Advertisement

Photosynthetic response of a wetland- and an upland-adapted tree species to seasonal variations in hydrology in the Brazilian Cerrado and Pantanal

  • Higo J. Dalmagro
  • Francisco de A. Lobo
  • George L. Vourlitis
  • Ândrea C. Dalmolin
  • Mario Z. AntunesJr.
  • Carmen E. R. Ortíz
  • José de S. Nogueira
Original Article

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.

Keywords

Ecophysiology Curatella americana Leaf gas exchange Neotropical wetlands Vochysia divergens 

Abbreviations

Ci

Intercellular CO2 concentration

Ca

Environmental CO2 concentration

Ci/Ca

Relationship between partial pressure intercellular and environmental CO2

gs

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

Vcmax

Capacity of RuBP carboxylation (expressed as the maximum rate of Rubisco carboxylation)

Jmax

Rate of regeneration of RuBP (expressed as the maximum rate of electron transport)

TPU

Triose phosphate utilization

Rd

Rate of mitochondrial respiration

Rp

Photorespiration rate

WUE

Intrinsic water use efficiency

Notes

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.

Compliance with ethical standards

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.

Supplementary material

11738_2016_2125_MOESM1_ESM.docx (1.2 mb)
Supplementary material 1 (DOCX 1187 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. Braga JM, Defelipo B (1974) Spectrophotometric determination of phosphorus in soil and plant extracts. Rev Ceres 21:73–85Google Scholar
  4. 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 PauloGoogle Scholar
  5. 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 21:417–425CrossRefGoogle Scholar
  6. 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):1–24Google Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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) Google Scholar
  9. 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 24:75–84CrossRefGoogle Scholar
  10. 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 216:407–417CrossRefGoogle Scholar
  11. Eiten G (1972) The cerrado vegetation of Brazil. Bot Rev 38:201–341. doi: 10.1007/BF02859158 CrossRefGoogle Scholar
  12. Farquhar G, von Caemmerer SV, Berry J (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefPubMedGoogle Scholar
  13. 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, CambridgeGoogle Scholar
  14. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. Galterman H (1978) Methods for physical and chemical analysis of fresh water IBP HandbookGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 10:143–148CrossRefPubMedGoogle Scholar
  19. Herrera A, Rengifo E, Tezara W (2010) Respuestas ecofisiológicas a la inundación en árboles tropicales tolerantes de un igapó. Ecossistemas 19:37–51Google Scholar
  20. Hintze J (2008) NCSS and PASS. Number cruncher statistical systems, Kaysville, UT, USA. http://www.NCSS.com
  21. Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42:1003–1011CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. Knops JMH, Reinhart K (2000) Specific leaf area along a nitrogen fertilization gradient. Am Midl Nat 144:265–272CrossRefGoogle Scholar
  25. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer, New York. doi: 10.1007/978-0-387-78341-3 CrossRefGoogle Scholar
  26. Larcher W (2000) Ecofisiologia vegetal. Rima, São Carlos, São PauloGoogle Scholar
  27. Lorenzi H (2009) Árvores Brasileiras-Manual de Identificação e Cultivo de Plantas Arbóreas Nativas do Brasil São Paulo, Brasil, p 384Google Scholar
  28. 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 55:2581–2588CrossRefPubMedGoogle Scholar
  29. Matos DMS, Pivello VR (2009) O impacto das plantas invasoras nos recursos naturais de ambientes terrestres: alguns casos brasileiros. Ciência e Cultura 61:27–30Google Scholar
  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 CrossRefPubMedGoogle Scholar
  31. Medina E, Francisco M (1994) Photosynthesis and water relations of savanna tree species differing in leaf phenology. Tree Physiol 14:1367–1381CrossRefPubMedGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 Google Scholar
  34. Parolin P (2000) Phenology and CO2-assimilation of trees in Central Amazonian floodplains. J Trop Ecol 16:465–473CrossRefGoogle Scholar
  35. Parolin P, Waldhoff D, Piedade MT (2011) Gas exchange and photosynthesis. Amazonian Floodplain Forests. Springer, Berlin, pp 203–222Google Scholar
  36. Pezeshki SR, DeLaune RD (2012) Soil oxidation-reduction in wetlands and its impact on plant functioning. Biology 1:196CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pierce LL, Running SW, Walker J (1994) Regional-scale relationships of leaf area index to specific leaf area and leaf nitrogen. Ecol Appl 4:313–321CrossRefGoogle Scholar
  38. Pintó-Marijuan M, Munné-Bosch S (2013) Ecophysiology of invasive plants: osmotic adjustment and antioxidants. Trends Plant Sci 18:660–666CrossRefPubMedGoogle Scholar
  39. Pott A, Pott VJ (1994) Plantas do Pantanal. EMBRAPA-SPI, CorumbáGoogle Scholar
  40. Radambrasil (1982) Levantamentos dos Recursos Naturais Ministério das Minas de Energia. Projeto RADAMBRASIL. Folha SD 21. Rio de JaneiroGoogle Scholar
  41. 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 90:814–819CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Sanches L, Vourlitis GL, Alves MC et al (2011) Seasonal patterns of evapotranspiration for a vochysia divergens forest in the brazilian Pantanal. Wetlands 31:1215–1225CrossRefGoogle Scholar
  46. 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 45Google Scholar
  47. Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73:147–152CrossRefGoogle Scholar
  48. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040CrossRefPubMedGoogle Scholar
  49. 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 32:1710–1723CrossRefPubMedGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. 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 624Google Scholar
  52. 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 61:117–125CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 77:1370–1379CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 355:1517–1529CrossRefGoogle Scholar
  57. 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 15:423–434CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2016

Authors and Affiliations

  • Higo J. Dalmagro
    • 1
  • Francisco de A. Lobo
    • 2
  • George L. Vourlitis
    • 3
  • Ândrea C. Dalmolin
    • 4
  • Mario Z. AntunesJr.
    • 5
  • Carmen E. R. Ortíz
    • 6
  • José de S. Nogueira
    • 7
  1. 1.Programa de Pós Graduação em Ciências AmbientaisUniversidade de Cuiabá, UNICCuiabáBrazil
  2. 2.Departamento de Solos, Engenharia Rural e ZootecniaUniversidade Federal de Mato Grosso, UFMTCuiabáBrazil
  3. 3.Biological Sciences DepartmentCalifornia State UniversitySan MarcosUSA
  4. 4.Departamento de Ciências BiológicasUniversidade Estadual de Santa Cruz, UESCIlhéusBrazil
  5. 5.Centro Universitário de Várzea Grande, UNIVAGVárzea GrandeBrazil
  6. 6.Departamento de Botânica e Ecologia, Instituto de BiociênciasUniversidade Federal de Mato Grosso, UFMTCuiabáBrazil
  7. 7.Programa de Pós-Graduação em Física Ambiental, Instituto de FísicaUniversidade Federal de Mato Grosso, UFMTCuiabáBrazil

Personalised recommendations