Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T11:15:38.909Z Has data issue: false hasContentIssue false
  • English
  • Français

Cyanolichens: a link between the phosphorus and nitrogen cycles in a Hawaiian montane forest

Published online by Cambridge University Press:  08 December 2011

Jon W. Benner  and
Peter M. Vitousek
Jon W. Benner*
Affiliation:
Department of Biological Sciences, Stanford University, Stanford, CA, USA
Peter M. Vitousek
Affiliation:
Department of Biological Sciences, Stanford University, Stanford, CA, USA
*
1Corresponding author. Email: jbenner@alumni.princeton.edu
Get access Rights & Permissions [Opens in a new window]

Abstract:

Low phosphorus (P) supply frequently has been shown to limit the abundance and activity of nitrogen (N)-fixing organisms, potentially constraining N inputs to ecosystems. Previous research in a montane Hawaiian forest has shown that ground-level P-fertilization led to significant increases in the population size of epiphytic N-fixing lichens (cyanolichens), as well as a shift in community composition from crustose to leafy species. In this study, we ask whether these changes in the cyanolichen community have resulted in increased N inputs to the forest, and also whether the very high levels of P in the canopy of P-fertilized forest stimulate individual lichen fixation rates over those of lichens from a nearby unfertilized reference forest. We used acetylene reduction (AR) assays to measure the fixation rates of 14 cyanolichen species from P-fertilized forest, and calibrated these rates by measuring 15N2 fixation incorporation in four species. We found that the ratio of acetylene reduced to N fixed ranged from 2.4 ± 0.4 in Pseudocyphellaria crocata to 9.3 ± 2.4 in Leptogium denticulatum. Nitrogen fixation rates in the P-fertilized forest ranged from 0.64 ± 0.05 nmol N cm−2 h−1 in Nephroma helveticum to 3.97 ± 1.48 nmol N cm−2 h−1 in Parmeliella nigrocincta. Fixation rates did not vary greatly among species from P-fertilized forest. We compared these P-fertilized rates to those of 10 species from the reference forest, and found that mass-based fixation rates of P-fertilized lichens were not greater than those of lichens from the unfertilized forest. Using the measured AR rates, we estimate that the P additions increase cyanolichen N inputs to the forest 30-fold, from ~0.3 kg N ha−1 y−1 to ~9 kg N ha−1 y−1. These results suggest that P additions to this ecosystem increase N inputs primarily by increasing the abundance of cyanolichens, and that shifts in cyanolichen community composition and changes in individual fixation rate were of lesser importance in determining ecosystem N inputs.

