Advertisement

Biogeochemistry

, Volume 136, Issue 1, pp 91–102 | Cite as

Iron reduction: a mechanism for dynamic cycling of occluded cations in tropical forest soils?

  • Steven J. Hall
  • Wenjuan Huang
Article

Abstract

Nutrient cations can limit plant productivity in highly weathered soils, but have received much less attention than phosphorus and nitrogen. The reduction of iron (Fe) in anaerobic microsites of surface soils can solubilize organic matter and P sorbed or occluded with short-range-ordered (SRO) Fe phases. This mechanism might also release occluded cations. In the Luquillo Experimental Forest, Puerto Rico, we measured cation release during anaerobic laboratory incubations, and assessed patterns of cation availability in surface soils spanning ridge-slope-valley catenas. During anaerobic incubations, potassium (K), calcium (Ca) and magnesium (Mg) significantly increased with reduced Fe (Fe(II)) in both water and 0.5 M HCl extractions, but did not change during aerobic incubations. In the field, 0.5 M HCl-extractable Fe(II) and Fe(III) were the strongest predictors of K, Mg, and Ca on ridges (R2 0.57–0.75). Here, both Ca and Mg decreased with Fe(III), while K, Ca, and Mg increased with Fe(II), consistent with release of Fe-occluded cations following Fe reduction. Manganese in ridge soils was extremely low, consistent with leaching following reductive dissolution of Mn(IV). On slopes, soil C was the strongest cation predictor, consistent with the importance of organic matter for cation exchange in these highly weathered Oxisols. In riparian valleys, cation concentrations were up to 16-fold greater than in other topographic positions but were weakly or unrelated to measured predictors, potentially reflecting cation-rich groundwater. Predictors of cation availability varied with topography, but were consistent with the potential importance of microsite Fe reduction in liberating occluded cations, particularly in the highly productive ridges. This mechanism may explain discrepancies among indices of “available” soil cations and plant cation uptake observed in other tropical forests.

Keywords

Cation Luquillo Experimental Forest Iron Occluded Redox Walker-Syers model 

Notes

Acknowledgements

This work was supported by NSF grant DEB-1457805, by the NSF Luquillo Critical Zone Observatory, and by Iowa State University. SJH gratefully acknowledges mentorship by W. Silver on related research at this site. We thank A. Russell for discussion about the conceptual model, S. Rathke and S. Bakshi for assistance with ICP analyses, the USFS International Institute of Tropical Forestry for logistical support, and O. Gutierrez del Arroyo for collecting soil for the incubation experiment.

