, Volume 173, Issue 1, pp 23–32 | Cite as

Physiological mechanisms drive differing foliar calcium content in ferns and angiosperms

Physiological Ecology - Original Research


Recent evidence points to ferns containing significantly lower contents of foliar calcium and other cations than angiosperms. This is especially true of more ancient ‘non-polypod’ fern lineages, which predate the diversification of angiosperms. Calcium is an important plant nutrient, the lack of which can potentially slow plant growth and litter decomposition, and alter soil invertebrate communities. The physiological mechanisms limiting foliar calcium (Ca) content in ferns are unknown. While there is a lot we do not know about Ca uptake and transport in plants, three physiological processes are likely to be important. We measured transpiration rate, cation exchange capacity, and leaching loss to determine which process most strongly regulates foliar Ca content in a range of fern and co-occurring understory angiosperm species from a montane Hawaiian rainforest. We found higher instantaneous and lifetime (corrected for leaf lifespan) transpiration rates in angiosperms relative to ferns. Ferns preferentially incorporated Ca into leaves relative to strontium, which suggests that root or stem cation exchange capacity differs between ferns and angiosperms, potentially affecting calcium transport in plants. There were no differences in foliar Ca leaching loss between groups. Among the physiological mechanisms measured, foliar Ca was most strongly correlated with leaf-level transpiration rate and leaf lifespan. This suggests that inter-specific differences in a leaf’s lifetime transpiration may play a significant role in determining plant nutrition.


Transpiration Calcium:strontium Cation exchange capacity Cation leaching Decomposition Leaf lifespan 

Supplementary material

442_2013_2591_MOESM1_ESM.docx (38 kb)
Online Resource (DOCX 38 kb)


