Advertisement

Trees

pp 1–14 | Cite as

Maximum CO2 assimilation in young Eucalyptus plantations is higher than in Brazilian savanna trees during dry field seasons

  • Mariana G. ReisEmail author
  • Aristides Ribeiro
  • Elton E. N. Alves
  • Yhasmin P. Rody
  • Rodolfo A. Loos
  • Aline A. Vasconcelos
  • Wagner L. Araújo
Original Article
  • 64 Downloads

Abstract

Key message

In terms of some specifics parameters, Eucalyptus and savanna trees were characterized by similar responses of resource use under field conditions. Remarkably, young eucalypt exhibited greater photosynthetic capacity, primarily in the dry season.

Abstract

Although a growing demand for paper and pulp is enhancing pressure for land use to increase eucalypt plantations in tropical savanna regions around the world, it has not been thoroughly characterized to date how eucalypt plantations perform in terms of energy, water and CO2 assimilation exchange compared to native savanna species. In this study, we performed an integrative analysis of diurnal changes in gas exchange, chlorophyll fluorescence (Fv/Fm) and water use efficiency of eucalypt and savanna species over a whole year in the Brazilian tropical savanna region in eastern Mato Grosso do Sul State. We also evaluated the response curves of net photosynthetic rate (A) in response to photosynthetic photon flux density in leaves of these species during both wet and dry seasons. Although dry season conditions led to decreases in all parameters, primarily in stomatal conductance (gs), Fv/Fm values remained above the level that causes photoinhibition. Young eucalypt exhibited mostly similar Amax values in wet and dry seasons, but adult eucalypt and savanna trees decreased their Amax by 83% and 69% in the dry season, respectively. Overall, all species were similar in photosynthetic terms and intrinsic water use efficiency (WUEi), as demonstrated via principal component analysis. Despite major differences between wet and dry seasons, eucalypt plantations and savanna woody species were characterized by similar responses of resource use efficiency under field conditions. Remarkably, young eucalypt was characterized by higher photosynthetic capacity, particularly during the dry season.

Keywords

Apparent quantum efficiency Brazilian savanna Chlorophyll fluorescence Eucalyptus grandis Leaf gas exchange Light response curve Water use efficiency 

Notes

Acknowledgements

We are grateful to Fibria Celulose S.A. for financial support and for logistical and human resources. The contributions of all field staff of Fibria Celulose S.A. are gratefully acknowledged, in addition to the support of Ms. Hugo Thaner dos Santos and Ms. Marcel Carvalho Abreu with the statistical analysis. We equally acknowledge Dr. Richard W. Bell (Murdoch University) for critical English language review of and suggestions regarding this work. We also thank two anonymous reviewers for their comments and suggestions which helped improve the manuscript.

Funding

This research was financially supported by the National Council for Scientific and Technological Development (CNPq, process 184179/2015-1), Coordination for Scientific Support for Post-Graduate Level Training (CAPES), Foundation for Research Assistance of the Minas Gerais State (FAPEMIG) and Fibria Celulose S.A. Company.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2018_1800_MOESM1_ESM.docx (265.5 mb)
Supplementary material 1 (DOCX 271874 KB)

