Skip to main content
Log in

Sulfur dynamics during long-term ecosystem development

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Long-term soil and ecosystem development involves predictable changes in nitrogen (N) and phosphorus (P) availability and limitation, but far less is known about comparable changes in sulfur (S) despite its importance as an essential plant macronutrient and component of soil organic matter. We used a combination of elemental analysis, X-ray absorption spectroscopy, hydrolytic enzyme assays, and stable S isotope ratios to examine S in soil and leaf tissue along the 120,000-year Franz Josef chronosequence, New Zealand. Total soil S concentrations increased during the early stages of pedogenesis and then declined as soils aged. There was little variation in soil N:S ratios along the chronosequence other than in the youngest (5 year old) soil, although the carbon (C):S ratio increased markedly in the oldest soils and the P:S ratio decreased continuously along the chronosequence. Foliar S concentrations and N:S ratios varied widely among common plant species but did not change consistently with increasing soil age, although foliar P:S declined for several species in the older stages of the chronosequence. The chemical nature of soil organic S extracted from mineral and organic horizons and determined by S K-edge X-ray absorption near-edge fine-structure (XANES) spectroscopy was dominated by C-bonded S distributed approximately equally in highly-reduced and intermediate oxidation states, although ester-bonded S was also abundant throughout the chronosequence. Soil sulfatase activity expressed on a soil C basis was highest in young soils, indicating low S availability in the early stage of pedogenesis. Enzymatic C:S and N:S ratios varied little during ecosystem development, although the enzymatic P:S ratio increased continuously along the chronosequence. Stable S isotope ratios (δ34S) increased along the chronosequence, particularly in the early stages of pedogenesis, reflecting a shift in S inputs from primary mineral S to oceanic sulfate in atmospheric deposition. Overall, this first comprehensive assessment of S along a long-term soil chronosequence suggests that S availability is low in the earliest stage of pedogenesis, but then remains stable throughout the progressive and retrogressive phases of ecosystem development, despite pronounced shifts in the chemistry and dynamics of other nutrients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781

    Article  Google Scholar 

  • Almond PC, Moar NT, Lian OB (2001) Reinterpretation of the glacial chronology of South Westland, New Zealand. N Z J Geol Geophys 44:1–15

    Article  Google Scholar 

  • Bern CR, Townsend AR (2008) Accumulation of atmospheric sulfur in some Costa Rican soils. J Geophys Res 113:G03001

    Article  Google Scholar 

  • Bern CR, Chadwick OA, Kendall C, Pribil MJ (2015) Steep gradients of volcanic and marine sulfur in Hawaiian rainfall and ecosystems. Sci Total Environ 514:250–260

    Article  Google Scholar 

  • Bol R, Eriksen J, Smith P, Garnett MH, Coleman K, Christensen BT (2005) The natural abundance of 13C, 15N, 34S and 14C in archived (1923–2000) plant and soil samples from the Askov long-term experiments on animal manure and mineral fertilizer. Rapid Commun Mass Spectrom 19:3216–3226

    Article  Google Scholar 

  • Bünemann EK, Condron LM (2007) Phosphorus and sulphur cycling in terrestrial ecosystems. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Soil biology, vol 10. Springer-Verlag, New York, pp 65–94

    Chapter  Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR (2001) Effects of land-use change from grassland to forest on soil sulfur and arylsulfatase activity in New Zealand. Soil Res 39:749–757

    Article  Google Scholar 

  • Coomes DA, Bentley W, Tanentzap A, Burrows L (2013) Soil drainage and phosphorus depletion contribute to retrogressive succession along a New Zealand chronosequence. Plant Soil 367:77–91

    Article  Google Scholar 

  • Dijkshoorn W, van Wijk L (1967) The sulphur requirements of plants as evidenced by the sulphur-nitrogen ratio in the organic matter. A review of published data. Plant Soil 26:129–157

    Article  Google Scholar 

  • Forsyth DM, Coomes DA, Nugent G, Hall GM (2002) Diet and diet preferences of introduced ungulates (Order: Artiodactyla) in New Zealand. N Z J Zool 29:323–343

    Article  Google Scholar 

  • Freney JR, Williams CH (1983) The sulfur cycle in soil. In: Ivanov MV, Freney JR (eds) The global biogeochemical sulphur cycle. Scientific Committee on Problems of the Environment (SCOPE) 19. Wiley, Chichester, pp 129–201

    Google Scholar 

  • Gertheiss J (2014) ANOVA for factors with ordered levels. J Agric Biol Environ Stat 19:258–277

