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Persistent anthropogenic legacies structure depth dependence of regenerating rooting systems and their functions

Abstract

Biotically-mediated weathering helps to shape Earth’s surface. For example, plants expend carbon (C) to mobilize nutrients in forms whose relative abundances vary with depth. It thus is likely that trees’ nutrient acquisition strategies—their investment in rooting systems and exudates—may function differently following disturbance-induced changes in depth of rooting zones and soil nutrient stocks. These changes may persist across centuries. We test the hypothesis that plant C allocation for nutrient acquisition is depth dependent as a function of rooting system development and relative abundances of organic vs. mineral nutrient stocks. We further posit that patterns of belowground C allocation to nutrient acquisition reveal anthropogenic signatures through many decades of forest regeneration. To test this idea, we examined fine root abundances and rooting system C in organic acid exudates and exo-enzymes in tandem with depth distributions of organically- and mineral-bound P stocks. Our design permitted us to estimate C tradeoffs between organic vs. mineral nutrient benefits in paired forests with many similar aboveground traits but different ages: post-agricultural mixed-pine forests and older reference hardwoods. Fine roots were more abundant throughout the upper 2 m in reference forest soils than in regenerating stands. Rooting systems in all forests exhibited depth-dependent C allocations to nutrient acquisition reflecting relative abundances of organic vs. mineral bound P stocks. Further, organic vs. mineral stocks underwent redistribution with historic land use, producing distinct ecosystem nutritional economies. In reference forests, rooting systems are allocating C to relatively deep fine roots and low-C exudation strategies that can increase mobility of mineral-bound P stocks. Regenerating forests exhibit relatively shallower fine root distributions and more diverse exudation strategies reflecting more variable nutrient stocks. We observed these disparities in rooting systems’ depth and nutritional mechanisms even though the regenerating forests have attained aboveground biomass stocks similar to those in reference hardwood forests. These distinctions offer plausible belowground mechanisms for observations of continued C sink strength in relatively old forests, and have implications for soil C fates and soil development on timescales relevant to human lifetimes. As such, depth-dependent nutrient returns on plant C investments represent a subtle but consequential signal of the Anthropocene.

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References

  1. Aber JD, Melillo JM (2001) Terrestrial ecosystems. Academic, Burlington

  2. Adams MA, Pate JS (1992) Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.). Plant Soil 145:107–113

  3. Amrhein V, Greenland S, McShane B (2019) Scientists rise up against statistical significance. Nature 567:305–307

  4. Andrino A, Boy J, Mikutta R, Sauheitl L, Guggengerger G (2019) Carbon investment required for mobilization of inorganic and organic phosphorus bound to goethite by an arbuscular mycorrhiza (Solanum lycopersicum x Rhizophagus irregularis). Front Environ Sci 7:1–15

  5. Aoki M, Fujii K, Kitayama K (2012) Environmental control of root exudation of low-molecular weight organic acids in tropical rainforests. Ecosystems. https://doi.org/10.1007/s10021-012-9575-6

  6. Austin JC, Perry A, Richter DD, Schroeder PA (2018) Modifications of 2:1 clay minerals in a kaolinite dominated ultisol under changing land use regimes. Clay Clay Miner 66:61–73

  7. 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

  8. Band LE, Mcdonnell JJ, Duncan JM, Barros A, Bejan A, Burt T, Dietrich WE, Emanuel R, Hwang T, Katul G, Kim Y, McGlynn B, Miles B, Porporato A, Scaife C, Troch PA (2014) Ecohydrological flow networks in the subsurface. Ecohydrology. https://doi.org/10.1002/eco.1525

  9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

  10. Berner RA (1992) Weathering, plants and the long-term carbon cycle. Geochim Cosmochim Acta 56:3225–3231

  11. Berner RA (2003) The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426:323–326

  12. Billings SA, Hirmas D, Sullivan PL, Lehmeier CA, Bagchi S, Min K, Brecheisen Z, Hauser E, Stair R, Flournoy R, Richter DD (2018) Loss of deep roots limits biogenic agents of soil development that are only partially restored by decades of forest regeneration. Elem Sci Anth 6:34

  13. Bond BJ, Meinzer FC, Brooks JR (2008) How trees influence the hydrological cycle in forest ecosystems. In: Wood PJ, Hannah DM, SadlerJP (eds) Hydroecology and ecohydrology: past, present and future. Wiley, Sussex, pp 7–28.

