Abstract
The Pantanal is the largest wetland in the world with extremely high plant and animal diversity, but large areas have been invaded by Vochysia divergens Pohl (Vochysiaceae), a tree that is native to the Amazon Basin, and Curatella americana L. (Dilleniaceae), a tree that is native to the Brazilian savanna (cerrado). V. divergens is reportedly floodadapted, thus its ability to invade the Pantanal may not be surprising, but the invasion of C. americana is counterintuitive, because this species is adapted to the well-drained soils of the cerrado. Thus, we were interested in comparing the photosynthetic capacity, in terms of CO2 conductance, carboxylation, and electron transport of these species over a seasonal flooding cycle. Given that V. divergens is reportedly flood-adapted, we predicted that this species would have a higher photosynthetic capacity than C. americana, especially under flooding. To test this hypothesis we measured the photosynthetic CO2 response (P N/C c) of V. divergens and C. americana within 1 year to determine, if photosynthetic capacity varied systematically over time and between species. Contrary to our hypothesis, V. divergens did not always have a higher photosynthetic capacity than C. americana. Rather, species differences were influenced by temporal variations in flooding and the leaf age. Leaf CO2 assimilation and photosynthetic capacity of both species were lower during the flood period, but the differences were not statistically significant. The physiological performance of both species was strongly related to leaf N and P concentrations, but P limitation appeared to be more important than N limitation for these species and ecosystem. Photosynthetic capacity was higher and more stable for V. divergens, but such an advantage did not result in a statistically significant increase in P N. Our results suggest that both species are tolerant to flooding even though they are adapted to very different hydrological conditions. Such physiological plasticity, especially for C. americana, might be a key feature for the ability to survive and persist in the seasonally flooded Pantanal.
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Abbreviations
- C c :
-
molar concentration of CO2 in the chloroplast
- C i :
-
molar concentration of CO2 in the intercellular air space
- ET:
-
evapotranspiration
- g m :
-
mesophyll conductance
- g s :
-
stomatal conductance
- J max :
-
light-saturated rate of electron transport
- L:
-
leaf age
- N:
-
concentration of nitrogen
- P:
-
concentration of phosphorus
- P N :
-
net photosynthesis
- P N/C c :
-
photosynthetic response curves to variations in concentration of CO2 in the chloroplast
- PPFD:
-
photosynthetic photon flux density
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase
- S:
-
species
- SLA:
-
specific leaf area
- T:
-
time
- TPU:
-
triose phosphate utilization
- T l :
-
leaf temperature
- V cmax :
-
maximum rate of Rubisco activity
- VPD:
-
atmospheric vapor pressure deficit
- YL:
-
young leaves
- OL:
-
old leaves
- Γ:
-
CO2 compensation point
- Γ*:
-
CO2 compensation point in the absence of mitochondrial respiration
References
Adam, N.R., Wall, G.W., Kimball, B.A. et al.: Acclimation response of spring wheat in a free-air CO2 enrichment (FACE) atmosphere with variable soil nitrogen regimes. 1. Leaf position and phenology determine acclimation response. — Photosynth. Res. 66: 65–77, 2000.
Aerts, R., Chapin, F.S.: The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. — Adv. Ecol. Res. 30: 1–67, 2000.
Arieira, J., Nunes da Cunha, C.: [Phytosocialogy of a flooded forest monodiminant with Vochysia divergens Pohl (Vochysiaceae) in the northern Pantanal, Mato Grosso, Brazil.] — Acta Bot. Bras. 20: 569–580, 2006. [In Port.]
Baruch, Z., Goldstein, G.: Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. — Oecologia 121: 183–192, 1999.
Biudes, M.S., Valentini, C.M.A., Campelo, J.H., Jr., Nogueira, J.de S.: [Estimating evapotranspiration in a mixed pasture of the cerrado using the Bowen ratio and Penman-Monteith methods.] — Ciência Natura 30: 71–86, 2008. [In Port.]
Braga, J.M., Defelipo, B.V.: [Spectrophotometric determination of phosphorus in soil and plant extracts.]. — Rev. Ceres 21: 73–85, 1974. [In Port.]
Carswell, F.E., Meir, P., Wandelli, E.V. et al.: Photosynthetic capacity in a central Amazonian rain forest. — Tree Physiol. 20: 179–186, 2000.
Coste, S., Roggy, J.C., Imbert, P. et al.: Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance. — Tree Physiol. 25: 1127–1137, 2005.
Crawford, R.M.M.: Oxygen availability as an ecological limit to plant distribution. — In: Begon, M., Fitter, A.H. (ed.): Advances in Ecological Research. Vol. 23. Pp. 93–185. Academic Press, New York 1992.
