Plant Ecology

, Volume 207, Issue 2, pp 347–358 | Cite as

Short-term effect of deep shade and enhanced nitrogen supply on Sphagnum capillifolium morphophysiology

  • Samuel Alexander Festing Bonnett
  • Nick Ostle
  • Chris Freeman
Article

Abstract

Sphagnum capillifolium mesocosms collected from an ombrotrophic blanket bog were subjected to controlled photon flux densities (control and shaded) and nitrogen (low and high) treatments between November 2003 and August 2004. Shading significantly reduced biomass of S. capillifolium (P < 0.001), whilst nitrogen (N) supply significantly increased biomass (P < 0.05) suggesting that S. capillifolium was limited by N. There was no significant interaction between shading and N on biomass. S. capillifolium responded to shading via morphophysiological and biochemical alterations to the photosynthetic tissues such as (1) break down of anthocyanins involved in photoprotection of chloroplasts, (2) translocation of N from mineralized N or old tissues and (3) allocation of translocated N to photosynthetic pigments. The results suggest that S. capillifolium can tolerate both low and high light intensities, as well as high N supply via morphophysiological responses but does not acclimate to deep shade, since biomass was reduced. Anthocyanins rather than carotenoids appear to play an essential role in photoprotection with translocation serving as the important source of N. It has been suggested that global change in temperature and N availability may lead to increased vascular plant growth that could increase shade leading to a shift from Sphagnum spp. to vascular species in peatlands. However, the species S. capillifolium appears to tolerate deep shade and high N deposition due to the mechanisms shown here suggesting that this species may continue to persist in peatland ecosystems.

Keywords

Sphagnum capillifolium (Ehrh.) Hedw Shading Nitrogen Biomass Photosynthetic pigments Anthocyanin 

