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Photosynthesis Research

, Volume 129, Issue 2, pp 159–170 | Cite as

The effects of CO2 and nutrient fertilisation on the growth and temperature response of the mangrove Avicennia germinans

  • Ruth ReefEmail author
  • Martijn Slot
  • Uzi Motro
  • Michal Motro
  • Yoav Motro
  • Maria F. Adame
  • Milton Garcia
  • Jorge Aranda
  • Catherine E. Lovelock
  • Klaus Winter
Original Article

Abstract

In order to understand plant responses to both the widespread phenomenon of increased nutrient inputs to coastal zones and the concurrent rise in atmospheric CO2 concentrations, CO2–nutrient interactions need to be considered. In addition to its potential stimulating effect on photosynthesis and growth, elevated CO2 affects the temperature response of photosynthesis. The scarcity of experiments testing how elevated CO2 affects the temperature response of tropical trees hinders our ability to model future primary productivity. In a glasshouse study, we examined the effects of elevated CO2 (800 ppm) and nutrient availability on seedlings of the widespread mangrove Avicennia germinans. We assessed photosynthetic performance, the temperature response of photosynthesis, seedling growth and biomass allocation. We found large synergistic gains in both growth (42 %) and photosynthesis (115 %) when seedlings grown under elevated CO2 were supplied with elevated nutrient concentrations relative to their ambient growing conditions. Growth was significantly enhanced under elevated CO2 only under high-nutrient conditions, mainly in above-ground tissues. Under low-nutrient conditions and elevated CO2, root volume was more than double that of seedlings grown under ambient CO2 levels. Elevated CO2 significantly increased the temperature optimum for photosynthesis by ca. 4 °C. Rising CO2 concentrations are likely to have a significant positive effect on the growth rate of A. germinans over the next century, especially in areas where nutrient availability is high.

Keywords

Climate change CO2 Eutrophication Mangrove Nitrogen Phosphorus Photosynthesis RUBISCO Temperature response Tropics 

Notes

Acknowledgements

We would like to thank Dr Aurelio Virgo for technical support. Funding for this study was provided by an Australian Research Council Discovery Early Career Research Award to RR (DE120101706) and a Marie Curie Fellowship to RR (FP7-623720—STORM). Propagules were collected under Autoridad Nacional del Ambiente, Panama scientific permit No. SC/P-7-14. All data used in this manuscript are presented in the manuscript.

