A review of carbon isotopes of phytoliths: implications for phytolith-occluded carbon sources

  • Shilei Yang
  • Qian Hao
  • Hailong Wang
  • Lukas Van Zwieten
  • Changxun Yu
  • Taoze Liu
  • Xiaomin Yang
  • Xiaodong Zhang
  • Zhaoliang SongEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Review Article



Phytolith-occluded carbon (PhytOC) is mainly derived from the products of photosynthesis, which can be preserved in soils and sediments for hundreds-to-thousands of years due to the resilient nature of the amorphous phytolith silica. Therefore, stable and radioactive carbon (C) isotopes of phytoliths can be effectively utilized in paleoecological and archeological research. However, there still exists debate about the applicability of C isotopes of phytoliths, as a “two-pool” hypothesis to characterize PhytOC sources has been proposed, whereby a component of the PhytOC is derived from soil organic matter (SOM) absorbed through plant roots. Therefore, it is necessary to review this topic to better understand the source of PhytOC.

Materials and method

We introduce the stable and radioactive C isotopic compositions of PhytOC, present the impacts of different extraction methods on the study of PhytOC, and discuss the implications of these factors for determining the sources of PhytOC.

Results and discussion

Based on this review, we suggest that organic matter synthesized by photosynthesis is the main source of PhytOC. However, it is important to make clear whether and how SOM-derived C present in phytoliths influence the controversial “too-old” skew and isotopic fractionation.


Though the two-pool hypothesis has been proved by many researches, the carbon isotopes of phytoliths still have potential in paleoecology and archeology, because the main source is photosynthesis and many previous studies put forward the availability of these parameters. This review also shows that phytolith C isotopes may vary with different organic C compounds within phytoliths, which needs further study at the molecular scale. Different phytolith extraction methods can influence 14C dating results.


C3 and C4 plants δ1314C dating Phytolith extraction method 


Funding information

This work was supported by the National Natural Science Foundation of China [grant numbers 41930862, 41571130042, 41701049] and the State’s Key Project of Research and Development Plan of China [grant number 2016YFA0601002 and 2017YFC0212700].