Dalmolin, Â.C., Dalmagro, H.J., de Lobo, F.A. et al.: Effects of flooding and shading on growth and gas exchange of Vochysia divergens (Vochysiaceae) an invasive species in the Brazilian Pantanal. — Braz. J. Plant Physiol. 24: 75–84, 2012.
Domingues, T.F., Berry, J.A., Martinelli, L.A. et al.: Parameterization of canopy structure and leaf-level gas exchange for an eastern Amazonian tropical rain forest (Tapajos National Forest, Pará, Brazil). — Earth Interact. 9: 1–23, 2005.
Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. — An. Rev. Plant Physiol. 48: 223–250, 1997.
Eiten, G.: The cerrado vegetation of Brazil. — Bot. Rev. 38: 201–341, 1972.
Epron, D., Goddard, D., Cornic, G., Gentry, B.: Limitation of net CO2 assimilation rate by internal resistance to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). — Plant Cell Environ. 18: 43–51, 1995.
Epstein, E., Bloom, A.J.: Mineral Nutrition of Plants: Principles and Perspectives. 2nd Ed. — Sinauer Associates, Sunderland 2005.
Farquhar, G.D., von Caemmerer, S., Berry, J.A.: A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. — Planta 149: 78–90, 1980.
Farquhar, G.D., Wong, S.C.: An empirical model of stomatal conductance. — Aust. J. Plant Physiol. 11: 191–210, 1984.
Field, C., Mooney, H.A.: The photosynthesis-nitrogen relationship in wild plants. — In: Givnish, T. (ed.): On the Economy of Plant Form and Function. Pp. 25–55. Cambridge Univ. Press, Cambridge 1986.
Furley, P.A., Ratter, J.A.: Soil resources and plant communities of the central Brazilian cerrado and their development. — J. Biogeogr. 15: 97–108, 1988.
Goldstein, G., Rada, F., Rundel, P. et al.: Gas exchange and water relations of evergreen and deciduous tropical savanna trees. — Ann. Sci. For. 46: 448–453, 1989.
Golterman, H.L., Clymo, R.S., Ohnstad, M.A.M.: Methods for Physical and Chemical Analysis of Fresh Water. — Blackwell Sci. Publications, Oxford 1978.
Grotkopp, E., Rejmánek, M.: High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. — Amer. J. Bot. 94: 526–532, 2007.
Gulías, J., Flexas, J., Mus, M. et al.: Relationship between maximum leaf photosynthesis, nitrogen content and specific leaf area in Balearic endemic and non-endemic Mediterranean species. — Ann. Bot. 92: 215–222, 2003.
Haase, R.: Litterfall and nutrient return in seasonally flooded and non-flooded forest of the Pantanal, Mato Grosso, Brazil. — Forest Ecol. Man. 117: 129–147, 1999.
Harley, P.C., Thomas, R.B., Reynolds, J.F., Strain, B.R.: Modelling photosynthesis of cotton grown in elevated CO2. — Plant Cell Environ. 15: 271–282, 1992.
Heldt, H.W., Rapley, L.: Specific transport of inorganic phosphate, 3-phosphoglycerate and dihydroxyacetone phosphate and of dicarboxylate across the inner membrane of spinach chloroplasts. — FEBS Letters 10: 143–148. 1970.
Iwanaga, F., Yamamoto, F.: Effects of flooding depth on growth, morphology and photosynthesis in Alnus japonica species. — New Forest. 35: 1–14, 2008.
Jacob, J., Lawlor, D.W.: Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. — J. Exp. Bot. 42: 1003–1011, 1991.
Junk, W.J., Nunes da Cunha, C.: Pantanal: a large South American wetland at a crossroads. — Ecol. Eng. 24: 391–401, 2005.
Junk, W.J., Nunes da Cunha, C., Wantzen, K.M. et al.: Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. — Aqu. Sci. 68: 278–309, 2006.
Kenzo, T., Ichie, T., Watanabe, Y. et al.: Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in tropical rain forest. — Tree Physiol. 26: 865–873, 2006.
Kitajima, K., Mulkey, S.S., Samaniego, M., Wright, S.J.: Decline of photosynthetic capacity with leaf age and position in two tropical pioneer tree species. — Amer. J. Bot. 89: 1925–1932, 2002.
Kramer, K., Vreudenhil, S.J., van der Werf, D.C.: Effects of flooding on recruitment, damage and mortality of riparian tree species: A field and simulation study on Rhine floodplain. — Forest Ecol. Man. 255: 3893–3903, 2008.
Kozlowski, T.T.: Flooding and Plant Growth. — Academic Press, San Diego 1984.
Long, S.P., Postl, W.F., Bolhár-Nordenkampf, H.R.: Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic groupings. — Planta 189: 226–234, 1993.
Long, S.P., Zhu, X., Naidu, S.L., Ort, D.R.: Can improvement in photosynthesis increase crop yields? — Plant Cell Environ. 29: 315–330, 2006.
