Skip to main content
SpringerLink
Log in

Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms

  • Community Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

We examined 15 traits in leaves and stems related to leaf C economy and water use for 32 co-existing angiosperms at ridge sites with shallow soil in the Bonin Islands. Across species, stem density was positively correlated to leaf mass per area (LMA), leaf lifespan (LLS), and total phenolics and condensed tannins per unit leaf N (N-based), and negatively correlated to leaf osmotic potential and saturated water content in leaves. LMA and LLS were negatively correlated to photosynthetic parameters, such as area-, mass-, and N-based assimilation rates. Although stem density and leaf osmotic potential were not associated with photosynthetic parameters, they were associated with some parameters of the leaf C economy, such as LMA and LLS. In the principal component (PCA) analysis, the first three axes accounted for 74.4% of total variation. Axis 1, which explained 41.8% of the total variation, was well associated with parameters for leaf C and N economy. Similarly, axis 2, which explained 22.3% of the total variation, was associated with parameters for water use. Axis 3, which explained 10.3% of the total variation, was associated with chemical defense within leaves. Axes 1 and 2 separated functional types relatively well, i.e., creeping trees, ruderal trees, other woody plants, C3 shrubs and forbs, palms, and CAM plants, indicating that plant functional types were characterized by similar attributes of traits related to leaf C and N economy and water use. In addition, when the plot was extended by two unrelated traits, leaf mass-based assimilation rates and stem density, it also separated these functional types. These data indicate that differences in the functional types with contrasting plant strategies can be attributed to functional integration among leaf C economy, hydraulics, and leaf longevity, and that both leaf mass-based assimilation rates and stem density are key factors reflecting the different functions of plant species.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackerly DD (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol Monogr 74:25–44

    Article  Google Scholar 

  • Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402–407

    Article  Google Scholar 

  • Bate-Smith EC (1977) Astringent tannins of Acer species. Phytochemistry 16:1421–1426

    Article  CAS  Google Scholar 

  • Bucci SJ, Goldstein G, Meinzer FC, Scholz FG, Franco AC, Bustamante M (2004) Functional convergence in hydraulic architecture and water relations of tropical savanna trees: from leaf to whole plant. Tree Physiol 24:891–899

    PubMed  CAS  Google Scholar 

  • Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536

    Article  Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Steege ter H, Morgan HD, Heijden van der MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Craine JM, Froehle J, Tilman DG, Wedin DA, Chapin FS III (2001) The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos 93:274–285

    Article  Google Scholar 

  • Craine JM, Tilman D, Wedin D, Reich P, Tjoelker M, Knops J (2002) Functional traits, productivity and effects on nitrogen cycling of 33 grassland species. Funct Ecol 16:563–574

    Article  Google Scholar 

  • Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecology 69:569–588

    Google Scholar 

  • Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Diez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304

    Article  Google Scholar 

  • Eamus D, Prichard H (1998) A cost-benefit analysis of leaves of four Australian savanna species. Tree Physiol 18:537–545

    PubMed  Google Scholar 

  • Escudero A, del Arco JM, Sanz IC, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90:80–87

    Article  Google Scholar 

  • Garnier E, Laurent G (1994) Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytol 128:725–736

    Article  Google Scholar 

  • Garnier E, Cordonnier P, Guillerm J-L, Sonié L (1997) Specific leaf area and leaf nitrogen concentration in annual and perennial grass species growing in Mediterranean old-fields. Oecologia 111:490–498

    Article  Google Scholar 

  • Givnish TJ (1995) Plant stems: biomechanical adaptation for energy capture and influence on species distributions. In: Gartner BL (ed) Plant stems. Physiology and functional morphology. Academic Press, California, pp 3–49

    Google Scholar 

  • Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194

    Article  Google Scholar 

  • Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Jalili A, Liu Z, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, Ross-Fraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281

    Article  Google Scholar 

  • Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–15

    Article  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 126:457–461

    Article  Google Scholar 

  • Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243

    Article  PubMed  Google Scholar 

  • Ishida A, Nakano T, Uemura A, Yamashita N, Tanabe H, Koike N (2001) Light-use properties in two sun-adapted shrubs with contrasting canopy structures. Tree Physiol 21:497–504

    PubMed  CAS  Google Scholar 

  • Ishida A, Diloksumpun S, Ladpala P, Staporn D, Panuthai S, Gamo M, Yazaki K, Ishizuka M, Puangchit L (2006) Contrasting seasonal leaf habits of canopy trees between tropical dry-deciduous and evergreen forests in Thailand. Tree Physiol 26:643–656

    PubMed  CAS  Google Scholar 

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

    Article  CAS  Google Scholar 

  • Kobayashi S (1978) A list of the vascular plants occurring in the Ogasawara (Bonin) Islands (in Japanese with English abstract). Ogasawara Res 1–2:1–33

