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.
Similar content being viewed by others
References
Aber JD, Melillo JM (2001) Terrestrial ecosystems. Academic, Burlington
Adams MA, Pate JS (1992) Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.). Plant Soil 145:107–113
Amrhein V, Greenland S, McShane B (2019) Scientists rise up against statistical significance. Nature 567:305–307
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
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
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
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
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
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Berner RA (1992) Weathering, plants and the long-term carbon cycle. Geochim Cosmochim Acta 56:3225–3231
Berner RA (2003) The long-term carbon cycle, fossil fuels and atmospheric composition. Nature 426:323–326
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
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.
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
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
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
Bunemann EK, Oberson A, Frossard E (eds) (2011) Phosphorus in action: biological processes in soil phosphorus cycling. Springer, Berlin
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
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
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
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
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
D'Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209
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
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
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
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
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
Dupouey JL, Dambrine E, Laffite JD, Moares C (2002) Irreversible impacts of past land use on forest soils and biodiversity. Ecology 83:2978–2984
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
Ellis EC (2011) Anthropogenic transformation of the terrestrial biosphere. Philos Trans R Soc 369:1010–1135
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
Fan J, McConkey B, Wang H, Janzen H (2016) Root distribution by depth for temperate agricultural crops. Field Crop Res 189:68–74
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
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
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
Ganor J, Reznik IJ, Rosenberg YO (2009) Organics in water-rock interactions. Rev Mineral Geochem 70:259–369
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
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
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
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
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
Jackson RB, Manwaring JH, Caldwell MM (1990) Rapid physiological adjustment of roots to localized soil enrichment. Nature 344:58–60
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
Janzen HH (2006) The soil carbon dilemma: Shall we hoard or use it? Soil Biol Biochem 38:419–424
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
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
Jobbagy EG, Jackson RB (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51–77
Jobbagy EG, Jackson RB (2004) The uplift of soil nutrients by plants: biogeochemical consequences across scales. Ecology 85:2380–2389
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
Kelly EF, Chadwick OA, Hilinski ET (1998) The effect of plants on mineral weathering. Biogeochemistry 42:21–53
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
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
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.
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103
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
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
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
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
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
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
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56
Maeght JL, Rewald B, Pierret A (2013) How to study deep roots and why it matters. Front Plant Sci 4:299
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
Marschner P, Rengel Z (2007) Nutrient cycling in terrestrial ecosystems. Springer, New York
Martin PA, Newton AC, Bullock JM (2013) Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc Roy Soc 280:20132236
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
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
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
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
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
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
Nadelhoffer KJ, Raich JW (1992) Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73:1139–1147
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
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
Pawlik L (2013) The role of trees in the geomorphic system of forested hillslopes—a review. Earth Sci Rev 126:250–265
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
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
Pregitzer KS (2002) Fine roots of trees—a new perspective. New Phytol 154:267–270
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
Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilization. Plant Soil 269:341–356
Richter DD, Billings SA (2015) ‘One physical system’: Tansley’s ecosystem as Earth’s critical zone. New Phytol 206:900–912
Richter DD, Markewitz D (2001) Understanding soil change: soil sustainability over millennia, centuries, and decades. Cambridge, New York
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
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
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
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
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
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
RStudio Team (2017) RStudio: integrated development for R. RStudio Inc, Boston. https://www.rstudio.com/. Accessed 8 May 2019.
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
Ryan MG, Law BE (2005) Interpreting, measuring and modeling soil respiration. Biogeochemistry 73:3–27
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
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
Scientific T (2012) IonPac AS11-HC product manual. Thermo Fisher Scientific, Waltham
Shukla RP, Ramakrishnan PS (1984) Biomass allocation strategies and productivity of tropical trees related to successional status. For Ecol Manag 9:315–324
Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331
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
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
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
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
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
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
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
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.
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.
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
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
Yuan ZY, Chen HYH (2012) Fine root dynamics with stand development in the boreal forest. Funct Ecol 26:991–998
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Sasha C. Reed.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-020-00641-2