  1. Ackerly D (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119:300–310CrossRefGoogle Scholar
  2. Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141:612–619PubMedCrossRefGoogle Scholar
  3. Amatangelo KL, Vitousek PM (2008) Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia 157:619–627PubMedCrossRefGoogle Scholar
  4. Amatangelo KL, Vitousek PM (2009) Contrasting predictors of fern versus angiosperm decomposition in a common garden. Biotropica 41:154–161CrossRefGoogle Scholar
  5. Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Schnitzer S, Carson W (eds) Tropical forest community ecology. Blackwell, Oxford, pp 254–271Google Scholar
  6. Baran EJ, Rolleri CH (2010) IR-spectroscopic characterization of biominerals in marattiaceaeus ferns. Rev Bras Bot 33:519–523CrossRefGoogle Scholar
  7. Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach, 2nd edn. Wiley, New YorkGoogle Scholar
  8. Berch SM, Kendrick B (1982) Vesicular–arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74:769–776CrossRefGoogle Scholar
  9. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc R Soc Lond B 276:1771–1776CrossRefGoogle Scholar
  10. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54:1431–1446PubMedCrossRefGoogle Scholar
  11. Brodersen CR, Roark LC, Pittermann J (2012) The physiological implications of primary xylem organization in two ferns. Plant Cell Environ 35:1898–1911PubMedCrossRefGoogle Scholar
  12. Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162:663–670CrossRefGoogle Scholar
  13. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898PubMedCrossRefGoogle Scholar
  14. Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol 183:839–847PubMedCrossRefGoogle Scholar
  15. Carlquist S, Schneider EL (2000) SEM studies on vessels in ferns. 16. Pacific tree ferns (Blechnaceae, Cyatheaceae, Dicksoniaceae). Pac Sci 54:75–86Google Scholar
  16. Carlquist S, Schneider EL (2001) Vessels in ferns: structural, ecological, and evolutionary significance. Am J Bot 88:1–13PubMedCrossRefGoogle Scholar
  17. Chapin FS III, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64:376–391CrossRefGoogle Scholar
  18. Cramer W et al (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models. Glob Change Biol 7:357–373CrossRefGoogle Scholar
  19. 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 76:1407–1424CrossRefGoogle Scholar
  20. Dasch AA, Blum JD, Eagar C, Fahey TJ, Driscoll CT, Siccama TG (2006) The relative uptake of Ca and Sr into tree foliage using a whole-watershed calcium addition. Biogeochemistry 80:21–41CrossRefGoogle Scholar
  21. De Guzman CC, Dela Fuente RK (1984) Polar calcium flux in sunflower Helianthus annuus hypocotyl segments. 1. The effect of auxin. Plant Physiol 76:347–352PubMedCrossRefGoogle Scholar
  22. Dearden FM, Wardle DA (2008) The potential for forest canopy litterfall interception by a dense fern understorey, and the consequences for litter decomposition. Oikos 117:83–92CrossRefGoogle Scholar
  23. Dijkstra FA (2003) Calcium mineralization in the forest floor and surface soil beneath different tree species in the northeastern US. For Ecol Manag 175:185–194CrossRefGoogle Scholar
  24. Enright N (1999) Litterfall dynamics in a mixed conifer–angiosperm forest in northern New Zealand. J Biogeogr 26:149–157CrossRefGoogle Scholar
  25. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives. Sinauer, SunderlandGoogle Scholar
  26. Franceschi VR, Horner HT (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427CrossRefGoogle Scholar
  27. Herbette S, Cochard H (2010) Calcium is a major determinant of xylem vulnerability to cavitation. Plant Physiol 153:1932–1939PubMedCrossRefGoogle Scholar
  28. Kagawa A, Sack L, Duarte K, James S (2009) Hawaiian native forest conserves water relative to timber plantation: species and stand traits influence water use. Ecol Appl 19:1429–1443PubMedCrossRefGoogle Scholar
  29. Karley AJ, Leigh RA, Sanders D (2000) Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends Plant Sci 5:465–470PubMedCrossRefGoogle Scholar
  30. Kessler M, Siorak Y, Wunderlich M, Wegner C (2007) Patterns of morphological leaf traits among pteridophytes along humidity and temperature gradients in the Bolivian Andes. Funct Plant Biol 34:963–971CrossRefGoogle Scholar