References

  1. Baribault TW, Kobe RK, Finley AO (2011) Tropical tree growth is correlated with soil phosphorus, potassium, and calcium, though not for legumes. Ecol Monogr 82:189–203. doi: 10.1890/11-1013.1 CrossRefGoogle Scholar
  2. Brinkman R (1970) Ferrolysis, a hydromorphic soil forming process. Geoderma 3:199–206. doi: 10.1016/0016-7061(70)90019-4 CrossRefGoogle Scholar
  3. Buettner SW, Kramer MG, Chadwick OA, Thompson A (2014) Mobilization of colloidal carbon during iron reduction in basaltic soils. Geoderma 221–222:139–145. doi: 10.1016/j.geoderma.2014.01.012 CrossRefGoogle Scholar
  4. Chacon 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. doi: 10.1007/s10533-005-2343-3 CrossRefGoogle Scholar
  5. Chadwick OA, Derry LA, Vitousek PM et al (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497. doi: 10.1038/17276 CrossRefGoogle Scholar
  6. Cleveland CC, Townsend AR, Taylor P et al (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947. doi: 10.1111/j.1461-0248.2011.01658.x CrossRefGoogle Scholar
  7. Cornell RM, Schwertmann U (1996) The Iron Oxides: Structure, Properties, Reactions. Occurrences and Uses. John Wiley & Sons, HobokenGoogle Scholar
  8. Cuevas E, Medina E (1988) Nutrient dynamics within Amazonian forests. II. Fine root growth, nutrient availability and leaf litter decomposition. Oecologia 76:222–235CrossRefGoogle Scholar
  9. Dubinsky EA, Silver WL, Firestone MK (2010) Tropical forest soil microbial communities couple iron and carbon biogeochemistry. Ecology 91:2604–2612. doi: 10.1890/09-1365.1 CrossRefGoogle Scholar
  10. Fabris JD, de Jesus Filho MF, Coey JMD et al (1997) Iron-rich spinels from Brazilian soils. Hyperfine Interact 110:23–32. doi: 10.1023/A:1012619331408 CrossRefGoogle Scholar
  11. Gee G, Bauder J (1986) Particle size analysis. In: Klute A (ed) Methods of soil analysis, Part 1, physical and mineralogical methods, 2nd edn. American Society of Agronomy, Madison, pp 383–411Google Scholar
  12. Ginn BR, Habteselassie MY, Meile C, Thompson A (2014) Effects of sample storage on microbial Fe-reduction in tropical rainforest soils. Soil Biol Biochem 68:44–51. doi: 10.1016/j.soilbio.2013.09.012 CrossRefGoogle Scholar
  13. Ginn B, Meile C, Wilmoth J et al (2017) Rapid iron reduction rates are stimulated by high-amplitude redox fluctuations in a tropical forest soil. Environ Sci Technol 51:3250–3259. doi: 10.1021/acs.est.6b05709 CrossRefGoogle Scholar
  14. Giovanoli R, Cornell RM (1992) Crystallization of metal substituted ferrihydrites. Z Für Pflanzenernähr Bodenkd 155:455–460. doi: 10.1002/jpln.19921550517 CrossRefGoogle Scholar
  15. Grybos M, Davranche M, Gruau G, Petitjean P (2007) Is trace metal release in wetland soils controlled by organic matter mobility or Fe-oxyhydroxides reduction? J Colloid Interface Sci 314:490–501. doi: 10.1016/j.jcis.2007.04.062 CrossRefGoogle Scholar
  16. Hall SJ, Silver WL (2015) Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest. Biogeochemistry 125:149–165. doi: 10.1007/s10533-015-0120-5 CrossRefGoogle Scholar
  17. Hall SJ, McDowell WH, Silver WL (2013) When wet gets wetter: decoupling of moisture, redox biogeochemistry, and greenhouse gas fluxes in a humid tropical forest soil. Ecosystems 16:576–589. doi: 10.1007/s10021-012-9631-2 CrossRefGoogle Scholar
  18. Hall SJ, Treffkorn J, Silver WL (2014) Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils. Ecology 95:2964–2973. doi: 10.1890/13-2151.1 CrossRefGoogle Scholar
  19. Hall SJ, Liptzin D, Buss HL et al (2016) Drivers and patterns of iron redox cycling from surface to bedrock in a deep tropical forest soil: a new conceptual model. Biogeochemistry 130:177–190. doi: 10.1007/s10533-016-0251-3 CrossRefGoogle Scholar
  20. Henderson R, Kabengi N, Mantripragada N et al (2012) Anoxia-induced release of colloid- and nanoparticle-bound phosphorus in grassland soils. Environ Sci Technol 46:11727–11734. doi: 10.1021/es302395r CrossRefGoogle Scholar