References

  1. ABRAF (2013) Abraf Statistical Yearbook, base year 2012. Brazilian Association of Forest Plantation Producers, Brasília, p 148Google Scholar
  2. Almeida AC, Soares JV, Landsberg JJ, Rezende GD (2007) Growth and water balance of Eucalyptus grandis hybrid plantations in Brazil during a rotation for pulp production. For Ecol Manag 251:10–21CrossRefGoogle Scholar
  3. Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728CrossRefGoogle Scholar
  4. Alvares CA, Sentelhas PC, Mattos EM, Miranda AC, Moraes WB, Silva PHM, Furtado EL, Stape JL (2016) Climatic favourability zones for Eucalyptus rust in Brazil. Forest Pathol 47:1–17Google Scholar
  5. Arndt SK, Sanders GJ, Bristow M, Hutley LB, Beringer J, Livesley SJ (2015) Vulnerability of native savanna trees and exotic Khaya senegalensis to seasonal drought. Tree Physiol 35:783–791CrossRefGoogle Scholar
  6. Arunyawat S, Shrestha RP (2016) Assessing land use change and its impact on ecosystem services in Northern Thailand. Sustainability 8:1–22CrossRefGoogle Scholar
  7. Baker IT, Harper AB, da Rocha HR, Denning AS, Araújo AC, Borma LS, Freitas HC, Goulden ML, Manzi AO, Miller SD, Nobre AD, Restrepo Coupe N, Saleska SR, StöckliR, von Randow C, Wofsy SC (2013) Surface ecophysiological behavior across vegetation and moisture gradients in tropical South America. Agric For Meteorol 182– 183:177–188CrossRefGoogle Scholar
  8. Binkley D, Stape JL, Ryan MG (2004) Thinking about efficiency of resource use in forests. For Ecol Manag 193:5–14CrossRefGoogle Scholar
  9. Binkley D, Stape JL, Bauerle WL, Ryan MG (2010) Explaining growth of individual trees: light interception and efficiency of light use by Eucalyptus at four sites in Brazil. For Ecol Manag 259:1704–1713CrossRefGoogle Scholar
  10. Björkman O, Demmig B (1987) Photo yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:61–66CrossRefGoogle Scholar
  11. Campoe OC, Stape JL, Laclau JP, Marsden C, Nouvellon Y (2012b) Stand level patterns of carbon fluxes and partitioning in a Eucalyptus grandis plantation across a gradient of productivity, in São Paulo state, Brazil. Tree Physiol 32:696–706CrossRefGoogle Scholar
  12. Campoe OC, Stape JL, Albaugh TJ, Allen HL, Fox TR, Rubilar R, Binkley D (2013a) Fertilization and irrigation effects on tree level aboveground net primary production, light interception and light use efficiency in a loblolly pine plantation. For Ecol Manag 288:43–48CrossRefGoogle Scholar
  13. Campoe OC, Stape JL, Nouvellon Y, Laclau JP, Bauerle WL, Binkley D, Maire GL (2013b) Stem production, light absorption and light use efficiency between dominant and non-dominant trees of Eucalyptus grandis across a productivity gradient in Brazil. For Ecol Manag 288:14–20CrossRefGoogle Scholar
  14. Campoe OC, Munhoz JS, Alvares CA, Carneiro RL, de Mattos EM, Ferez APC, Stape JL (2016) Meteorological seasonality affecting individual tree growth in forest plantations in Brazil. Forest Ecol Manag 380:149–160CrossRefGoogle Scholar
  15. Chen YP, Chen YN, LI WH, Xu CC (2006) Characterization of photosynthesis of Populus euphratica grown in the arid region. Photosynthetica 44:622–626CrossRefGoogle Scholar
  16. Cleverly J, Boulain N, Villalobos-Vega R, Grant N, Faux R, Wood C, Cook PC, Yu Q, Leigh A, Eamus D (2013) Dynamics of component carbon fluxes in a semi-arid Acacia woodland, central Australia. J Geophys Res-Biogeo 118:1168–1185CrossRefGoogle Scholar
  17. Colodette JL, Gomes CM, Gomes FJ, Cabral CP (2014) The Brazilian wood biomass supply and utilization focusing on eucalypt. Chem Biol Technol Agric 1:1–8CrossRefGoogle Scholar
  18. Costa AC, Rezende-Silva SL, Megguer CA, Moura LMF, Rosa M, Silva AA (2015) The effect of irradiance and water restriction on photosynthesis in young jatobá-do-cerrado (Hymenaea stigonocarpa) plants. Photosynthetica 53:118–127CrossRefGoogle Scholar
  19. da Rocha HR, Freitas HC, Rosolem R, Juarez R, Tannus RN, Ligo MA, Cabral OMR, Silva Dias MAF (2002) Measurements of CO2 exchange over a woodland savanna (Cerrado Sensu strictu) in southeast Brazil. Biota Neotrop 2:1–11CrossRefGoogle Scholar