References

  1. Aerts R, Wallen B, Malmer N (1992) Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. J Ecol 80:131–140CrossRefGoogle Scholar
  2. Aldous AR (2002a) Nitrogen retention by Sphagnum mosses: responses to atmospheric nitrogen deposition and drought. Can J Bot 80:721–731CrossRefGoogle Scholar
  3. Aldous AR (2002b) Nitrogen translocation in Sphagnum mosses: effects of atmospheric nitrogen deposition. New Phytol 156:241–253CrossRefGoogle Scholar
  4. Arp WJ (1991) Effect of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–875CrossRefGoogle Scholar
  5. Arróniz-Crespo M, Leake JR, Horton P, Phoenix GK (2008) Bryophyte physiological responses to, and recovery from, long-term nitrogen deposition and phosphorus fertilisation in acidic grassland. New Phytol 180:864–874CrossRefPubMedGoogle Scholar
  6. Berendse F, Van Breeman N, Rydin H, Buttler A, Heijmans M, Hoosbeek MR, Lee JA, Mitchell E, Saarinen T, Vasander H, Wallen Bo (2001) Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Glob Change Biol 7:591–598CrossRefGoogle Scholar
  7. Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Ann Rev Plant Physiol 28:355–377CrossRefGoogle Scholar
  8. Bonnett SAF (2005) Biogeochemical implications of plant-soil interactions in peatland ecosystems. Ph.D. thesis, University of Wales, BangorGoogle Scholar
  9. Bragazza L, Tahvanainen T, Kutnar L, Rydin H, Limpens J, Hájek M, Grosvernier P, Hájek T, Hajkova P, Hansen I, Iacumin P, Gerdol R (2004) Nutritional constraints in ombrotrophic Sphagnum plants under increasing atmospheric nitrogen deposition in Europe. New Phytol 163:609–616CrossRefGoogle Scholar
  10. Bragazza L, Limpens J, Gerdol R, Grosvernier P, Hájeks M, Hájek T, Hajkovas P, Hansen I, Iacumin P, Kutnar L, Rydin H, Tahvanainenss T (2005) Nitrogen concentration and δ15N signature of ombrotrophic Sphagnum mosses at different N deposition levels in Europe. Glob Change Biol 11:106–114CrossRefGoogle Scholar
  11. Breeuwer A, Heijmans M, Gleichman M, Robroeck B, Berendse F (2009) Response of Sphagnum species mixtures to increased temperature and nitrogen availability. Plant Ecol 204:97–111CrossRefGoogle Scholar
  12. Bridgham SD (2002) Nitrogen, translocation and Sphagnum mosses. New Phytol 156:137–144CrossRefGoogle Scholar
  13. Clymo RS, Hayward PM (1982) The ecology of Sphagnum. In: Smith AJE (ed) Bryophyte ecology. Chapman and Hall, London, pp 229–289Google Scholar
  14. Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev 74:311–345CrossRefPubMedGoogle Scholar
  15. Cove D, Knight CD, Lamparter T (1997) Mosses as model systems. Trends Plant Sci 2:99–105CrossRefGoogle Scholar
  16. Cundill AP, Chapman PJ, Adamson JK (2007) Spatial variation in concentrations of dissolved nitrogen species in an upland blanket peat catchment. Sci Total Environ 373:166–177CrossRefPubMedGoogle Scholar
  17. Daniels RE, Eddy A (1990) Handbook of European Sphagna, 2nd edn. HMSO, LondonGoogle Scholar
  18. Davey MC, Rothery P (1997) Interspecific variation in respiratory and photosynthetic parameters in Antarctic bryophytes. New Phytol 137:231–240CrossRefGoogle Scholar
  19. Dunn JL, Robinson SA (2006) Ultraviolet B screening potential is higher in two cosmopolitan moss species than in a co-occurring Antarctic endemic moss: implications of continuing ozone depletion. Glob Change Biol 12:2282–2296CrossRefGoogle Scholar
  20. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  21. Fenner N, Ostle NJ, McNamara N, Sparks T, Harmens H, Reynolds B, Freeman C (2007) Elevated CO2 effects on peatland plant community carbon dynamics and DOC production. Ecosystems 10:635–647CrossRefGoogle Scholar
  22. Gerdol R, Bonora A, Marchesini R, Gualandri R, Pancaldi S (1998) Growth response of Sphagnum capillifolium to nighttime temperature and nutrient level: mechanisms and implications for global change. Arc Alp Res 30:388–395CrossRefGoogle Scholar
  23. Grace SC, Logon BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philos Trans R Soc B 355:1499–1510CrossRefGoogle Scholar
  24. Granath G, Strngbom J, Breeuwer A, Heijman MMPD, Berendse F, Rydin H (2009) Photosynthetic performance in Sphagnum transplanted along a latitudinal nitrogen deposition gradient. Oecologia 159:705–715CrossRefPubMedGoogle Scholar
  25. Gunnarsson U, Rydin H (2000) Nitrogen fertilisation reduces Sphagnum production in bog communities. New Phytol 147:527–537CrossRefGoogle Scholar
  26. Gunnarsson U, Granberg G, Nilsson M (2004) Growth, production and interspecific competition in Sphagnum: effects of temperature, nitrogen and sulphur treatments on a boreal mire. New Phytol 163:349–359CrossRefGoogle Scholar
  27. Holden J, Adamson JK (2002) The Moor House long-term upland temperature record: new evidence of recent warming. Weather 57:119–127Google Scholar
  28. Husain SR, Cillard J, Cillard P (1987) Hydroxyl radical scavenging activity of flavonoids. Phytochemistry 26:2489–2491CrossRefGoogle Scholar
  29. Jauhiainen J, Wallén B, Malmer N (1998) Potential NH4 + and NO3 uptake in seven Sphagnum species. New Phytol 138:287–293CrossRefGoogle Scholar
  30. Krol M, Gray GR, Hurry VM, Öquist G, Malek L, Huner NPA (1995) Low-temperature stress and photoperiod effect an increased tolerance to photoinhibition in Pinus banksiana seedlings. Can J Bot 73:1119–1127CrossRefGoogle Scholar