Lopes, A.S., Cox, F.R.: Cerrado vegetation in Brazil: an edaphic gradient. — Agron. J. 69: 828–831, 1977.
Lorenzi, H.: [Brazilian Trees.] — Instituto Plantarum de Estudos da Flora, São Paulo 2002. [In Port.]
Mack, R.N., Simberloff, D., Lonsdale, W.M. et al.: Biotic invasions: causes, epidemiology, global consequences, and control. — Ecol. Appl. 10: 689–710, 2000.
McDowell, N., Pockman, W.T., Allen, C.D. et al.: Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? — New Phytol. 178: 719–739, 2008.
Manter, D.K., Kerrigan, J.: A/Ci curve analysis across a range of woody plant species: influence of regression analysis parameters and mesophyll conductance. — J. Exp. Bot. 55: 2581–2588, 2004.
Maurenza, D., Marenco, R.A., Piedade, M.T.F.: [Effect of long term inundation on the growth of Pouteria glomerata (Sapotaceae), a tree of the Central Amazon Varzea.] — Acta Amer. 39: 519–526, 2009. [In Port.]
Maurenza, D., Marenco, R.A., Parolin, P., Piedade, M.T.F.: Physiological responses to flooding and light in two tree species native to the Amazonian floodplains. — Aqua. Bot. 96: 7–13, 2011.
Medina, E., Francisco, M.: Photosynthesis and water relations of savanna tree species differing in leaf phenology. — Tree Physiol. 14: 1367–1381, 1994.
Medina, E.: Physiological ecology of neotropical savanna plants. — In: Huntley, B.J., Walker, B.H. (ed.): Ecology of Tropical Savannas. Ecological Studies Series 42. Pp 308–335. Springer-Verlag, Berlin 1982.
Mielke, M.S., Almeida, A.F., Gomes, F.P. et al.: Leaf gas exchange, chlorophyll fluorescence and growth responses of Genipa americana seedlings to soil flooding. — Environ. Exp. Bot. 50: 221–231, 2003.
Nunes da Cunha, C., Junk, W.J.: Distribution of woody plants communities along the flood gradient in the Pantanal of Poconé, Mato Grosso, Brazil. — Int. J. Ecol. Environ. Sci. 27: 63–70, 2001.
Nunes da Cunha, C., Junk, W.J.: Year-to-year changes in water level drive the invasion of Vochysia divergens in Pantanal grasslands. — Appl. Veg. Sci. 7: 103–110, 2004.
Oliveira, V.C., Joly, C.A.: Flooding tolerance of Calophyllum brasiliense Camb. (Clusiaceae): morphological, physiological and growth response. — Trees 24: 185–193, 2010.
Parolin, P., Armbrüster, N., Junk, W.J.: Two Amazonian Trop. Ecol. 47: 243–250, 2006.
Parolin, P., Lucas, C., Piedade, M.T.F., Wittmann, F.: Drought responses of flood-tolerant trees in Amazonian floodplains. — Ann. Bot. 105: 129–139, 2010a.
Parolin, P., Waldhoff, D., Piedade, M.T.F.: Gas exchange and photosynthesis. — In: Junk, W, Piedade, M.T.F., Wittmann, F; Schoengart, J, Parolin, P. (ed.).: Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management (Ecological Studies). Pp. 195–214. Springer, Dordrecht 2010b.
Pezeshki, S.R., Pardue, J.H., DeLaune, R.D.: Leaf gas exchange and growth of flood-tolerant and flood-sensitive tree species under low soil redox conditions. — Tree Physiol. 16: 453–458, 1996.
Pezeshki, S.R., DeLaune, R.D.: Responses of seedlings of selected woody species to soil oxidation-reductions. — Environ. Exp. Bot. 40: 123–133, 1998.
Piedade, M.T.F., Ferreira, C.S., Wittmann, A.O. et al.: Biochemistry of Amazonian floodplain trees. — In: Junk, W., Piedade, M.T.F., Wittmann, F., et al. (ed.): Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management (Ecological Studies). Pp. 123–134. Springer, Dordrecht 2010.
Pott, A., Pott, V.J.: [Plants of the Pantanal.] — Embrapa — CPAP, Corumbá 1994. [In Port.]
Rao, M., Terry, N.: Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes. — Plant Physiol. 90: 814–819, 1989.
Reich, P.B., Ellsworth, D.S., Walters, M.B.: Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: Evidence from within and across species and functional groups. — Funct. Ecol. 12: 948–958, 1998.
Rejmánek, M., Richardson, D.M.: What attributes make some plant species more invasive? — Ecology 77: 1655–1661, 1996.
Rhodenbaugh, E.J., Pallardy, S.G.: Water stress, photosynthesis and early growth patterns of cuttings of three Populus clones. — Tree Physiol. 13: 213–226, 1993.