  14. Brantley SL, Lebedeva M, Hausrath EM (2012) A geobiological view of weathering and erosion. In: Knoll AH, Canfield DE, Konhauser KO (eds) Fundamentals of geobiology. Blackwell, Oxford

  15. Brantley SL, Eissenstat DM, Marshall JA, Godsey SE, Balough-Brunstad A, Karwan DL, Papuga SA, Roering J, Dawson TE, Dvaristo J, Chadwick O, McDonnell JJ, Weathers KC (2017) Reviews and synthesis: on the roles trees play in building and plumbing the critical zone. Biogeosciences. https://doi.org/10.5194/bg-2017-61

  16. Brecheisen ZS, Cook CW, Heine PR, Richter D (2019) Micro-topographic roughness analysis (MTRA) highlights minimally eroded terrain in a landscape severely impacted by historic agriculture. Rem Sens Environ 222:78–89

  17. Bunemann EK, Oberson A, Frossard E (eds) (2011) Phosphorus in action: biological processes in soil phosphorus cycling. Springer, Berlin

  18. Canadell J, Jackson RB, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) Maximum rooting depth of vegetation types at the global scale. Oecologia 108:583–595

  19. Cherkinsky A, Brecheisen ZS, Richter D (2018) Carbon and oxygen isotope composition in soil carbon dioxide within deep ultisols at the Calhoun CZO, South Carolina, USA. Radiocarbon 60:1357–1366

  20. Crews TE, Kitayam K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombolis D, Vitousek PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424

  21. Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

  22. Crow SE, Lajtha K, Filley TR, Swanston CW, Bowden RD, Caldwell BA (2009) Sources of plant-derived carbon and stability of organic matter in soil: Implications for global change. Glob Change Biol 15:2003–2019

  23. D'Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209

  24. Darch T, Blackwell MSA, Chadwick D, Haygarth PM, Hawkins JMB, Turner BL (2016) Assessment of bioavailable organic phosphorus in tropical forest soils by organic acid extraction and phosphatase hydrolysis. Geoderma 284:93–102

  25. DeForest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41:1180–1186

  26. Deluca TH, Glanville HC, Harris M, Emmet BA, Pingree MRA, de Sosa LL, Jone DL (2015) A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–119

  27. Devine S, Markewitz D, Hendrix P, Coleman D (2011) Soil carbon change through 2 m during forest succession alongside a 30-year agroecosystem experiment. For Sci 57:36–50

  28. Drew MC (1975) Comparison of the effect of a localized supply of phosphate, nitrate, ammonium, and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490

  29. Dupouey JL, Dambrine E, Laffite JD, Moares C (2002) Irreversible impacts of past land use on forest soils and biodiversity. Ecology 83:2978–2984

  30. Eaton JM, Lawrence D (2006) Loss of carbon sequestration potential after several decades of shifting cultivation in the Southern Yucatan. For Ecol Manag 258:949–958

  31. Ellis EC (2011) Anthropogenic transformation of the terrestrial biosphere. Philos Trans R Soc 369:1010–1135

  32. Ellsworth DS, Anderson IC, Crous KY, Cooke J, Drake JE, Gherlenda AN, GimenoTE MCA, Medlyn BE, Powell JR, Tjoelker MG, Reich PB (2017) Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat Clim Change 7:279–282

  33. Fan J, McConkey B, Wang H, Janzen H (2016) Root distribution by depth for temperate agricultural crops. Field Crop Res 189:68–74

  34. Fan Y, Miguez-Macho G, Jobbagy EG, Jackson RB, Otero-Casal C (2017) Hydrologic regulation of plant rooting depth. Proc Natl Acad Sci USA 114:10572–10577

  35. Finér L, Messier C, Grandpré LD (1997) Fine-root dynamics in mixed boreal confer-broad-leaved forest stands at different successional stages after fire. Can J For Res 27:304–314