  31. Kessler M, Kluge J, Hemp A, Ohlemueller R (2011) A global comparative analysis of elevational species richness patterns of ferns. Glob Ecol Biogeogr 20:868–880CrossRefGoogle Scholar
  32. Kitayama K, Mueller-Dombois D (1995) Vegetation changes along gradients of long-term soil development in the Hawaiian mountain rain-forest zone. Vegetatio 120:1–20Google Scholar
  33. Lee JJ, Weber DE (1979) The effect of simulated acid rain on seedling emergence and growth of eleven woody species. For Sci 25:393–398Google Scholar
  34. Lee JS, Mulkey TJ, Evans ML (1983) Gravity induced polar transport of calcium across root tips of maize. Plant Physiol 73:874–876PubMedCrossRefGoogle Scholar
  35. Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol Evol 17:457–461CrossRefGoogle Scholar
  36. Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier, AmsterdamGoogle Scholar
  37. Marrs RH, Le Duc MG, Mitchell RJ, Goddard D, Paterson S, Pakeman RJ (2000) The ecology of bracken: its role in succession and implications for control. Ann Bot 85:3–15CrossRefGoogle Scholar
  38. Marschner H (2002) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  39. Mazumdar J (2011) Phytoliths of pteridophytes. S Afr J Bot 77:10–19CrossRefGoogle Scholar
  40. McAdam SAM, Brodribb TJ (2012a) Stomatal innovation and the rise of seed plants. Ecol Lett 15:1–8PubMedCrossRefGoogle Scholar
  41. McAdam SAM, Brodribb TJ (2012b) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24:1510–1521PubMedCrossRefGoogle Scholar
  42. McElwain JC (2011) Ferns: a xylem success story. New Phytol 192:307–310PubMedCrossRefGoogle Scholar
  43. McLaughlin SB, Wimmer R (1999) Calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417CrossRefGoogle Scholar
  44. McNair JB (1932) The interrelation between substances in plants: essential oils and resins, cyanogen and oxalate. Am J Bot 19:255–272CrossRefGoogle Scholar
  45. Mecklenburg RA, Tukey HB, Morgan JV (1966) A mechanism for leaching of calcium from foliage. Plant Physiol 41:610–613PubMedCrossRefGoogle Scholar
  46. Montanaro G, Dichio B, Xiloyannis C (2010) Significance of fruit transpiration on calcium nutrition in developing apricot fruit. J Plant Nutr Soil Sci 173:618–622CrossRefGoogle Scholar
  47. Palmer DD (2003) Hawaii’s ferns and fern allies. University of Hawaii Press, HonoluluGoogle Scholar
  48. Perez-Harguindeguy N, Vendramini F, Diaz S, Cabido M, Cornelissen JH, Gurvich DE, Castellanos A (2000) Decomposition and foliar traits of pteridophytes and angiosperms species from the Chaco Serrano, Cordoba, Argentina. Kurtziana 28:35–44Google Scholar
  49. Pittermann J, Limm E, Rico C, Christman MA (2011) Structure–function constraints of tracheid-based xylem: a comparison of conifers and ferns. New Phytol 192:449–461PubMedCrossRefGoogle Scholar
  50. Popper ZA, Fry SC (2004) Primary cell wall composition of pteridophytes and spermatophytes. New Phytol 164:165–174CrossRefGoogle Scholar
  51. Poszwa A, Dambrine E, Pollier B, Atteia O (2000) A comparison between Ca and Sr cycling in forest ecosystems. Plant Soil 225:299–310CrossRefGoogle Scholar
  52. Prychid CJ, Rudall PJ, Gregory M (2003) Systematics and biology of silica bodies in monocotyledons. Bot Rev 69:377–440CrossRefGoogle Scholar
  53. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598PubMedCrossRefGoogle Scholar
  54. Qian H, Wang S, Li Y, Xiao M, Wang X (2012) Disentangling the relative effects of ambient energy, water availability, and energy-water balance on pteridophyte species richness at a landscape scale in China. Plant Ecol 213:749–756CrossRefGoogle Scholar
  55. Raich JW, Russell AE, Vitousek PM (1997) Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawaii. Ecology 78:707–721Google Scholar
  56. Reich PB, Oleksyn J, Modrzynski J, Mrozinski P, Hobbie SE, Eissenstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818CrossRefGoogle Scholar
  57. Richardson SJ, Peltzer DA, Allen RB, McGlone MS (2005) Resorption proficiency along a chronosequence: responses among communities and within species. Ecology 86:20–25CrossRefGoogle Scholar
  58. Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21:1030–1035PubMedCrossRefGoogle Scholar
  59. Schneider EL, Carlquist S (1998) SEM studies on vessels in ferns. 9. Dicranopteris (Gleicheniaceae) and vessel patterns in Leptosporangiate ferns. Am J Bot 85:1028–1032PubMedCrossRefGoogle Scholar
