Abstract
Savanna (Cerrado) of the Brazilian Pantanal exhibits large variations in hydrology, ranging from well drained to intermittently flooded. Climate and land use change has led to the expansion of “super-dominant” tree species in both habitats, including Vochysia divergens, which is adapted to flooding, and Curatella americana, which is adapted to upland Cerrado. There is both theoretical and practical interest in evaluating the potential net photosynthesis rate of these species to help explain their success in invading new areas with widely differing hydrological regimes. We hypothesized that these species have physical or biochemical adjustments their photosynthetic characteristics that allow them to thrive in their native and invaded environments. To test these hypotheses, we measured chloroplast CO2 concentration response curves, leaf nitrogen and phosphorus concentrations, and specific leaf area of both species over a year in the Pantanal and Cerrado. Neither species displayed a significant decline in potential net photosynthesis in their invaded habitats compared to their native habitats. The relatively constant rate of leaf gas exchange may be important for their success at invading novel habitats, however, there were statistically significant interactions between species, ecosystem, and season that were due in part to complex interactions between biophysical, biochemical, and phenological variables. The specific leaf area (SLA) for both species was higher in their invaded habitats; however, V. divergens exhibited a significant decline in stomatal conductance and an increase in intrinsic water use efficiency in the Cerrado, especially during the dry season. High physiological flexibility, and the ability to maintain a relatively constant value of A, may allow these species to cope with large seasonal variations in soil hydrology and expand into habitats with completely different hydrological conditions.
Similar content being viewed by others
Abbreviations
- C i :
-
Intercellular CO2 concentration
- C a :
-
Environmental CO2 concentration
- C i/C a :
-
Relationship between partial pressure intercellular and environmental CO2
- g s :
-
Stomatal conductance
- SLA:
-
Specific leaf area
- N:
-
Mass-based leaf nitrogen concentration
- P:
-
Mass-based leaf phosphorus concentration
- A:
-
Potential net photosynthesis rate
- VPD :
-
Atmospheric vapor pressure deficit
- PPT :
-
Accumulated monthly rainfall
- WL :
-
Water level
- V cmax :
-
Capacity of RuBP carboxylation (expressed as the maximum rate of Rubisco carboxylation)
- J max :
-
Rate of regeneration of RuBP (expressed as the maximum rate of electron transport)
- TPU :
-
Triose phosphate utilization
- R d :
-
Rate of mitochondrial respiration
- Rp :
-
Photorespiration rate
- WUE :
-
Intrinsic water use efficiency
References
Baker TR, Affum-Baffoe K, Burslem DFRP, Swaine MD (2002) Phenological differences in tree water use and the timing of tropical forest inventories: conclusions from patterns of dry season diameter change. For Ecol Manage 171:261–274. doi:10.1016/S0378-1127(01)00787-3
Barrios E, Herrera R (1994) Nitrogen Cycling in a venezuelan tropical seasonally flooded forest: soil nitrogen mineralization and nitrification. J Trop Ecol 10:399–416. doi:10.2307/2560324
Braga JM, Defelipo B (1974) Spectrophotometric determination of phosphorus in soil and plant extracts. Rev Ceres 21:73–85
Bruno RD (2004) Variabilidade observada da umidade do solo em Floresta Tropical e Cerrado. Dissertação (Mestrado em Meteorologia), Instituto de Astronomia, Geofísica e Ciências Atmosféricas. Universidade de São Paulo, São Paulo
Cook AC, Tissue DT, Roberts SW, Oechel WC (1998) Effects of long-term elevated CO2 from natural CO2 springs on nardus stricta: photosynthesis, biochemistry, growth and phenology. Plant Cell Environ 21:417–425
Dalmagro HJ, Lobo FA, Ortíz CER, Biudes MS, Nogueira JS, Vourlitis GL, Pinto OB Jr (2011) Trocas gasosas de uma espécie lenhosa na floresta de transição amazônia-cerrado. Ciência e Natura 31(2):1–24
Dalmagro HJ, Lobo FA, Vourlitis GL, Dalmolin ÂC, Antunes MZJ, Ortíz CER, Nogueira JS (2013) Photosynthetic parameters of two invasive tree species of the Brazilian Pantanal in response to seasonal flooding. Photosynthetica 51:281–294. doi:10.1007/s11099-013-0024-3
Dalmagro HJ et al (2016) Physiological responses to extreme hydrological events in the Pantanal wetland: heterogeneity of a plant community containing super-dominant species. J Veg Sci. (in press)