  36. Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Change Biol 21:2082–2094

  37. Ganor J, Reznik IJ, Rosenberg YO (2009) Organics in water-rock interactions. Rev Mineral Geochem 70:259–369

  38. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56

  39. Haff PK (2010) Hillslopes, rivers, plows, and trucks: mass transport on Earth’s surface by natural and technological processes. Earth Surf Process Landf 35:1157–1166

  40. Hasegawa S, MacDonald CA, Power SA (2015) Elevated carbon dioxide increases soil nitrogen and phosphorus availability in a phosphorus-limited Eucalyptus woodland. Glob Change Biol 22:1628–1643

  41. Hasenmueller EA, Gu X, Weitzman JN, Adams TS, Stinchcomb GE, Eissenstat DM, Drohan PJ, Brantley SL, Kaye JP (2017) Weathering of rock to regolith: the activity of deep roots in bedrock fractures. Geoderma 300:11–31

  42. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24

  43. Jackson RB, Manwaring JH, Caldwell MM (1990) Rapid physiological adjustment of roots to localized soil enrichment. Nature 344:58–60

  44. Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA 94:7362–7366

  45. Janzen HH (2006) The soil carbon dilemma: Shall we hoard or use it? Soil Biol Biochem 38:419–424

  46. Jin L, Ramesh R, Ketchum PR, Heany P, White T, Brantley SL (2010) Mineral weathering and elemental transport during hillslope evolution at the Susquehanna/Shale Hills Critical Zone Observatory. Geochim Cosmochim Acta 74:3669–3691

  47. Jipp PH, Nepstad DC, Cassel DK, de Carvalho CR (1998) Deep soil moisture storage and transpiration in forests and pastures of seasonally-dry Amazonia. In: Markham A (eds) Potential impacts of climate change on tropical forest ecosystems. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-2730-3_11

  48. Jobbagy EG, Jackson RB (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51–77

  49. Jobbagy EG, Jackson RB (2004) The uplift of soil nutrients by plants: biogeochemical consequences across scales. Ecology 85:2380–2389

  50. Keiluweit M, Bourgoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Change 5:588–595

  51. Kelly EF, Chadwick OA, Hilinski ET (1998) The effect of plants on mineral weathering. Biogeochemistry 42:21–53

  52. Knops JMH, Bradley KL (2009) Soil carbon and nitrogen accumulation and vertical distribution across a 74-year chronosequence. Soil Sci Soc Am J 73:2096–2104

  53. Kong DL, Wang JJ, Kardol P, Wu HF, Zheng H, Deng XB, Deng Y (2016) Economic strategies of plant absorptive roots vary with root diameter. Biogeosciences 13:415–424

  54. Lambers H, Atkin OK, Millenaar FF (2000) Respiratory patterns in roots in relation to their function. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots. The hidden half, 1st edn. Marcel Dekker, New York, pp 521–552.

  55. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

  56. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breeman T (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254

  57. Lehmeier CA, Min K, Niehues ND, Ballantyne F, Billings SA (2013) Temperature-mediated changes of exoenzyme-substrate reaction rates and their consequences for the carbon to nitrogen flow ratio of liberated resources. Soil Biol Biochem 57:374–382

  58. Liu B, Hongbo L, Zhu B, Koide RT, Eissenstat DM, Guo D (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136

  59. Lucas Y (2001) The role of plants in controlling rates and products of weather: importance of biological pumping. Annu Rev Earth Planet Sci 29:135–163

  60. Lugli L, Andersen KM, Aragao LEOC, Cordiero AL, Cunha HFV, Fuchslueger L, Meir P, Mercado LM, Oblitas E, Quesada CA, Rosa JS, Schaap KJ, Valverde-Barrantes O, Hartley IP (2019) Multiple phosphorus acquisition strategies adopted by fine roots in low-fertility soils in Central Amazonia. Plant Soil. https://doi.org/10.1007/s11104-019-03963-9

  61. Luyssaert S, Schulze ED, Borner A, Knohl A, Hessenmoller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215

  62. Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56

  63. Maeght JL, Rewald B, Pierret A (2013) How to study deep roots and why it matters. Front Plant Sci 4:299

  64. Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentiti R, Grace J (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature. https://doi.org/10.1038/nature05847

