Advertisement

Trees

, 22:105 | Cite as

Comparison of the performance of three different ecophysiological life forms in a sandy coastal restinga ecosystem of SE-Brazil: a nodulated N2-fixing C3-shrub (Andira legalis (Vell.) Toledo), a CAM-shrub (Clusia hilariana Schltdl.) and a tap root C3-hemicryptophyte (Allagoptera arenaria (Gomes) O. Ktze.)

  • Arthur Gessler
  • Renate Nitschke
  • Eduardo A. de Mattos
  • Henrique L. T. Zaluar
  • Fabio R. Scarano
  • Heinz Rennenberg
  • Ulrich Lüttge
Original Paper

Abstract

In a sandy coastal restinga ecosystem NE of Rio de Janeiro, Brazil, subject to environmental stress due to high irradiance, high temperature and low water supply, a comparative ecophysiological study of three species of different morphotypes and physiotypes was conducted during the dry season. The morphotypes were two shrubs, Clusia hilariana Schltdl. and Andira legalis (Vell.) Toledo, and the taproot hemicryptophyte Allagoptera arenaria (Gomes) O. Ktze. The physiotype differences were that C. hilariana was performing crassulacean acid metabolism (CAM), A. legalis was a nodulated N2 fixing legume and A. arenaria had ample access to water by ground water tapping roots. All three species were light stressed and showed photoinhibition and high maximum values of non-photochemical quenching of chlorophyll fluorescence. δ13C values of bulk leaf organic matter (which integrate over the life span of the leaf) and instantaneous gas exchange patterns demonstrated that C. hilariana was performing CAM and the other two species C3-photosynthesis. A. arenaria performed generous and A. legalis conserving use of water. Based on the CO2 concentrating mechanism of CAM C. hilariana had the highest maximum rates of apparent photosynthetic electron transport, ETRmax. Uptake of atmospheric CO2 in the afternoon (phase IV of CAM) was expressed weakly showing that the plants were under some but not severe water stress. A. legalis showed the highest levels of total N and soluble non-protein N-compounds in its organs due to N2 fixation which, however, did not confer a higher photosynthetic capacity that must have been limited by factors other than nitrogen supply. Accumulation of amino compounds like proline and γ-aminobutyric acid in leaves of A. legalis which are known to act as osmoprotectants is likely to indicate drought stress in the dry season. Maximum net CO2 uptake of photosynthesis was higher in the water spending A. arenaria than in A. legalis. The comparative analysis of physiological traits characterised either instantaneously or integrated over the longer term shows that in addition to morphotypic characteristics physiotypic characteristics are important for space occupation and niche acquisition of the plants in the restinga.

Keywords

Allagoptera arenaria Andira legalis Clusia hilariana Crassulacean acid metabolism (CAM) Photosynthesis Restinga Stable isotopes Soluble N compounds 

Notes

Acknowledgments

We thank M. Eiblmeier and P. Escher for technical assistance in the laboratory. PROBRAL (CAPES-DAAD) is acknowledged for financial support. EAM and FRS thank CNPq (Brazilian Research Council) for productivity grants.