Dalmolin ÂC, Dalmagro HJ, Lobo FA, Antunes Junior MZ, Ortíz CER, Vourlitis GL (2012) Effects of flooding and shading on growth and gas exchange of Vochysia divergens Pohl (Vochysiaceae) of invasive species in the Brazilian Pantanal. Braz J Plant Physiol 24:75–84
Dalmolin ÂC, Lobo FA, Vourlitis GL, Silva PR, Dalmagro HJ, Antunes MZ Jr, Ortíz CER (2015) Is the dry season an important driver of phenology and growth for two Brazilian savanna tree species with contrasting leaf habits? Plant Ecol 216:407–417
Eiten G (1972) The cerrado vegetation of Brazil. Bot Rev 38:201–341. doi:10.1007/BF02859158
Farquhar G, von Caemmerer SV, Berry J (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Field C, Mooney H (1986) Photosynthesis–nitrogen relationship in wild plants. In: On the economy of plant form and function: Proceedings of the Sixth Maria Moors Cabot Symposium, Evolutionary Constraints on Primary Productivity, Adaptive Patterns of Energy Capture in Plants, Harvard Forest. Cambridge University Press, Cambridge
Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189
Franco AC et al (2005) Leaf functional traits of neotropical savanna trees in relation to seasonal water deficit. Trees 19:326–335. doi:10.1007/s00468-004-0394-z
Galterman H (1978) Methods for physical and chemical analysis of fresh water IBP Handbook
Girard P, Fantin-Cruz I, de Oliveira SL, Hamilton S (2010) Small-scale spatial variation of inundation dynamics in a floodplain of the Pantanal (Brazil). Hydrobiologia 638:223–233. doi:10.1007/s10750-009-0046-9
Heldt HW, Rapley L (1970) Specific transport of inorganic phosphate, 3-phosphoglycerate and dihydroxyacetone phosphate and of dicarboxylate across the inner membrane of spinach chloroplasts. FEBS Lett 10:143–148
Herrera A, Rengifo E, Tezara W (2010) Respuestas ecofisiológicas a la inundación en árboles tropicales tolerantes de un igapó. Ecossistemas 19:37–51
Hintze J (2008) NCSS and PASS. Number cruncher statistical systems, Kaysville, UT, USA. http://www.NCSS.com
Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42:1003–1011
Junk WJ, Nunes da Cunha C (2005) Pantanal: a large South American wetland at a crossroads. Ecol Eng 24:391–401. doi:10.1016/j.ecoleng.2004.11.012
Junk W, da Cunha C, Wantzen K, Petermann P, Strüssmann C, Marques M, Adis J (2006) Biodiversity and its conservation in the Pantanal of Mato Grosso, Brazil. Aquat Sci 68:278–309. doi:10.1007/s00027-006-0851-4
Knops JMH, Reinhart K (2000) Specific leaf area along a nitrogen fertilization gradient. Am Midl Nat 144:265–272
Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer, New York. doi:10.1007/978-0-387-78341-3
Larcher W (2000) Ecofisiologia vegetal. Rima, São Carlos, São Paulo
Lorenzi H (2009) Árvores Brasileiras-Manual de Identificação e Cultivo de Plantas Arbóreas Nativas do Brasil São Paulo, Brasil, p 384
Manter DK, Kerrigan J (2004) 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
Matos DMS, Pivello VR (2009) O impacto das plantas invasoras nos recursos naturais de ambientes terrestres: alguns casos brasileiros. Ciência e Cultura 61:27–30
McDowell SC (2002) Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438. doi:10.3732/ajb.89.9.1431
Medina E, Francisco M (1994) Photosynthesis and water relations of savanna tree species differing in leaf phenology. Tree Physiol 14:1367–1381
Meir P, Levy P, Grace J, Jarvis P (2007) Photosynthetic parameters from two contrasting woody vegetation types in West Africa. Plant Ecol 192:277–287. doi:10.1007/s11258-007-9320-y
Nunes da Cunha C, Junk WJ (2004) Year-to-year changes in water level drive the invasion of Vochysia divergens in Pantanal grasslands. Appl Veg Sci 7:103–110. doi:10.1111/j.1654-109X.2004.tb00600.x
Parolin P (2000) Phenology and CO2-assimilation of trees in Central Amazonian floodplains. J Trop Ecol 16:465–473
Parolin P, Waldhoff D, Piedade MT (2011) Gas exchange and photosynthesis. Amazonian Floodplain Forests. Springer, Berlin, pp 203–222
Pezeshki SR, DeLaune RD (2012) Soil oxidation-reduction in wetlands and its impact on plant functioning. Biology 1:196
Pierce LL, Running SW, Walker J (1994) Regional-scale relationships of leaf area index to specific leaf area and leaf nitrogen. Ecol Appl 4:313–321
Pintó-Marijuan M, Munné-Bosch S (2013) Ecophysiology of invasive plants: osmotic adjustment and antioxidants. Trends Plant Sci 18:660–666
Pott A, Pott VJ (1994) Plantas do Pantanal. EMBRAPA-SPI, Corumbá
Radambrasil (1982) Levantamentos dos Recursos Naturais Ministério das Minas de Energia. Projeto RADAMBRASIL. Folha SD 21. Rio de Janeiro