  65. Marschner P, Rengel Z (2007) Nutrient cycling in terrestrial ecosystems. Springer, New York

  66. Martin PA, Newton AC, Bullock JM (2013) Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc Roy Soc 280:20132236

  67. Mayer A, Hausfather Z, Jones AD, Silver WL (2018) The potential of agricultural land management to contribute to lower global surface temperatures. Sci Adv 4:eaaq0932

  68. McCormack LM, Iversen CM (2019) Physical and functional constraints on viable belowground acquisition strategies. Front Plant Sci. https://doi.org/10.3389/fpls.2019.01215

  69. McCormak LM, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of belowground contributions to terrestrial biosphere processes. New Phytol 207:505–518

  70. Min K, Lehmeier CA, Ballantyne F, Tatarko A, Billings SA (2014) Differential effects of pH on temperature sensitivity of organic carbon and nitrogen decay. Soil Biol Biochem 76:193–200

  71. Mobley ML, Richter DD, Heine PR (2013) Accumulation and decay of woody detritus in a humid subtropical secondary pine forest. Can J For Res 43:109–118

  72. Mobley ML, Lajtha K, Kramer MG, Bacon AR, Heine PR, Richter DD (2015) Surficial gains and subsoil loses of soil carbon and nitrogen during secondary forest development. Glob Change Biol 21:986–996

  73. Nadelhoffer KJ, Raich JW (1992) Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73:1139–1147

  74. NADP, NOAA, others (2017) CZO dataset: national—air temperature, flux tower, meteorology (2017)—NADP and NOAA or other weather stations. http://criticalzone.org/calhoun/data/dataset/6112/. Accessed 5 Dec 2019

  75. Newmann G (2007) Root exudates and nutrient cycling. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Springer, New York, pp 123–157

  76. Pawlik L (2013) The role of trees in the geomorphic system of forested hillslopes—a review. Earth Sci Rev 126:250–265

  77. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: A new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51

  78. Pierret A, Maeght JL, Clement C, Montoroi JP, Hartman C, Gonkhamdee S (2016) Understanding deep roots and their functions in ecosystems: An advocacy for more unconventional research. Ann Bot 118:621–635

  79. Pregitzer KS (2002) Fine roots of trees—a new perspective. New Phytol 154:267–270

  80. Qiao NA, Schaefer D, Blagodatskaya E, Zou X, Xu X, Kuzyakov Y (2013) Labile carbon retention compensates for CO2 released by priming in forest soils. Glob Change Biol. https://doi.org/10.1111/gcb.12458

  81. Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilization. Plant Soil 269:341–356

  82. Richter DD, Billings SA (2015) ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone. New Phytol 206:900–912

  83. Richter DD, Markewitz D (2001) Understanding soil change: soil sustainability over millennia, centuries, and decades. Cambridge, New York

  84. Richter DD, Markewitz D, Trumbore SE, Wells CG (1999) Rapid accumulation and turnover of soil carbon in a re-establishing forest. Nature 400:56–58

  85. Richter DD, Markewitz D, Heine PR, Jin V, Raikes J, Tian K, Wells CG (2000) Legacies of agriculture and forest regrowth in the nitrogen of old-field soils. For Ecol Manag 138:233–248

  86. Richter DD, Allen HL, Li J, Markewitz D, Raikes J (2006) Bioavailability of slowly cycling soil phosphorus: major restructuring of soil P fractions over four decades in an aggrading forest. Oecologia 150:259–271

  87. Richter DD, Oh NH, Fimmen R, Jackson J (2007) The rhizosphere and soil formation. In: Cardon ZG, Whitbeck JL (eds) The rhizosphere: An ecological perspective. Elsevier, London, pp 179–200

  88. Rodina ABL, Tonon BC, Marques LEA, Hungria LM, Nogueria AM, Zangaro W (2019) Plants of distinct successional stages have different strategies for nutrient acquisition in an Atlantic rain forest ecosystem. Int J Plant Sci 180:186–199

  89. Roering JJ, Marshall J, Booth AM, Mort M, Jin Q (2010) Evidence for biotic controls on topography and soil production. Earth Planet Sci Lett 298:183–190

  90. RStudio Team (2017) RStudio: integrated development for R. RStudio Inc, Boston. https://www.rstudio.com/. Accessed 8 May 2019.

