Abstract
Symbiotic nitrogen (N)-fixing plants can enrich ecosystems with N, which can alter the cycling and demand for other nutrients. Researchers have hypothesized that fixed N could be used by plants and soil microbes to produce extracellular phosphatase enzymes, which release P from organic matter. Consistent with this speculation, the presence of N-fixing plants is often associated with high phosphatase activity, either in the soil or on root surfaces, although other studies have not found this association, and the connection between phosphatase and rates of N fixation—the mechanistic part of the argument—is tenuous. Here, we measured soil phosphatase activity under N-fixing trees and non-fixing trees transplanted and grown in tropical and temperate sites in the USA: two sites in Hawaii, and one each in New York and Oregon. This provides a rare example of phosphatase activity measured in a multi-site field experiment with rigorously quantified rates of N fixation. We found no difference in soil phosphatase activity under N-fixing vs. non-fixing trees nor across rates of N fixation, though we note that no sites were P limited and only one was N limited. Our results add to the literature showing no connection between N fixation rates and phosphatase activity.
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References
Allison SD, Nielsen C, Hughes RF (2006) Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biol Biochem 38:1537–1544. https://doi.org/10.1016/j.soilbio.2005.11.008
Alster CJ, German DP, Lu Y, Allison SD (2013) Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland. Soil Biol Biochem 64:68–79. https://doi.org/10.1016/j.soilbio.2013.03.034
Aplet GH (1990) Alteration of earthworm community biomass by the alien Myrica faya in Hawai’i. Oecologia 82:414–416. https://doi.org/10.1007/BF00317491
Baker PJ, Snowcroft PG, Ewel JJ (2009) Koa (Acacia koa) Ecology and Silviculture. General Technical Report PSW-GTR-211. Albany, CA, USA. Department of Agriculture, Forest Service, Pacific Southwest Research Station
Barrett DJ, Richardson AE, Gifford RM (1998) Elevated atmospheric CO2 concentrations increase wheat root phosphatase activity when growth is limited by phosphorus. Aust J Plant Physiol 25:87–93. https://doi.org/10.1071/PP97045
Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013a) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227. https://doi.org/10.1038/nature12525
Batterman SA, Wurzburger N, Hedin LO (2013b) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408. https://doi.org/10.1111/1365-2745.12138
Batterman SA, Hall JS, Turner BL, Hedin LO, LaHaela Walter JK, Sheldon P, van Breugel M (2018) Phosphatase activity and nitrogen fixation reflect species differences, not nutrient trading or nutrient balance, across tropical rainforest trees. Ecol Lett 21:1486–1495. https://doi.org/10.1111/ele.13129
Binkley D (2003) Seven decades of stand development in mixed and pure stands of conifers and nitrogen-fixing red alder. Can J for Res 33:2274–2279. https://doi.org/10.1139/X03-158
Binkley D (2005) How nitrogen-fixing trees change soil carbon. In: Binkley D, Menyailo O (eds) Tree species effects on soils: implications for global change. Springer, Dordrecht, pp 155–164
Binkley D, Sollins P, Bell R, Sachs D, Myrold D (1992) Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73:2022–2033. https://doi.org/10.2307/1941452
Binkley D, Cromack K Jr, Baker DD (1994) Nitrogen fixation by red alder: Biology, rates and controls. In: Hibbs D, DeBell D, Tarrant R (eds) The biology and management of red alder. Oregon State University Press, Corvallis, pp 57–72
