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Soil organic phosphorus in lowland tropical rain forests

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Abstract

Phosphorus is widely considered to constrain primary productivity in tropical rain forests, yet the chemistry of soil organic phosphorus in such ecosystems remains poorly understood. We assessed the composition of soil organic phosphorus in 19 contrasting soils under lowland tropical forest in the Republic of Panama using NaOH–EDTA extraction and solution 31P nuclear magnetic resonance spectroscopy. The soils spanned a strong rainfall gradient (1730–3404 mm y−1) and contained a wide range of chemical properties (pH 3.3–7.0; total carbon 2.8–10.4%; total phosphorus 74–1650 mg P kg−1). Soil organic phosphorus concentrations ranged between 22 and 494 mg P kg−1 and were correlated positively with total soil phosphorus, pH, and total carbon, but not with annual rainfall. Organic phosphorus constituted 26 ± 1% (mean ± STD error, n = 19) of the total phosphorus, suggesting that this represents a broad emergent property of tropical forest soils. Organic phosphorus occurred mainly as phosphate monoesters (68–96% of total organic phosphorus) with smaller concentrations of phosphate diesters in the form of DNA (4–32% of total organic phosphorus). Phosphonates, which contain a direct carbon–phosphorus bond, were detected in only two soils (3% of the organic phosphorus), while pyrophosphate, an inorganic polyphosphate with a chain length of two, was detected in all soils at concentrations up to 13 mg P kg−1 (3–13% of extracted inorganic phosphorus). Phosphate monoesters were a greater proportion of the total organic phosphorus in neutral soils with high concentrations of phosphorus and organic matter, whereas the proportion of phosphate diesters was greater in very acidic soils low in phosphorus and organic matter. Most soils did not contain detectable concentrations of either myo- or scyllo-inositol hexakisphosphate, which is in marked contrast to many temperate mineral soils that contain abundant inositol phosphates. We conclude that soil properties exert a strong control on the amounts and forms of soil organic phosphorus in tropical rain forests, but that the proportion of the total phosphorus in organic forms is relatively insensitive to variation in climate and soil properties. Further work is now required to assess the contribution of soil organic phosphorus to the nutrition and diversity of plants in these species-rich ecosystems.

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References

  • Alexander I (1989) Mycorrhizas in tropical forests. In: Proctor J (ed) Mineral nutrients in tropical forest and savanna ecosystems. Blackwell Scientific, Oxford, UK, pp 169–188

    Google Scholar 

  • Baillie IC (1989) Soil characteristics and classification in relation to the mineral nutrition of tropical wooded ecosystems. In: Proctor J (ed) Mineral nutrients in tropical forest and savanna ecosystems. Blackwell Scientific, Oxford, UK, pp 15–26

    Google Scholar 

  • Baillie I, Elsenbeer H, Barthold F, Grimm R, Stallard R (2007) Semi-detailed soil survey of Barro Colorado Island, Panama. Soil Report [Online] available at http://biogeodb.stri.si.edu/bioinformatics/bci_soil_map/index.php (verified 16 November 2009)

  • Bates JAR, Baker TCN (1960) Studies on a Nigerian forest soil. II. The distribution of phosphorus in the profile and in various soil fractions. J Soil Sci 11:257–265

    Article  Google Scholar 

  • Bawa KS (1990) Plant–pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21:399–422

    Article  Google Scholar 

  • Bowman RA, Cole CV (1978) Transformations of organic phosphorus substrates in soils as evaluated by NaHCO3 extraction. Soil Sci 125:49–54

    Article  Google Scholar 

  • Bowman RA, Moir JO (1993) Basic EDTA as an extractant for soil organic phosphorus. Soil Sci Soc Am J 57:1516–1518

    Article  Google Scholar 

  • Cade-Menun BJ (2005) Using phosphorus-31 nuclear magnetic resonance spectroscopy to characterize organic phosphorus in environmental samples. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CAB International, Wallingford, UK, pp 21–44

    Chapter  Google Scholar 

  • Cade-Menun BJ, Preston CM (1996) A comparison of soil extraction procedures for 31P NMR spectroscopy. Soil Sci 161:770–785

    Article  Google Scholar 

  • Cade-Menun BJ, Berch SM, Preston CM, Lavkulich LM (2000) Phosphorus forms and related soil chemistry of Podzolic soils on northern Vancouver Island. 1. A comparison of two forest types. Can J For Res 30:1714–1725