References

  1. Adams MA, Grierson PF (2001) Stable isotopes at natural abundance in terrestrial plant ecology and ecophysiology: an update. Plant Biol 3:299–310CrossRefGoogle Scholar
  2. Ain-Lhout F, Zunzunegui M, Diaz-Barradas MC, Tirado R, Clavijo A, Garcia-Novo F (2001) Comparison of proline accumulation in two Mediterranean shrubs subjected to natural and experimental water deficit. Plant Soil 230:175–183CrossRefGoogle Scholar
  3. Araujo DSD, Scarano FR, Sá CFC, Kurtz BC, Zaluar HTL, Montezuma RCM, Oliveira RC (1998) Comunidades vegetais do Parque Nacional da Restinga de Jurubatiba. In: Esteves FA (ed) Ecologia das Lagoas Costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ). Nupem-UFRJ, Rio de Janeiro, pp 39–62Google Scholar
  4. Araujo DSD, Pereira MCA, Pimentel MCP (2004) Flora e estrutura de comunidades na restinga de Jurubatiba – Síntese dos conhecimentos com enfoque especial para a formação aberta de Clusia. In: Rocha CFD, Esteves FA, Scarano FR (eds) Pesquisas de Longa Duração na Restinga de Jurubatiba. Editora Rima, São Carlos, pp 59–76Google Scholar
  5. Barbour MM, Schurr U, Henry BK, Wong SC, Farquhar GD (2000) Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean. Evidence in support of the Péclet effect. Plant Physiol 123:671–679PubMedCrossRefGoogle Scholar
  6. Bilger W, Schreiber U, Bock M (1995) Determination of quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102:425–432CrossRefGoogle Scholar
  7. Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504CrossRefGoogle Scholar
  8. Bolarin MC, Santa-Cruz A, Cayuela E, Perez-Alfoceae E (1995) Short-term solute changes in leaves and roots of cultivated and wild tomato seedlings under salinity. J Plant Physiol 147:463–468Google Scholar
  9. Brendel O (2001). Does bulk-needle δ13C reflect short-term discrimination? Ann For Sci 58:135–141CrossRefGoogle Scholar
  10. Cirne P, Scarano FR (2001) Resprouting and growth dynamics after fire on the clonal shrub Andira legalis (Leguminosae) in a sandy coastal plain in south-eastern Brazil. J Ecol 89:351–357CrossRefGoogle Scholar
  11. Cirne P, Zaluar HLT, Scarano FR (2003) Plant diversity, interspecific associations, and postfire resprouting on a sandy spit in a Brazilian coastal plain. Ecotropica 9:33–38Google Scholar
  12. Cramer VA, Schmidt S, Stewart GR, Thornburn PJ (2002) Can the nitrogenous composition of xylem sap be used to assess salinity stress in Casuarina glauca? Tree Physiol 22:1019–1026PubMedGoogle Scholar
  13. Dias ATC, Scarano FR (2007) Clusia as nurse plant. In: Lüttge U (ed) Clusia—a woody neotropical genus with remarkable plasticity and diversity. Springer, Heidelberg, pp 55–72Google Scholar
  14. Dias ATC, de Mattos EA, Vieira SA, Azeredo JV, Scarano FR (2006) Aboveground biomass stock of native woodland on a Brazilian sandy coastal plain: estimates based on the dominant tree species. For Ecol Manage 226:364–367CrossRefGoogle Scholar
  15. Dluzniewska P, Gessler A, Dietrich H, Schnitzler J-P, Teuber M, Rennenberg H (2007) Nitrogen uptake and metabolism in Populus x canescens as affected by salinity. New Phytol 173:279–293PubMedCrossRefGoogle Scholar
  16. Dongmann G, Nürnberg HW, Förstel H, Wagener K (1974) On the enrichment of H2 18O in the leaves of transpiring plants. Radiat Environ Biophys 11:41–52PubMedCrossRefGoogle Scholar
  17. Duarte HM, Gessler A, Scarano FR, Franco AC, de Mattos EA, Nahm M, Rennenberg H, Rodigues PJFP, Zaluar HLT Lüttge U (2005) Ecophysiology of six selected shrub species in different plant communities at the periphery of the Atlantic Forest of SE-Brazil. Flora 200:456–476Google Scholar
  18. Duquesnay A, Breda N, Stievenard M, Dupouey JL (1998) Changes of tree-ring delta C-13 and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell Environ 21:565–572CrossRefGoogle Scholar
  19. Evans JR (1988) Acclimation by the thylakoid membranes to growth irradiance and the partitioning of nitrogen between soluble and thylakoid proteins. Aust J Plant Physiol 15:93–106Google Scholar
  20. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  21. Field CB (1988) On the role of photosynthetic responses in constraining the habitat distribution of rainforest plants. Aust J Plant Physiol 15:343–353Google Scholar
  22. Fotelli NM, Rennenberg H, Gessler A (2002) Effects of drought on the competitive interference of an early successional species (Rubus fruticosus) on Fagus sylvatica L. seedlings: 15N uptake and partitioning responses of amino acids and other N compounds. Plant Biol 4:311–320CrossRefGoogle Scholar