  20. da Rocha HR, Manzi AO, Cabral OM, Miller SD, Goulden ML, Saleska SR, Coupe NR, Wofsy SC, Borma LS, Artaxo P, Vourlitis G, Nogueira JS, Cardoso FL, Nobre AD, Kruijt B, Freitas HC, von Randow C, Aguiar RG, Maia JF (2009) Patterns of water and heat flux across a biome gradient from tropical forest to savanna in Brazil. J Geophys Res 114:1–8CrossRefGoogle Scholar
  21. Dalmagro HJ, Lobo FA, Vourlitis GL, Dalmolin AC, Antunes Jr MZ, Ortíz CER, Nogueira JS (2014) The physiological light response of two tree species across a hydrologic gradient in Brazilian savanna (Cerrado). Photosynthetica 52:22–35CrossRefGoogle Scholar
  22. De Almeida MR, Aumond M, Da Costa CT, Schwambach J, Ruedell CM, Correa LR, Fett-Neto AG (2017) Environmental control of adventitious rooting in Eucalyptus and Populus cuttings. Trees 31:1377–1390CrossRefGoogle Scholar
  23. de Lara NOT, da Silva MR, Nogueira A, Marcati CR (2017) Duration of cambial activity is determined by water availability while cambial stimulus is day-length dependent in a Neotropical evergreen species. Environ Exp Bot 141:50–59CrossRefGoogle Scholar
  24. Dias LCP, Pimenta FM, Santos AB, Costa MH, Ladle RJ (2016) Patterns of land use, extensification, and intensification of Brazilian agriculture. Glob Change Biol 22:2887–2903CrossRefGoogle Scholar
  25. Eamus D, Hutley LB, O’Grady AP (2001) Daily and seasonal patterns of carbon and water fluxes above a north Australian savanna. Tree Physiol 21:977–988CrossRefGoogle Scholar
  26. Eamus D, Cleverly J, Boulain N, Grant N, Faux R, Villalobos-Vega R (2013) Carbon and water fluxes in an arid-zone Acacia savanna woodland: An analyses of seasonal patterns and responses to rainfall events. Agric For Meteorol 182–183:225–238CrossRefGoogle Scholar
  27. Eiten G (1972) The cerrado vegetation of Brazil. Bot Rev 38:201–341CrossRefGoogle Scholar
  28. Epron D, Laclau JP, Almeida JCR, Gonçalves JLM, Ponton S, SetteJr CR, Delgado-Rojas JS, Bouillet JP, Nouvellon Y (2011) Do changes in carbon allocation account for the growth response to potassium and sodium applications in tropical. Eucalyptus Plantations? Tree Physiol 32:667–679CrossRefGoogle Scholar
  29. Fan PG, Li LS, Duan W, Li WD, Li S (2010) Photosynthesis of young apple trees in response to low sink demand under different air temperatures. Tree Physiol 30:313–325CrossRefGoogle Scholar
  30. Fan Z, Neff JC, Hanan NP (2015) Modeling pulsed soil respiration in an African savanna ecosystem. Agr Forest Meteorol 200:282–292CrossRefGoogle Scholar
  31. FAO (2014) State of the word’s forest. Food and Agriculture Organization of the United Nations, Rome, p 133Google Scholar
  32. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Phys 40:503–537CrossRefGoogle Scholar
  33. Forrester DI, Collopy JJ, Beadle CL, Baker TG (2013) Effect of thinning, pruning and nitrogen fertilizer on light interception and light-use efficiency in a young Eucalyptus nitens plantation. For Ecol Manag 288:21–30CrossRefGoogle Scholar
  34. Franco AC, Lüttge U (2002) Midday depression in savanna trees: coordinated adjustments in photochemical, efficiency, photorespiration, CO2 assimilation and water use efficiency. Oecologia 131:356–365CrossRefGoogle Scholar
  35. Franco AC, Matsubara S, Orthen B (2007) Photoinhibition, carotenoid composition and the co-regulation of photochemical and non-photochemical quenching in neotropical savanna trees. Tree Physiol 27:717–725CrossRefGoogle Scholar
  36. Furley PA (1999) The nature and diversity of neotropical savanna vegetation with particular reference to the Brazilian cerrados. Global Ecol Biogeogr 8:223–241CrossRefGoogle Scholar
  37. Giambelluca TW, Scholz FG, Bucci SJ, Meinzer FC, Goldstein G, Hoffmann WA, Franco AC, Buchert MP (2009) Evapotranspiration and energy balance of Brazilian savannas with contrasting tree density. Agric For Meteorol 149:1365–1376CrossRefGoogle Scholar
  38. Gonçalves JLM, Stape JL, Laclau JP, Bouillet JP, Ranger J (2008) Assessing the effects of early silvicultural management on long-term site productivity of fast growing eucalypt plantations: the Brazilian experience. South For 70:105–118CrossRefGoogle Scholar
