Journal of Plant Research

, Volume 122, Issue 3, pp 245–251 | Cite as

A paradox of leaf-trait convergence: why is leaf nitrogen concentration higher in species with higher photosynthetic capacity?

Current Topics in Plant Research

Abstract

It is well known that leaf photosynthesis per unit dry mass (Amass) is positively correlated with nitrogen concentration (Nmass) across naturally growing plants. In this article we show that this relationship is paradoxical because, if other traits are identical among species, plants with a higher Amass should have a lower Nmass, because of dilution by the assimilated carbon. To find a factor to overcome the dilution effect, we analyze the Nmass–Amass relationship using simple mathematical models and literature data. We propose two equations derived from plant-growth models. Model prediction is compared with the data set of leaf trait spectrum obtained on a global scale. The model predicts that plants with a higher Amass should have a higher specific nitrogen absorption rate in roots (SAR), less biomass allocation to leaves, and/or greater nitrogen allocation to leaves. From the literature survey, SAR is suggested as the most likely factor. If SAR is the sole factor maintaining the positive relationship between Nmass and Amass, the variation in SAR is predicted to be much greater than that in Amass; given that Amass varies 130-fold, SAR may vary more than 2000-fold. We predict that there is coordination between leaf and root activities among species on a global scale.

Keywords

Leaf trait variation Photosynthesis–nitrogen relationship Growth model Root activity Carbon and nitrogen economy 

Abbreviations

Amass

CO2 uptake rate per unit standing leaf mass

k

Conversion coefficient from CO2 to biomass

LL

Leaf life span

LM

Standing leaf mass

LMF

Fraction of biomass allocated to leaves

LMP

Leaf mass production

LN

Standing leaf N

LNF

Fraction of N allocated to leaves

LNP

Leaf N production

MRT

Mean residence time of N in leaves

Nmass

Leaf N concentration per unit leaf dry mass

PM

Standing plant mass

PMP

Plant biomass production

PN

Standing plant nitrogen

PNP

Plant N production

R

N resorption efficiency

RL

Root life span

RM

Standing root mass

RMF

Fraction of biomass allocated to roots

RMP

Root mass production

SAR

N uptake rate per unit standing root mass

Notes

Acknowledgment

We thank H. Nagashima, N.P.R. Anten and Y. Yasumura for valuable comments. This study was supported in part by grants from the Japan Ministry of Education, Culture, Sports, Science and Technology and by the Global Environment Research Fund (F-052) from the Japan Ministry of the Environment.