  21. Huang W, Hall SJ (2017) Optimized high-throughput methods for quantifying iron biogeochemical dynamics in soil. Geoderma 306:67–72. doi: 10.1016/j.geoderma.2017.07.013 CrossRefGoogle Scholar
  22. Jenny H, Leonard C (1934) Functional relationships between soil properties and rainfall. Soil Sci 38:363–381CrossRefGoogle Scholar
  23. 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. doi: 10.1007/s00442-002-1164-5 CrossRefGoogle Scholar
  24. Johnson AH, Xing HX, Scatena FN (2015) Controls on soil carbon stocks in El Yunque National Forest, Puerto Rico. Soil Sci Soc Am J 79:294. doi: 10.2136/sssaj2014.05.0199 CrossRefGoogle Scholar
  25. Kaspari M, Garcia MN, Harms KE et al (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43. doi: 10.1111/j.1461-0248.2007.01124.x Google Scholar
  26. Kleber M, Eusterhues K, Keiluweit M et al (2015) Mineral–organic associations: formation, properties, and relevance in soil environments. In: Advances in agronomy. Elsevier, pp 1–140Google Scholar
  27. Liptzin D, Silver WL (2009) Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil. Soil Biol Biochem 41:1696–1702CrossRefGoogle Scholar
  28. Liptzin D, Silver WL, Detto M (2011) Temporal dynamics in soil oxygen and greenhouse gases in two humid tropical forests. Ecosystems 14:171–182. doi: 10.1007/s10021-010-9402-x CrossRefGoogle Scholar
  29. Lloyd J, Domingues TF, Schrodt F et al (2015) Edaphic, structural and physiological contrasts across Amazon Basin forest–savanna ecotones suggest a role for potassium as a key modulator of tropical woody vegetation structure and function. Biogeosciences 12:6529–6571. doi: 10.5194/bg-12-6529-2015 CrossRefGoogle Scholar
  30. Lovley DR, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540Google Scholar
  31. Markewitz D, Davidson EA, de O Figueiredo R et al (2001) Control of cation concentrations in stream waters by surface soil processes in an Amazonian watershed. Nature 410:802–805. doi: 10.1038/35071052 CrossRefGoogle Scholar
  32. McBride MB (1978) Retention of Cu2+, Ca2+, Mg2+, and Mn2+ by amorphous alumina. Soil Sci Soc Am J 42:27. doi: 10.2136/sssaj1978.03615995004200010007x CrossRefGoogle Scholar
  33. McBride MB (1989) Reactions controlling heavy metal solubility in soils. In: Stewart BA (ed) Advances in Soil Science. Springer, New York, pp 1–56Google Scholar
  34. McDowell WH (1998) Internal nutrient fluxes in a Puerto Rican rain forest. J Trop Ecol 14:521–536CrossRefGoogle Scholar
  35. McDowell WH, Asbury CE (1994) Export of carbon, nitrogen, and major ions from three tropical montane watersheds. Limnol Oceanogr 39:111–125. doi: 10.4319/lo.1994.39.1.0111 CrossRefGoogle Scholar
  36. McDowell WH, Bowden WB, Asbury CE (1992) Riparian nitrogen dynamics in two geomorphologically distinct tropical rain forest watersheds: subsurface solute patterns. Biogeochemistry 18:53–75CrossRefGoogle Scholar
  37. McKenzie RM (1989) Manganese oxides and hydroxides. In: Dixon JB, Weed SB (eds) Minerals in soil environments, pp 439–465Google Scholar
  38. Pan W, Kan J, Inamdar S et al (2016) Dissimilatory microbial iron reduction release DOC (dissolved organic carbon) from carbon-ferrihydrite association. Soil Biol Biochem 103:232–240. doi: 10.1016/j.soilbio.2016.08.026 CrossRefGoogle Scholar
  39. Peretyazhko T, Sposito G (2005) Iron(III) reduction and phosphorous solubilization in humid tropical forest soils. Geochim Cosmochim Acta 69:3643–3652. doi: 10.1016/j.gca.2005.03.045 CrossRefGoogle Scholar
  40. Phillips IR, Greenway M (1998) Changes in water-soluble and exchangeable ions, cation exchange capacity, and phosphorus max in soils under alternating waterlogged and drying conditions. Commun Soil Sci Plant Anal 29:51–65. doi: 10.1080/00103629809369928 CrossRefGoogle Scholar