    Article  Google Scholar 

  • Haneklaus S, Bloem E, Schnug E (2007) Sulfur interactions in crop ecosystems. In: Hawkesford MJ, De Kok LJ (eds) Sulfur in plants—an ecological perspective. Springer, Berlin, pp 17–58

    Chapter  Google Scholar 

  • Hell R, Kruse C (2007) Sulfur in biotic interactions of plants. In: Hawkesford MJ, De Kok LJ (eds) Sulfur in plants—an ecological perspective. Springer, Berlin, pp 197–224

    Chapter  Google Scholar 

  • Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666

    Article  Google Scholar 

  • Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371

    Article  Google Scholar 

  • Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963

    Article  Google Scholar 

  • Jangid K, Whitman WB, Condron LM, Turner BL, Williams MA (2013) Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415–3424

    Article  Google Scholar 

  • Jehne W, Thompson CH (1981) Endomycorrhizae in plant colonization on sand-dunes at Cooloola, Australia. Aust J Ecol 6:221–230

    Article  Google Scholar 

  • Johnson DW (1984) Sulfur cycling in forests. Biogeochemistry 1:29–43

    Article  Google Scholar 

  • Kelly J, Lambert MJ (1972) The relationship between sulphur and nitrogen in the foliage of Pinus radiata. Plant Soil 37:395–407

    Article  Google Scholar 

  • Kirkby CA, Kirkegaard JA, Richardson AE, Wade LJ, Blanchard C, Batten G (2011) Stable soil organic matter: A comparison of C:N:P:S ratios in Australian and other world soils. Geoderma 163:197–208

    Article  Google Scholar 

  • Krouse HR, Coplen TB (1997) Reporting of relative sulfur isotope-ratio data. Pure Appl Chem 69:293–295

    Article  Google Scholar 

  • Krouse HR, Stewart JWB, Grinenko VA (1991) Pedosphere and biosphere. In: Krouse HR, Grinenko VA (eds) Stable isotopes in the assessment of natural and anthropogenic sulphur in the environment. Wiley, Chichester, pp 267–306

    Google Scholar 

  • Kusakabe MTA, Rafter TA, Stout JD, Collie TW (1976) Sulphur isotopic variations in nature. 12. Isotopic ratios of sulphur extracted from some plants, soils and related materials. N Z J Sci 19:433–440

    Google Scholar 

  • Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll K-H, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–642

    Article  Google Scholar 

  • Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–1605

    Article  Google Scholar 

  • Lambert MJ, Turner J (1998) Sulfur nutrition and cycling in Southern Hemisphere temperate and subtropical forest ecosystems. In: Maynard DG (ed) Sulfur in the environment. Marcel Dekker Inc, New York, pp 263–293

    Google Scholar 

  • Ledgard SF, Upsdell MP (1991) Sulphur inputs from rainfall throughout New Zealand. N Z J Agric Res 34:105–111

    Article  Google Scholar 

  • Lee WG (1988) Mineral element concentrations in foliage and bark of woody species on Auckland Island, New Zealand. N Z J Ecol 11:109–111

    Google Scholar 

  • Lee WG, Johnson PN (1984) Mineral element concentrations in foliage of divaricate and non-divaricate Coprosma species. N Z J Ecol 7:169–174

    Google Scholar 

  • Lehmann J, Solomon D, Zhao F-J, McGrath SP (2008) Atmospheric SO2 emissions since the late 1800 s change organic sulfur forms in humic substance extracts of soils. Environ Sci Technol 42:3550–3555

    Article  Google Scholar 

  • Marschner H (2006) Mineral nutrition of higher plants. Academic Press, San Diego

    Google Scholar 

  • Mathot M, Mertens J, Verlinden G, Lambert R (2008) Positive effects of sulphur fertilisation on grasslands yields and quality in Belgium. Eur J Agron 28:655–658

    Article  Google Scholar 

  • Mayer B, Feger KH, Giesemann A, Jäger H-J (1995) Interpretation of sulfur cycling in two catchments in the Black Forest (Germany) using stable sulfur isotopes and oxygen isotope data. Biogeochemistry 30:31–58

    Article  Google Scholar 

  • Maynard DG, Stewart JWB, Bettany JR (1984) Sulfur cycling in grassland and parkland soils. Biogeochemistry 1:97–111

    Article  Google Scholar 

  • McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S, and P through soil organic matter. Geoderma 26:267–286

    Article  Google Scholar 

  • McGrath SP, Zhao FJ (1995) A risk assessment of sulphur deficiency in cereals using soil and atmospheric deposition data. Soil Use Manag 11:110–114