  1. Agrawal S, Sanyal P, Sarkar A, Jaiswal MK, Dutta K (2012) Variability of Indian monsoonal rainfall over the past 100 ka and its implication for C3-C4 vegetational change. Quat Res 77:159–170CrossRefGoogle Scholar
  2. Alexandre A, Basile-Doelsch I, Delhaye T, Borshneck D, Mazur JC, Reyerson P, Santos GM (2015) New highlights of phytolith structure and occluded carbon location: 3-D X-ray microscopy and NanoSIMS results. Biogeosciences 12:863–873CrossRefGoogle Scholar
  3. Alexandre A, Balesdent J, Cazevieille P, Chevassus-Rosset C, Signoret P, Mazur JC, Harutyunyan A, Doelsch E, Basile-Doelsch I, Miche H, Santos GM (2016) Direct uptake of organically derived C by grass roots and allocation in leaves and phytoliths: 13C labeling evidence. Biogeosciences 13:1693–1703CrossRefGoogle Scholar
  4. Asscher Y, Weiner S, Boaretto E (2017) A new method for extracting the insoluble occluded C in archaeological and modern phytoliths: detection of 14C depleted C fraction and implications for radioC dating. J Archaeol Sci 78:57–65CrossRefGoogle Scholar
  5. Bartoli F, Wilding LP (1980) Dissolution of biogenic opal as a function of its physical and chemical properties. Soil Sci Soc Am J 44:873–878CrossRefGoogle Scholar
  6. Basu S, Agrawal S, Sanyal P, Mahato P, Kumar S, Sarkar A (2015) C isotopic ratios of modern C3-C4 plants from the gangetic plain, India and its implications to paleovegetational reconstruction. Palaeogeo Palaeoclim Palaeoecol 440:22–32CrossRefGoogle Scholar
  7. Blecker SW, Mcculley RL, Chadwick OA, Kelly EF (2006) Biologic cycling of silica across a grassland bioclimosequence. Global Biogeochem Cy 20:4253–4274CrossRefGoogle Scholar
  8. Bremond L, Alexandre A, Vela E, Guiot J (2004) Advantages and disadvantages of phytolith analysis for the reconstruction of Mediterranean vegetation: an assessment based on modern phytolith, pollen and botanical data (Luberon, France). Rev Paleobot Palynol 129:213–228CrossRefGoogle Scholar
  9. Carter JA (2009) Atmospheric C isotope signatures in phytolith-occluded C. Quat Int 193:20–29CrossRefGoogle Scholar
  10. Cerling TE, Quade J, Wang Y, Bowman JR (1989) C isotopes in soils and paleosols as ecology and palaeoecology indicators. Nature 341:138–139CrossRefGoogle Scholar
  11. Cerling TE, Wang Y, Quade J (1993) Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361:344–345CrossRefGoogle Scholar
  12. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158CrossRefGoogle Scholar
  13. Collister JW, Rieley G, Stern B, Eglinton G, Fry B (1994) Compound-specific δ13C analyses of leaf lipids from plants with differing photosynthetic pathways. Org Geochem 21:619–627CrossRefGoogle Scholar
  14. Corbineau R, Reyerson PE, Alexandre A, Santos GM (2013) Towards producing pure phytolith concentrates from plants that are suitable for C isotopic analysis. Rev Palaeobot Palynol 197:179–185CrossRefGoogle Scholar
  15. Currie HA (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 100:1383–1389CrossRefGoogle Scholar
  16. Elbaum R, Melamed-Bessudo C, Tuross N, Levy AA, Weiner S (2009) New methods to isolate organic materials from silicified phytoliths reveal fragmented glycoproteins but no DNA. Quat Int 193:11–19CrossRefGoogle Scholar
  17. Farquhar GD, And JRE, Hubick KT (2003) C isotope discrimination and photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  18. Ford CR, Wurzburger N, Hendrick RL, Teskey RO (2007) Soil DIC uptake and fixation in Pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal fungi. Tree Physiol 27:375–383CrossRefGoogle Scholar
  19. Freeman KH, Colarusso LA (2001) Molecular and isotopic records of C4 grassland expansion in the late Miocene. Geochim Cosmochim Ac 65:1439–1454CrossRefGoogle Scholar
  20. Gallagher KL, Alfonso-Garcia A, Sanchez J, Potma EO, Santos GM (2015) Plant growth conditions alter phytolith carbon. Front Plant Sci 6Google Scholar
  21. Gillon J, Yakir D (2001) Influence of carbonic anhydrase activity in terrestrial vegetation on the 18O content of atmospheric CO2. Science 291:2584–2587CrossRefGoogle Scholar
  22. Gröcke Darren R (2002) The C isotope composition of ancient CO2 based on higher-plant organic matter. Phil Trans R Soc Lond 360:633CrossRefGoogle Scholar