  91. Rumpel C, Kogel-Knaber I (2011) Deep soil organic matter—a key but poorly understood component of the terrestrial C cycle. Plant Soil 338:143–158

  92. Ryan MG, Law BE (2005) Interpreting, measuring and modeling soil respiration. Biogeochemistry 73:3–27

  93. Schlesinger WH (1984) Soil organic matter: a source of atmospheric CO2. In: Woodwell GM (ed) The role of terrestrial vegetation in the global carbon cycle: measurement by remote sensing. Wiley, New York, pp 111–127

  94. Schneckenberger K, Demin D, Stahr K, Kuzyakov Y (2008) Microbial utilization and mineralization of [14C]glucose added in 6 orders of concentration to soil. Soil Biol Biochem 40:1981–1988

  95. Scientific T (2012) IonPac AS11-HC product manual. Thermo Fisher Scientific, Waltham

  96. Shukla RP, Ramakrishnan PS (1984) Biomass allocation strategies and productivity of tropical trees related to successional status. For Ecol Manag 9:315–324

  97. Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331

  98. Soper FM, Chamberlain SD, Crumsey JM, Gregor S, Derry LA, Sparks JP (2018) Biological cycling of mineral nutrients in a temperate forested shale catchment. J Geophys Res Biogeosciences 1:1. https://doi.org/10.1029/2018jg004639

  99. Thorley RMS, Taylor LL, Banwart SA, Leake JR, Beerling DJ (2015) The role of forest trees and their mycorrhizal fungi in carbonate rock weathering and its significance for global carbon cycling. Plant Cell Environ 38:1947–1961

  100. Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. In: Carter MR (ed) Soil Sampling and methods of analysis. Louis, Boca Raton, Florida, USA, pp 75–86

  101. van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in the soil. Plant Soil 178:185–192

  102. Vitousek P, Chadwick O, Crews T, Fownes J, Hendricks D, Herbert D (1997) Soil and ecosystem development across the Hawaiian islands. GSA Today 7:3–7

  103. Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Galuszka A, Cearreta A, Edgeworth M, Ellis EC, Ellis M, Jeandel C, Leinfelder R, McNeill JR, Richter DD, Steffen W, Syvitski J, Vidas D, Wagreich M, Williams M, Zhisheng A, Grinevald J, Odada E, Oreskes N, Wolfe AP (2016) The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351:aad2622

  104. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

  105. Winter B (2013) Linear models and linear mixed effects models in R with linguistic applications. arXiv:1308.5499. https://arxiv.org/pdf/1308.5499.pdf. Accessed 9 May 2019.

  106. World Bank Group (2015) Forest area (% of land area). Food and Agricultural Organization, Rome. https://data.worldbank.org/indicator/ag.lnd.frst.zs. Accessed 9 May 2019.

  107. Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221

  108. Yoo K, Fisher B, Ji J, Aufdenkampe A, Klaminder J (2015) The geochemical transformation of soils by agriculture and its dependence on soil erosion: an application of the geochemical mass balance approach. Sci Total Environ 251:326–335

  109. Yuan ZY, Chen HYH (2012) Fine root dynamics with stand development in the boreal forest. Funct Ecol 26:991–998

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Acknowledgements

We thank Dr. Dan Reuman for enriching our understanding of some of the intricacies of post hoc statistical testing, Rena Stair for her work developing the fine root dataset, the assistance of the Kansas State University Soil Testing Lab, and National Science Foundation grant EAR-1331846.

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Correspondence to Emma Hauser.

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Hauser, E., Richter, D.D., Markewitz, D. et al. Persistent anthropogenic legacies structure depth dependence of regenerating rooting systems and their functions. Biogeochemistry 147, 259–275 (2020). https://doi.org/10.1007/s10533-020-00641-2

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Keywords

  • Root exudates
  • Carbon allocation
  • Forest regeneration
  • Mineral-bound phosphorus
  • Soil organic matter
  • Anthropocene