Skip to main content
SpringerLink
Log in

Stem Hydraulic Traits are Decoupled from Leaf Ecophysiological Traits in Mangroves in Southern Philippines

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The association between stem hydraulic traits and leaf functional traits in mangroves is unclear. We investigated the functional coordination between stem and leaf hydraulic traits and their integration with leaf economic spectrum (LES) in mangroves from the Sarangani Bay Protected Seascape in southern Philippines. We examined stem and leaf hydraulic traits and LES traits in 14 and 18 mangrove species, respectively, and compared them with the data on mangroves from southern China and the global plant dataset. The stem and leaf hydraulic traits were independent of each other, and they were generally decoupled from LES traits of the Philippine mangroves, which was largely attributable to leaf succulence. Mangroves from both countries had higher foliar P and K at a given leaf mass per area than the global plants. The stomatal (SD) and vein (VD) densities were not significantly correlated in the Philippine mangroves, in contrast to the strong SD–VD correlation in the Chinese mangroves and global vascular plants. This study illustrated the decoupling between hydraulic and economic leaf traits and their independence from stem hydraulic traits in mangroves in southern Philippines.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alongi DM (2009) The energetics of mangrove forests. Springer SBM, Dordrecht

    Google Scholar 

  • Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219

    Article  Google Scholar 

  • Aritsara ANA, Razakandraibe VM, Ramananantoandro T, Gleason SM, Cao KF (2020) Increasing axial parenchyma fraction in the Malagasy Magnoliids facilitated the co-optimization of hydraulic efficiency and safety. New Phytol 229(3):1467–1480

    Article  PubMed  CAS  Google Scholar 

  • Atkinson CJ, Else MA, Taylor L, Dover CJ (2003) Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.). J Exp Bot 54(385):1221–1229

    Article  CAS  PubMed  Google Scholar 

  • Ball M, Chow W, Anderson J (1987) Salinity-induced potassium deficiency causes loss of functional photosystem II in leaves of the grey mangrove, Avicennia marina, through depletion of the atrazine-binding polypeptide. Funct Plant Biol 14(3):351–361

    Article  CAS  Google Scholar 

  • Baraloto C, Timothy Paine CE, Poorter L, Beauchêne J, Bonal D, Domenach AM, Hérault B, Patiño S, Roggy JC, Chave J (2010) Decoupled leaf and stem economics in rain forest trees. Ecol Lett 13:1338–1347

    Article  PubMed  Google Scholar 

  • Blackman CJ, Aspinwall MJ, Resco de Dios V, Smith RA, Tissue DT (2016) Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2. Funct Ecol 30(9):1491–1500

    Article  Google Scholar 

  • Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecol Lett 14(2):91–100

    Article  PubMed  Google Scholar 

  • Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Sci 177(4):245–251

    Article  CAS  Google Scholar 

  • Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytol 192(2):437–448

    Article  PubMed  Google Scholar 

  • Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytol 199(2):559–570

    Article  PubMed  Google Scholar 

  • Bryant C, Fuenzalida TI, Zavafer A, Nguyen HT, Brothers N, Harris RJ, Beckett HAA, Holmlund HI, Binks O, Ball MC (2021) Foliar water uptake via cork warts in mangroves of the Sonneratia genus. Plant Cell Environ 44(9):2925–2937

    Article  CAS  PubMed  Google Scholar 

  • Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez-Castillo M, Rockwell FA, Manna LL, Guerra P, Bernal PL, Troncoso O, Enricci J, Holbrook MN, Goldstein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiol 32(7):880–893

    Article  PubMed  Google Scholar 

  • Burkhardt J, Basi S, Pariyar S, Hunsche M (2012) Stomatal penetration by aqueous solutions – an update involving leaf surface particles. New Phytol 196(3):774–787

    Article  CAS  PubMed  Google Scholar 

  • Cao JJ, Chen J, Yang QP, Xiong YM, Ren WZ, Kong DL (2022) Leaf hydraulics coordinated with leaf economics and leaf size in mangrove species along a salinity gradient. Plant Divers

  • Chen XY (2021) Relationship between leaf anatomical structure and photosynthetic capacity of mangrove plants in Hainan, China. Thesis, Guangxi University, Nanning, China (in Chinese with English abstract)

  • Choong MF, Lucas PW, Ong JSY, Pereira B, Tan HTW, Turner IM (1992) Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytol 121(4):597–610

    Article  Google Scholar 

  • de la Riva EG, Olmo M, Poorter H, Ubera JL, Villar R (2016) Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. PLoS ONE 11(2):e0148788