Rao IM, Terry N (1989) 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
Rengifo E, Tezara W, Herrera A (2005) Water relations, chlorophyll a fluorescence, and contents of saccharides in tree species of a tropical forest in response to flood. Photosynthetica 43:203–210. doi:10.1007/s11099-005-0034-x
Rodrigues TR, Vourlitis GL, Lobo FA, Oliveira RG, Nogueira JS (2014) Seasonal variation in energy balance and canopy conductance for a tropical savanna ecosystem of south central Mato Grosso, Brazil. J Geophys Res Biogeosci 119:1–13. doi:10.1002/2013JG002472
Rossatto DR, Hoffmann WA, Franco AC (2009) Differences in growth patterns between co-occurring forest and savanna trees affect the forest–savanna boundary. Funct Ecol 23:689–698. doi:10.1111/j.1365-2435.2009.01568.x
Sanches L, Vourlitis GL, Alves MC et al (2011) Seasonal patterns of evapotranspiration for a vochysia divergens forest in the brazilian Pantanal. Wetlands 31:1215–1225
Santos SA, Nunes da Cunha C, Tomás W, Abreu UGP, Arieira J (2006) Plantas Invasoras no Pantanal: Como Entender o Problema e Soluções de Manejo por Meio de Diagnóstico Participativo. In: Empresa Brasileira de Pesquisa Agropecuária: Centro de Pesquisa Agropecuária do Pantanal, M.d.A., Pecuária e Abastecimento (ed) Embrapa Pantanal: Boletim de Pesquisa e Desenvolvimento 66. Corumbá, MS, p 45
Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73:147–152
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040
Su Y, Zhu G, Miao Z, Feng Q, Chang Z (2009) Estimation of parameters of a biochemically based model of photosynthesis using a genetic algorithm. Plant Cell Environ 32:1710–1723
Tissue DT, Griffin KL, Ball JT (1999) Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevated CO2. Tree Physiol 19(4–5):221–228. doi:10.1093/treephys/19.4-5.221
Vourlitis GL, da Rocha HR (2011) Flux dynamics in the Cerrado and Cerrado-forest transition of Brazil. In: Hill MJHN (ed) Ecosystem function in global Savannas: measurement and modeling at landscape to global scales. CRC Press, Boca Raton, p 624
Vourlitis GL, Kroon JL (2013) Growth and resource use of the invasive grass, pampasgrass (Cortaderia selloana), in response to nitrogen and water availability. Weed Sci 61:117–125
Vourlitis GL, de Almeida Lobo F, Biudes MS, Rodríguez Ortíz CE, de Souza Nogueira J (2011) Spatial variations in soil chemistry and organic matter content across a invasion front in the Brazilian Pantanal. Soil Sci Soc Am J 75:1554–1561. doi:10.2136/sssaj2010.0412
Vourlitis GL et al (2013) Variations in stand structure and diversity along a soil fertility gradient in a Brazilian savanna (Cerrado) in southern Mato Grosso. Soil Sci Soc Am J 77:1370–1379
Vourlitis GL, de Almeida Lobo F, Lawrence S, Holt K, Zappia A, Pinto O Jr, de Souza Nogueira J (2014) Nutrient resorption in tropical savanna forests and woodlands of central Brazil. Plant Ecol 215:963–975. doi:10.1007/s11258-014-0348-5
Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Transact Royal Soc B Biol Sci 355:1517–1529
Wright IJ, Reich P, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high-and low-rainfall and high-and low-nutrient habitats. Funct Ecol 15:423–434
Acknowledgments
The authors thank the Graduate Program in Environmental Physics, Universidade Federal de Mato Grosso for laboratory support, the SESC reserve – RPPN, particularly to the park-rangers for the support field and Dr. Y. Su, for his help with curve A/Cc analysis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This research was supported by the National Institute for Science and Technology in Wetlands (INAU), National Science Foundation-Office of International Science and Engineering (NSF-OISE) Grant to GLV, We acknowledge project support 457824/2013-1 of the National Council for Scientific and Technological Development and Ministry of Science and Technology (CNPq), the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT-PRONEX) and Coordination of improvement of Higher Education Personnel (CAPES), which provided scholarships to HJD, ACD and MZAJ.
Additional information
Communicated by U Feller.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dalmagro, H.J., de A. Lobo, F., Vourlitis, G.L. et al. Photosynthetic response of a wetland- and an upland-adapted tree species to seasonal variations in hydrology in the Brazilian Cerrado and Pantanal. Acta Physiol Plant 38, 107 (2016). https://doi.org/10.1007/s11738-016-2125-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2125-7