Keywords

cyanolichenHawaiinitrogen fixationphosphorustropical montane forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 28 , Issue 1 , January 2012 , pp. 73 - 81
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ANTOINE, M. E. 2004. An ecophysiological approach to quantifying nitrogen fixation by Lobaria oregana. Bryologist 107:82–87.CrossRefGoogle Scholar
BENNER, J. W. 2011. Epiphytes preferentially colonize high-phosphorus trees in unfertilized Hawaiian montane forests. Bryologist 114:335–345.CrossRefGoogle Scholar
BENNER, J. W. & VITOUSEK, P. M. 2007. Development of a diverse epiphyte community in response to phosphorus fertilization. Ecology Letters 10:628–636.CrossRefGoogle ScholarPubMed
BENNER, J. W., CONROY, S., LUNCH, C. K., TOYODA, N. & VITOUSEK, P. M. 2007. Phosphorus fertilization increases the abundance and nitrogenase activity of the cyanolichen Pseudocyphellaria crocata in Hawaiian montane forests. Biotropica 39:400–405.CrossRefGoogle Scholar
BURRIS, R. H. 1974. Methodology. Pp. 9–33 in Quispel, A. (ed). The biology of nitrogen fixation. North Holland Publishing Co., Amsterdam.Google Scholar
CARRILLO, J. H., HASTINGS, M. G., SIGMAN, D. M. & HUEBERT, B. J. 2002. Atmospheric deposition of inorganic and organic nitrogen and base cations in Hawaii. Global Biogeochemical Cycles 16: 1076 [doi: 10.1029/2002GB001892]CrossRefGoogle Scholar
CREWS, T. 1993. Phosphorus regulation of nitrogen fixation in a traditional Mexican agroecosystem. Biogeochemistry 21:141–166.CrossRefGoogle Scholar
CREWS, T., KITAYAMA, K., FOWNES, J. H., RILEY, R. H., HERBERT, D. A., MUELLER-DOMBOIS, D. & VITOUSEK, P. M. 1995. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424.CrossRefGoogle Scholar
CREWS, T., FARRINGTON, H. & VITOUSEK, P. 2000. Changes in asymbiotic, heterotrophic nitrogen fixation on leaf litter of Metrosideros polymorpha with long-term ecosystem development in Hawaii. Ecosystems 3:386–395.CrossRefGoogle Scholar
CUSACK, D. F., SILVER, W. & McDOWELL, W. H. 2009. Biological nitrogen fixation in two tropical forests: ecosystem-level patterns and effects of nitrogen fertilization. Ecosystems 12:1299–1315.CrossRefGoogle Scholar
DENISON, W. C. 1979. Lobaria oregana, a nitrogen-fixing lichen in old-growth Douglas fir forests. Pp. 266–275 in Gordon, J. C., Wheeler, C. T. & Perry, D. A. (eds.). Symbiotic nitrogen fixation in the management of temperate forests. Forest Research Laboratory, Oregon State University, Corvallis.Google Scholar
DIAL, R. & TOBIN, S. T. 1994. Description of arborist methods for forest canopy access and movement. Selbyana 15: 24–37.Google Scholar
EISELE, K. A., SCHIMEL, D. S., KAPSUTKA, L. A. & PARTON, W. J. 1989. Effects of available phosphorus and nitrogen–phosphorus ratios on non-symbiotic dinitrogen fixation in tallgrass prairie soils. Oecologia 79:471–474.CrossRefGoogle Scholar
FORMAN, R. T. T. 1975. Canopy lichens with blue-green algae – nitrogen source in a Colombian rainforest. Ecology 56:1176–1184.CrossRefGoogle Scholar
GIAMBELLUCA, T. W., NULLET, M. A. & SCHROEDER, T. A. 1986. Hawaii rainfall atlas. Hawai'i Division of Water and Land Development, Department of Land and Natural Resources, Honolulu. 267 pp.Google Scholar
GOWARD, T. & ARSENAULT, A. 2000. Cyanolichens and conifers: implications for global conservation. Forest Snow Landscape Research 75:303–318.Google Scholar
HARDY, R. W. F., HOLSTEN, R. D., JACKSON, E. K. & BURNS, R. C. 1968. The acetylene–ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiology 43:1185–1207.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
HERBERT, D. A. & FOWNES, J. H. 1995. Phosphorus limitation of forest leaf-area and net primary production on a highly weathered soil. Biogeochemistry 29:223–235.CrossRefGoogle Scholar
HIETZ, P., WANEK, W., WANIA, R. & NADKARNI, N. M. 2002. Nitrogen-15 natural abundance in a montane cloud forest canopy as an indicator of nitrogen cycling and epiphyte nutrition. Oecologia 131:350–355.CrossRefGoogle Scholar
HOULTON, B. Z., WANG, Y.-P., VITOUSEK, P. M. & FIELD, C. B. 2008. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–331.CrossRefGoogle ScholarPubMed
KERSHAW, K. A. 1985. Physiological ecology of lichens. Cambridge University Press, Cambridge. 293 pp.Google Scholar
KERSHAW, K. A., MACFARLANE, J. D. & TYSIACZNY, M. J. 1977. Physiological–environmental interactions in lichens V. The interaction of temperature with nitrogenase activity in the dark. New Phytologist 79:409–416.CrossRefGoogle Scholar