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edwards EJ (2006) Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae). New Phytol 172(3):479–789

    Article  PubMed  Google Scholar 

  • Emperua L, Donia E, Biaca M, Pechon R, Pautong AA, Balonos TA (2018) The Small Pelagic Fisheries of Sarangani Bay, Southern Mindanao Philippines. Philipp J Fish 25(1):118–127

    Article  Google Scholar 

  • Fortunel C, Fine PV, Baraloto C (2012) Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct Ecol 26:1153–1161

    Article  Google Scholar 

  • Franks PJ, Beerling DJ (2009a) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7(2):227–236

    Article  CAS  PubMed  Google Scholar 

  • Franks PJ, Beerling DJ (2009b) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106(25):10343–10347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardner RO (1975) An overview of botanical clearing technique. Stain Technol 50:99–105

    Article  CAS  PubMed  Google Scholar 

  • Griffiths H, Males J (2017) Succulent plants. Curr Biol 27(17):R890–R896

    Article  CAS  PubMed  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126(4):457–461

    Article  PubMed  Google Scholar 

  • Jiang GF, Goodale UM, Liu YY, Hao GY, Cao KF (2017) Salt management strategy defines the stem and leaf hydraulic characteristics of six mangrove tree species. Tree Physiol 37(3):389–401

    CAS  PubMed  Google Scholar 

  • Jiang X (2021) Xylem hydraulic structure and function in mangroves. Ph.D. Dissertation, Guangxi University, Nanning, China (in Chinese with English abstract)

  • Jin Y, Wang C, Zhou Z, Li Z (2016) Co-ordinated performance of leaf hydraulics and economics in 10 Chinese temperate tree species. Funct Plant Biol 43(11):1082–1090

    Article  CAS  PubMed  Google Scholar 

  • Joswig JS, Wirth C, Schuman MC et al (2022) Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation. Nat Ecol Evol 6(1):36–50

    Article  PubMed  Google Scholar 

  • Karst AL, Lechowicz MJ (2007) Are correlations among foliar traits in ferns consistent with those in the seed plants? New Phytol 173(2):306–312

    Article  PubMed  Google Scholar 

  • Kattge J, Bönisch G, Díaz S et al (2020) TRY plant trait database–enhanced coverage and open access. Glob Chang Biol 26:119–188

    Article  PubMed  Google Scholar 

  • Kurze S, Engelbrecht BMJ, Bilton MC, Tielbörger K, Álvarez-Cansino L (2021) Rethinking the plant economics spectrum for annuals: a multi-species study. Front Plant Sci 12:640862

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamont BB, Groom PK, Williams M, He T (2015) LMA, density and thickness: recognizing different leaf shapes and correcting for their nonlaminarity. New Phytol 207:942–947

    Article  PubMed  Google Scholar 

  • Landsberg J, Waring R (2016) Water relations in tree physiology: where to from here? Tree Physiol 37:18–32

    Google Scholar 

  • Laughlin DC, Leppert JJ, Moore MM, Sieg CH (2010) A multi-trait test of the leaf-height-seed plant strategy scheme with 133 species from a pine forest flora. Funct Ecol 24(3):493–501

    Article  Google Scholar 

  • Li L, McCormack ML, Ma C, Kong D, Zhang Q, Chen X, Zeng H, Niinemets Ü, Guo D (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18(9):899–906

    Article  CAS  PubMed  Google Scholar 

  • Lin YM, Liu XW, Zhang H, Fan HQ, Lin GH (2010) Nutrient conservation strategies of a mangrove species Rhizophora stylosa under nutrient limitation. Plant Soil 326(1):469–479

    Article  CAS  Google Scholar 

  • Liang DM (2021) The characteristics of the leaf economic spectrum of mangrove trees in Hainan, China. Thesis, Guangxi University, Nanning, China (in Chinese with English abstract)

  • Loomis RS (1997) On the utility of nitrogen in leaves. Proc Natl Acad Sci USA 99:13378–13379

    Article  Google Scholar 

  • López R, Cano FJ, Martin-StPaul NK, Cochard H, Choat B (2021) Coordination of stem and leaf traits define different strategies to regulate water loss and tolerance ranges to aridity. New Phytol 230(2):497–509

    Article  PubMed  Google Scholar 

  • López-Portillo J, Ewers FW, Angeles G (2005) Sap salinity effects on xylem conductivity in two mangrove species. Plant Cell Environ 28(10):1285–1292

