Skip to main content
SpringerLink
Log in

Stoichiometry of ferns in Hawaii: implications for nutrient cycling

  • Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We asked if element concentrations in ferns differ systematically from those in woody dicots in ways that could influence ecosystem properties and processes. Phylogenetically, ferns are deeply separated from angiosperms; for our analyses we additionally separated leptosporangiate ferns into polypod ferns, a monophyletic clade of ferns which radiated after the rise of angiosperms, and all other leptosporangiate (non-polypod) ferns. We sampled both non-polypod and polypod ferns on a natural fertility gradient and within fertilized and unfertilized plots in Hawaii, and compared our data with shrub and tree samples collected previously in the same plots. Non-polypod ferns in particular had low Ca concentrations under all conditions and less plasticity in their N and P stoichiometry than did polypod ferns or dicots. Polypod ferns were particularly rich in N and P, with low N:P ratios, and their stoichiometry varied substantially in response to differences in nutrient availability. Distinguishing between these two groups has the potential to be useful both in and out of Hawaii, as they have distinct properties which can affect ecosystem function. These differences could contribute to the widespread abundance of polypod ferns in an angiosperm-dominated world, and to patterns of nutrient cycling and limitation in sites where ferns are abundant.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. In: Fitter AH, Raffaelli DG (eds) Advances in ecological research, vol 30. Academic Press, London, pp 1–67

    Google Scholar 

  • Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141:612–619

    Article  PubMed  Google Scholar 

  • Bangerth F (1979) Calcium-related physiological disorders of plants. Annu Rev Phytopathol 17:97–122

    Article  CAS  Google Scholar 

  • Bowman WD, Bahnj L, Damm M (2003) Alpine landscape variation in foliar nitrogen and phosphorus concentrations and the relation to soil nitrogen and phosphorus availability. Arct Antarct Alp Res 35:144–149

    Article  Google Scholar 

  • Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152:9–27

    Article  CAS  Google Scholar 

  • Broadley MR et al (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54:1431–1446

    Article  PubMed  CAS  Google Scholar 

  • Broadley MR et al (2004) Phylogenetic variation in the shoot mineral concentration of angiosperms. J Exp Bot 55:321–336

    Article  PubMed  CAS  Google Scholar 

  • Chenery EM, Sporne KR (1976) A note on the evolutionary status of Aluminum accumulators among dicotyledons. New Phytol 76:551–554

    Article  CAS  Google Scholar 

  • Cornelissen JHC, Thompson K (1997) Functional leaf attributes predict litter decomposition rate in herbaceous plants. New Phytol 135:109–114

    Article  Google Scholar 

  • Crews TE et al (1995) Changes in soil-phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424

    Article  Google Scholar 

  • Enright N, Ogden J (1987) Decomposition of litter from common woody species of Kauri (Agathis astralis Salisb) forest in northern New Zealand. Aust J Ecol 12:109–124

    Google Scholar 

  • Feild TS, Arens NC, Dawson TE (2003) The ancestral ecology of angiosperms: emerging perspectives from extant basal lineages. Int J Plant Sci 164:S129–S142

    Article  Google Scholar 

  • Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ (2004) Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30:82–107

    Article  Google Scholar 

  • Foy CD, Chaney RL, White MC (1978) Physiology of metal toxicity in plants. Annu Rev Plant Physiol Plant Mol Biol 29:511–566

    CAS  Google Scholar 

  • Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. In: Briggs WR (ed) Annual review of plant physiology, vol 37. Annual Reviews, Palo Alto, pp 165–186

    Google Scholar 

  • Galtier J, Phillips TM (1996) Structure and evolutionary significance of early ferns. In: Camus JM, Gibby M, Johns RJ (eds) Pteridology in perspective. Royal Botanic Gardens, Kew, pp 417–433

    Google Scholar 

  • Garten C (1976) Correlations between concentrations of elements in plants. Nature 261:686–688

    Article  CAS  Google Scholar 

  • Harrington R, Fownes J, Vitousek P (2001) Production and resource use efficiencies in N- and P-limited tropical forests: a comparison of responses to long-term fertilization. Ecosystems 4:646–657

    Article  CAS  Google Scholar 

  • Herbert DA, Fownes JH (1995) Phosphorus limitation of forest leaf area and net primary production on a highly weathered soil. Biogeochemistry 29:223–235

    Article  CAS  Google Scholar 

  • Hobbie S, Vitousek P (2000) Nutrient limitation of decomposition in Hawaiian forests. Ecology 81:1867–1877

    Google Scholar 

  • Hobbie SE, et al. (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297

    Article  PubMed  Google Scholar 

  • Hodson MJ, Evans DE (1995) Aluminium/silicon interactions in higher plants. J Exp Bot 46:161–171

    Article  CAS  Google Scholar 

  • Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96:1027–1046

    Article  PubMed  CAS  Google Scholar 

  • Hohne H, Richter B (1981) Investigations on the mineral element and nitrogen content in ferns. Flora 171:1–10

    Google Scholar 

  • Kawai H, et al. (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421:287–290

    Article  PubMed  CAS  Google Scholar 

  • Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168:E103–E122

    Article  PubMed  Google Scholar 

  • Knecht MR, Goransson A (2004) Terrestrial plants require nutrients in similar proportions. Tree Physiol 24:447–460

    PubMed  CAS  Google Scholar 

  • Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier, Amsterdam

    Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin SB, Wimmer R (1999) Tansley review no. 104: calcium physiology and terrestrial ecosystem processes. New Phytol 142:373–417

    Article  CAS  Google Scholar 

  • Meerts P (1997) Foliar macronutrient concentrations of forest understorey species in relation to Ellenberg’s indices and potential relative growth rate. Plant Soil 189:257–265

