org/10.1007/s11104-014-2200-z
Fanin N, Lin D, Freschet GT et al (2021) Home-field advantage of litter decomposition: from the phyllosphere to the soil. New Phytol 231:1353–1358. https://doi.org/10.1111/nph.17475
Fernández-Alonso MJ, CurielYuste J, Kitzler B et al (2018a) Changes in litter chemistry associated with global change-driven forest succession resulted in time-decoupled responses of soil carbon and nitrogen cycles. Soil Biol Biochem 120:200–211. https://doi.org/10.1016/j.soilbio.2018.02.013
Fernández-Alonso MJ, Díaz-Pinés E, Ortiz C, Rubio A (2018b) Disentangling the effects of tree species and microclimate on heterotrophic and autotrophic soil respiration in a Mediterranean ecotone forest. For Ecol Manage 430:533–544. https://doi.org/10.1016/j.foreco.2018.08.046
Fernández-Alonso MJ, Díaz-Pinés E, Rubio A (2021) Drivers of soil respiration in response to nitrogen addition in a Mediterranean mountain forest. Biogeochemistry. https://doi.org/10.1007/s10533-021-00827-2
Fernández-Alonso MJ, Díaz-Pinés E, Kitzler B, Rubio A (2022) Data for: tree species composition shapes the assembly of microbial decomposer communities during litter decomposition. Figshare. https://doi.org/10.6084/m9.figshare.19130213.v1
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. https://doi.org/10.1890/05-1839
Fierer N, Strickland MS, Liptzin D et al (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249. https://doi.org/10.1111/j.1461-0248.2009.01360.x
Freschet GT, Aerts R, Cornelissen JHC (2012) Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis. J Ecol 100:619–630. https://doi.org/10.1111/j.1365-2745.2011.01943.x
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65. https://doi.org/10.1007/BF00384433
Frostegård Å, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163. https://doi.org/10.1016/0167-7012(91)90018-L
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246. https://doi.org/10.1111/j.0030-1299.2004.12738.x
Gliksman D, Rey A, Seligmann R et al (2017) Biotic degradation at night, abiotic degradation at day: positive feedbacks on litter decomposition in drylands. Glob Chang Biol 23:1564–1574. https://doi.org/10.1111/gcb.13465
IUSS Working Group WRB (2015) World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. FAO, Rome
Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett 17:680–690. https://doi.org/10.1111/ele.12269
Keiser AD, Strickland MS, Fierer N, Bradford MA (2011) The effect of resource history on the functioning of soil microbial communities is maintained across time. Biogeosciences 8:1477–1486. https://doi.org/10.5194/bg-8-1477-2011
Koranda M, Kaiser C, Fuchslueger L et al (2013) Seasonal variation in functional properties of microbial communities in beech forest soil. Soil Biol Biochem 60:95–104. https://doi.org/10.1016/j.soilbio.2013.01.025
Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Lenth RV (2016) Least-Squares Means: The R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
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. https://doi.org/10.1111/j.1469-8137.2012.04225.x
Mooshammer M, Wanek W, Hämmerle I et al (2014) Adjustment of microbial nitrogen use efficiency to carbon: Nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:1–7. https://doi.org/10.1038/ncomms4694
Morales-Molino C, Colombaroli D, Valbuena-Carabaña M et al (2017) Land-use history as a major driver for long-term forest dynamics during the last millennia in the Sierra de Guadarrama National Park (central Spain) and implications for forest conservation and management. Glob Planet Change. https://doi.org/10.1016/j.gloplacha.2017.02.012
Moreno-Fernández D, Hernández L, Sánchez-González M et al (2016) Space-time modeling of changes in the abundance and distribution of tree species. For Ecol Manage 372:206–216. https://doi.org/10.1016/j.foreco.2016.04.024
Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331. https://doi.org/10.2307/1932179
Ortiz C, Fernández-Alonso MJ, Kitzler B et al (2022) Variations in soil aggregation, microbial community structure and soil organic matter cycling associated to long-term afforestation and woody encroachment in a Mediterranean alpine ecotone. Geoderma 405:115450. https://doi.org/10.1016/j.geoderma.2021.115450
Osono T, Azuma J, Hirose D (2014) Plant species effect on the decomposition and chemical changes of leaf litter in grassland and pine and oak forest soils. Plant Soil 376:411–421. https://doi.org/10.1007/s11104-013-1993-5
Osono T, Takeda H (2004) Accumulation and release of nitrogen and phosphorus in relation to lignin decomposition in leaf litter of 14 tree species. Ecol Res 19:593–602
Osono T, Takeda H (2005) Decomposition of organic chemical components in relation to nitrogen dynamics in leaf litter of 14 tree species in a cool temperate forest. Ecol Res 20:41–49. https://doi.org/10.1007/s11284-004-0002-0
Pei G, Liu J, Peng B et al (2019) Nitrogen, lignin, C/N as important regulators of gross nitrogen release and immobilization during litter decomposition in a temperate forest ecosystem. For Ecol Manage 440:61–69. https://doi.org/10.1016/j.foreco.2019.03.001
Porre RJ, van der Werf W, De Deyn GB et al (2020) Is litter decomposition enhanced in species mixtures? A Meta-Analysis Soil Biol Biochem 145:107791. https://doi.org/10.1016/j.soilbio.2020.107791