    Article  Google Scholar 

  • Lovelock CE, Ball MC, Choat B, Engelbrecht BM, Holbrook NM, Feller IC (2006a) Linking physiological processes with mangrove forest structure: phosphorus deficiency limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf Rhizophora mangle. Plant Cell Environ 29(5):793–802

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Ball MC, Feller IC, Engelbrecht BMJ, Ewe ML (2006b) Variation in hydraulic conductivity of mangroves: influence of species, salinity, and nitrogen and phosphorus availability. Physiol Plant 127(3):457–464

    Article  CAS  Google Scholar 

  • Males J (2017) Secrets of succulence. J Exp Bot 68(9):2121–2134

    Article  CAS  PubMed  Google Scholar 

  • Males J, Griffiths H (2018) Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae. Plant Cell Environ 41(1):64–78

    Article  CAS  PubMed  Google Scholar 

  • Mao W, Li YL, Zhao XY, Zhang TH, Liu XP (2016) Variations of leaf economic spectrum of eight dominant plant species in two successional stages under contrasting nutrient supply. Pol J Ecol 64(1):14–24

    Google Scholar 

  • Mediavilla S, Martín I, Escudero A (2020) Vein and stomatal traits in leaves of three co-occurring Quercus species differing in leaf life span. Eur J for Res 139(5):829–840

    Article  Google Scholar 

  • Medina E, Fernandez W, Barboza F (2015) Element uptake, accumulation, and resorption in leaves of mangrove species with different mechanisms of salt regulation. Web Ecol 15(1):3–13

    Article  Google Scholar 

  • Meinzer FC (2003) Functional convergence in plant responses to the environment. Oecologia 134:1–11

    Article  PubMed  Google Scholar 

  • Messier J, McGill BJ, Enquist BJ, Lechowicz MJ (2016) Trait variation and integration across scales: is the leaf economic spectrum present at local scales? Ecography 40(6):685–697

    Article  Google Scholar 

  • Messier J, Lechowicz MJ, McGill BJ, Violle C, Enquist BJ (2017) Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network. J Ecol 105(6):1775–1790

    Article  Google Scholar 

  • Nguyen HT, Meir P, Sack L, Evans JR, Oliveira RS, Ball MC (2017a) Leaf water storage increases with salinity and aridity in the mangrove Avicennia marina: integration of leaf structure, osmotic adjustment and access to multiple water sources. Plant Cell Environ 40(8):1576–1591

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HT, Meir P, Wolfe J, Mencuccini M, Ball MC (2017b) Plumbing the depths: extracellular water storage in specialized leaf structures and its functional expression in a three-domain pressure—volume relationship. Plant Cell Environ 40(7):1021–1038

    Article  CAS  PubMed  Google Scholar 

  • Ogburn RM, Edwards EJ (2012) Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. Plant Cell Environ 35(9):1533–1542

    Article  PubMed  Google Scholar 

  • Pérez-Harguindeguy N, Díaz S, Garnier E et al (2016) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 64(8):715–716

    Article  Google Scholar 

  • Pfautsch S, Renard J, Tjoelker MG, Salih A (2015) Phloem as capacitor: radial transfer of water into xylem of tree stems occurs via symplastic transport in ray parenchyma. Plant Physiol 167(3):963–971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quadros AF, Helfer V, Nordhaus I, Reuter H, Zimmer M (2021) Functional traits of terrestrial plants in the intertidal: a review on mangrove trees. The Biol Bull 241(2):123–139

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Reef R, Lovelock CE (2015) Regulation of water balance in mangroves. Ann Bot 115(3):385–395

    Article  CAS  PubMed  Google Scholar 

  • Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30(9):1148–1160

    Article  CAS  PubMed  Google Scholar 

  • Reich PB (1993) Reconciling apparent discrepancies among studies relating life span, structure and function of leaves in contrasting plant life forms and climates: “the blind men and the elephant retold.” Funct Ecol 7:721–725

    Article  Google Scholar 

  • Reich PB (2014) The world-wide “fast-slow” plant economics spectrum: a traits manifesto. J Ecol 102(2):275–301

    Article  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969

    Article  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: Traits, spectra, and strategies. Int J Plant Sci 164(3 Suppl.):S143–S164

    Article  Google Scholar 

  • Ripley BS, Abraham T, Klak C, Cramer MD (2013) How succulent leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought. J Exp Botany 64:5485–5496

    Article  CAS  Google Scholar 

  • Rosas T, Mencuccini M, Barba J, Cochard H, Saura-Mas S, Martínez-Vilalta J (2019) Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytol 223(2):632–646