    Article  Google Scholar 

  • Mitchell MJ, David MB, Harrison RB (1992) Sulphur dynamics of forest ecosystems. In: Howarth RW, Stewart JWB, Ivanov MV (eds) SCOPE 48: sulfur cycling on the continents. Wiley, New York, pp 215–254

    Google Scholar 

  • Morra MJ, Fendorf SE, Brown PD (1997) Speciation of S in humic and fulvic acids using X-ray absorbtion near-edge structure (XANES) spectroscopy. Geochim Cosmochim Acta 61:683–688

    Article  Google Scholar 

  • Parfitt RL, Smart RSC (1978) The mechanism of sulfate adsorption on iron oxides. Soil Sci Soc Am J 42:48–50

    Article  Google Scholar 

  • Parfitt RL, Ross DJ, Coomes DA, Richardson SJ, Smale MC, Dahlgren RA (2005) N and P in New Zealand soil chronosequences and relationships with foliar N and P. Biogeochemistry 75:305–328

    Article  Google Scholar 

  • Parton WJ, Stewart JWB, Cole CV (1988) Dynamics of C, N, P and S in grassland soils: a model. Biogeochemistry 5:109–131

    Article  Google Scholar 

  • Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR (2010) Understanding ecosystem retrogression. Ecol Monogr 80:509–529

    Article  Google Scholar 

  • Prietzel J, Thieme J, Salome M, Knicker H (2007) Sulfur K-edge XANES spectroscopy reveals differences in sulfur speciation of bulk soils, humic acid, fulvic acid, and particle size seperates. Soil Biol Biochem 39:877–890

    Article  Google Scholar 

  • Prietzel J, Wu Y, Dümig A, Zhou J, Klysubun W (2013) Soil sulphur speciation in two glacier forefield soil chronosequences assessed by S K-edge XANES spectroscopy. Eur J Soil Sci 64:260–272

    Article  Google Scholar 

  • Reimann C, Koller F, Frengstad B, Kashulina G, Niskavaara H, Englmaier P (2003) Total sulphur in leaves of several plant species from nine catchments within a 1,500,000 km2 area in northern Europe: local vs. regional variability. Geochem 3:205–215

    Google Scholar 

  • Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139:267–276

    Article  Google Scholar 

  • Richardson SJ, Peltzer DA, Allen RB, McGlone MS (2005) Resorption proficiency along a chronosequence: responses among communities and within species. Ecology 86:20–25

    Article  Google Scholar 

  • Schmalenberger A, Noll M (2010) Shifts in desulfonating bacterial communities along a soil chronosequence in the forefield of a receding glacier. FEMS Microbiol Ecol 71:208–217

    Article  Google Scholar 

  • Schroth AW, Bostick BC, Graham M, Kaste JM, Mitchell MJ, Friedland AJ (2007) Sulfur species behavior in soil organic matter during decomposition. J Geophys Res 112:G04011

    Article  Google Scholar 

  • Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–799

    Article  Google Scholar 

  • Smith GS, Cornforth IS, Henderson HV (1985) Critical leaf concentrations for deficiencies of nitrogen, potassium, phosphorus, sulphur, and magnesium in perennial ryegrass. New Phytol 101:393–409

    Article  Google Scholar 

  • Solomon D, Lehmann J, Martínez CE (2003) Sulfur K-edge XANES spectroscopy as a tool for understanding sulfur dynamics in soil organic matter. Soil Sci Soc Am J 67:1721–1731

    Article  Google Scholar 

  • Solomon D, Lehmann J, Kinyangi J, Pell A, Theis J, Riha S, Ngoze S, Amelung W, Preez C, Machado S, Ellert B, Janzen H (2009) Anthropogenic and climate influences on biogeochemical dynamics and molecular-level speciation of soil sulfur. Ecol Appl 19:989–1002

    Article  Google Scholar 

  • Stevens PR (1968) A chronosequence of soils near the Franz Josef glacier. PhD thesis, Lincoln College. University of Canterbury, Canterbury, New Zealand, p 389

  • Stevenson FJ, Cole MA (1999) Cycles of soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, Chichester

    Google Scholar 

  • Sutherland MD (1947) The odour of Coprosma foetidissima. N Z J Sci Technol 29:94–99

    Google Scholar 

  • Syers JK, Adams JA, Walker TW (1970) Accumulation of organic matter in a chronosequence of soils developed on wind-blown sand in New Zealand. J Soil Sci 21:146–153

    Article  Google Scholar 

  • Tabatabai MA (1996) Sulfur. In: Sparks DL (ed) Methods of soil analysis, part 3—chemical methods. Soil Science Society of America and the American Society of Agronomy, Madison, pp 921–960

