Abstract
Forests provide essential ecosystem services such as wood production and soil carbon storage, which can be influenced by forest management. Fertilisation and understory removal are common practices set up in managed forests to reduce tree mortality and relieve trees from their main limitations, but their effects on belowground functioning and soil carbon storage are still unclear. In this study, we investigated the effects of phosphorus fertilisation, understory removal and their interaction on the carbon stored in the ecosystem and soil enzyme activities in two contrasting moorlands in south-western France (dry and wet moorlands) planted with maritime pines (Pinus pinaster Ait.). In the wet moorland, we found that fertilisation and understory removal had a positive effect on tree biomass, but they did not affect soil carbon stocks nor carbon-related enzyme activities. In the dry moorland, understory removal had a significant positive effect on tree biomass and a strong negative effect on topsoil organic carbon stocks and carbon-related enzyme activities. Overall, understory removal did not affect total carbon stocks at the ecosystem scale due to compensatory effects between carbon pools, i.e. the increase in carbon stored in the aboveground biomass was cancelled by a decrease in carbon stored in the soil. These results highlight the importance of adapting forest practices depending on the environmental context and carbon sequestration objectives.
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References
Achat DL, Bakker MR, Augusto L et al (2009) Evaluation of the phosphorus status of P-deficient podzols in temperate pine stands: combining isotopic dilution and extraction methods. Biogeochemistry 92:183–200. https://doi.org/10.1007/s10533-008-9283-7
Achat DL, Martel S, Picart D et al (2018) Modelling the nutrient cost of biomass harvesting under different silvicultural and climate scenarios in production forests. For Ecol Manag 429:642–653. https://doi.org/10.1016/j.foreco.2018.06.047
Albaugh TJ, Lee Allen H, Zutter BR, Quicke HE (2003) Vegetation control and fertilization in midrotation Pinus taeda stands in the southeastern United States. Ann for Sci 60:619–624. https://doi.org/10.1051/forest:2003054
Alberti G, Nock C, Fornasier F et al (2017) Tree functional diversity influences belowground ecosystem functioning. Appl Soil Ecol 120:160–168. https://doi.org/10.1016/j.apsoil.2017.07.038
Augusto L, Boča A (2022) Tree functional traits, forest biomass, and tree species diversity interact with site properties to drive forest soil carbon. Nat Commun 13:1–12. https://doi.org/10.1038/s41467-022-28748-0
Augusto L, Crampon N, Saur E et al (2005) High rates of nitrogen fixation of Ulex species in the understory of maritime pine stands and the potential effect of phosphorus fertilization. Can J for Res 35:1183–1192. https://doi.org/10.1139/X05-054
Augusto L, Bakker MR, Morel C et al (2010) Is “grey literature” a reliable source of data to characterize soils at the scale of a region? A case study in a maritime pine forest in southwestern France. Eur J Soil Sci 61:807–822. https://doi.org/10.1111/j.1365-2389.2010.01286.x
Augusto L, Achat DL, Bakker MR et al (2015) Biomass and nutrients in tree root systems–sustainable harvesting of an intensively managed Pinus pinaster (Ait.) planted forest. GCB Bioenergy 7(2):231–243. https://doi.org/10.1111/gcbb.12127
Augusto L, Achat DL, Jonard M et al (2017) Soil parent material—A major driver of plant nutrient limitations in terrestrial ecosystems. Glob Chang Biol 23:3808–3824. https://doi.org/10.1111/gcb.13691
Balandier P, Collet C, Miller JH et al (2006) Designing forest vegetation management strategies based on the mechanisms and dynamics of crop tree competition by neighbouring vegetation. Forestry 79:3–27. https://doi.org/10.1093/forestry/cpi056
Bell CW, Fricks BE, Rocca JD et al (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J vis Exp 81:1–16. https://doi.org/10.3791/50961
Bert D, Danjon F (2006) Carbon concentration variations in the roots, stem and crown of mature Pinus pinaster (Ait.). For Ecol Manag 222:279–295. https://doi.org/10.1016/j.foreco.2005.10.030
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. https://doi.org/10.1126/science.1155121
Burns RG, DeForest JL, Marxsen J et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Carlson CA, Fox TR, Lee Allen H, Albaugh TJ (2008) Modeling mid-rotation fertilizer responses using the age-shift approach. For Ecol Manag 256:256–262. https://doi.org/10.1016/j.foreco.2008.04.020