References

  1. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165(2):351–372. doi: 10.1111/j.1469-8137.2004.01224.x CrossRefPubMedGoogle Scholar
  2. Ainsworth EA, Rogers A, Blum H, Nösberger J, Long SP (2003) Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to Free Air CO2 Enrichment (FACE). J Exp Bot 54(393):2769–2774. doi: 10.1093/jxb/erg309 CrossRefPubMedGoogle Scholar
  3. Alongi DM, Christoffersen P, Tirendi F (1993) The influence of forest type on microbial-nutrient relationships in tropical mangrove sediments. J Exp Mar Biol Ecol 171(2):201–223. doi: 10.1016/0022-0981(93)90004-8 CrossRefGoogle Scholar
  4. Andrews TJ, Muller GJ (1985) Photosynthetic gas exchange of the mangrove, Rhizophora stylosa Griff., in its natural environment. Oecologia 65(3):449–455. doi: 10.1007/BF00378922 CrossRefGoogle Scholar
  5. Balke T, Bouma T, Horstman E, Webb E, Erftemeijer P, Herman P (2011) Windows of opportunity: thresholds to mangrove seedling establishment on tidal flats. Mar Ecol Prog Ser 440:1–9CrossRefGoogle Scholar
  6. Ball MC, Cowan IR, Farquhar GD (1988) Maintenance of leaf temperature and the optimisation of carbon gain in relation to water loss in a tropical mangrove forest. Aust J Plant Physiol 15:263–276CrossRefGoogle Scholar
  7. Ball MC, Cochrane MJ, Rawson HM (1997) Growth and water use of the mangroves Rhizophora apiculata and R. stylosa in response to salinity and humidity under ambient and eievated concentrations of atmospheric CO2. Plant Cell Environ 20:1158–1166CrossRefGoogle Scholar
  8. Battaglia M, Beadle C, Loghhead S (1996) Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. Tree Physiol 16:81–89CrossRefPubMedGoogle Scholar
  9. Beaumont LJ, Pitman A, Perkins S, Zimmermann NE, Yoccoz NG, Thuiller W (2011) Impacts of climate change on the world’s most exceptional ecoregions. Proc Natl Acad Sci 108(6):2306–2311. doi: 10.1073/pnas.1007217108 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24(2):253–259. doi: 10.1111/j.1365-3040.2001.00668.x CrossRefGoogle Scholar
  11. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31(1):491–543. doi: 10.1146/annurev.pp.31.060180.002423 CrossRefGoogle Scholar
  12. Björkman O, Demmig B, Andrews T (1988) Mangrove photosynthesis: response to high-irradiance stress. Funct Plant Biol 15(2):43–61. doi: 10.1071/PP9880043 Google Scholar
  13. Cernusak LA, Winter K, Martínez C, Correa E, Aranda J, Garcia M, Jaramillo C, Turner BL (2011a) Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiol 157(1):372–385. doi: 10.1104/pp.111.182436 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cernusak LA, Winter K, Turner BL (2011b) Transpiration modulates phosphorus acquisition in tropical tree seedlings. Tree Physiol 31(8):878–885. doi: 10.1093/treephys/tpr077 CrossRefPubMedGoogle Scholar
  15. Cernusak LA, Winter K, Dalling JW, Holtum JAM, Jaramillo C, Körner C, Leakey ADB, Norby RJ, Poulter B, Turner BL, Wright SJ (2013) Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Funct Plant Biol 40:531–551CrossRefGoogle Scholar
  16. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  17. Cheeseman JM, Clough BF, Carter DR, Lovelock CE, Eong O, Sim RG (1991) The analysis of photosynthetic performance in leaves under field conditions: a case study using Bruguiera mangroves. Photosynth Res 29(1):11–22. doi: 10.1007/BF00035202 PubMedGoogle Scholar
  18. Chen R, Twilley R (1999) Patterns of mangrove forest structure and soil nutrient dynamics along the Shark River estuary, Florida. Estuaries 22(4):955–970. doi: 10.2307/1353075 CrossRefGoogle Scholar
  19. Dillaway DN, Kruger EL (2010) Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect. Plant Cell Environ 33(6):888–899. doi: 10.1111/j.1365-3040.2010.02114.x CrossRefPubMedGoogle Scholar
  20. Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48(1):609–639. doi: 10.1146/annurev.arplant.48.1.609 CrossRefPubMedGoogle Scholar
  21. Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marba N (2013) The role of coastal plant communities for climate change mitigation and adaptation. Nat Clim Change 3(11):961–968. doi: 10.1038/nclimate1970 CrossRefGoogle Scholar
  22. Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7(1):27–47. doi: 10.2307/2997695 CrossRefGoogle Scholar
  23. Dybzinski R, Farrior CE, Pacala SW (2015) Increased forest carbon storage with increased atmospheric CO2 despite nitrogen limitation: a game-theoretic allocation model for trees in competition for nitrogen and light. Glob Change Biol 21(3):1182–1196. doi: 10.1111/gcb.12783 CrossRefGoogle Scholar
  24. Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63(9):3367–3377. doi: 10.1093/jxb/err379 CrossRefPubMedGoogle Scholar
  25. Farnsworth EJ, Ellison AM, Gong WK (1996) Elevated CO2 alters anatomy, physiology, growth, and reproduction of red mangrove (Rhizophora mangle L.). Oecologia 108(4):599–609. doi: 10.1007/bf00329032 CrossRefGoogle Scholar