    Article  CAS  PubMed  Google Scholar 

  • Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000

    Article  PubMed  Google Scholar 

  • Sack L, Caringella M, Scoffoni C, Mason C, Rawls M, Markesteijn L, Poorter L (2014) Leaf vein length per unit area is not intrinsically dependent on image magnification: avoiding measurement artifacts for accuracy and precision. Plant Physiol 166:829–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saenger P, West PW (2016) Determinants of some leaf characteristics of Australian mangroves. Bot J Linn Soc 180(4):530–541

    Article  Google Scholar 

  • Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140(4):543–550

    Article  CAS  PubMed  Google Scholar 

  • Sartori K, Vasseur F, Violle C, Baron E, Gerard M, Rowe N, Ayala-Garay O, Christophe A, Jalón MD, Harscouet E, Granado MDR, Chassagneux A, Kazakou E, Vile D (2019) Leaf economics and slow-fast adaptation across the geographic range of Arabidopsis thaliana. Sci Rep 9(1):10758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmitz N, Verheyden A, Kairo JG, Beeckman H, Koedam N (2007) Successive cambia development in Avicennia marina (Forssk.) Vierh. is not climatically driven in the seasonal climate at Gazi Bay, Kenya. Dendrochronologia 25:87–96

    Article  Google Scholar 

  • Schmitz N, Roberts EMR, Verheyden A, Kairo JG, Beeckman H, Koedam N (2008) A patchy growth via successive and simultaneous cambia: key to success of the most widespread mangrove species Avicennia marina?. Ann Bot 101(1):49–58

    Article  PubMed  Google Scholar 

  • Schmitz N, Egerton JG, Lovelock CE, Ball MC (2012) Light-dependent maintenance of hydraulic function in mangrove branches: do xylary chloroplasts play a role in embolism repair? New Phytol 195(1):40–46

    Article  CAS  PubMed  Google Scholar 

  • Smith WK (1978) Temperatures of desert plants: another perspective on the adaptability of leaf size. Science 201(4356):614–616

    Article  CAS  PubMed  Google Scholar 

  • Taffouo V, Fonkou T, Kenne M, Wamba O, Akao A (2007) Salinity effect on seedling growth, water, sodium and potassium distributions in the mangrove species (Avicennia germinans L. (Avicenniaceae)) in semi-controlled conditions. Agron Afr 19(3):263–270

    Google Scholar 

  • The USAID Oceans and Fisheries Partnership (2019) Sustainable Fisheries Management Plan for the Sarangani Bay and Sulawesi Sea. United States Agency for International Development

  • Tian SQ, Zhu SD, Zhu JJ, Shen ZH, Cao KF (2016) Impact of leaf morphological and anatomical traits on mesophyll conductance and leaf hydraulic conductance in mangrove plants. Plant Sci J 34(6):909–919 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

    Article  Google Scholar 

  • Vendramini F, Díaz S, Gurvich DE, Wilson PJ, Thompson K, Hodgson JG (2002) Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytol 154(1):147–157

    Article  Google Scholar 

  • Villagra M, Campanello PI, Bucci SJ, Goldstein G (2013) Functional relationships between leaf hydraulics and leaf economic traits in response to nutrient addition in subtropical tree species. Tree Physiol 33(12):1308–1318

    Article  PubMed  Google Scholar 

  • Villar R, Ruiz-Robleto J, Ubera JL, Poorter H (2013) Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. Am J Bot 100(10):1969–1980

    Article  PubMed  Google Scholar 

  • Vinya R, Malhi Y, Fisher JB, Brown N, Brodribb TJ, Aragao LE (2013) Xylem cavitation vulnerability influences tree species’ habitat preferences in miombo woodlands. Oecologia 173:711–720

    Article  PubMed  Google Scholar 

  • Vleminckx J, Fortunel C, Valverde‐Barrantes OJ, Timothy Paine CE, Engel J, Pétronelli P, Dourdain A, Guevara JE, Béroujon S, Baraloto C (2021) Resolving whole‐plant economics from leaf, stem and root traits of 1467 Amazonian tree species. Oikos

  • Wang WQ, Wang M, Lin P (2003) Seasonal changes in element contents in mangrove element retranslocation during leaf senescence. Plant Soil 252:187–193

    Article  CAS  Google Scholar 

  • Wen Y, Zhao WL, Cao KF (2020) Global convergence in the balance between leaf water supply and demand across vascular land plants. Funct Plant Biol 47(10):904–911

    Article  PubMed  Google Scholar 

  • Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Evol Syst 33:125–159

    Article  Google Scholar 

  • Wilson PJ, Thompson K, Hodgson JG (1999) Specific leaf area and dry matter content as alternative predictors of plant strategies. New Phytol 143:155–162