    Article  Google Scholar 

  • Celi L, Barberis E (2007) Abiotic reactions of inositol phosphates in soil. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, UK, pp 207–220

    Chapter  Google Scholar 

  • Chacón N, Silver WL, Dubinsky EA, Cusack DF (2006) Iron reduction and soil phosphorus solubilization in humid tropical forest soils: the roles of labile carbon pools and an electron shuttle compound. Biogeochemistry 78:67–84

    Article  Google Scholar 

  • Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5:680–691

    Google Scholar 

  • Clinebell RR, Phillips OL, Stark N, Zuuring H (1995) Prediction of neotropical tree and liana species richness from soil and climatic data. Biodivers Conserv 4:56–90

    Article  Google Scholar 

  • Condit R, Pitman N, Leigh EG, Chave J, Terborgh J, Foster RB, Nunez P, Aguilar S, Valencia R, Villa G, Muller-Landau HC, Losos E, Hubbell SP (2002) Beta diversity in tropical forest trees. Science 295:666–669

    Article  Google Scholar 

  • Condron LM, Tiessen H (2005) Interactions of organic phosphorus in terrestrial ecosystems. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CAB International, Wallingford, UK, pp 295–308

    Chapter  Google Scholar 

  • Condron LM, Moir JO, Tiessen H, Stewart JWB (1990) Critical evaluation of methods for determining total organic phosphorus in tropical soils. Soil Sci Soc Am J 54:1261–1266

    Article  Google Scholar 

  • Condron LM, Turner BL, Cade-Menun BJ (2005) Chemistry and dynamics of soil organic phosphorus. In: Sharpley AN, Sims JT (eds) Phosphorus: agriculture and the environment. ASA-CSSA-SSSA, Madison, WI, pp 87–121

    Google Scholar 

  • Cosgrove DJ (1980) Inositol phosphates: their chemistry, biochemistry and physiology. Elsevier Scientific, Amsterdam

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dahnke WC, Malcolm JL, Menéndez ME (1964) Phosphorus fractions in selected soil profiles of El Salvador as related to their development. Soil Sci 98:33–38

    Article  Google Scholar 

  • Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell S (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82

    Article  Google Scholar 

  • Forster JC, Zech W (1993) Phosphorus status of a soil catena under Liberian evergreen rain forest: results of 31P NMR spectroscopy and phosphorus adsorption experiments. Z Pflanzenernähr Bodenkd 156:61–66

    Article  Google Scholar 

  • Gee GW, Or D (2002) Particle size analysis. In: Dane JH, Topp C (eds) Methods of soil analysis, part 4—physical methods. Soil Science Society of America, Madison, WI, pp 255–293

    Google Scholar 

  • Giaveno C, Celi L, Cessa RMA, Prati M, Bonifacio E, Barberis E (2008) Interaction of organic phosphorus with clays extracted from Oxisols. Soil Sci 173:694–706

    Article  Google Scholar 

  • Harrison AF (1982) Labile organic phosphorus mineralization in relationship to soil properties. Soil Biol Biochem 14:343–351

    Article  Google Scholar 

  • Harrison AF (1987) Soil organic phosphorus: a review of world literature. CAB International, Wallingford, UK

    Google Scholar 

  • Hawkes GE, Powlson DS, Randall EW, Tate KR (1984) A 31P nuclear magnetic resonance study of the phosphorus species in alkali extracts from soils from long-term field experiments. J Soil Sci 35:35–45

    Article  Google Scholar 

  • Hill JE, Richardson AE (2007) Isolation and assessment of microorganisms that utilize phytate. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, UK, pp 61–77

    Chapter  Google Scholar 

  • Jenny H (1941) Factors of soil formation: a system of quantitative pedology. McGraw-Hill, London

    Google Scholar 

  • Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499

    Google Scholar 

  • Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43

    Google Scholar 

  • Koukol O, Novák F, Hrabal R (2008) Composition of the organic phosphorus fraction in basidiocarps of saprotrophic and mycorrhizal fungi. Soil Biol Biochem 40:2464–2467

    Article  Google Scholar 

  • Loeppert RH, Inskeep WP (1996) Iron. In: Sparks DL et al (eds) Methods of soil analysis, part 3—chemical methods. Soil Science Society of America, Madison, WI, pp 639–664