  23. Guo F, Song Z, Sullivan L, Wang H, Liu X, Wang X, Li ZM, Zhao YY (2015) Enhancing phytolith C sequestration in rice ecosystems through basalt powder amendment. Sci Bull 60:591–597CrossRefGoogle Scholar
  24. Hildebrandt TM, Nesi AN, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579CrossRefGoogle Scholar
  25. Hodson MJ (2019) The relative importance of cell wall and lumen phytoliths in carbon sequestration in soil: a hypothesis. Front Earth Sci 7Google Scholar
  26. Jones RL, Beavers AH (1964) Aspects of catenary and depth distribution of opal phytoliths in Illinois soils. Soil Sci Soc Amer Proc 28:413–416CrossRefGoogle Scholar
  27. Jones LHP, Milne AA, Wadham SM (1963) Studies of silica in the oat plant:II. Distribution of the silica in the plant. Plant Soil 18:358–371CrossRefGoogle Scholar
  28. Kelly EF, Amundson RG, Marino BD, Deniro MJ (1991) Stable isotope ratios of C in phytoliths as a quantitative method of monitoring vegetation and climate change. Quat Res 35:222–233CrossRefGoogle Scholar
  29. Krull ES, Skjemstad JO, Graetz D, Grice K, Dunning W, Cook G, Parr JF (2003) 13C depleted charcoal from C4 grasses and the role of occluded C in phytoliths. Org Geochem 34:1337–1352CrossRefGoogle Scholar
  30. Latorre C, Quade J, Mcintosh WC (1997) The expansion of C4 grasses and global change in the late Miocene: stable isotope evidence from the Americas. Earth Planet Sc Lett 146:83–96CrossRefGoogle Scholar
  31. Li R, Xie S, Gu Y (2010) Advances in the biogeochemical study of phytolith stable isotope. Adv Earth Sci 25:812–819Google Scholar
  32. Li Z, Song Z, Cornelis JT (2014) Impact of rice cultivar and organ on elemental composition of phytoliths and the release of bio-available silicon. Front Plant Sci 5Google Scholar
  33. Lü H, Wang Y, Wang G, Yang H, Zhen LI (2000) Analysis of C isotope in phytoliths from C3 and C4 plants and modern soils. Chin Sci Bull 45:1804–1808CrossRefGoogle Scholar
  34. Madella M, Lancelotti C (2012) Taphonomy and phytoliths: a user manual. Quat Int 275:76–83CrossRefGoogle Scholar
  35. McClaran And Umlauf (2000) Desert grassland dynamics estimated from C isotopes in grass phytoliths and soil organic matter. J Veg Sci 11:71–76Google Scholar
  36. McMichael CH, Bush MB, Piperno DR, Silman MR, Zimmerman AR, Anderson C (2012) Spatial and temporal scales of pre-Columbian disturbance associated with western Amazonianlakes. Holocene 22: 131e141.CrossRefGoogle Scholar
  37. Nasholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, Hogberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916CrossRefGoogle Scholar
  38. Pan W, Song Z, Liu H, Van Zwieten L, Li Y, Yang X, Han Y, Liu X, Zhang X, Xu Z, Wang H (2017) The accumulation of phytolith-occluded C in soils of different grasslands. J Soils Sediments 17:2420–2427CrossRefGoogle Scholar
  39. Parr JF, Sullivan LA (2005) Soil C sequestration in phytoliths. Soil Biol Biochem 37:117–124CrossRefGoogle Scholar
  40. Parr JF, Sullivan LA (2011) Phytolith occluded C and silica variability in wheat cultivars. Plant Soil 342:165–171CrossRefGoogle Scholar
  41. Parr JF, Dolic V, Lancaster G, Boyd WE (2001a) A microwave digestion method for the extraction of phytoliths from her-barium specimens. Rev Palaeobot Palynol 116:203–212CrossRefGoogle Scholar
  42. Parr JF, Lentfer CJ, Boyd WE (2001b) A comparative analysis of wet and dry ashing techniques for the extraction of phytoliths from plant material. J Archaeol Sci 28:875–886CrossRefGoogle Scholar
  43. Parr JF, Boyd WE (2002) The probable industrial origin of archae-ological daub at an iron age site in Northeast Thailand. Geoarchaeology 17:285–303 CrossRefGoogle Scholar
  44. Parr JF, Sullivan LA (2014) Comparison of two methods for the isolation of phytolith occluded C from plant material. Plant Soil 374:45–53CrossRefGoogle Scholar
  45. Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. P Natl Acad Sci USA 105:4524–4529CrossRefGoogle Scholar
  46. Piperno DR (1990) Phytolith analysis: an archaeological and geological perspective. Arct Alp Res 54Google Scholar
  47. Piperno DR (2006) Phytoliths: a comprehensive guide for archaeologists and paleoecologists. AltaMira Press, LanhamGoogle Scholar
  48. Piperno DR (2015) Phytolith radioCarbon dating in archaeological and paleoecological research: a case study of phytoliths from modern neotropical plants and a review of the previous dating evidence. J Archaeol Sci 68:54–61CrossRefGoogle Scholar