Chen Y, Zhang Y, Cao J et al (2019) Stand age and species traits alter the effects of understory removal on litter decomposition and nutrient dynamics in subtropical Eucalyptus plantations. Glob Ecol Conserv 20:e00693. https://doi.org/10.1016/j.gecco.2019.e00693
Clemmensen KE, Finlay RD, Dahlberg A et al (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536. https://doi.org/10.1111/nph.13208
DeForest JL, Moorhead DL (2020) Effects of elevated pH and phosphorus fertilizer on soil C, N and P enzyme stoichiometry in an acidic mixed mesophytic deciduous forest. Soil Biol Biochem 150:107996. https://doi.org/10.1016/j.soilbio.2020.107996
Demounem R (1965) Relations entre les sols, la composition floristique de la lande girondine et la croissance du Pin maritime. Comptes Rendus L’academie Des Sci 261:2513–2516
Demounem R (1967) Influence des variations du niveau de la nappe phréatique et de la pluviosité sur la croissance du pin maritime dans les landes girondines. Comptes Rendus L’academie Des Sci 264:1172–1175
Epron D, Laclau J-P, Almeida JCR et al (2012) Do changes in carbon allocation account for the growth response to potassium and sodium applications in tropical Eucalyptus plantations? Tree Physiol 32:667–679. https://doi.org/10.1093/treephys/tpr107
Fanin N, Moorhead D (2016) Eco-enzymatic stoichiometry and enzymatic vectors reveal differential C, N, P dynamics in decaying litter along a land-use gradient. Biogeochemistry 129:21–36. https://doi.org/10.1007/s10533-016-0217-5
Fanin N, Barantal S, Fromin N et al (2012) Distinct microbial limitations in litter and underlying soil revealed by carbon and nutrient fertilization in a tropical rainforest. PLoS One 7. https://doi.org/10.1371/journal.pone.0049990
Fanin N, Moorhead D, Bertrand I (2016) Eco-enzymatic stoichiometry and enzymatic vectors reveal differential C, N, P dynamics in decaying litter along a land-use gradient. Biogeochemistry 129:21–36. https://doi.org/10.1007/s10533-016-0217-5
Fanin N, Clemmensen KE, Lindahl BD et al (2022a) Ericoid shrubs shape fungal communities and suppress organic matter decomposition in boreal forests. New Phytol. https://doi.org/10.1111/nph.18353
Fanin N, Mooshammer M, Sauvadet M et al (2022b) Soil enzymes in response to climate warming: Mechanisms and feedbacks. Funct Ecol. https://doi.org/10.1111/1365-2435.14027
Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176. https://doi.org/10.1016/S0038-0717(02)00251-1
Fox TR, Comerford NB (1992) Rhizosphere phosphatase activity and phosphatase hydrolyzable organic phosphorus in two forested spodosols. Soil Biol Biochem 24:579–583
Ganjegunte GK, Condron LM, Clinton PW, Davis MR (2005) Effects of mixing radiata pine needles and understory litters on decomposition and nutrients release. Biol Fertil Soils 41:310–319. https://doi.org/10.1007/s00374-005-0851-x
Gaudio N, Balandier P, Dumas Y, Ginisty C (2011) Growth and morphology of three forest understorey species (Calluna vulgaris, Molinia caerulea and Pteridium aquilinum) according to light availability. For Ecol Manag 261:489–498. https://doi.org/10.1016/j.foreco.2010.10.034
Gholz HL, Ewel KC, Teskey RO (1990) Water and forest productivity. For Ecol Manag 30:1–18. https://doi.org/10.1016/0378-1127(90)90122-R
Gonzalez M, Augusto L, Gallet-budynek A et al (2013) Contribution of understory species to total ecosystem aboveground and belowground biomass in temperate Pinus pinaster (Ait.) forests. For Ecol Manag 289:38–47. https://doi.org/10.1016/j.foreco.2012.10.026
Grau-Andrés R, Wardle DA, Gundale MJ et al (2020) Effects of plant functional group removal on CO2 fluxes and belowground C stocks across contrasting ecosystems. Ecology 101:1–12. https://doi.org/10.1002/ecy.3170
Guada G, Camarero JJ, Sánchez-Salguero R, Cerrillo RMN (2016) Limited growth recovery after drought-induced forest dieback in very defoliated trees of two pine species. Front Plant Sci 7:1–12. https://doi.org/10.3389/fpls.2016.00418
Güsewell S, Gessner MO (2009) N: P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219. https://doi.org/10.1111/j.1365-2435.2008.01478.x
Hartmann H, Moura CF, Anderegg WRL et al (2018) Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol 218:15–28. https://doi.org/10.1111/nph.15048
He X, Augusto L, Goll DS et al (2021) Global patterns and drivers of soil total phosphorus concentration. Earth Syst Sci Data 13:5831–5846. https://doi.org/10.5194/essd-13-5831-2021
Hoorens B, Aerts R, Stroetenga M (2003) Is there a trade-off between the plant’s growth response to elevated CO2 and subsequent litter decomposability? Oikos 103:17–30. https://doi.org/10.1034/j.1600-0706.2003.12276.x