    Article  Google Scholar 

  • Wright IJ, Westoby M (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytol 155(3):403–416

    Article  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Wang H, Prentice IC, Harrison SP, Wright IJ (2021) Plant hydraulics coordinated with photosynthetic traits and climate. BioRxiv. Preprint

  • Yan L, Sunoj VSJ, Short AW, Lambers H, Elsheery NI, Kajita T, Wee AKS, Cao KF (2021) Correlations between allocation to foliar phosphorus fractions and maintenance of photosynthetic integrity in six mangrove populations as affected by chilling. New Phytol 232(6):2267–2282

    Article  CAS  PubMed  Google Scholar 

  • Yates EJ, Ashwath N, Midmore DJ (2002) Responses to nitrogen, phosphorus, potassium and sodium chloride by three mangrove species in pot culture. Trees Struct Funct 16(2–3):120–125

    Article  CAS  Google Scholar 

  • Yin Q, Wang L, Lei M, Dang H, Quan J, Tian T, Chai Y, Yue M (2018) The relationships between leaf economics and hydraulic traits of woody plants depend on water availability. Sci Total Environ 621:245–252

    Article  CAS  PubMed  Google Scholar 

  • Zhang JL, Cao KF (2009) Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Funct Ecol 23(4):658–667

    Article  Google Scholar 

  • Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF, Hu H (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PLoS ONE 7(6):e40080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SB, Sun M, Cao KF, Hu H, Zhang JL (2014) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS ONE 9(1):e84682

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang YJ, Cao KF, Sack L, Li N, Wei XM, Goldstein G (2015) Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytol 206(2):817–829

    Article  CAS  PubMed  Google Scholar 

  • Zhao WL, Chen YJ, Brodribb TJ, Cao KF (2016) Weak co-ordination between vein and stomatal densities in 105 angiosperm tree species along altitudinal gradients in Southwest China. Funct Plant Biol 43(12):1126–1133

    Article  PubMed  Google Scholar 

  • Zhao WL, Siddiq Z, Fu PL, Zhang JL, Cao KF (2017) Stable stomatal number per minor vein length indicates the coordination between leaf water supply and demand in three leguminous species. Sci Rep 7(1):2211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu YF (2014) The xylem and leaf anatomical features of mangroves. Master degree dissertation, University of Science and Technology of China, Hefei, 57pp (in Chinese)

Download references

Acknowledgements

The authors are grateful to all local government units and key offices of Sarangani province in the Republic of the Philippines, various levels of management and bureaus of the Department of Environment and Natural Resources, and other institutions and individuals that facilitated the successful completion of the study. The authors also gratefully acknowledge the two anonymous reviewers for their insightful comments to help improve the manuscript.

Funding

This study was supported through grants from the National Natural Science Foundation of China (31670406) and Bagui Scholars Program of Guangxi Zhuang Autonomous Region of China (C33600992001) to KFC, and a fellowship from the China Scholarship Council (2016GXZS81) to ARA.

Author information

Authors and Affiliations

  1. State Key Laboratory for Conservation and Utilization of Subtropical Agrobioresources, Guangxi University, Nanning, 530004, Guangxi, China

    Angelo Rellama Agduma, Xin Jiang, Dong-Miao Liang, Xin-Ying Chen & Kun-Fang Cao

  2. Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, Guangxi, China

    Angelo Rellama Agduma, Xin Jiang, Dong-Miao Liang, Xin-Ying Chen & Kun-Fang Cao

  3. Ecology and Conservation Research Laboratory, Department of Biological Sciences, College of Science and Mathematics, University of Southern Mindanao, 9407, Kabacan, Cotabato, Philippines

    Angelo Rellama Agduma

  4. Environmental Conservation and Protection Center, Provincial Capitol Compound, 9501, Alabel, Sarangani, Philippines

    Angelo Rellama Agduma

Authors
  1. Angelo Rellama Agduma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong-Miao Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin-Ying Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kun-Fang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ARA and KFC conceived and designed the study. Data collection was performed by ARA, XJ, DML, and XYC. Data analysis was performed by ARA and KFC. The first draft of the manuscript was written by ARA, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Kun-Fang Cao.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agduma, A.R., Jiang, X., Liang, DM. et al. Stem Hydraulic Traits are Decoupled from Leaf Ecophysiological Traits in Mangroves in Southern Philippines. J. Plant Biol. 65, 389–401 (2022). https://doi.org/10.1007/s12374-022-09361-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-022-09361-6

Keywords

Search

Navigation