  26. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149(1):78–90. doi: 10.1007/BF00386231 CrossRefPubMedGoogle Scholar
  27. Feller IC, McKee KL, Whigham DF, O’Neill JP (2003) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175CrossRefGoogle Scholar
  28. Fromard F, Vega C, Proisy C (2004) Half a century of dynamic coastal change affecting mangrove shorelines of French Guiana. A case study based on remote sensing data analyses and field surveys. Mar Geol 208(2–4):265–280. doi: 10.1016/j.margeo.2004.04.018 CrossRefGoogle Scholar
  29. Griffin KL, Anderson OR, Gastrich MD, Lewis JD, Lin G, Schuster W, Seemann JR, Tissue DT, Turnbull MH, Whitehead D (2001) Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure. Proc Natl Acad Sci 98(5):2473–2478. doi: 10.1073/pnas.041620898 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hättenschwiler S, Körner C (1997) Biomass allocation and canopy development in spruce model ecosystems under elevated CO2 and increased N deposition. Oecologia 113(1):104–114. doi: 10.1007/s004420050358 CrossRefGoogle Scholar
  31. Hutchison J, Manica A, Swetnam R, Balmford A, Spalding M (2014) Predicting global patterns in mangrove forest biomass. Conserv Lett 7(3):233–240. doi: 10.1111/conl.12060 CrossRefGoogle Scholar
  32. IPCC (2013) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York. doi: 10.1017/CBO9781107415324
  33. Jordan D, Ogren W (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Planta 161(4):308–313. doi: 10.1007/BF00398720 CrossRefPubMedGoogle Scholar
  34. Kirschbaum MUF (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiol 155(1):117–124. doi: 10.1104/pp.110.166819 CrossRefPubMedGoogle Scholar
  35. Koch MS, Coronado C, Miller MW, Rudnick DT, Stabenau E, Halley RB, Sklar FH (2015) Climate change projected effects on coastal foundation communities of the Greater Everglades using a 2060 scenario: need for a new management paradigm. Environ Manag 55(4):857–875. doi: 10.1007/s00267-014-0375-y CrossRefGoogle Scholar
  36. Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172(3):393–411. doi: 10.1111/j.1469-8137.2006.01886.x CrossRefPubMedGoogle Scholar
  37. Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, Virgo A (2010) High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations. Funct Plant Biol 37(9):890–900. doi: 10.1071/FP10034 CrossRefGoogle Scholar
  38. Krause GH, Winter K, Krause B, Virgo A (2014) Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium. Funct Plant Biol 42(1):42–51. doi: 10.1071/FP14095 CrossRefGoogle Scholar
  39. Krauss KW, McKee KL, Lovelock CE, Cahoon DR, Saintilan N, Reef R, Chen L (2014) How mangrove forests adjust to rising sea level. New Phytol 202(1):19–34. doi: 10.1111/nph.12605 CrossRefPubMedGoogle Scholar
  40. Leakey ADB, Xu F, Gillespie KM, McGrath JM, Ainsworth EA, Ort DR (2009) Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proc Natl Acad Sci 106(9):3597–3602. doi: 10.1073/pnas.0810955106 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lloyd J, Farquhar GD (2008) Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philos Trans R Soc Lond B Biol Sci. doi: 10.1098/rstb.2007.0032 PubMedPubMedCentralGoogle Scholar
  42. Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ 14(8):729–739. doi: 10.1111/j.1365-3040.1991.tb01439.x CrossRefGoogle Scholar
  43. Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw RM, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54(8):731–739CrossRefGoogle Scholar
  44. McKee KL, Rooth JE (2008) Where temperate meets tropical: multi-factorial effects of elevated CO2, nitrogen enrichment, and competition on a mangrove-salt marsh community. Glob Change Biol 14(5):971–984. doi: 10.1111/j.1365-2486.2008.01547.x CrossRefGoogle Scholar
  45. Miller PC (1972) Bioclimate, leaf temperature, and primary production in red mangrove canopies in South Florida. Ecology 53(1):22–45. doi: 10.2307/1935708 CrossRefGoogle Scholar
  46. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107(45):19368–19373. doi: 10.1073/pnas.1006463107 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162(2):253–280. doi: 10.1111/j.1469-8137.2004.01033.x CrossRefGoogle Scholar
  48. Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schafer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472CrossRefPubMedGoogle Scholar
  49. Osland MJ, Enwright N, Day RH, Doyle TW (2013) Winter climate change and coastal wetland foundation species: salt marshes vs. mangrove forests in the southeastern United States. Glob Change Biol 19(5):1482–1494. doi: 10.1111/gcb.12126 CrossRefGoogle Scholar
  50. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14(2):187–194. doi: 10.1111/j.1461-0248.2010.01570.x CrossRefPubMedGoogle Scholar
  51. Pierret A, Gonkhamdee S, Jourdan C, Maeght J-L (2013) IJ_Rhizo: an open-source software to measure scanned images of root samples. Plant Soil 373(1–2):531–539. doi: 10.1007/s11104-013-1795-9 CrossRefGoogle Scholar