  60. Schneider EL, Carlquist S (1999a) SEM studies on vessels in ferns. 13. Nephrolepis. Am Fern J 89:171–177CrossRefGoogle Scholar
  61. Schneider EL, Carlquist S (1999b) SEM studies on vessels in ferns. XV. Selected rosette epiphytes (Aspleniaceae, Elaphoglossaceae, Vittariaceae). Int J Plant Sci 160:1013–1020PubMedCrossRefGoogle Scholar
  62. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557PubMedCrossRefGoogle Scholar
  63. Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci USA 106:11200–11205PubMedCrossRefGoogle Scholar
  64. Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419Google Scholar
  65. Singh C, Jacobson L (1979) The accumulation and transport of calcium in barley roots. Physiol Plant 45:443–447CrossRefGoogle Scholar
  66. Smith KA (1971) The comparative uptake and translocation by plants of calcium, strontium, barium and radium. II. Triticum vulgare (wheat). Plant Soil 34:643–651CrossRefGoogle Scholar
  67. Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PC (2006) A classification for extant ferns. Taxon 55:705–731CrossRefGoogle Scholar
  68. Tibbitts TW (1979) Humidity and plants. Bioscience 29:358–363CrossRefGoogle Scholar
  69. Tukey HB (1970) Leaching of substances from plants. Annu Rev Plant Physiol 21:305–324CrossRefGoogle Scholar
  70. Tuomisto H, Ruokolainen K, Poulsen AD, Moran RC, Quintana C, Cañas G, Celi J (2002) Distribution and diversity of pteridophytes and Melastomataceae along edaphic gradients in Yasuni National Park, Ecuadorian Amazonia. Biotropica 34:516–533Google Scholar
  71. Valier K (1995) Ferns of Hawaii. University of Hawaii Press, HonoluluGoogle Scholar
  72. Veresoglou DS, Barbayiannis N, Matsi T, Anagnostopoulos C, Zalidis GC (1996) Shoot Sr concentrations in relation to shoot Ca concentrations and to soil properties. Plant Soil 178:95–100CrossRefGoogle Scholar
  73. Vitousek P (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, PrincetonGoogle Scholar
  74. Vitousek PM, Gerrish G, Turner DR, Walker LR, Mueller-Dombois D (1995a) Litterfall and nutrient cycling in four Hawaiian montane rainforests. J Trop Ecol 11:189–203CrossRefGoogle Scholar
  75. Vitousek PM, Turner DR, Kitayama K (1995b) Foliar nutrients during long-term soil development in Hawaiian montane rain-forest. Ecology 76:712–720CrossRefGoogle Scholar
  76. Vitousek P, Asner GP, Chadwick OA, Hotchkiss S (2009) Landscape-level variation in forest structure and biogeochemistry across a substrate age gradient in Hawaii. Ecology 90:3074–3086PubMedCrossRefGoogle Scholar
  77. Wagner WL, Herbst DR, Sohmer SH (1999) Manual of the flowering plants of Hawaii. University of Hawaii Press, HonoluluGoogle Scholar
  78. Walker LR (1994) Effects of fern thickets on woodland development on landslides in Puerto Rico. J Veg Sci 5:525–532CrossRefGoogle Scholar
  79. Watkins JE, Rundel PW, Cardelus CL (2007) The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. Oecologia 153:225–232PubMedCrossRefGoogle Scholar
  80. Watkins JE, Holbrook NM, Zwieniecki MA (2010) Hydraulic properties of fern sporophytes: consequences for ecological and evolutionary diversification. Am J Bot 97:2007–2019PubMedCrossRefGoogle Scholar
  81. White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899PubMedCrossRefGoogle Scholar
  82. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedCrossRefGoogle Scholar
  83. Wiebe HJ, Schaetzler HP, Kuehn W (1978) On the movement and distribution of calcium in white cabbage in dependence of the water status. Plant Soil 48:409–416CrossRefGoogle Scholar
  84. Wiegand BA, Chadwick OA, Vitousek PM, Wooden JL (2005) Ca cycling and isotopic fluxes in forested ecosystems in Hawaii. Geophys Res Lett 32:L11404. doi:10.1029/2005GL022746 CrossRefGoogle Scholar
  85. Woodhouse RM, Nobel PS (1982) Stipe anatomy, water potentials, and xylem conductances in seven species of ferns (Filicopsida). Am J Bot 69:135–140CrossRefGoogle Scholar
  86. Xiao Q, McPherson EG, Ustin SL, Grismer ME (2000) A new approach to modeling tree rainfall interception. J Geophys Res 105:29173–29188CrossRefGoogle Scholar
  87. Zamierowski EE (1975) Leaching losses of minerals from leaves of trees in montane in Kenya. J Ecol 63:679–687CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.School of Earth and Environmental SciencesChapman UniversityOrangeUSA
  2. 2.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA

Personalised recommendations