  39. Hammer O, Harper DAT, Ryan PD (2001) PAST: Palaeontological statistics software package for education and data analysis. Palaeontol Electron 4:9–17Google Scholar
  40. Hok L, Sá JCM, Boulakia S, Reyes M, Leng V, Kong R, Tivet FE, Briedis C, Hartman D, Ferreira LA (2015) Short-term conservation agriculture and biomass-C input impacts on soil C dynamics in a savanna ecosystem in Cambodia. Agric Ecosyst Environ 214:54–67CrossRefGoogle Scholar
  41. IBÁ (2016) Brazilian Tree Industry. Performance indicators for the Brazilian planted tree sector, base year 2015. Brasília, p 100Google Scholar
  42. Iqbal RM, Rao AU, Rasul E, Wahid A (1996) Mathematical models and response functions in photosynthesis: an exponential model. In: Pessarakli M (ed) Handbook of photosynthesis. Dekker, New York, pp 803–810Google Scholar
  43. Laclau JP, Deleporte P, Ranger J, Bouillet JP, Kazotti G (2003) Nutrient dynamics throughout the rotation of Eucalyptus clonal stands in Congo. Ann Bot 91:879–892CrossRefGoogle Scholar
  44. Lapola DM, Martinelli LA, Peres CA, Ometto JP, Ferreira ME, Nobre CA, Aguiar APD, Bustamante MM, Cardoso MF, Costa MH (2014) Pervasive transition of the Brazilian land-use system. Nat Clim Chang 4:27–35CrossRefGoogle Scholar
  45. Larchevêque M, Maurel M, Desrochers A, Larocque GR (2011) How does drought tolerance compare between two improved hybrids of balsam poplar and an unimproved native species? Tree Physiol 31:240–249CrossRefGoogle Scholar
  46. Lewis JD, Phillips NG, Logan BA, Hricko CR, Tissue DT (2011) Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden. Tree Physiol 31:997–1006CrossRefGoogle Scholar
  47. Lobo FA, Barros MP, Dalmagro HJ, Dalmolin ÂC, Pereira WE, Souza ÉC, Vourlitis GL, Rodriguez Ortiz CE (2013) Fitting net photosynthetic light-response curves with Microsoft Excel – a critical look at the models. Photosynthetica 51:445–456CrossRefGoogle Scholar
  48. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and source of errors. J Exp Bot 54:2393–2401CrossRefGoogle Scholar
  49. Long SP, Farage PK, Garcia RL (1996) Measurement of leaf and canopy photosynthetic CO2 exchange in the field. J Exp Bot 47:1629–1642CrossRefGoogle Scholar
  50. Mayr MJ, Samimi C (2015) Comparing the dry season in-situ Leaf Area Index (LAI) derived from high-resolution rapideye imagery with MODIS LAI in a namibian Savanna. Rem Sens 7:4834–4857CrossRefGoogle Scholar
  51. Meinzer FC, Goldstein G, Franco AC, Bustamante M, Igler E, Jackson O, Caldas L, Rundel PW (1999) Atmospheric and hydraulic limitations on transpiration in Brazilian cerrado woody species. Funct Ecol 13:273–282CrossRefGoogle Scholar
  52. Miranda AC, Miranda HS, Lloyd J, Grace J, Francey RJ, McIntyre JA, Meir P, Riggan P, Lockwood R, Brass J (1997) Fluxes of carbon, water and energy over Brazilian cerrado: an analysis using eddy covariance and stable isotopes. Plant Cell Environ 20:315–328CrossRefGoogle Scholar
  53. Nobel PS (2009) Physicochemical and environmental plant physiology, 4th edn. Academic Press, BurlingtonGoogle Scholar
  54. Nogueira A, Martinez CA, Ferreira LL, Prado CHBA (2004) Photosynthesis and water use efficiency in twenty tropical tree species of differing succession status in a Brazilian reforestation. Photosynthetica 42:351–356CrossRefGoogle Scholar
  55. Noormets A, Epron D, Domec JC, McNulty SG, Fox T, Sun G, King JS (2015) Effects of forest management on productivity and carbon sequestration: a review and hypothesis. For Ecol Manag 355:124–140CrossRefGoogle Scholar
  56. Novick KA, Ficklin DL, Stoy PC, Williams CA, Bohrer G, Oishi AC, Papuga SA, Blanken PD, Noormets A, Sulman BN, Scott RL, Wang L, Phillips RP (2016) The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nat Clim Change 6:1023–1027 (online)CrossRefGoogle Scholar
  57. O’Grady AP, Worledge D, Battaglia M (2008) Constraints on transpiration of Eucalyptus globulus in southern Tasmania, Australia. Agric For Meteorol 148:453–465CrossRefGoogle Scholar
  58. Oliveira PTS, Wendland E, Nearing MA, Scott RL, Rosolem R, da Rocha HR (2015) The water balance components of undisturbed tropical woodlands in the Brazilian cerrado. Hydrol Earth Syst Sc 19:2899–2910CrossRefGoogle Scholar