KURINA, L. M. & VITOUSEK, P. M. 2001. Nitrogen fixation rates of Stereocaulon vulcani on young Hawaiian lava flows. Biogeochemistry 55:179–194.CrossRefGoogle Scholar
MACFARLANE, J. D., MAIKAWA, E., KERSHAW, K. A. & OAKS, A. 1976. Physiological–environmental interactions in lichens I. The interaction of light/dark periods and nitrogenase activity in Peltigera polydactyla. New Phytologist 77:705–711.CrossRefGoogle Scholar
MATZEK, V. & VITOUSEK, P. 2003. Nitrogen fixation in bryophytes, lichens, and decaying wood along a soil–age gradient in Hawaiian montane rain forest. Biotropica 35:12–19.Google Scholar
MENGE, D. N. L. & HEDIN, L. O. 2009. Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90:2190–2201.CrossRefGoogle ScholarPubMed
MILLBANK, J. W. 1981. The assessment of nitrogen fixation and throughput by lichens I. The use of a controlled environment chamber to relate acetylene reduction estimates to nitrogen fixation. New Phytologist 89:647–655.CrossRefGoogle Scholar
PORDER, S., ASNER, G. P. & VITOUSEK, P. M. 2005. Ground-based and remotely sensed nutrient availability across a tropical landscape. Proceedings of the National Academy of Sciences USA 102:10909–10912.CrossRefGoogle ScholarPubMed
REED, S. C., SEASTEDT, T. R., MANN, C. M., SUDING, K. N., TOWNSEND, A. R. & CHERWIN, K. L. 2007a. Phosphorus fertilization stimulates nitrogen fixation and increases in inorganic nitrogen concentrations in restored prairie. Applied Soil Ecology 36:238–242.CrossRefGoogle Scholar
REED, S. C., CLEVELAND, C. C. & TOWNSEND, A. R. 2007b. Controls over leaf litter and soil nitrogen fixation in two tropical lowland forests. Biotropica 39:585–592.CrossRefGoogle Scholar
REED, S. C., CLEVELAND, C. C. & TOWNSEND, A. R. 2008. Tree species control rates of free-living nitrogen fixation in a tropical rain forest. Ecology 89:2924–2934.CrossRefGoogle Scholar
REED, S. C., TOWNSEND, A. R., CLEVELAND, C. C. & NEMERGUT, D. R. 2010. Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164:521–531.CrossRefGoogle ScholarPubMed
SCHINDLER, D. W. 1977. Evolution of phosphorus limitation in lakes. Science 195:260–262.CrossRefGoogle ScholarPubMed
SCHLESINGER, W. H. 1997. Biogeochemistry: an analysis of global change. Academic Press, San Diego. 588 pp.Google Scholar
SHEARER, G. & KOHL, D. H. 1986. N2-fixation in field settings: estimations based on natural 15N abundance. Australian Journal of Plant Physiology 13:699–756.Google Scholar
SILLETT, S. C. & MCCUNE, B. 1998. Survival and growth of cyanolichen transplants in Douglas-fir forest canopies. Bryologist 101:20–31.CrossRefGoogle Scholar
SMITH, V. 1992. Effects of nitrogen–phosphorus supply rations on nitrogen fixation in agricultural and pastoral ecosystems. Biogeochemistry 18:19–35.CrossRefGoogle Scholar
SOLLINS, P., GRIER, C., MCCORISON, F., CROMACK, K. & FOGEL, R. 1980. The internal element cycles of an old-growth Douglas fir ecosystem in western Oregon. Ecological Monographs 50:261–285.CrossRefGoogle Scholar
VITOUSEK, P. M. 1994. Potential nitrogen fixation during primary succession in Hawai'i Volcanoes National Park. Biotropica 26;234–240.CrossRefGoogle Scholar
VITOUSEK, P. M. 1999. Nutrient limitation to nitrogen fixation in young volcanic sites. Ecosystems 2:505–510.CrossRefGoogle Scholar
VITOUSEK, P. M. 2004. Nutrient cycling and limitation – Hawai'i as a model system. Princeton University Press, Princeton. 227 pp.CrossRefGoogle Scholar
VITOUSEK, P.M. & FIELD, C.B. 1999. Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202.CrossRefGoogle Scholar
VITOUSEK, P. M. & HOWARTH, R. W. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115.CrossRefGoogle Scholar
VITOUSEK, P. M., CHADWICK, O., MATSON, P., ALLISON, S., DERRY, L., KETTLEY, L., LUERS, A., MECKING, E., MONASTRA, V. & PORDER, S. 2003. Erosion and the rejuvenation of weathering-derived nutrient supply in an old tropical landcape. Ecosystems 6:762–772.CrossRefGoogle Scholar
VITOUSEK, P. M., PORDER, S., HOULTON, B. Z. & CHADWICK, O. A. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecological Applications 20:5–15.CrossRefGoogle ScholarPubMed
ZOTZ, G. 1999. Altitudinal changes in diversity and abundance of non-vascular epiphytes in the tropics: an ecophysiological explanation. Selbyana 20:256–260.Google Scholar