Cabugao KG, Yaffar D, Stenson N, Childs J, Phillips J, Mayes MA, Yang X, Weston DJ, Norby RJ (2021) Bringing function to structure: root-soil interactions sha** phosphatase activity throughout a soil profile in Puerto Rico. Ecol Evol 11:1150–1164. https://doi.org/10.1002/ece3.7036
Caldwell BA (2006) Effects of invasive scotch broom on soil properties in a Pacific coastal prairie soil. Appl Soil Ecol 32:149–152. https://doi.org/10.1016/j.apsoil.2004.11.008
Carreras Pereira, KA, Wolf AA, Kou-Giesbrecht S, Akana PR, Funk JL, Menge DNL (in revision) Allometric relationships for eight species of 4-5 year old nitrogen-fixing and non-fixing trees. PLoS ONE (in revision)
Chalk PM (1985) Estimation of N2 fixation by isotope dilution: An appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 17:389–410. https://doi.org/10.1016/0038-0717(85)90001-X
Chapin FS III, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New York. https://doi.org/10.1007/978-1-4419-9504-9
Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological flora of the British isles: Robinia pseudoacacia. J Ecol 101:1623–1640. https://doi.org/10.1111/1365-2745.12162
Compton JE, Cole DW (2001) Fate and effects of phosphorus additions in soils under N2-fixing red alder. Biogeochemistry 53:225–247. https://doi.org/10.1023/A:1010646709944
Compton JE, Church MR, Larned ST, Hogsett WE (2003) Nitrogen export from forested watersheds in the Oregon coast range: the role of N2-fixing red alder. Ecosystems 6:773–785. https://doi.org/10.1007/s10021-002-0207-4
Cooke PT (1987) Role of density and proportion in allometric equations of Douglas fir and red alder seedlings. MS Thesis, Oregon State University, Corvallis, OR, USA
Dracup MNH, Barrett-Lennard EG, Greenway H, Robson AD (1984) Effect of phosphorus deficiency on phosphatase activity of cell walls from roots of subterranean clover. J Exp Bot 35:466–480. https://doi.org/10.1093/jxb/35.4.466
Dynarski KA, Pett-Ridge JC, Perakis SS (2020) Decadal-scale decoupling of soil phosphorus and molybdenum cycles by temperate nitrogen-fixing trees. Biogeochemistry 149:355–371. https://doi.org/10.1007/s10533-020-00680-9
Elevitch CR, Wilkinson KM, Friday JB (2006) Acacia koa (koa) and Acacia koaia (koai ‘a). Species profiles for Pacific Island agroforestry. In Elevitch CR (Eds) Permanent Agriculture Resources (PAR), Holualoa, Hawaii, pp 1-29
Fries LLM, Pacovsky RS, Safir GR, Kaminski J (1998) Phosphorus effect on phosphatase activity in endomycorrhizal maize. Physiol Plant 103:162–171. https://doi.org/10.1034/j.1399-3054.1998.1030203.x
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397. https://doi.org/10.1016/j.soilbio.2011.03.017
Giardina CP, Huffman S, Binkley D, Caldwell BA (1995) Alders increase soil-phosphorus availability in a douglas-fir plantation. Can J for Res 25:1652–1657. https://doi.org/10.1139/x95-179
Hayes JE, Richardson AE, Simpson RJ (1999) Phytase and acid phosphatase activities in extracts from roots of temperate pasture grass and legume seedlings. Aust J Plant Physiol 26:801–809. https://doi.org/10.1071/PP99065
Helgerson OT (1981) Nitrogen fixation by scotch broom (Cytisus scoparius L.) and red alder (Alnus rubra Bong.) planted under precommercially thinned Douglas fir (Pseudotsuga menziesii (Mirb.) Franco). PhD dissertation, Oregon State University, Corvallis, OR, USA
Huss-Danell K (1997) Tansley review no. 93. Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405. https://doi.org/10.1046/j.1469-8137.1997.00755.x
Kou-Giesbrecht S, Menge DNL (2021) Nitrogen-fixing trees increase soil nitrous oxide emissions: a meta-analysis. Ecology 102:e03415. https://doi.org/10.1002/ecy.3415