Hou E, Wen D, Jiang L et al (2021) Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol Lett 24:1420–1431. https://doi.org/10.1111/ele.13761
Huys R, Poirier V, Bourget MY et al (2022) Plant litter chemistry controls coarse-textured soil carbon dynamics. J Ecol. https://doi.org/10.1111/1365-2745.13997
Jastrow JD, Amonette JE, Bailey VL (2007) Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Clim Change 80:5–23. https://doi.org/10.1007/s10584-006-9178-3
Jolivet C, Augusto L, Trichet P, Arrouays D (2007) Les sols du massif forestier des landes de gascogne: formation, histoire, propriétŕs et variabilité spatiale. Rev for Fr 59:7–30. https://doi.org/10.4267/2042/8480
Krieger D (2001) Economic value of forest ecosystem services : a review
Lei L, Xiao W, Zeng L et al (2021) Effects of thinning intensity and understory removal on soil microbial community in Pinus massoniana plantations of subtropical China. Appl Soil Ecol 167:104055. https://doi.org/10.1016/j.apsoil.2021.104055
Lemoine B (1991) Growth and yield of maritime pine (Pinus pinaster Ait): the average dominant tree of the stand. Ann for Sci 48:593–611. https://doi.org/10.1051/forest:19910508
Lewis NB, Harding JH (1963) Soil factors in relation to pine growth in South Australia. Aust for 27:27–34. https://doi.org/10.1080/00049158.1963.10675927
Liu Q, Wang F, Liu R et al (2022) Aboveground litter input alters the effects of understory vegetation removal on soil microbial communities and enzyme activities along a 60-cm profile in a subtropical plantation forest. Appl Soil Ecol 176:104489. https://doi.org/10.1016/j.apsoil.2022.104489
Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Enzyme properties down the soil profile-a matter of substrate quality in rhizosphere and detritusphere. Soil Biol Biochem 103:274–283. https://doi.org/10.1016/j.soilbio.2016.08.023
Ma S, He F, Tian D et al (2018) Variations and determinants of carbon content in plants: a global synthesis. Biogeosciences 15(3):693–702
Matala J, Kellomáki S, Nuutinen T (2008) Litterfall in relation to volume growth of trees: analysis based on literature. Scand J for Res 23:194–202. https://doi.org/10.1080/02827580802036176
Matejovic I (1997) Communications in soil science and plant analysis determination of carbon and nitrogen in samples of various soils by the dry combustion determination of carbon and nitrogen in samples of various soils by the dry combustion. Commun Soil Sci Plantanal 28:1499–1511
Maxwell TL, Augusto L, Bon L et al (2020) Effect of a tree mixture and water availability on soil nutrients and extracellular enzyme activities along the soil profile in an experimental forest. Soil Biol Biochem 148:107864. https://doi.org/10.1016/j.soilbio.2020.107864
Mendes MP, Ribeiro L, David TS, Costa A (2016) How dependent are cork oak (Quercus suber L.) woodlands on groundwater? A case study in southwestern Portugal. For Ecol Manag 378:122–130. https://doi.org/10.1016/j.foreco.2016.07.024
Miller GR (1979) Quantity and quality of the annual production of shoots and flowers by calluna vulgaris in north-east scotland. J Ecol 67:109. https://doi.org/10.2307/2259340
Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19. https://doi.org/10.1007/s00374-017-1245-6
Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front Ecol Environ 3:421–428. https://doi.org/10.1890/1540-9295(2005)003[0421:UVAAFE]2.0.CO;2
Nohrstedt HÖ (2001) Response of coniferous forest ecosystems on mineral soils to nutrient additions: a review of Swedish experiences. Scand J for Res 16:555–573. https://doi.org/10.1080/02827580152699385
Osburn ED, Elliottt KJ, Knoepp JD et al (2018) Soil microbial response to Rhododendron understory removal in southern Appalachian forests: effects on extracellular enzymes. Soil Biol Biochem 127:50–59. https://doi.org/10.1016/j.soilbio.2018.09.008
Pan Y, Birdsey RA, Fang J 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
Riegel GM, Miller RF, Krueger WC (1992) Competition for resources between understory vegetation and overstory pinus ponderosa in northeastern oregon. Ecol Appl 2:71–85
Schlesinger WH, Dietze MC, Jackson RB et al (2016) Forest biogeochemistry in response to drought. Glob Chang Biol 22:2318–2328. https://doi.org/10.1111/gcb.13105
Shaiek O, Loustau D, Trichet P et al (2011) Generalized biomass equations for the main aboveground biomass components of maritime pine across contrasting environments. Ann for Sci 68:443–452. https://doi.org/10.1007/s13595-011-0044-8