  49. Piperno DR (2016) Standard evaluations of bomb curves and age calibrations along with consideration of environmental and biological variability show the rigor of phytolith dates on modern neotropical plants: review of comment by Santos, Alexandre, and prior. J Archaeol Sci 71:59–67CrossRefGoogle Scholar
  50. Piperno DR, Becker P (1996) Vegetational history of a site in the central amazon basin derived from phytolith and charcoal records from natural soils. Quat Res 45:202–209CrossRefGoogle Scholar
  51. Piperno DR, Stothert KE (2003) Phytolith evidence for early Holocene cucurbita domestication in Southwest Ecuador. Science 299:1054–1057CrossRefGoogle Scholar
  52. Quade J, Cerling TE (1995) Expansion of C4 grasses in the Late Miocene of northern Pakistan: evidence from stable isotopes in paleosols. Palaeogeo Palaeoclim Palaeoecol 115:91–116CrossRefGoogle Scholar
  53. Quade J, Cerling TE, Bowman JR (1989) Development of Asian monsoon revealed by marked ecological shift during the latest Miocene in northern Pakistan. Nature 342:163–166CrossRefGoogle Scholar
  54. Reyerson PE, Alexandre A, Harutyunyan A, Corbineau R, Martinez De La Torre HA, Badeck F, Cattivelli L, Santos GM (2016) Unambiguous evidence of old soil C in grass biosilica particles. Biogeosciences 13:1269–1286CrossRefGoogle Scholar
  55. Sage RF, Li M, Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 551–584CrossRefGoogle Scholar
  56. Santos GM, Alexandre A, Coe HHG, Reyerson PE, Southon J, De Carvalho CN (2010a) The phytolith 14C puzzle: a tale of background determinations and accuracy tests. RadioC 52:113–128CrossRefGoogle Scholar
  57. Santos GM, Southon JR, Drenzek NJ, Ziolkowski LA, Druffel E, Xu X, Zhang D, Trumbore S, Eglinton TI, Hughen KA (2010b) Blank assessment for ultra-small radiocarbon samples: chemical extraction and separation versus AMS. RadioC 52:1322–1335CrossRefGoogle Scholar
  58. Santos GM, Alexandre A, Southon JR, Treseder KK, Corbineau R, Reyerson PE (2012a) Possible source of ancient C in phytolith concentrates from harvested grasses. Biogeosciences 9:1873–1884CrossRefGoogle Scholar
  59. Santos GM, Southon JR, Alexandre A, Treseder KK, Corbineau R, Reyerson PE (2012b) Interactive comment on “comment on possible source of ancient C in phytolith concentrates from harvested grasses” by GM Santos et al., by LA Sullivan and JF Parr. Biogeosciences 9:6114–6124Google Scholar
  60. Santos GM, Masion A, Alexandre A (2018) When the carbon being dated is not what you think it is: insights from phytolith carbon research. Quaternary Sci Rev 197:162–174CrossRefGoogle Scholar
  61. Sanyal P, Bhattacharya SK, Kumar R, Ghosh SK, Sangode SJ (2004) Mio–pliocene monsoonal record from himalayan foreland basin (indian siwalik) and its relation to vegetational change. Palaeogeo Palaeoclim Palaeoeco 205:23–41CrossRefGoogle Scholar
  62. Sanyal P, Sarkar A, Bhattacharya SK, Kumar R, Ghosh SK, Agrawal S (2010) Intensification of monsoon, microclimate and asynchronous C4 appearance: isotopic evidence from the Indian siwalik sediments. Palaeogeo Palaeoclim Palaeoecol 296:165–173CrossRefGoogle Scholar
  63. Shillito LM (2013) Grains of truth or transparent blindfolds? A review of current debates in archaeological phytolith analysis. Veg Hist Archaeobot 22:71–82CrossRefGoogle Scholar
  64. Smith FA, Anderson KB (2001) Characterization of organic compounds in phytoliths: improving the resolving power of phytolith δ13C as a tool for paleoecological reconstruction of C3 and C4 grasses. In: Meunier JD, Colin F (eds) Phytoliths: applications in earth science and human history. A.A. Balkema Publishers, Rotterdam, pp 317–327Google Scholar
  65. Smith FA, White JWC (2004) Modern calibration of phytolith C isotope signatures for C3/C4 paleograssland reconstruction. Palaeogeo Palaeoclim Palaeoecol 207:277–304CrossRefGoogle Scholar
  66. Song Z, Liu H, Li B, Yang X (2013a) The production of phytolith-occluded C in China's forests: implications to biogeochemical C sequestration. Glob Chang Biol 19:2907–2915CrossRefGoogle Scholar
  67. Song Z, Parr JF, Guo F (2013b) Potential of global cropland phytolith C sink from optimization of cropping system and fertilization. PLoS One 8:e73747CrossRefGoogle Scholar