  31. Lamers L, Bobbink R, Roelofs JGM (2000) Natural nitrogen filter fails in polluted raised bogs. Glob Change Biol 6:583–586CrossRefGoogle Scholar
  32. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  33. Limpens J, Berendse F (2003) Growth reduction of Sphagnum magellanicum subjected to high nitrogen deposition: the role of amino acid nitrogen concentration. Oecologia 135:339–345PubMedGoogle Scholar
  34. Limpens J, Berendse F, Klees H (2003) N deposition affects N availability in interstitial water, growth of Sphagnum and invasion of vascular plants in bog vegetation. New Phytol 157:339–347CrossRefGoogle Scholar
  35. Lovelock CE, Robinson SA (2002) Surface reflectance properties of Antarctic moss and their relationship to plant species, pigment composition and photosynthetic function. Plant Cell Environ 25:1239–1250CrossRefGoogle Scholar
  36. Mancinelli A (1984) Photoregulation of anthocyanin synthesis. VIII. Effects of light pre-treatments. Plant Physiol 75:447–453CrossRefPubMedGoogle Scholar
  37. Marschall M, Proctor CFM (2004) Are bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Ann Bot 94:593–603CrossRefPubMedGoogle Scholar
  38. Martin CE, Churchill SP (1982) Chlorophyll concentrations and a:b ratios in mosses collected from exposed and shaded habitats in Kansas. J Bryol 12:297–304Google Scholar
  39. Mues R (2002) Chemical constituents and biochemistry. In: Shaw AJ, Goffinet B (eds) Bryophyte biology. Cambridge University Press, New YorkGoogle Scholar
  40. Murray KJ, Tenhunen JD, Nowak RS (1993) Photoinhibition as a control on photosynthesis and production of Sphagnum mosses. Oecologia 96:200–207CrossRefGoogle Scholar
  41. NEGTAP (2001) Transboundary air pollution: acidification, eutrophication and ground-level ozone in the UK. Prepared on behalf of the UK Department for Environment, Food and Rural Affairs (DEFRA) and the devolved administrationsGoogle Scholar
  42. Pietrini F, Iannelli MA, Massacci A (2002) Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis. Plant Cell Environ 25:1251–1259CrossRefGoogle Scholar
  43. Pitcairn CER, Fowler D, Grace J (1995) Deposition of fixed atmospheric nitrogen and foliar nitrogen content of bryophytes and Calluna vulgaris (L.) Hull. Environ Pollut 88:193–205CrossRefPubMedGoogle Scholar
  44. Pitcairn C, Fowler D, Leith I, Sheppard L, Tang S, Sutton M, Famulari D (2006) Diagnostic indicators of elevated nitrogen deposition. Environ Pollut 144:941–950CrossRefPubMedGoogle Scholar
  45. Proctor MCF (2002) Physiological ecology. In: Shaw AJ, Goffinet B (eds) Bryophyte biology. Cambridge University Press, New YorkGoogle Scholar
  46. Rice SK, Aclander L, Hanson DT (2008) Do bryophyte shoot systems function like vascular plant leaves or canopies? Functional trait relationships in Sphagnum mosses (Sphagnaceae). Am J Bot 95:1366–1374CrossRefGoogle Scholar
  47. Rodwell JS (1991) British plant communities: mires and heaths, vol 2. Cambridge University Press, CambridgeGoogle Scholar
  48. Rosevear MJ, Young AJ, Johnson GN (2001) Growth conditions are more important than species origin in determining leaf pigment content of British plant species. Funct Ecol 15:474–480CrossRefGoogle Scholar
  49. Skiba U, Pitcairn C, Sheppard L, Kennedy V, Fowler D (2004) The influence of atmospheric deposition on nitrous oxide and nitric oxide fluxes and soil ammonium and nitrate concentrations. Water Air Soil Pollut Focus 4:37–43CrossRefGoogle Scholar
  50. Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361CrossRefGoogle Scholar
  51. Taiz L, Zeiger E (1998) Plant physiology. Sinauer, SunderlandGoogle Scholar
  52. Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–409CrossRefGoogle Scholar
  53. Valanne N (1984) Photosynthesis and photosynthetic products of mosses. In: Dyer AF, Duckett JG (eds) The experimental biology of bryophytes. Academic Press, London, pp 257–273Google Scholar
  54. Van Breeman N (1995) How Sphagnum bogs down other plants. Trends Ecol Evol 10:270–275CrossRefGoogle Scholar
  55. Van der Heijden E, Verbeek SK, Kuiper PJC (2000) Elevated CO2 and increased nitrogen deposition: effects on C and N metabolism and growth of the peat moss Sphagnum recurvum P. Beauv. Var. mucronatum (Russ.) Warnst. Glob Change Biol 6:201–212CrossRefGoogle Scholar
  56. Vitt DH, Wieder RK, Halsey LA, Turetsky MR (2003) Response of Sphagnum fuscum to nitrogen deposition: a case study of ombrogenous peatlands in Alberta, Canada. Bryologist 106:235–245CrossRefGoogle Scholar
  57. Woodin SJ, Lee JA (1987) The effects of nitrate, ammonium and temperature on nitrate reductase activity in Sphagnum species. New Phytol 105:103–115CrossRefGoogle Scholar
  58. Wrolstad RE (1976) Colour and pigment analyses in fruit products. Oregon State Univ Agric Exp Stat Bull 624:1–17Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Samuel Alexander Festing Bonnett
    • 1
  • Nick Ostle
    • 2
  • Chris Freeman
    • 3
  1. 1.Institute for Sustainable Water, Integrated Management and Ecosystem ResearchUniversity of LiverpoolLiverpoolUK
  2. 2.Centre for Ecology and HydrologyLancaster Environment CentreBailrigg, LancasterUK
  3. 3.Biological Sciences, Memorial BuildingUniversity of WalesBangorUK

Personalised recommendations