Kou-Giesbrecht S, Funk JL, Perakis SS, Wolf AA, Menge DNL (2021) N supply mediates the radiative balance of N2O emissions and CO2 sequestration driven by N-fixing vs. non-fixing trees. Ecology 102:e03414. https://doi.org/10.1002/ecy.3414
Lai HR, Hall JS, Batterman SA, Turner BL, van Breugel M (2018) Nitrogen fixer abundance has no effect on biomass recovery during tropical secondary forest succession. J Ecol 106:1415–1427. https://doi.org/10.1111/1365-2745.12979
Lenth RV (2022) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.3 https://CRAN.R-project.org/package=emmeans
Levy-Varon JH, Batterman SA, Medvigy D, Xu X, Hall JS, van Breugel M, Hedin LO (2019) Tropical carbon sink accelerated by symbiotic dinitrogen fixation. Nat Commun 10:1–8. https://doi.org/10.1038/s41467-019-13656-7
Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195:161–169. https://doi.org/10.1023/A:1004264002524
Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercrop**. Ann Bot 94:297–303. https://doi.org/10.1093/aob/mch140
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus deficient soils. Proc Natl Acad Sci 104:11192–11196. https://doi.org/10.1073/pnas.070459110
Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704
Marron N, Gana C, Gérant D, Maillard P, Priault P, Epron D (2018) Estimating symbiotic N2 fixation in Robinia pseudoacacia. J Plant Nutr Soil Sci 181:296–304. https://doi.org/10.1002/jpln.201700503
Mead DJ, Preston CM (1992) Nitrogen fixation in Sitka alder by 15N isotope dilution after eight growing seasons in a lodgepole pine site. Can J for Res 22:1192–1194. https://doi.org/10.1139/x92-15
Menge DNL, Wolf AA, Funk JL, Perakis SS, Akana PR, Arkebauer R, Bytnerowicz TA, Carreras Pereira KA, Huddell AM, Kou-Giesbrecht S, Ortiz SK (2023) Tree symbioses sustain nitrogen fixation despite excess nitrogen supply. Ecol Monogr. https://doi.org/10.1002/ecm.1562
Mitchell HL (1936) Trends in the nitrogen, phosphorus, potassium and calcium content of the leaves of some forest trees during the growing season. Black Rock For Pap 1:30–44
Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17:1282–1289. https://doi.org/10.1111/ele.12335
Nasto MK, Osborne BB, Lekberg Y, Asner GP, Balzotti CS, Porder S, Taylor PG, Townsend AR, Cleveland CC (2017) Nutrient acquisition, soil phosphorus partitioning and competition among trees in a lowland tropical rain forest. New Phytol 214:1506–1517. https://doi.org/10.1111/nph.14494
Nasto MK, Winter K, Turner BL, Cleveland CC (2019) Nutrient acquisition strategies augment growth in tropical N2-fixing trees in nutrient-poor soil and under elevated CO2. Ecology 100:e02646. https://doi.org/10.1002/ecy.2646
NRCS (2022) Web soil survey, natural resources conservation service, United States department of agriculture. Available online at http://websoilsurvey.nrcs.usda.gov/ accessed [12/1/2022]
Nuruzzuman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120. https://doi.org/10.1007/s11104-005-3936-2
Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190. https://doi.org/10.1023/A:1006316117817
Olde Venterink H (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant Soil 347:137–146. https://doi.org/10.1007/s11104-011-0834-7
Parrotta JA (1993) Casuarina equisetifolia L. ex JR & G Forst. General Technical Report SO-ITF-SM-56. Department of Agriculture, Forest Service
Perakis SS, Pett-Ridge JC (2019a) Nitrogen-fixing red alder trees tap rock-derived nutrients. Proc Natl Acad Sci 116:5009–5014. https://doi.org/10.1073/pnas.1814782116
Perakis SS, Pett-Ridge JC (2019b) Reply to Lambers et al.: how does nitrogen-fixing red alder eat rocks? Proc Natl Acad Sci 116:11577–11578. https://doi.org/10.1073/pnas.1906596116