Sanches, L., Vourlitis, G.L., Alves, M.C. et al.: Seasonal patterns of evapotranspiration for a Vochysia divergens forest in the Brazilian Pantanal. — Wetlands 31: 1215–1225, 2011.
Santos, S.A., Nunes da Cunha, N., Tomás, W. et al.: [Invasive plants of the Pantanal: How to understand the problem and management solutions by means of participatory diagnosis.]. — Embrapa Pantanal Boletim de Pesquisa e Desenvolvimento 66 — Empresa Brasileira de Pesquisa Agropecuária: Centro de Pesquisa Agropecuária do Pantanal, Ministério da Agricultura, Pecuária e Abastecimento, Corumbá 2006.
Sarmiento, G.: The Ecology of Neotropical Savannas. — Univ. Press, Harvard 1984.
Sharkey, T.D., Bernacchi, C.J., Farquhar, G.D., Singsaas, E.L.: Fitting photosynthetic carbon dioxide response curves for C3 leaves. — Plant Cell Environ. 30: 1035–1040, 2007.
Smith, E.W., Tolbert, N.E., Ku, H.S.: Variables affecting the CO2 compensation point. — Plant Physiol. 58: 143–146, 1976.
Sinclair, T.R., Purcell, L.C., Sneller, C.H.: Crop transformation and the challenge to increase yield potential. — Trends Plant Sci. 9: 70–75, 2004.
Stitt, M., Huber, S., Kerr, P.: Control of photosynthetic sucrose formation. — In: Stumpf, P.K., Conn, E.E. (ed.): The Biochemistry of Plants. Vol 10. Pp. 327–409. Academic Press, San Diego - New York - Berkeley - Boston - London - Sydney - Tokyo - Toronto 1987.
Su, Y., Zhu, G., Miao, Z. et al.: Estimation of parameters of a biochemically based model of photosynthesis using a genetic algorithm. — Plant Cell Environ. 32: 1710–1723, 2009.
Terashima, I., Hikosaka, K.: Comparative ecophysiology of leaf and canopy photosynthesis. — Plant Cell Environ. 18: 1111–1128, 1995.
Terry, N., Ulrich, A.: Effects of phosphorus deficiency on the photosynthesis and respiration of leaves of sugar beet. — Plant Physiol. 51: 43–47, 1973.
Vitousek, P.M.: Litterfall, nutrient cycling, and nutrient limitation in tropical forests. — Ecology 65: 285–298, 1984.
von Caemmerer, S., Evans, J.R.: Enhancing C3 photosynthesis. — Plant Physiol. 154: 589–592, 2010.
Vourlitis, G.L., de Lobo, F.A., Biudes, M.S. et al.: Spatial variations in soil chemistry and organic matter content across a Vochysia divergens invasion front in the Brazilian Pantanal. — Soil Sci. Soc. Amer. J. 75: 1553–1560, 2011.
Wilkinson, S., Davies, W.J.: ABA-based chemical signaling: the co-ordination of responses to stress in plants. — Plant Cell Environ. 25: 195–210, 2002.
Wullschleger, S.D.: Biochemical limitations to carbon assimilation in C3 plants a retrospective analysis of the A/Ci curves from 109 species. — J. Exp. Bot. 44: 907–920, 1993.
Zeilhofer, P.: Soil mapping in the Pantanal of Mato Grosso, Brazil, using multitemporal Landsat TM data. — Wetl. Ecol. Man. 14: 445–461, 2006.
Zeilhofer, P., Schessl, M.: Relationship between vegetation and environmental conditions in the northern Pantanal of Mato Grosso, Brazil. — J. Biogeogr. 27: 159–168, 1999.
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Acknowledgments: This research was supported by the National Institute for Science and Technology in Wetlands (INAU), National Council for Scientific and Technological Development and Ministry of Science and Technology (CNPq/MCT), National Science Foundation-Office of International Science and Engineering (NSF-OISE), Research Foundation of Mato Grosso (FAPEMAT) and Coordination of Improvement of Higher Education Personnel (CAPES), which provided scholarships to the authors (Dalmagro, Dalmolin, and Antunes Jr.). The authors thank the Graduate Program in Environmental Physics, Universidade Federal de Mato Grosso for laboratory support. The authors thank the Long Term Ecological Research (PELD), in particular, Susana Souza dos Santos and the RPPN-SESC park rangers, for their logistical support.
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Dalmagro, H.J., de Lobo, F.A., Vourlitis, G.L. et al. Photosynthetic parameters of two invasive tree species of the Brazilian Pantanal in response to seasonal flooding. Photosynthetica 51, 281–294 (2013). https://doi.org/10.1007/s11099-013-0024-3
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DOI: https://doi.org/10.1007/s11099-013-0024-3