    Article  CAS  Google Scholar 

  • Meharg AA (2002) Arsenic and old plants. New Phytol 156:1–4

    Article  Google Scholar 

  • Neff JC, Reynolds R, Sanford RL, Fernandez D, Lamothe P (2006) Controls of bedrock geochemistry on soil and plant nutrients in southeastern Utah. Ecosystems 9:879–893

    Article  CAS  Google Scholar 

  • Page CN (2002) Ecological strategies in fern evolution: a neopteridological overview. Rev Palaeobot Palynol 119:1–33

    Article  Google Scholar 

  • Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758

    Article  PubMed  Google Scholar 

  • 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 91:1582–1598

    Article  CAS  Google Scholar 

  • Quigg A et al (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–294

    Article  PubMed  CAS  Google Scholar 

  • Raich JW, Russell AE, Vitousek PM (1997) Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawaii. Ecology 78:707–721

    Google Scholar 

  • Rathinasabapathi B (2006) Ferns represent an untapped biodiversity for improving crops for environmental stress tolerance. New Phytol 172:385–390

    Article  PubMed  Google Scholar 

  • Reiners WA (1986) Complementary models for ecosystems. Am Nat 127:59–73

    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 

  • Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177

    Google Scholar 

  • Rothwell GW (1996) Pteridophytic evolution: an often underappreciated phytological success story. Rev Palaeobot Palynol 90:209–222

    Article  Google Scholar 

  • Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557

    Article  PubMed  CAS  Google Scholar 

  • Scowcroft P (1997) Mass and nutrient dynamics of decaying litter from Passiflora mollissima and selected native species in a Hawaiian montane rain forest. J Trop Ecol 13:407–426

    Article  Google Scholar 

  • Shaver GR, Chapin FS (1980) Response to fertilization by various plant-growth forms in an Alaskan tundra—nutrient accumulation and growth. Ecology 61:662–675

    Article  CAS  Google Scholar 

  • Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419

    Google Scholar 

  • Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PC (2006) A classification for extant ferns. Taxon 55:705–731

    Google Scholar 

  • Snowden RED, Wheeler BD (1993) Iron toxicity to fen plant species. J Ecol 81:35–46

    Article  CAS  Google Scholar 

  • Sterner R, Elser J (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Tanner E (1977) Four montane rain forests of Jamaica—quantitative characterization of floristics, soils, and foliar mineral levels, and a discussion of interrelations. J Ecol 65:883–918

    Article  CAS  Google Scholar 

  • Thompson K, Parkinson JA, Band SR, Spencer RE (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136:679–689

    Article  CAS  Google Scholar 

  • Tuomisto H, Poulsen AD (1996) Influence of edaphic specialization on pteridophyte distribution in neotropical rain forests. J Biogeogr 23:283–293

    Article  Google Scholar 

  • Tuomisto H et al (2002) Distribution and diversity of pteridophytes and Melastomataceae along edaphic gradients in Yasuni National Park, Ecuadorian Amazonia. Biotropica 34:516–533

    Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • Van Arendoonk JJCM, Poorter H (1994) The chemical composition and anatomical structure of leaves of grass species differing in relative growth rate. Plant Cell Environ 17:963–970

    Article  Google Scholar 

  • Violle C, et al. (2007) Let the concept of trait be functional! Oikos 116:882–892

    Article  Google Scholar 

  • Vitousek P (1998) Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1:401–407

    Article  CAS  Google Scholar 

  • Vitousek P (2003) Stoichiometry and flexibility in the Hawaiian model system. In: Melillo J, Field C, Moldan B (eds) SCOPE 61: interactions of the major biogeochemical cycles. Island Press, Washington D.C., pp 117–134

    Google Scholar 

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

    Google Scholar 

  • Vitousek P, Walker L, Whiteaker L, Matson P (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23:197–215

    Article  Google Scholar 

  • Vitousek P, Gerrish G, Turner D, Walker L, Muellerdombois D (1995a) Litterfall and nutrient cycling in 4 Hawaiian montane rain forests. J Trop Ecol 11:189–203

    Google Scholar 

  • Vitousek PM, Turner DR, Kitayama K (1995b) Foliar nutrients during long-term soil development in Hawaiian montane rainforest. Ecology 76:712–720

    Article  Google Scholar 

  • Waksman SA, Tenney FG (1928) Composition of natural organic materials and their decomposition in the soil. III. The influence of nature of plant upon the rapidity of its decomposition. Soil Sci 26:155–171

    Article  CAS  Google Scholar 

  • Walker L, Aplet G (1994) Growth and fertilization responses of Hawaiian tree ferns. Biotropica 26:378–383

    Article  Google Scholar 

  • Wardle D, Bonner K, Barker G (2002) Linkages between plant litter decomposition, litter quality, and vegetation responses to herbivores. Funct Ecol 16:585–595

    Article  Google Scholar 

  • Wegner C, Wunderlich M, Kessler M, Schawe M (2003) Foliar C:N ratio of ferns along an Andean elevational gradient. Biotropica 35:486–490

    Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank R. Aguraiuja, L. Arnold, H. Farrington, M. Meyer, and D. Turner for help in the field and in the lab, and J. Benner, C. Lunch, J. Funk, K. Pryer, and two anonymous reviewers for comments on a draft of the manuscript. This work was supported by NSF DEB-0508954 and NSF DEB-0516491.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Stanford University, Stanford, CA, 94305, USA

    Kathryn L. Amatangelo & Peter M. Vitousek

Authors
  1. Kathryn L. Amatangelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Vitousek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathryn L. Amatangelo.

Additional information

Communicated by Todd Dawson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amatangelo, K.L., Vitousek, P.M. Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia 157, 619–627 (2008). https://doi.org/10.1007/s00442-008-1108-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1108-9

Keywords

Search

Navigation