  52. Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193(1):30–50. doi: 10.1111/j.1469-8137.2011.03952.x CrossRefPubMedGoogle Scholar
  53. Quisthoudt K, Adams J, Rajkaran A, Dahdouh-Guebas F, Koedam N, Randin C (2013) Disentangling the effects of global climate and regional land-use change on the current and future distribution of mangroves in South Africa. Biodivers Conserv 22(6–7):1369–1390. doi: 10.1007/s10531-013-0478-4 CrossRefGoogle Scholar
  54. Reef R, Lovelock CE (2014a) Historical analysis of mangrove leaf traits throughout the 19th and 20th centuries reveals differential responses to increases in atmospheric CO2. Glob Ecol Biogeogr 23(11):1209–1214. doi: 10.1111/geb.12211 CrossRefGoogle Scholar
  55. Reef R, Lovelock CE (2014b) Regulation of water balance in mangroves. Ann Bot. doi: 10.1093/aob/mcu174 PubMedPubMedCentralGoogle Scholar
  56. Reef R, Ball MC, Feller IC, Lovelock CE (2010a) Relationships among RNA: DNA ratio, growth and elemental stoichiometry in mangrove trees. Funct Ecol 24(5):1064–1072CrossRefGoogle Scholar
  57. Reef R, Feller IC, Lovelock CE (2010b) Nutrition of mangroves. Tree Physiol 30(9):1148–1160. doi: 10.1093/treephys/tpq048 CrossRefPubMedGoogle Scholar
  58. Reef R, Schmitz N, Rogers BA, Ball MC, Lovelock CE (2012) Differential responses of the mangrove Avicennia marina to salinity and abscisic acid. Funct Plant Biol 39(12):1038–1046. doi: 10.1071/FP12178 CrossRefGoogle Scholar
  59. Reef R, Winter K, Morales J, Adame MF, Reef DL, Lovelock CE (2015) The effect of atmospheric carbon dioxide concentrations on the performance of the mangrove Avicennia germinans over a range of salinities. Physiol Plant 154(3):358–368. doi: 10.1111/ppl.12289 CrossRefPubMedGoogle Scholar
  60. Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440(7086):922–925. http://www.nature.com/nature/journal/v440/n7086/suppinfo/nature04486_S1.html
  61. Saintilan N, Wilson NC, Rogers K, Rajkaran A, Krauss KW (2014) Mangrove expansion and salt marsh decline at mangrove poleward limits. Glob Change Biol 20(1):147–157. doi: 10.1111/gcb.12341 CrossRefGoogle Scholar
  62. Slot M, Winter K (2016) The effects of rising temperature on the ecophysiology of tropical forest trees. In: Goldstein G, Santiago LS (eds) Tropical tree physiology—adaptations and responses in a changing environment. Springer, Switzerland, p 467Google Scholar
  63. Smith JAC, Popp M, Luttge U, Cram WJ, Diaz M, Griffiths H, Lee HSJ, Medina E, Schafer C, Stimmel KH, Thonke B (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. VI. Water relations and gas exchange of mangroves. New Phytol 111(2):293–307. doi: 10.2307/2556867 CrossRefGoogle Scholar
  64. Taub DR, Seemann JR, Coleman JS (2000) Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ 23:649–656CrossRefGoogle Scholar
  65. Team RDC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  66. van der Sleen P, Groenendijk P, Vlam M, Anten NPR, Boom A, Bongers F, Pons TL, Terburg G, Zuidema PA (2015) No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat Geosci 8(1):24–28. doi: 10.1038/ngeo2313 CrossRefGoogle Scholar
  67. Winter K, Aranda J, Garcia M, Virgio A, Paton S (2001a) Effect of elevated CO2 and soil fertilization on whole-plant growth and water use in seedlings of a tropical pioneer tree, Ficus insipida. Flora Morphol Geobot Ecophysiol 196(6):458–464Google Scholar
  68. Winter K, Garcia M, Gottsberger R, Popp M (2001b) Marked growth response of communities of two tropical tree species to elevated CO2 when soil nutrient limitation is removed. Flora 196(1):47–58Google Scholar
  69. Woodroffe CD, Grindrod J (1991) Mangrove biogeography: the role of quaternary environmental and sea-level change. J Biogeogr 18(5):479–492. doi: 10.2307/2845685 CrossRefGoogle Scholar
  70. Yamori W, Hikosaka K, Way DA (2013) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119(1):101–117. doi: 10.1007/s11120-013-9874-6 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Ruth Reef
    • 1
    • 2
    • 3
    Email author
  • Martijn Slot
    • 4
  • Uzi Motro
    • 5
  • Michal Motro
    • 6
  • Yoav Motro
    • 7
  • Maria F. Adame
    • 8
  • Milton Garcia
    • 4
  • Jorge Aranda
    • 4
  • Catherine E. Lovelock
    • 2
  • Klaus Winter
    • 4
  1. 1.Cambridge Coastal Research UnitThe University of CambridgeCambridgeUK
  2. 2.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  3. 3.School of Earth, Atmosphere and EnvironmentMonash UniversityClaytonAustralia
  4. 4.Smithsonian Tropical Research InstituteBalboa, AnconRepublic of Panama
  5. 5.Department of Ecology, Evolution and Behavior, Department of Statistics, The Federmann Centre for the Study of RationalityThe Hebrew University of JerusalemJerusalemIsrael
  6. 6.The David Yellin Academic College of EducationJerusalemIsrael
  7. 7.Plant Protection and Inspection ServicesMinistry of Agriculture and Rural DevelopmentBeit DaganIsrael
  8. 8.Australian Rivers InstituteGriffith UniversityNathanAustralia

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