Skip to main content
Log in

Photosynthesis, respiration, and growth patterns of Rhizophora stylosa seedlings in relation to growth temperature

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Rhizophora stylosa Griff. exhibits thermal acclimatization of leaf respiration, but does not maintain high photosynthetic performance under new growth temperatures.

Abstract

Mangrove plants are distributed across the majority of the world’s tropical and subtropical coastlines. How they respond to new growth temperatures is poorly understood. To obtain this information, we collected Rhizophora stylosa Griff. diaspores from a subtropical region with average daily mean and maximum temperatures of 24.0 and 26.7 °C. After 1-year-old seedlings had been grown in four glasshouse chambers at an air temperature of 15, 20, 25, or 30 °C for about 50 days, we evaluated photosynthesis, respiration, and growth. Seedlings grown at 15 and 20 °C showed PSII photoinhibition, especially in newly emerged leaves. The assimilation rate was greatest at 25 °C. Thermal acclimatization of respiration was observed at 20–30 °C in both newly emerged and pre-existing leaves, was unclear in stems, and was absent in roots. Stem growth rate was greatest at 25 °C, but seedlings grown at 30 °C produced the largest number of new leaves and marginally decreased biomass allocation to roots, which lacked thermal acclimatization capacity. These results indicate that R. stylosa growing in subtropical regions adapts its photosynthesis to the average daily mean or maximum temperatures, and minimizes carbon loss due to warm temperatures by use of the thermal acclimatization capacity of leaf respiration and plasticity of biomass allocation, which contribute to optimizing growth performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andrews TJ, Muller GJ (1985) Photosynthetic gas exchange of the mangrove, Rhizophora stylosa Griff., in its natural environment. Oecologia 65:449–455

    Article  CAS  PubMed  Google Scholar 

  • Araki MG, Gyokusen K, Kajimoto T (2017) Vertical and seasonal variations in temperature responses of leaf respiration in a Chamaecyparis obtusa canopy. Tree Physiol 37:1269–1284

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32:87–105

    Article  PubMed  Google Scholar 

  • Ball MC (1988) Ecophysiology of mangroves. Trees Struct Funct 2:129–142

    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

    Google Scholar 

  • Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Callaway RM, Delucia EH, Schlesinger WH (1994) Biomass allocation of montane and desert ponderosa pine: an analog for response to climate change. Ecology 75:1474–1481

    Article  Google Scholar 

  • Campbell C, Atkinson L, Zaragoza-Castells J, Lundmark M, Atkin O, Hurry V (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytol 176:375–389

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Wang W, Li QQ, Zhang Y, Yang S, Osland MJ, Huang J, Peng C (2017) Mangrove species’ responses to winter air temperature extremes in China. Ecosphere 8:e01865

    Article  Google Scholar 

  • Collier CJ, Ow YX, Langlois L, Uthicke S, Johansson CL, O’Brien KR, Hrebien V, Adams MP (2017) Optimum temperatures for net primary productivity of three tropical seagrass species. Front Plant Sci 8:1446

    Article  PubMed  PubMed Central  Google Scholar 

  • Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M (2011) Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–297

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363

    Article  Google Scholar 

  • JMA (Japan Meteorological Agency) (2018) http://www.data.jma.go.jp/obd/stats/etrn/index.php. Accessed 20 Mar 2018

  • Kadoya T, Inoue T (2015) Spatio-temporal pattern of specific gravity of mangrove diaspore: implications for upstream dispersal. Ecography 38:472–479

    Article  Google Scholar 

  • Krauss KW, Lovelock CE, McKee KL, López-Hoffman L, Ewe SML, Sousa WP (2008) Environmental drivers in mangrove establishment and early development: a review. Aquat Bot 89:105–127

    Article  Google Scholar 

  • Lovelock CE, Krauss KW, Osland MJ, Reef R, Ball MC (2016) The physiology of mangrove trees with changing climate. In: Goldstein G, Santiago LS (eds) Tropical tree physiology: adaptations and responses in a changing environment. Springer, New York, pp 149–179

    Chapter  Google Scholar 

  • Loveys BR, Atkinson LJ, Sherlock DJ, Roberts RL, Fitter AH, Atkin OK (2003) Thermal acclimation of leaf and root respiration, an investigation comparing inherently fast- and slow-growing plant species. Glob Chang Biol 9:895–910

    Article  Google Scholar 

  • Olszyk DM, Johnson MG, Tingey DT, Rygiewicz PT, Wise C, VanEss E, Benson A, Storm MJ, King R (2003) Whole-seedling biomass allocation, leaf area, and tissue chemistry for Douglas-fir exposed to elevated CO2 and temperature for 4 years. Can J For Res 33:269–278

    Article  CAS  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 19:1482–1494

    Article  Google Scholar 

  • Osland MJ, Day RH, Hall CT, Brumfield MD, Dugas JL, Jones WR (2017a) Mangrove expansion and contraction at a poleward range limit: climate extremes and land–ocean temperature gradients. Ecology 98:125–137

    Article  PubMed  Google Scholar 

  • Osland MJ, Feher LC, Griffith KT, Cavanaugh KC, Enwright NM, Day RH, Stagg CL, Krauss KW, Howard R, Grace JB, Rogers K (2017b) Climatic controls on the global distribution, abundance, and species richness of mangrove forests. Ecol Monogr 87:341–359

    Article  Google Scholar 

  • Ow LF, Griffin KL, Whitehead D, Walcroft AS, Turnbull MH (2008a) Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoides × nigra. New Phytol 178:123–134