References

  1. Ackerly DD, Bazzaz FA (1995) Leaf dynamics, self shading and carbon gain in seedlings of a tropical pioneer tree. Oecologia 101:289–298CrossRefGoogle Scholar
  2. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608CrossRefGoogle Scholar
  3. Aerts R, Chapin FSIII (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  4. Berendse E, Aerts R (1987) Nitrogen use efficiency: a biologically meaningful definition? Funct Ecol 1:293–296Google Scholar
  5. Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Funct Ecol 18:388–397CrossRefGoogle Scholar
  6. Comas LH, Bouma TJ, Eissenstat DM (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia 132:34–43CrossRefGoogle Scholar
  7. Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005) Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86:12–19CrossRefGoogle Scholar
  8. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  9. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  10. Field C, Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  11. Garnier E (1991) Resource capture, biomass allocation and growth in herbaceous plants. Trend Ecol Evol 6:126–131CrossRefGoogle Scholar
  12. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36:703–743Google Scholar
  13. Hikosaka K (2003) A model of dynamics of leaves and nitrogen in a plant canopy: an integration of canopy photosynthesis, leaf life span, and nitrogen use efficiency. Amer Nat 162:149–164CrossRefGoogle Scholar
  14. Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res 117:481–494PubMedCrossRefGoogle Scholar
  15. Hikosaka K (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Ann Bot 95:521–533PubMedCrossRefGoogle Scholar
  16. Hirose T (1987) A vegetative plant growth mode: adaptive significance of phenotypic plasticity in matter partitioning. Funct Ecol 1:195–202CrossRefGoogle Scholar
  17. Hirose T, Werger MJA (1987) Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of Solidago altissima stand. Physiol Plant 70:215–222CrossRefGoogle Scholar
  18. Jackson RB, Manwaring JH, Caldwell MM (1990) Rapid physiological adjustment of roots of localized soil enrichment. Nature 344:58–60PubMedCrossRefGoogle Scholar
  19. Kinugasa T, Hikosaka K, Hirose T (2005) Respiration and reproductive effort in Xanthium canadense. Ann Bot 96:81–89PubMedCrossRefGoogle Scholar
  20. Mediavilla S, Escudero A (2003) Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytol 159:203–211CrossRefGoogle Scholar
  21. Oikawa S, Hikosaka K, Hirose T (2005) Dynamics of leaf area in a canopy of an annual herb, Xanthium canadense. Oecologia 143:517–526PubMedCrossRefGoogle Scholar
  22. Osone Y, Tateno M (2005) Nitrogen absorption by roots as a cause of interspecific variations in leaf nitrogen concentration and photosynthetic capacity. Funct Ecol 19:460–470CrossRefGoogle Scholar
  23. Osone Y, Ishida A, Tateno M (2008) Correlation between relative growth rate and specific leaf area requires associations of specific leaf area with nitrogen absorption rate of roots. New Phytol 179:417–427PubMedCrossRefGoogle Scholar
  24. Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559CrossRefGoogle Scholar
  25. Poorter H, Villar A (1994) The fate of acquired carbon in plants: chemical composition and construction costs. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Academic Press, New York, pp 39–72Google Scholar
  26. Poorter H, van der Werf A, Atkin OK, Lambers H (1991) Respiratory energy requirements of roots vary with the potential growth rate of a plant species. Physiol Plant 83:469–475CrossRefGoogle Scholar
  27. Reich PB, Uhl C, Walters MB, Ellsworth DS (1991) Leaf lifespan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86:16–24CrossRefGoogle Scholar
  28. Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392CrossRefGoogle Scholar
  29. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734PubMedCrossRefGoogle Scholar
  30. Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998) Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Funct Ecol 12:395–405CrossRefGoogle Scholar
  31. Ryser P (1996) The importance of tissue density for growth and life span of leaves and roots: a comparison of five ecologically contrasting grasses. Funct Ecol 10:713–723CrossRefGoogle Scholar
  32. Shipley B (2006) Trade-offs between net assimilation rate and specific leaf area in determining relative growth rate: relationship with daily irradiance. Funct Ecol 16:682–689CrossRefGoogle Scholar
  33. Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol 167:493–508PubMedCrossRefGoogle Scholar
  34. van der Krift TA, Berendse F (2002) Root life spans of four grass species from habitats differing in nutrient availability. Funct Ecol 16:198–203CrossRefGoogle Scholar
  35. Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–892CrossRefGoogle Scholar
  36. Wikström F, Ågren GI (1995) The relationship between the growth rate of young plants and their total-N concentration is unique and simple: a comment. Ann Bot 75:541–544CrossRefGoogle Scholar
  37. Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Funct Ecol 15:351–359CrossRefGoogle Scholar
  38. Wright IJ, Westoby M (2000) Cross-species relationships between seedling relative growth rate, nitrogen productivity and root versus leaf function in 28 Australian woody species. Funct Ecol 14:97–107CrossRefGoogle Scholar
  39. Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19CrossRefGoogle Scholar
  40. Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol 15:423–434CrossRefGoogle Scholar
  41. Wright IJ, Reich PB, Westoby B et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar
  42. Wright IJ, Reich PB, Cornelissen JHC et al (2005) Assessing the generality of global leaf trait relationships. New Phytol 166:485–496PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2009

Authors and Affiliations

  1. 1.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  2. 2.Department of Natural ScienceInternational Christian UniversityMitakaJapan
  3. 3.Department of Plant EcologyForestry and Forest Products Research InstituteTsukubaJapan

Personalised recommendations