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2020) nlme: linear and nonlinear mixed effects models. R package version 3.1–147 https://CRAN.R-project.org/package=nlme
Png GK, Turner BL, Albornoz FE, Hayes PE, Lambers H, Laliberté E (2017) Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. J Ecol 105:1246–1255. https://doi.org/10.1111/1365-2745.12758
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Accessed Dec 2020
Ruess RW, McFarland JM, Trummer LM, Rohrs-Richey JK (2009) Disease-mediated declines in N-fixation inputs by Alnus tenuifolia to early-successional floodplains in interior and south-central Alaska. Ecosystems 12:489–502. https://doi.org/10.1007/s10021-009-9237-5
Schmidt CB, Funk JL, Wolf AA, Akana PR, Palmer MI, Menge DNL (2023) Nitrogen fixation responds to soil nitrogen at low light but not high light in two understory species. J Ecol. https://doi.org/10.1111/1365-2745.14071
Schuster WS, Griffin KL, Roth H, Turnbull MH, Whitehead D, Tissue DT (2008) Changes in composition, structure and aboveground biomass over 76 years (1930–2006) in the Black Rock Forest, Hudson Highlands, southeastern New York State. Tree Physiol 28:537–549. https://doi.org/10.1093/treephys/28.4.537
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Funct Plant Biol 13:699–756. https://doi.org/10.1071/PP9860699
Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593. https://doi.org/10.2307/1940086
Sitter J, Edwards PJ, Olde Venterink H (2013) Increases of soil C, N, and P pools along an Acacia tree density gradient and their effects on trees and grasses. Ecosystems 16:347–357. https://doi.org/10.1007/s10021-012-9621-4
Soper FM, Nasto MK, Osborne BB, Cleveland CC (2019) Nitrogen fixation and foliar nitrogen do not predict phosphorus acquisition strategies in tropical trees. J Ecol 107:118–126. https://doi.org/10.1111/1365-2745.13044
Soper FM, Taylor BN, Winbourne JB, Wong MY, Dynarski KA, Reis CR, Peoples MB, Cleveland CC, Reed SC, Menge DNL, Perakis SS (2021) A roadmap for sampling and scaling biological nitrogen fixation in terrestrial ecosystems. Methods Ecol Evol 12:1122–1137. https://doi.org/10.1111/2041-210X.13586
Speir TW, Ross DJ (1978) Soil phosphatase and sulphatase. In: Burns RG (ed) Soil enzymes. Academic Press, London, UK, pp 197–250
Spiers GA, McGill WB (1979) Effects of phosphorus additions and energy supply on acid phosphatase production and activity in soils. Soil Biol Biochem 11:3–8. https://doi.org/10.1016/0038-0717(79)90110-X
Sprent JI (2009) Legume nodulation: a global perspective. Wiley-Blackwell, Ames, IA, USA
Staccone A, Liao W, Perakis SS, Compton J, Clark CM, Menge DNL (2020) A spatially explicit, empirical estimate of tree-based biological nitrogen fixation in forests of the United States. Global Biogeochem Cy 34:e2019GB006241. https://doi.org/10.1029/2019GB006241
Staccone AP, Kou-Giesbrecht S, Taylor BN, Menge DNL (2021) Nitrogen-fixing trees have no net effect on forest growth in the coterminous United States. J Ecol 109:877–887. https://doi.org/10.1111/1365-2745.13513
Stewart JL, Allison GE, Simons AJ (eds) (1996) Gliricidia sepium: Genetic resources for farmers. Tropical forestry papers No 33. Oxford Forestry Institute, University of Oxford, Oxford
Stout BB (1956) Studies of the root systems of deciduous trees. Harvard University Printing, Cambridge, MA
Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil 155(156):95–98. https://doi.org/10.1007/978-94-011-1880-4_13
Tang JY (1997) Nitrogen fixation and cycling in a mixture of young red alder and Douglas-fir. MA thesis, Oregon State University, Corvallis, OR, USA
Taylor BN, Chazdon RL, Bachelot B, Menge DNL (2017) Nitrogen-fixing trees inhibit growth of regenerating Costa Rican rainforest. Proc Natl Acad Sci 114:8817–8822. https://doi.org/10.1073/pnas.1707094114