    Article  PubMed  Google Scholar 

  • Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2008b) Thermal acclimation of respiration but not photosynthesis in Pinus radiata. Funct Plant Biol 35:448–461

    Article  PubMed  Google Scholar 

  • Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2010) Seasonal variation in foliar carbon exchange in Pinus radiata and Populus deltoides: respiration acclimates fully to changes in temperature but photosynthesis does not. Glob Change Biol 16:288–302

    Article  Google Scholar 

  • Pilon J, Santamaría L (2001) Seasonal acclimation in the photosynthetic and respiratory temperature responses of three submerged freshwater macrophyte species. New Phytol 151:659–670

    Article  CAS  PubMed  Google Scholar 

  • Quisthoudt K, Schmitz N, Randin CF, Dahdouh-Guebas F, Robert EMR, Koedam N (2012) Temperature variation among mangrove latitudinal range limits worldwide. Trees Struct Funct 26:1919–1931

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 24 May 2017

  • Reef R, Slot M, Motro U, Motro M, Motro Y, Adame MF, Garcia M, Aranda J, Lovelock CE, Winter K (2016) The effects of CO2 and nutrient fertilisation on the growth and temperature response of the mangrove Avicennia germinans. Photosynth Res 129:159–170

    Article  CAS  PubMed  Google Scholar 

  • Robinson E, Davison W (2008) The Antarctic notothenioid fish Pagothenia borchgrevinki is thermally flexible: acclimation changes oxygen consumption. Pol Biol 31:317–326

    Article  Google Scholar 

  • Sandblom E, Gräns A, Axelsson M, Seth H (2014) Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future. Proc R Soc B 281:20141490

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandblom E, Clark TD, Gräns A, Ekström A, Brijs J, Sundström LF, Odelström A, Adill A, Aho T, Jutfelt F (2016) Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat Commun 7:11447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slot M, Kitajima K (2015) General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types. Oecologia 177:885–900

    Article  PubMed  Google Scholar 

  • Slot M, Winter K (2017a) In situ temperature response of photosynthesis of 42 tree and liana species in the canopy of two Panamanian lowland tropical forests with contrasting rainfall regimes. New Phytol 214:1103–1117

    Article  CAS  PubMed  Google Scholar 

  • Slot M, Winter K (2017b) Photosynthetic acclimation to warming in tropical forest tree seedlings. J Exp Bot 68:2275–2284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slot M, Winter K (2018) High tolerance of tropical sapling growth and gas exchange to moderate warming. Funct Ecol 32:599–611

    Article  Google Scholar 

  • Spalding M, Kainuma M, Collins L (2010) World atlas of mangroves. Earthscan, London

    Book  Google Scholar 

  • Stuart SA, Choat B, Martin KC, Holbrook NM, Ball MC (2007) The role of freezing in setting the latitudinal limits of mangrove forests. New Phytol 173:576–583

    Article  CAS  PubMed  Google Scholar 

  • Tropical Coastal Ecosystems Portal (2018) http://www.nies.go.jp/TroCEP/index.html. Accessed 20 July 2018

  • Ulqodry TZ, Matsumoto F, Okimoto Y, Nose A, Zheng SH (2014) Study on photosynthetic responses and chlorophyll fluorescence in Rhizophora mucronata seedlings under shade regimes. Acta Physiol Plant 36:1903–1917

    Article  CAS  Google Scholar 

  • Wang W, You S, Wang Y, Huang L, Wang M (2011) Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant Soil 342:105–115

    Article  CAS  Google Scholar 

  • Wang J, Duan B, Zhang Y, Bughio MA, Jia W (2013) Density-dependent responses of Picea purpurea seedlings for plant growth and resource allocation under elevated temperature. Trees Struct Funct 27:1775–1787

    Article  Google Scholar 

  • Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Phisiol 30:669–688

    Article  Google Scholar 

  • Woodroffe CD, Grindrod J (1991) Mangrove biogeography: the role of quaternary environmental and sea-level change. J Biogeogr 18:479–492

    Article  Google Scholar 

  • Yamamoto K (2003) LIA for Win32. https://www.agr.nagoya-u.ac.jp/~shinkan/LIA32/. Accessed 25 Oct 2018

  • Yamori W, Noguchi K, Terashima I (2005) Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant Cell Environ 28:536–547

    Article  CAS  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Liu Q (2009) Growth and physiological responses of Picea asperata seedlings to elevated temperature and to nitrogen fertilization. Acta Physiol Plant 31:163–173

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. M. Aono, Dr. A. Takenaka, and Dr. M. Ogasa for their helpful advice and comments; and Dr. S. Baba for assistance with seed sampling. We also thank Mr. Y. Yamao and the staff of the Kawakami farm company—Mr. Y. Suzuki, Ms. H. Yaguchi, Mr. A. Kawada, and Mr. J. Arai—for management of plants and equipment. The comments of two anonymous reviewers substantially improved this manuscript. This study was partly funded by the Strategic Research and Development Fund of the Ministry of the Environment, Japan (Project nos. 2-1712 and S-14). This work is a contribution to the Climate Change Adaptation Research Program of NIES.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasuaki Akaji.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Lin.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 94 KB)

Supplementary material 2 (XLSX 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akaji, Y., Inoue, T., Tomimatsu, H. et al. Photosynthesis, respiration, and growth patterns of Rhizophora stylosa seedlings in relation to growth temperature. Trees 33, 1041–1049 (2019). https://doi.org/10.1007/s00468-019-01840-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-019-01840-7

Keywords

Navigation