  23. Gessler A, Rennenberg H (2000) The effect of liming on the soluble nitrogen pool in Norway spruce (Picea abies) exposed to high loads of nitrogen. Phyton 40:51–64Google Scholar
  24. Gessler A, Rennenberg H, Kopriva S (2004) Regulation of nitrate uptake on the whole plant level: Interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiol 24:1313–1321PubMedGoogle Scholar
  25. Gessler A, Duarte HM, Franco AC, Lüttge U, de Mattos EA, Nahm M, Scarano FR, Zaluar HLT, Rennenberg H (2005) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE-Brazil II. Spatial and ontogenetic dynamics in Andira legalis, a deciduous legume tree. Trees 19:510–522CrossRefGoogle Scholar
  26. Gessler A, Peuke AD, Keitel C, Farquhar GD (2007) Oxygen isotope enrichment of organic matter in Ricinus communis during the diel course and as affected by assimilate transport. New Phytol 174:600–613PubMedCrossRefGoogle Scholar
  27. Haberer K, Grebenc T, Alexou M, Gessler A, Kraigher H, Rennenberg H (2007) Effects of long-term free-air ozone fumigation on δ15N and total N in Fagus sylvatica and associated mycorrhizal fungi. Plant Biol 9:242–252PubMedCrossRefGoogle Scholar
  28. Hansen J, Møller I (1975) Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal Biochem 68:87–94PubMedCrossRefGoogle Scholar
  29. Henriques RPB, Araujo DSD, Hay JD (1986) Descrição e classificação dos tipos de vegetação da restinga de Carapebus, Rio de Janeiro. Rev Brasil Bot 9:173–189Google Scholar
  30. Heuer B (1994) Osmoregulatory role of proline in water- and salt-stressed plants. In: Pessarakli M (Ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 363–381Google Scholar
  31. Keitel C, Matzarakis A, Rennenberg H, Gessler A (2006) Carbon isotope composition and oxygen isotope enrichment in phloem and total leaf organic matter of European beech (Fagus sylvatica L.) along a climate gradient. Plant Cell Environ 29:1492–1507PubMedCrossRefGoogle Scholar
  32. Kinnersley A, Turano F (2000) Gamma-aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509CrossRefGoogle Scholar
  33. Kreuzer M, Vaasen A, Scarano FR, Hampp R (2007) Mycorrhiza of Clusia species: types, abundance, responses to environmental conditions. In: Lüttge U (ed) Clusia—a woody neotropical genus with remarkable plasticity and diversity. Springer, Heidelberg, pp 235–242Google Scholar
  34. Lacerda LD, Araujo DSD, Maciel NC (1993) Dry coastal ecosystems of the tropical Brazilian coast. In: van der Maarel E (ed) Dry coastal ecosystems: Africa, America, Asia and Oceania. Elösevier, Amsterdam, pp 477–493Google Scholar
  35. Liebig M, Scarano FR, de Mattos EA, Zaluar HLT, Lüttge U (2001) Sex differentiation in the dioecious neotropical CAM tree Clusia hilariana Schltdl.: ecophysiological and floristic implications. Trees 15:278–288CrossRefGoogle Scholar
  36. Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53:2131–2142PubMedCrossRefGoogle Scholar
  37. Lüttge U (2006) Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytol 171:7–25PubMedCrossRefGoogle Scholar
  38. Lüttge U (2007a) Photosynthesis. In: Lüttge U (ed) Clusia: A woody neotropical genus of remarkable plasticity and diversity. Ecological Studies vol 194. Springer, Heidelberg, pp 135–186Google Scholar
  39. Lüttge U (2007b) Physiological ecology. In: Lüttge U (ed) Clusia: a woody neotropical genus of remarkable plasticity and diversity. Ecological studies vol 194. Springer, Heidelberg, pp 187–234Google Scholar
  40. Lüttge U, Scarano FR (2004) Ecophysiology. Revta Brasil Bot 17:1–10Google Scholar
  41. McNeill SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949CrossRefGoogle Scholar
  42. Menezes LFT, Araujo DSD (2000) Variação da biomassa aérea de Allagoptera arenaria (Gomes) O. Kuntze (Arecaceae) em uma comunidade arbustiva de Palmae na restinga de Marambaia, RJ. Rev Brasil Biol 60:147–157PubMedGoogle Scholar
  43. Nahm M, Holst T, Matzarakis A, Mayer H, Rennenberg H, Gessler A (2006) Soluble non-protein nitrogen compounds in various tissues of adult beech indicate nutritional changes mediated by local climate and silvicultural treatment. Eur J For Res 125:1–14Google Scholar
  44. Nahm M, Matzarakis A, Rennenberg H, Gessler A (2007) Seasonal courses of key parameters of nitrogen, carbon and water balance in European beech (Fagus sylvatica L.) grown on four different study sites along a European North–South climate gradient during the 2003 drought. Trees 21:79–92CrossRefGoogle Scholar
  45. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210PubMedCrossRefGoogle Scholar
  46. Pate JS, Unkovich MJ, Erskine PD, Stewart GR (1998) Australian mulga ecosystems—13C and 15N natural abundances of biota components and their ecophysiological significance. Plant Cell Environ 21:1231–1242CrossRefGoogle Scholar
