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

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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.

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References

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 440:1–9

    Article  Google Scholar 

  • 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 15:263–276

    Article  Google Scholar 

  • 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 20:1158–1166

    Article  Google Scholar 

  • Battaglia M, Beadle C, Loghhead S (1996) Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. Tree Physiol 16:81–89

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 40:531–551

    Article  CAS  Google Scholar 

  • Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63(9):3367–3377. doi:10.1093/jxb/err379

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Feller IC, McKee KL, Whigham DF, O’Neill JP (2003) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):731–739

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 411:469–472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reef R, Lovelock CE (2014b) Regulation of water balance in mangroves. Ann Bot. doi:10.1093/aob/mcu174

    PubMed  PubMed Central  Google Scholar 

  • 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):1064–1072

    Article  Google Scholar 

  • Reef R, Feller IC, Lovelock CE (2010b) Nutrition of mangroves. Tree Physiol 30(9):1148–1160. doi:10.1093/treephys/tpq048

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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 467

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Taub DR, Seemann JR, Coleman JS (2000) Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ 23:649–656

    Article  CAS  Google Scholar 

  • Team RDC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):458–464

    Google Scholar 

  • 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):47–58

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

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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.

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Reef, R., Slot, M., Motro, U. et al. The effects of CO2 and nutrient fertilisation on the growth and temperature response of the mangrove Avicennia germinans . Photosynth Res 129, 159–170 (2016). https://doi.org/10.1007/s11120-016-0278-2

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