    Google Scholar 

  • Makarov MI, Haumaier L, Zech W (2002) Nature of soil organic phosphorus: an assessment of peak assignments in the diester region of 31P NMR spectra. Soil Biol Biochem 34:1467–1477

    Article  Google Scholar 

  • McDowell RW, Cade-Menun B, Stewart I (2007) Organic phosphorus speciation and pedogenesis: analysis by solution 31P nuclear magnetic resonance spectroscopy. Eur J Soil Sci 58:1348–1357

    Article  Google Scholar 

  • Möller A, Kaiser K, Amelung W, Niamskul C, Udomsri S, Puthawong M, Haumaier L, Zech W (2000) Forms of organic C and P extracted from tropical soils as assessed by liquid-state 13C- and 31P-NMR spectroscopy. Aust J Soil Res 38:1017–1035

    Article  Google Scholar 

  • Murphy PNC, Bell A, Turner BL (2010) Phosphorus speciation in temperate basaltic grassland soils by solution 31P NMR spectroscopy. Eur J Soil Sci 61:638–651

    Google Scholar 

  • Okin GS, Mahowald N, Chadwick OA, Artaxo P (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Global Biogeochem Cycles 18:1–9

    Article  Google Scholar 

  • Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11

    Article  Google Scholar 

  • Porder S, Vitousek PM, Chadwick OA, Chamberlain CP, Hilley GE (2007) Uplift, erosion, and phosphorus limitation in terrestrial ecosystems. Ecosystems 10:158–170

    Article  Google Scholar 

  • Pyke CR, Condit R, Aguilar S, Lao S (2001) Floristic composition across a climatic gradient in a neotropical lowland forest. J Veg Sci 12:553–566

    Article  Google Scholar 

  • Raboy V (2007) Seed phosphorus and the development of low phytate crops. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, UK, pp 111–132

    Chapter  Google Scholar 

  • Schuur EAG, Chadwick OA, Matson PA (2001) Carbon cycling and soil carbon storage in mesic to wet Hawaiian montane forests. Ecology 82:3182–3196

    Article  Google Scholar 

  • Sharpley AN, Tiessen H, Cole CV (1987) Soil phosphorus forms extracted by soil tests as a function of pedogenesis. Soil Sci Soc Am J 51:362–365

    Article  Google Scholar 

  • Smeck NE (1985) Phosphorus dynamics in soils and landscapes. Geoderma 36:185–199

    Article  Google Scholar 

  • Smernik RJ, Dougherty WJ (2007) Identification of phytate in phosphorus-31 nuclear magnetic resonance spectra: the need for spiking. Soil Sci Soc Am J 71:1045–1050

    Article  Google Scholar 

  • Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. Agriculture Handbook Number 436, 2nd edn. United States Department of Agriculture—Natural Resources Conservation Service, Lincoln, NE

  • Solomon D, Lehmann J, Mamo T, Fritzsche F, Zech W (2002) Phosphorus forms and dynamics as influenced by land use changes in the sub-humid Ethiopian highlands. Geoderma 105:21–48

    Article  Google Scholar 

  • Stewart RH, Stewart JL, Woodring WP (1980) Geologic map of the Panama Canal and vicinity, Republic of Panama. Map I-1232. United States Geological Survey, Boulder, CO

    Google Scholar 

  • Sumann M, Amelung W, Haumaier L, Zech W (1998) Climatic effects on soil organic phosphorus in the North American Great Plains identified by phosphorus-31 nuclear magnetic resonance. Soil Sci Soc Am J 62:1580–1586

    Article  Google Scholar 

  • Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22

    Article  Google Scholar 

  • Tate KR, Newman RH (1982) Phosphorus fractions of a climosequence of soils in New Zealand tussock grassland. Soil Biol Biochem 14:191–196

    Article  Google Scholar 

  • Tiessen H (1998) Resilience of phosphorus transformations in tropical forest and derived ecosystems. In: Schulte A, Ruhiyat D (eds) Soils of tropical forest ecosystems: characteristics. Ecology and management. Springer, New York, pp 92–98

    Google Scholar 

  • Turner BL (2006) Organic phosphorus in Madagascan rice soils. Geoderma 136:279–288

    Article  Google Scholar 

  • Turner BL (2007) Inositol phosphates in soil: amounts, forms and significance of the phosphorlyated inositol stereoisomers. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: linking agriculture and the environment. CAB International, Wallingford, UK, pp 186–207