  41. Pinheiro J, Bates D, DebRoy S et al (2014) nlme: linear and nonlinear mixed effects modelsGoogle Scholar
  42. Porder S, Johnson AH, Xing HX et al (2015) Linking geomorphology, weathering and cation availability in the Luquillo Mountains of Puerto Rico. Geoderma 249–250:100–110. doi: 10.1016/j.geoderma.2015.03.002 CrossRefGoogle Scholar
  43. Ramirez Romero G (1950) Exchangeable cations extracted by 0.1 N hydrochloric acid and ammonium acetate in soils of the Valle. Acta Agron 1:51–56Google Scholar
  44. Rietra RPJJ, Hiemstra T, van Riemsdijk WH (2001) Interaction between calcium and phosphate adsorption on goethite. Environ Sci Technol 35:3369–3374. doi: 10.1021/es000210b CrossRefGoogle Scholar
  45. Russell AE, Hall SJ, Raich JW (2017) Tree species impact cation dynamics in a tropical rainforest: a new conceptual framework. Ecol Monogr. doi: 10.1002/ecm.1274 Google Scholar
  46. Sanchez PA (1976) Properties and management of soils in the tropics. Wiley, New YorkGoogle Scholar
  47. Scatena FN, Lugo AE (1995) Geomorphology, disturbance, and the soil and vegetation of two subtropical wet steepland watersheds of Puerto Rico. Geomorphology 13:199–213. doi: 10.1016/0169-555X(95)00021-V CrossRefGoogle Scholar
  48. Schwertmann U (1991) Solubility and dissolution of iron oxides. Plant Soil 130:1–25CrossRefGoogle Scholar
  49. Silver WL, Vogt KA (1993) Fine-root dynamics following single and multiple disturbances in a subtropical wet forest ecosystem. J Ecol 81:729–738CrossRefGoogle Scholar
  50. Silver WL, Scatena FN, Johnson AH et al (1994) Nutrient availability in a montane wet tropical forest—spatial patterns and methodological considerations. Plant Soil 164:129–145CrossRefGoogle Scholar
  51. Singh KD, Goulding KWT, Sinclair AH (1983) Assessment of potassium in soils. Commun Soil Sci Plant Anal 14:1015–1033. doi: 10.1080/00103628309367429 CrossRefGoogle Scholar
  52. Soil Survey Staff (2002) Soil survey of Caribbean National Forest and Luquillo Experimental Forest, Commonwealth of Puerto Rico. United States Department of Agriculture, Natural Resources Conservation ServiceGoogle Scholar
  53. Taylor RM, Graley AM (1967) The influence of ionic environment on the nature of iron oxides in soils. J Soil Sci 18:341–348. doi: 10.1111/j.1365-2389.1967.tb01512.x CrossRefGoogle Scholar
  54. Thompson A, Chadwick OA, Boman S, Chorover J (2006) Colloid mobilization during soil iron redox oscillations. Environ Sci Technol 40:5743–5749. doi: 10.1021/es061203b CrossRefGoogle Scholar
  55. Thompson A, Rancourt D, Chadwick O, Chorover J (2011) Iron solid-phase differentiation along a redox gradient in basaltic soils. Geochim Cosmochim Acta 75:119–133. doi: 10.1016/j.gca.2010.10.005 CrossRefGoogle Scholar
  56. Tishchenko V, Meile C, Scherer MM et al (2015) Fe2 + catalyzed iron atom exchange and re-crystallization in a tropical soil. Geochim Cosmochim Acta 148:191–202. doi: 10.1016/j.gca.2014.09.018 CrossRefGoogle Scholar
  57. Unger M, Leuschner C, Homeier J (2010) Variability of indices of macronutrient availability in soils at different spatial scales along an elevation transect in tropical moist forests (NE Ecuador). Plant Soil 336:443–458. doi: 10.1007/s11104-010-0494-z CrossRefGoogle Scholar
  58. Vitousek P, Sanford R (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167CrossRefGoogle Scholar
  59. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19. doi: 10.1016/0016-7061(76)90066-5 CrossRefGoogle Scholar
  60. Wright SJ, Yavitt JB, Wurzburger N et al (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625. doi: 10.1890/10-1558.1 CrossRefGoogle Scholar
  61. Yi-Balan SA, Amundson R, Buss HL (2014) Decoupling of sulfur and nitrogen cycling due to biotic processes in a tropical rainforest. Geochim Cosmochim Acta 142:411–428. doi: 10.1016/j.gca.2014.05.049 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA

Personalised recommendations