    Google Scholar 

  • Tanikawa T, Hashimoto Y, Yamaguchi N, Ito Y, Fukushima S, Kanda K, Uemura M, Hasegawa T, Takahashi M, Yoshinaga S (2014) Sulfur accumulation in Melanudands during development by upbuilding pedogenesis since 14–15 cal. ka. Geoderma 232–234:609–618

    Article  Google Scholar 

  • Turner BL, Condron LM (2013) Pedogenesis, nutrient dynamics, and ecosystem development: the legacy of T.W. Walker and J.K. Syers. Plant Soil 367:1–10

    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 

  • Turner BL, Lambers H, Condron LM, Cramer MD, Leake JR, Richardson AE, Smith SE (2013) Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant Soil 367:225–234

    Article  Google Scholar 

  • Vet R, Artz RS, Carou S, Shaw M, Ro C-U, Aas W, Baker A, Bowersox VC, Dentener F, Galy-Lacaux C, Hou A, Pienaar JJ, Gillett R, Forti MC, Gromov S, Hara H, Khodzher T, Mahowald NM, Nickovic S, Rao PSP, Reid NW (2014) A global assessment of precipitation chemistry and deposition of sulfur, nitrogen, sea salt, base cations, organic acids, acidity and pH, and phosphorus. Atmos Environ 93:3–100

    Article  Google Scholar 

  • Vitousek PM (2004) Nutrient cycling and limitation. Princeton University Press, Princeton

    Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    Article  Google Scholar 

  • Vitousek PM, Matson P, Van Cleve K (1989) Nitrogen availability and nitrification during succession: primary, secondary, and old-field seres. Plant Soil 115:229–239

    Article  Google Scholar 

  • Walker TW, Adams AFR (1958) Studies on soil organic matter: I. influence of phosphorus content of parent materials on accumulations of carbon, nitrogen, sulfur, and organic phosphorus in grassland soils. Soil Sci 85:307–318

    Article  Google Scholar 

  • Walker TW, Adams AFR (1959) Studies on soil organic matter: 2: Influence of increased leaching at various stages of weathering on levels of carbon, nitrogen, sulfur, and organic and total phosphorus. Soil Sci 87:1–10

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wardle P (1980) Primary succession in Westland National Park and its vicinity, New Zealand. N Z J Bot 18:221–232

    Article  Google Scholar 

  • Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–513

    Article  Google Scholar 

  • Williamson WM, Wardle DA, Yeates GW (2005) Changes in soil microbial and nematode communities during ecosystem decline across a long-term chronosequence. Soil Biol Biochem 37:1289–1301

    Article  Google Scholar 

  • Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus or nitrogen limit root allocation, tree growth and litter production in a lowland tropical forest. Ecology 92:1616–1625

    Article  Google Scholar 

  • Wu J, O’Donnell AG, He ZL, Syers JK (1994) Fumigation-extraction method for the measurement of soil microbial biomass-S. Soil Biol Biochem 26:117–125

    Article  Google Scholar 

  • Xia K, Weesner F, Bleam WF, Bloom PR, Skyllberg UL, Helmke PA (1998) XANES studies of oxidation states in aquatic and soil humic substances. Soil Sci Soc Am J 62:1240–1246

    Article  Google Scholar 

  • Zhao FJ, Wu J, McGrath SP (1996) Soil organic sulphur and its turnover. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier Science, Amsterdam, pp 467–506

    Chapter  Google Scholar 

  • Zhao FJ, Lehmann J, Solomon D, Fox MA, McGrath SP (2006) Sulphur speciation and turnover in soils: evidence from sulphur K-edge XANES spectroscopy and isotope dilution studies. Soil Biol Biochem 38:1000–1007

    Article  Google Scholar 

Download references

Acknowledgments

We thank Roger Cresswell for analytical support, Victoria Allison for assistance with sample collection, and Milton Solano and Ian Baillie for assistance in producing Fig. 1. The XANES measurements were supported by the National Research Initiative of the USDA–CSREES (2002-35107-122269). We thank W. Caliebe and S. Khalid for support during spectroscopic analyses. The XANES spectra were collected at the X-19A beam-line of the NSLS, Brookhaven National Laboratory, which is supported by the U.S. Department of Energy under the contract No. DE-AC02-76CH00016. Finally, we thank Carleton Bern and an anonymous reviewer for constructive criticism and insight that substantially improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benjamin L. Turner.

Additional information

Responsible Editor: Steven Perakis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 87 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turner, B.L., Condron, L.M., France, C.A.M. et al. Sulfur dynamics during long-term ecosystem development. Biogeochemistry 128, 281–305 (2016). https://doi.org/10.1007/s10533-016-0208-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-016-0208-6

Keywords

Navigation