  59. Pellegrini AF (2016) Nutrient limitation in tropical savannas across multiple scales and mechanisms. Ecology 97:313–324CrossRefGoogle Scholar
  60. Pfeifer M, Lefebvre V, Gonsamo A, Pellikka PK, Marchant R, Denu D, Platts PJ (2014) Validating and linking the GIMMS leaf area index (LAI3g) with environmental controls in tropical Africa. Remote Sens 6:1973–1990CrossRefGoogle Scholar
  61. Prado CHBA, Moraes JAPV (1997) Photosynthetic capacity and leaf specific mass in twenty woody species of cerrado vegetation. Photosynthetica 33:103–112CrossRefGoogle Scholar
  62. Reis MG, Ribeiro A, Baesso RCE, Souza WG, Fonseca S, Loos RA (2014) Balanço hídrico e de energia para plantios de eucalipto com cobertura parcial do solo. Cienc Florest 24:117–126Google Scholar
  63. Rodrigues TR, Vourlitis GL, Lobo FDA, Santanna FB, de Arruda PH, Nogueira JDS (2016) Modeling canopy conductance under contrasting seasonal conditions for a tropical savanna ecosystem of south central Mato Grosso, Brazil. Agric For Meteorol 218–219:218–229CrossRefGoogle Scholar
  64. Ryan MG, Stape JL, Binkley D, Fonseca S, Loos RA, Takahashi EN, Silva CR, Silva SR, Hakamada RE, Ferreira JM, Lima AMN, Gava JL, Leite FP, Andrade HB, Alves JM, Silva GGC (2010) Factors controlling Eucalyptus productivity: how resource availability and stand structure alter production and carbon allocation. For Ecol Manag 259:1695–1703CrossRefGoogle Scholar
  65. Ryu Y, Sonnentag O, Nilson T, Vargas R, Kobayashi H, Wenk R, Baldocchi DD (2010c) How to quantify tree leaf area index in a heterogeneous savanna ecosystem: a multi-instrument and multi-model approach. Agric For Meteorol 150:63–76CrossRefGoogle Scholar
  66. Silva FAS, Azevedo CAV (2016) The Assistat Software Version 7.7 and its use in the analysis of experimental data. Afr J Agric Res 11:3733–3740CrossRefGoogle Scholar
  67. Stape JL, Dan B, Ryan MG, Gomes AN (2004a) Water use, water limitation and water use efficiency in a Eucalyptus plantation. Bosque 25:35–41CrossRefGoogle Scholar
  68. Stape JL, Binkley D, Ryan MG (2004b) Eucalyptus production and the supply, use and efficiency of use of water, light and nitrogen across a geographic gradient in Brazil. For Ecol Manag 193:17–31CrossRefGoogle Scholar
  69. Stape JL, Binkley D, Ryan MG, Fonseca S, Loos RA, Takahashi EN, Silva CR, Silva SR, Hakamada RE, Ferreira JM, Lima AMN, Gava JL, Leite FP, Andrade HB, Alves JM, Silva GGC, Azevedo MR (2010) The Brazil Eucalyptus productivity project: influence of water, nutrients and stand uniformity on wood production. For Ecol Manag 259:1684–1694CrossRefGoogle Scholar
  70. Vourlitis GL, da Rocha HR (2011) Flux dynamics in the Cerrado and Cerrado-Forest Transition of Brazil. In: Hill MJ, Hanan NP (eds) Ecosystem Function in Savannas: Measurements and Modeling at Landscape to Global Scales. CRC Press, Boca RatonGoogle Scholar
  71. Vourlitis GL, Priante-Filho N, Hayashi MMS, Nogueira JS, Caseiro FT, CampeloJr JH (2001) Seasonal variations in the net ecosystem CO2 exchange of a mature Amazonian tropical transitional forest (cerradão). Funct Ecol 15:388–395CrossRefGoogle Scholar
  72. Vourlitis GL, Lobo FA, Lawrence S, Lucena IC, Dalmagro OBPHJ, Ortiz CER, Nogueira JS (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
  73. Welles JM, Norman JM (1991) Instrument for indirect measurement of canopy architecture. Agron J 83:818–825CrossRefGoogle Scholar
  74. Whitehead D, Beadle CL (2004) Physiological regulation of productivity and water use in Eucalyptus: a review. For Ecol Manag 193:113–140CrossRefGoogle Scholar
  75. Wijitkosum S (2016) The impact of land use and spatial changes on desertification risk in degraded areas in Thailand. Sustain Environ Res 26:84–92CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Engenharia AgrícolaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de SolosUniversidade Federal de ViçosaViçosaBrazil
  3. 3.Fibria CeluloseJacareíBrazil
  4. 4.Fibria CeluloseAracruzBrazil
  5. 5.Departamento de Biologia VegetalUniversidade Federal de ViçosaViçosaBrazil

Personalised recommendations