    Chapter  Google Scholar 

  • Turner BL (2008a) Resource partitioning for soil phosphorus: a hypothesis. J Ecol 96:698–702

    Article  Google Scholar 

  • Turner BL (2008b) Soil organic phosphorus in tropical forests: an assessment of the NaOH–EDTA extraction procedure for quantitative analysis by solution 31P NMR spectroscopy. Eur J Soil Sci 59:453–466

    Article  Google Scholar 

  • Turner BL, Richardson AE (2004) Identification of scyllo-inositol phosphates in soil by solution phosphorus-31 nuclear magnetic resonance spectroscopy. Soil Sci Soc Am J 68:802–808

    Article  Google Scholar 

  • Turner BL, Mahieu N, Condron LM (2003a) Phosphorus-31 nuclear magnetic resonance spectral assignments of phosphorus compounds in soil NaOH–EDTA extracts. Soil Sci Soc Am J 67:497–510

    Article  Google Scholar 

  • Turner BL, Mahieu N, Condron LM (2003b) Quantification of myo-inositol hexakisphosphate in alkaline soil extracts by solution 31P NMR spectroscopy and spectral deconvolution. Soil Sci 168:469–478

    Article  Google Scholar 

  • Turner BL, Cade-Menun BJ, Westermann DT (2003c) Organic phosphorus composition and potential bioavailability in semi-arid arable soils of the western United States. Soil Sci Soc Am J 67:1168–1179

    Article  Google Scholar 

  • Turner BL, Baxter R, Mahieu N, Sjogersten S, Whitton BA (2004) Phosphorus compounds in subarctic Fennoscandian soils at the mountain birch (Betula pubescens)–tundra ecotone. Soil Biol Biochem 36:815–823

    Article  Google Scholar 

  • Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005) Extraction of soil organic phosphorus. Talanta 66:294–306

    Article  Google Scholar 

  • Turner BL, Newman S, Reddy KR (2006) Overestimation of organic phosphorus in wetland soils by alkaline extraction and molybdate colorimetry. Environ Sci Technol 40:3349–3354

    Article  Google Scholar 

  • Turner BL, Condron LM, Richardson SJ, Peltzer DA, Allison VJ (2007) Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–1181

    Article  Google Scholar 

  • Uriyo AP, Kesseba A (1975) Amounts and distribution of organic phosphorus in some soil profiles in Tanzania. Geoderma 13:201–210

    Article  Google Scholar 

  • Vincent AG, Turner BL, Tanner EVJ (2010) Soil organic phosphorus dynamics following perturbation of litter cycling in a tropical moist forest. Eur J Soil Sci 61:48–57

    Article  Google Scholar 

  • Vitousek PM, Sanford RLJ (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  Google Scholar 

  • Williams JDH, Walker TW (1967) Comparison of ‘ignition’ and ‘extraction’ methods for the determination of organic phosphate in rocks and soils. Plant Soil 27:457–459

    Article  Google Scholar 

  • Windsor DM (1990) Climate and moisture availability in a tropical forest, long term record for Barro Colorado Island, Panama. Smithson Contrib Earth Sci 29:1–145

    Google Scholar 

  • Woodring WP (1958) Geology of Barro Colorado Island. Smithson Miscellaneous Collect 135:1–39

    Google Scholar 

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Acknowledgements

We thank Alex Blumenfeld, Tania Romero, Eric Manzane and Antonio Cueto for technical support, Rick Condit for valuable discussion and calculation of rainfall estimates, Suzanne Lao for assistance with Fig. 1, Nikki Strong for analysis of rock samples from Rio Paja, Sarah Morón and Carlos Jaramillo for assistance in identification of parent materials, and Alex Cheesman for comments on the manuscript. B.M.J.E. was supported by a grant from the German Science Foundation (DFG). The Panama National Environmental Authority (ANAM) granted permission to sample within National Parks.

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  1. Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama

    Benjamin L. Turner & Bettina M. J. Engelbrecht

  2. Department of Biology, Chemistry and Geological Sciences, University of Bayreuth, 95440, Bayreuth, Germany

    Bettina M. J. Engelbrecht

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  1. Benjamin L. Turner
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Correspondence to Benjamin L. Turner.

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Turner, B.L., Engelbrecht, B.M.J. Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103, 297–315 (2011). https://doi.org/10.1007/s10533-010-9466-x

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