Potthoff M, Steenwerth KL, Jackson LE et al (2006) Soil microbial community composition as affected by restoration practices in California grassland. Soil Biol Biochem 38:1851–1860. https://doi.org/10.1016/j.soilbio.2005.12.009
Prescott CE (2002) The influence of the forest canopy on nutrient cycling. Tree Physiol 22:1193–1200. https://doi.org/10.1093/treephys/22.15-16.1193
Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: Current knowledge and research needs. For Ecol Manage 309:19–27. https://doi.org/10.1016/j.foreco.2013.02.034
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Salomón R, Rodríguez-Calcerrada J, Zafra E et al (2016) Unearthing the roots of degradation of Quercus pyrenaica coppices: A root-to-shoot imbalance caused by historical management? For Ecol Manage 363:200–211. https://doi.org/10.1016/j.foreco.2015.12.040
Sánchez Palomares O, Roig S, Del Río M, et al (2008) Las estaciones ecológicas actuales y potenciales de los rebollares españoles. Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria. Ministerio de Ciencia e Innovación. Monografías INIA: Serie Forestal, No17
Schindlbacher A, Rodler A, Kuffner M et al (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425. https://doi.org/10.1016/j.soilbio.2011.03.005
Sheffer E, Canham CD, Kigel J, Perevolotsky A (2015) Countervailing effects on pine and oak leaf litter decomposition in human-altered Mediterranean ecosystems. Oecologia 177:1039–1051. https://doi.org/10.1007/s00442-015-3228-3
Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Veen GFC, Freschet GT, Ordonez A, Wardle DA (2015) Litter quality and environmental controls of home-field advantage effects on litter decomposition. Oikos 124:187–195. https://doi.org/10.1111/oik.01374
Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J Ecol 96:727–736. https://doi.org/10.1111/j.1365-2745.2008.01393.x
Waitz Y, Sheffer E (2021) Dynamics of mixed pine–oak forests. In: Ne’eman G, Osem Y (eds) Pines and their mixed forest ecosystems in the Mediterranean Basin. Springer, pp 345–362
Wang H, Boutton TW, Xu W et al (2015) Quality of fresh organic matter affects priming of soil organic matter and substrate utilization patterns of microbes. Sci Rep 5:10102. https://doi.org/10.1038/srep10102
Weedon JT, Cornwell WK, Cornelissen JHC et al (2009) Global meta-analysis of wood decomposition rates: a role for trait variation among tree species? Ecol Lett 12:45–56. https://doi.org/10.1111/j.1461-0248.2008.01259.x
Wei T, Simko V (2021) R package “corrplot”: Visualization of a Correlation Matrix (Version 0.92)
Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York
Wu F, Yang W, Zhang J, Deng R (2010) Litter decomposition in two subalpine forests during the freeze–thaw season. Acta Oecologica 36:135–140. https://doi.org/10.1016/j.actao.2009.11.002
Yuan Z, Gazol A, Wang X et al (2012) What happens below the canopy? Direct and indirect influences of the dominant species on forest vertical layers. Oikos 121:1145–1153. https://doi.org/10.1111/j.1600-0706.2011.19757.x
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M et al (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155. https://doi.org/10.1890/14-0777.1
Zhou S, Butenschoen O, Barantal S et al (2020) Decomposition of leaf litter mixtures across biomes: The role of litter identity, diversity and soil fauna. J Ecol 108:2283–2297. https://doi.org/10.1111/1365-2745.13452
Acknowledgements
We thank to Marta Rivas for her assistance in fieldwork, sample processing and laboratory analysis and Clara López Santuré for helping in the initial data exploration of PLFA biomarkers. We also acknowledge to the staff and facilities of the Austrian Research Centre for Forests where PLFA analysis were carried out and the Organismo Autónomo de Parques Nacionales for the permission to work in the study area.
Funding
This research received financial support from the REMEDINAL-TE-CM Project (S2018-4338) of the Madrid Regional Government and the FORADMIT project (AGL2016-77863-R) of the Spanish Government. M.J. Fernández-Alonso was supported by a Short Term Scientific Mission grant from the COST Action FP 1206 EuMiXFOR of the EU Framework Programme Horizon 2020, and by the project UNDERCLIME (POCI-01–0145-FEDER-030231 | PTDC/BIA-ECO/30231/2017) co-financed by the Portuguese Foundation for Science and Technology (FCT) and the European Regional Development Fund.
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A. Rubio, B. Kitzler and M.J. Fernández-Alonso acquired the funds. M.J. Fernández-Alonso and A. Rubio conceptualized and designed the experiment. M.J. Fernández-Alonso performed the material preparation, data collection and analysis. M.J. Fernández-Alonso wrote the first draft of the manuscript and all authors reviewed and edited the manuscript. All authors approved the final manuscript.
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Fernández-Alonso, M.J., Díaz-Pinés, E., Kitzler, B. et al. Tree species composition shapes the assembly of microbial decomposer communities during litter decomposition. Plant Soil 480, 457–472 (2022). https://doi.org/10.1007/s11104-022-05593-0
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DOI: https://doi.org/10.1007/s11104-022-05593-0