  68. Song Z, Mcgrouther K, Wang H (2016a) Occurrence, turnover and C sequestration potential of phytoliths in terrestrial ecosystems. Earth-Sci Rev 158:19–30CrossRefGoogle Scholar
  69. Song Z, Mcgrouther K, Wang H (2016b) High potential of phytoliths in terrestrial C sequestration at a centennial–millennial scale: reply to comments by Santos and Alexandre, Earth-Sci Rev
  70. Strömberg CAE (2004) Using phytolith assemblages to reconstruct the origin and spread of grass-dominated habitats in the Great Plains of North America during the late Eocene to early Miocene. Palaeogeogr Palaeoclimatol Palaeoecol 207:239–275CrossRefGoogle Scholar
  71. Sullivan LA, Parr JF (2008) Bomb pulse dating of phytolith-occluded carbon for quantification of carbon sequestration in perennial vegetation, Progress Report no. AINGRA08061, AINSE-Australian Institute of Nuclear Science and Engineering, Lucas Heights, AustraliaGoogle Scholar
  72. Sullivan LA, Parr JF (2013) Comment on “possible source of ancient C in phytolith concentrates from harvested grasses” by GM Santos et al. (2012). Biogeosciences 10:977–980CrossRefGoogle Scholar
  73. Talbot JM, Treseder KK (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53:169–179CrossRefGoogle Scholar
  74. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963CrossRefGoogle Scholar
  75. Wallis LA (2001) Environmental history of Northwest Australia based on phytolith analysis at Carpenter’s gap 1. Quat Int 83-85:103–117CrossRefGoogle Scholar
  76. Wang Y, Amundson R, Trumbore S (1996) Radiocarbon dating of soil organic matter. Quat Res 45:282–288CrossRefGoogle Scholar
  77. Watling KM, Parr JF, Rintoul L, Brown CL, Sullivan LA (2011) Raman, infrared and XPS study of bamboo phytoliths after chemical digestion. Spectrochim Acta A 80:106–111CrossRefGoogle Scholar
  78. Webb EA, Longstaffe FJ (2010) Limitations on the climatic and ecological signals provided by the δ13C values of phytoliths from a C4 north American prairie grass. Geochim Cosmochim Ac 74:3041–3050CrossRefGoogle Scholar
  79. Wilding LP (1967) RadioCarbon dating of biogenetic opal. Science 156:66–67CrossRefGoogle Scholar
  80. Yin J, Yang X, Zheng Y (2014) Influence of increasing combustion temperature on the AMS 14C dating of modern crop phytoliths. Sci Rep 4:6511–6514CrossRefGoogle Scholar
  81. Zhang X, Song Z, Zhao Z, van Zwieten L, Li J, Liu L, Xu S, Wang H (2017) Impact of climate and lithology on soil phytolith-occluded C accumulation in eastern China. J Soils Sediments 17:481–490CrossRefGoogle Scholar
  82. Zhang X, Song Z, Hao Q, Wang Y, Ding F, Song A (2019) Phytolith-occluded carbon storages in Forest litter layers in southern China: implications for evaluation of long-term forest carbon budget. Front Plant Sci.
  83. Zuo X, Lu H (2011) Carbon sequestration within millet phytoliths from dry-farming of crops in China. Chin Sci Bull 56: 3451–3456CrossRefGoogle Scholar
  84. Zuo X, Lu H, Gu Z (2014) Distribution of soil phytolith-occluded C in the Chinese loess plateau and its implications for silica-C cycles. Plant Soil 374:223–232CrossRefGoogle Scholar
  85. Zuo X, Lu H, Zhang J, Wang C, Sun G, Zheng Y (2016) Radiocarbon dating of prehistoric phytoliths: a preliminary study of archaeological sites in China. Sci Rep 6:26769CrossRefGoogle Scholar
  86. Zuo X, Lu H, Jiang L, Zhang J, Yang X, Huan X, He K, Wang C, Wu N (2017) Dating rice remains through phytolith 14C study reveals domestication at the beginning of the Holocene. P Natl Acad Sci USA 114:6486CrossRefGoogle Scholar
  87. Zuo X, Lu H, Huan X, Jiang L, Wang C (2018) Influence of different extraction methods on prehistoric phytolith radiocarbon dating. Quat Int. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Surface-Earth System ScienceTianjin UniversityTianjinChina
  2. 2.School of Environmental and Chemical EngineeringFoshan UniversityFoshanChina
  3. 3.Key Laboratory of Soil Contamination Bioremediation of Zhejiang ProvinceZhejiang A & F UniversityHangzhouChina
  4. 4.New South Wales Department of Primary IndustriesWollongbarAustralia
  5. 5.Department of Biology and Environmental ScienceLinnaeus UniversityKalmarSweden
  6. 6.State Key Laboratory of Environmental Geochemistry, Institute of GeochemistryChinese Academy of SciencesGuiyangChina

Personalised recommendations