Thilakarathna MS, McElroy MS, Chapagain T, Papadopoulos YA, Raizada MN (2016) Belowground nitrogen transfer from legumes to non-legumes under managed herbaceous crop** systems: a review. Agron Sustain Dev 36:58. https://doi.org/10.1007/s13593-016-0396-4
Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954. https://doi.org/10.1890/0012-9658(2001)082[0946:EOSNAOJ2.0.CO;2
Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Australian Centre for International Agricultural Research (ACIAR)
Verchot LV, Borelli T (2005) Application of para-nitrophenol (pNP) enzyme assays in degraded tropical soils. Soil Biol Biochem 37:625–633. https://doi.org/10.1016/j.soilbio.2004.09.005
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265. https://doi.org/10.2307/1942601
Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804. https://doi.org/10.1126/science.238.4828.8
Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos T R Soc B 368:20130119. https://doi.org/10.1098/rstb.2013.0119
Wang Y-P, Houlton BZ, Field CB (2007) A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Global Biogeochem Cy. https://doi.org/10.1029/2006GB002797
Winbourne JB, Harrison MT, Sullivan BW, Alvarez-Clare S, Lins SR, Martinelli L, Nasto M, Piotto D, Rolim S, Wong M, Porder S (2018) A new framework for evaluating estimates of symbiotic nitrogen fixation in forests. Am Nat 192:618–629. https://doi.org/10.1086/699828
Xu H, Detto M, Fang S, Chazdon RL, Li Y, Hau BCH, Fischer GA, Weiblen GD, Hogan JA, Zimmerman JK et al (2020) Soil nitrogen concentration mediates the relationship between leguminous trees and neighbor diversity in tropical forests. Commun Biol 3:1–8. https://doi.org/10.1038/s42003-020-1041-y
Yadav RS, Tarafdar JC (2001) Influence of organic and inorganic phosphorus supply on the maximum secretion of acid phosphatase by plants. Biol Fert Soils 34:140–143. https://doi.org/10.1007/s003740100376
Yelenik S, Perakis SS, Hibbs D (2013) Regional constraints to biological nitrogen fixation in post-fire forest communities. Ecology 94:739–750. https://doi.org/10.1890/12-0278.1
Zou XM, Binkley D, Caldwell BA (1995) Effects of dinitrogen-fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci Soc Am J 59:1452–1458. https://doi.org/10.2136/sssaj1995.03615995005900050035x
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This material was supported by the National Science Foundation under grant nos. DEB-1457650 and DEB-1457444. We are grateful for assistance from Starker Forests, April Strid and Chris Catricala for their help at the Oregon site; Angel Magno, Eric Magno, Angalee Kirby, JB Friday, and Rebecca Ostertag for their help at the Hawaii sites; the staff at Black Rock Forest, Rachel Arkebauer, Alex Huddell, and Tom Bytnerowicz for their support at the New York site; the assistance from dozens of undergraduates and other field and lab assistants; and the enzyme assay advice from Steven Allison. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U. S. Government.
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DNLM, AAW, JLF, and SSP designed the study. All authors collected data. EAJ and DNLM analyzed data and wrote the manuscript. All authors edited the manuscript.
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Jager, E.A., Quebbeman, A.W., Wolf, A.A. et al. Symbiotic nitrogen fixation does not stimulate soil phosphatase activity under temperate and tropical trees. Oecologia 201, 827–840 (2023). https://doi.org/10.1007/s00442-023-05339-4
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DOI: https://doi.org/10.1007/s00442-023-05339-4