Soong JL, Marañon-jimenez S, Cotrufo MF et al (2018) Soil microbial CNP and respiration responses to organic matter and nutrient additions: evidence from a tropical soil incubation. Soil Biol Biochem 122:141–149. https://doi.org/10.1016/j.soilbio.2018.04.011
South DB, Miller JH, Kimberley MO, Vanderschaaf CL (2006) Determining productivity gains from herbaceous vegetation management with “age-shift” calculations. Forestry 79:43–56. https://doi.org/10.1093/forestry/cpi058
Trichet P, Jolivet C, Arrouays D et al (1999) Le maintien de la fertilité des sols forestiers landais dans le cadre de la sylviculture intensive du pin maritime. Etude Gest Des Sols 6:20–21
Trichet P, Loustau D, Lambrot C, Linder S (2008) Manipulating nutrient and water availability in a maritime pine plantation: effects on growth, production, and biomass allocation at canopy closure. Ann for Sci 65:814–814. https://doi.org/10.1051/forest:2008060
Trichet P, Bakker MR, Augusto L et al (2009) Fifty years of fertilization experiments on Pinus pinaster in southwest France: the importance of phosphorus as a fertilizer. For Sci 55:390–402
Vanguelova EI, Bonifacio E, De Vos B et al (2016) Sources of errors and uncertainties in the assessment of forest soil carbon stocks at different scales—review and recommendations. Environ Monit Assess. https://doi.org/10.1007/s10661-016-5608-5
Vidal DF, Trichet P, Puzos L et al (2019) Intercropping N-fixing shrubs in pine plantation forestry as an ecologically sustainable management option. For Ecol Manag 437:175–187. https://doi.org/10.1016/j.foreco.2019.01.023
Vidal DF, Augusto L, Bakker MR et al (2021) Understorey-overstorey biotic and nutrient interactions are key factors for Pinus pinaster growth and development under oligotrophic conditions. Scand J for Res 36:563–574. https://doi.org/10.1080/02827581.2021.1992002
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15. https://doi.org/10.1890/08-0127.1
Wang F, Zou B, Li H, Li Z (2014) The effect of understory removal on microclimate and soil properties in two subtropical lumber plantations. J for Res 19:238–243. https://doi.org/10.1007/s10310-013-0395-0
Waring BG, Pérez-Aviles D, Murray JG, Powers JS (2019) Plant community responses to stand-level nutrient fertilization in a secondary tropical dry forest. Ecology 100:1–12. https://doi.org/10.1002/ecy.2691
Wendt JW, Hauser S (2013) An equivalent soil mass procedure for monitoring soil organic carbon in multiple soil layers. Eur J Soil Sci 58–65. https://doi.org/10.1111/ejss.12002
Yang Y, Zhang X, Zhang C et al (2018) Understory vegetation plays the key role in sustaining soil microbial biomass and extracellular enzyme activities. Biogeosciences 15:4481–4494. https://doi.org/10.5194/bg-15-4481-2018
Yang Y, Zhang X, Wang H et al (2019) How understory vegetation affects the catalytic properties of soil extracellular hydrolases in a Chinese fir (Cunninghamia lanceolata) forest. Eur J Soil Biol 90:15–21. https://doi.org/10.1016/j.ejsobi.2018.11.004
Acknowledgements
We thank J. Hochet, C. Gire and T. L. Maxwell for their help in the field and the laboratory. We thank the Forest Experimental Facility of Pierroton (UEFP) and the “Centre de Productivité et d’Action Forestière d’Aquitaine” (CPFA) for maintenance of the different experimental sites.
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This work was supported by the Region Nouvelle Aquitaine (AAPR2020A-2019–8472310) to NF, the ECODIV department at the “Institut national de la recherche en agriculture, alimentation, et environnement” (INRAE) and the “Agence de l'environnement et de la maîtrise de l'énergie” (ADEME) to LB, and finally by the project AGROECOFOR funded by the LabEX COTE to PT.
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LB, LA, and NF contributed to conceptualization; LB, JG, MRB, CL, and SM contributed to methodology; LB, LA, MRB, and NF performed formal analysis and investigation; LB contributed to writing—original draft preparation; all authors contributed to writing—review and editing; LB, PT, and NF performed funding acquisition; LA, MRB, and NF contributed to resources and supervision.
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Bon, L., Augusto, L., Gaudry, J. et al. Effects of fertilisation and understory removal on aboveground and belowground carbon stocks in wet and dry moorlands in south-western France. Eur J Forest Res 142, 723–737 (2023). https://doi.org/10.1007/s10342-023-01551-2
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DOI: https://doi.org/10.1007/s10342-023-01551-2