    Google Scholar 

  • Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T (2001) CO2 transfer conductance, leaf structure and carbon isotope composition of Polygonum cuspidatum leaves from low and high altitudes. Plant Cell Environ 24:529–538

    Article  CAS  Google Scholar 

  • Leishman MR, Westoby M (1992) Classifying plants into groups on the basis of associations of individual traits––evidence from Australian semi-arid woodlands. J Ecol 80:417–424

    Article  Google Scholar 

  • Matsuki S, Koike T (2006) Comparison of leaf life span, photosynthesis and defensive traits across seven species of deciduous broad-leaf tree seedlings. Ann Bot 97:813–817

    Article  PubMed  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mishio M (1992) Adaptations to drought in five woody species co-occurring on shallow-soil ridges. Aust J Plant Physiol 19:539–553

    Article  Google Scholar 

  • Morita Y (1981) The dark-red forest soils of the Ogasawara Islands (I) Site condition, and morphological, mechanical and chemical properties (in Japanese with English abstract). J Jpn For Soc 63:1–7

    Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS, Uhl C (1994) Photosynthesis-nitrogen relations in Amazonian tree species. I. Patterns among species and communities. Oecologia 97:62–72

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  PubMed  CAS  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(Suppl):S143–S164

    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 140:543–550

    Article  PubMed  CAS  Google Scholar 

  • Schulze E-D, Ehleringer JR (1984) The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta 162:268–275

    Article  CAS  Google Scholar 

  • Shimizu M, Ishida A, Hogetsu T (2005) Root hydraulic conductivity and whole-plant water balance in tropical saplings following a shade-to-sun transfer. Oecologia 143:189–197

    Article  PubMed  Google Scholar 

  • Shimizu Y (1983) Phenological studies of the subtropical broad-leaved evergreen forests at Chichijima island in the Bonin (Ogasawara) Islands. Jpn J Ecol 33:135–147

    Google Scholar 

  • Shimizu Y, Tabata H (1991) Forest structures, composition, and distribution on a Pacific island, with reference to ecological release and speciation. Pacific Sci 45:28–49

    Google Scholar 

  • Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:S115–S127

    Article  Google Scholar 

  • Tomlinson PB, Fisher JB, Spangler RE, Richer RA (2001) Stem vascular architecture in the rattan palm Calamus (Arecaceae-Calamoideae-Calaminae). Am J Bot 88:797–809

    Article  PubMed  Google Scholar 

  • Turner NC, Jones MM (1980) Turgor maintenance by osmotic adjustment: a review and evaluation. In: Turner NC, Kramer PJ (eds) Adaptation of plants to water and high temperature stress. Wiley, New York, pp 87–103

    Google Scholar 

  • Uemura A, Ishida A, Tobias DJ, Koike N, Matsumoto Y (2004) Linkage between seasonal gas exchange and hydraulic acclimation in the top canopy leaves of Fagus trees in a mesic forest in Japan. Trees 18:452–459

    Article  Google Scholar 

  • Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84:362–370

    Google Scholar 

  • Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21:261–268

    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 Syst 33:125–159

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wright IJ, Falster DS, Pickup M, Westoby M (2006) Cross-species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics. Physiol Plant 127:114–456

    Article  CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

  • Yamashita N, Ishida A, Kushima H, Tanaka N (2000) Acclimation to sudden increase in light favoring an invasive over native trees in subtropical islands, Japan. Oecologia 125:412–419

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by grants-in-aid (14360091, 18255011, 18658067) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. We wish to thank Drs H. Ikeda, Y. Yasumura, and N. M. Watanabe for helpful suggestions and Prof. N. Kachi, Dr Y. Yamamura, and Ms Y. Abe for helpful support.

Author information

Authors and Affiliations

  1. Department of Plant Ecology, Forestry and Forest Products Research Institute (FFPRI), Tsukuba, Ibaraki, 305-8687, Japan

    Atsushi Ishida, Kenichi Yazaki, Nobuya Koike & Michiru Shimizu

  2. Yamanashi Institute of Environmental Science (YIES), Fuji-Yoshida, Yamanashi, 403-0005, Japan

    Takashi Nakano

  3. Faculty of Agriculture, Iwate University, Morioka, 020-8550, Japan

    Sawako Matsuki

  4. Institute for Plant Pathology and Physiology, National Institute for Agricultural Technology, Cordoba, X50201CA, Argentina

    Diego L. Lauenstein

  5. Kansai Research Center, Forestry and Forest Products Research Institute (FFPRI), Kyoto, 612–0855, Japan

    Naoko Yamashita

Authors
  1. Atsushi Ishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Nakano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenichi Yazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sawako Matsuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nobuya Koike
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Diego L. Lauenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michiru Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Naoko Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Atsushi Ishida.

Additional information

Communicated by Kouki Hikosaka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishida, A., Nakano, T., Yazaki, K. et al. Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms. Oecologia 156, 193–202 (2008). https://doi.org/10.1007/s00442-008-0965-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-0965-6

Keywords

Search

Navigation