  47. Rascher U, Liebig M, Lüttge U (2000) Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant Cell Environ 23:1397–1405CrossRefGoogle Scholar
  48. Reich PB, Walters MB, Ellsworth DS, Uhl C (1994) Photosynthesis-nitrogen relations in Amazonian tree species. I. Patterns among species and communities. Oecologia 97:62–72CrossRefGoogle Scholar
  49. Reinert F, Roberts A, Wilson JM, deRibas L, Cardinot G, Griffith H (1997) Gradation in nutrient composition and photosynthetic pathways across the restinga vegetation of Brazil. Bot Acta 110:135–142Google Scholar
  50. Rizzini CT (1979) Tratado de Fitogeografia do Brasil. vol. 2. Edusp, São PauloGoogle Scholar
  51. Samaras Y, Bressan R, Csonka L, Garcia-Rios MG, Paino D’Urzo M, Rhodes D (1995) Proline accumulation during drought and salinity. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific, Oxford, pp 161–187Google Scholar
  52. Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rain forest. Ann Bot 90:517–524PubMedCrossRefGoogle Scholar
  53. Scarano FR, Cirne P, Nascimento MT, Sampaio MC, Villela D, Wendt T, Zaluar HLT (2004) Ecologia Vegetal: integrando ecossistema, comunidades, populações e organismos. In: Rocha CFD, Esteves FA, Scarano FR (eds) Pesquisas de Longa Duração na Restinga de Jurubatiba: Ecologia, História Natural e Conservação. Editora Rima, São Carlos, pp 77–97Google Scholar
  54. Scarano FR, Duarte HM, Franco AC, Gessler A, de Mattos EA, Nahm M, Rennenberg H, Zaluar HLT, Lüttge U (2005a) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE Brazil I. Performance of three different species of Clusia in an array of plant communities. Trees 19:497–509CrossRefGoogle Scholar
  55. Scarano FR, Duarte HM, Franco AC, Gessler A, de Mattos EA, Rennenberg H, Lüttge U (2005b) Physiological synecology of tree species in relation to geographic distribution and ecophysiological parameters at the Atlantic forest periphery in Brazil: an overview. Trees 19:493–496CrossRefGoogle Scholar
  56. Schneider S, Gessler A, Weber P, Sengbusch D, von Hanemann U, Rennenberg H (1996) Soluble N compounds in trees exposed to high loads of N: a comparison of spruce (Picea abies) and beech (Fagus sylvatica) grown under field conditions. New Phytol 134:103–114CrossRefGoogle Scholar
  57. Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the last years in retrospect. Progr Bot 54:151–173Google Scholar
  58. Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of gamma-aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102:79–86CrossRefGoogle Scholar
  59. Sprent JI, Geoghegan IE, Whitty PW, James EK (1996) Natural abundance of 15N and 13C in nodulated legumes and other plants in the cerrado and neighbouring regions of Brazil. Oecologia 105:440–446CrossRefGoogle Scholar
  60. Thiele A, Krause GH, Winter K (1998) In situ study of photoinhibition of photosynthesis and xanthophyll cycle activity in plants growing in natural gaps of the tropical forest. Aust J Plant Physiol 25:189–195CrossRefGoogle Scholar
  61. Ule E (1901) Die Vegetation von Cabo Frio an der Küste von Brasilien. Bot Jahrb Syst 28:511–528Google Scholar
  62. Von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  63. Wanek W, Arndt SK (2002) Difference in δ15N signatures between nodulated roots and shoots of soybean is indicative of the contribution of symbiotic N2 fixation to plant N. J Exp Bot 317:1109–1118CrossRefGoogle Scholar
  64. Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotope discrimination and the economics of water and nitrogen use in photosynthesis. Plant Cell Environ 29:192–201PubMedCrossRefGoogle Scholar
  65. Winter H, Lohaus G, Heldt W (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996–1004PubMedCrossRefGoogle Scholar
  66. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514PubMedGoogle Scholar
  67. Zaluar HLT, Scarano FR (2000) Facilitação em restingas de moitas: um século de buscas por espécies focais. In: Esteves FA, Lacerda LD (eds) Ecologia de Restingas e Lagoas Costeiras. NUPEM-UFRJ, Rio de Janeiro, pp 3–23Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Arthur Gessler
    • 1
  • Renate Nitschke
    • 1
  • Eduardo A. de Mattos
    • 2
  • Henrique L. T. Zaluar
    • 2
  • Fabio R. Scarano
    • 2
  • Heinz Rennenberg
    • 1
  • Ulrich Lüttge
    • 3
  1. 1.Institut für Forstbotanik und BaumphysiologieProfessur für Baumphysiologie, Freiburg UniversityFreiburgGermany
  2. 2.Departamento de EcologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Institut für BotanikDarmstadt University of TechnologyDarmstadtGermany

Personalised recommendations