Oecologia

, Volume 148, Issue 4, pp 564–572

Nitrogen response efficiency increased monotonically with decreasing soil resource availability: a case study from a semiarid grassland in northern China

  • Zhi-You Yuan
  • Ling-Hao Li
  • Xing-Guo Han
  • Shi-Ping Chen
  • Zheng-Wen Wang
  • Quan-Sheng Chen
  • Wen-Ming Bai
Ecophysiology

Abstract

The concept of nutrient use efficiency is central to understanding ecosystem functioning because it is the step in which plants can influence the return of nutrients to the soil pool and the quality of the litter. Theory suggests that nutrient efficiency increases unimodally with declining soil resources, but this has not been tested empirically for N and water in grassland ecosystems, where plant growth in these ecosystems is generally thought to be limited by soil N and moisture. In this paper, we tested the N uptake and the N use efficiency (NUE) of two Stipa species (S. grandis and S. krylovii) from 20 sites in the Inner Mongolia grassland by measuring the N content of net primary productivity (NPP). NUE is defined as the total net primary production per unit N absorbed. We further distinguished NUE from N response efficiency (NRE; production per unit N available). We found that NPP increased with soil N and water availability. Efficiency of whole-plant N use, uptake, and response increased monotonically with decreasing soil N and water, being higher on infertile (dry) habitats than on fertile (wet) habitats. We further considered NUE as the product of the N productivity (NP the rate of biomass increase per unit N in the plant) and the mean residence time (MRT; the ratio between the average N pool and the annual N uptake or loss). The NP and NUE of S. grandis growing usually in dry and N-poor habitats exceeded those of S. krylovii abundant in wet and N-rich habitats. NUE differed among sites, and was often affected by the evolutionary trade-off between NP and MRT, where plants and communities had adapted in a way to maximize either NP or MRT, but not both concurrently. Soil N availability and moisture influenced the community-level N uptake efficiency and ultimately the NRE, though the response to N was dependent on the plant community examined. These results show that soil N and water had exerted a great impact on the N efficiency in Stipa species. The intraspecific differences in N efficiency within both Stipa species along soil resource availability gradient may explain the differences in plant productivity on various soils, which will be conducive to our general understanding of the N cycling and vegetation dynamics in northern Chinese grasslands.

Keywords

Habitat preference Nitrogen use efficiency Nitrogen response efficiency Production Plant strategies 

References

  1. Aerts R (1990) Nutrient use efficiency in evergreen and species from heathlands. Oecologia 84:391–397Google Scholar
  2. Aerts R, de Caluwe H (1994) Nitrogen use efficiency of Carex species in relation to nitrogen supply. Ecology 75:2362–2372CrossRefGoogle Scholar
  3. Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  4. del Arco JM, Escudero A, Garrido B (1991) Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology 72:701–708CrossRefGoogle Scholar
  5. Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184PubMedCrossRefGoogle Scholar
  6. Berendse F, Aerts R (1987) Nitrogen use efficiency: a biologically meaningful definition? Funct Ecol 1:293–296Google Scholar
  7. Bertiller MB, Beeskow AM, Coronato FR (1991) Seasonal environmental variation and plant phenology in arid Patagonia (Argentina). J Arid Environ 21:1–11Google Scholar
  8. Binkley D, Stape JL, Ryan MG (2004) Thinking about efficiency of resource use in forests. For Ecol Manage 193:5–16CrossRefGoogle Scholar
  9. Biondini ME, Lauenroth WK, Sala OE (1991) Correcting estimates of net primary production: are we overestimating plant production in rangelands? J Range Manage 44:194–1988CrossRefGoogle Scholar
  10. Bremner JM, Mulvaney CS (1982) Nitrogen—total. In: Page AL (ed) Methods of soil analysis. II. Chemical and microbiological properties. American Society of Agronomy, Madison, Wis., pp 596–624Google Scholar
  11. Bridgham SD, Pastor J, McClaugherty CA, Richardson CJ (1995) Nutrient-use efficiency: a litterfall index, a model, and a test along a nutrient-availability gradient in North Carolina peat-lands. Am Nat 145:1–21CrossRefGoogle Scholar
  12. Bridgham SD, Updegraff K, Pastor J (2001) A comparison of nutrient availability indices along an ombrotrophic-minerotrophic gradient in Minnesota wetlands. Soil Sci Soc Am J 65:259–269CrossRefGoogle Scholar
  13. Carrera AL, Bertiller MB, Sain CL, Mazzarino MJ (2003) Relationship between plant nitrogen conservation strategies and the dynamics of soil nitrogen in the arid Patagonian Monte, Argentina. Plant Soil 255:595–604CrossRefGoogle Scholar
  14. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  15. Chapin FS III, Vitousek PM, Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58CrossRefGoogle Scholar
  16. Clark DA, Brown S, Kicklighter D, Chambers J, Thomlinson JR, Ni J, Holland EA (2001a) NPP in tropical forests: an evaluation and synthesis of existing field data. Ecol Appl 11:371–384CrossRefGoogle Scholar
  17. Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson JR, Ni J (2001b) Measuring net primary production in forests: concepts and field methods. Ecol Appl 11:356–370CrossRefGoogle Scholar
  18. Eckstein RL, Karlsson PS (2001a) The effect of reproduction on nitrogen use-efficiency of three species of the carnivorous genus Pinguicula. J Ecol 89:798–806CrossRefGoogle Scholar
  19. Eckstein RL, Karlsson PS (2001b) Variation in nitrogen-use efficiency among and within subarctic graminoids and herbs. New Phytol 150:641–651CrossRefGoogle Scholar
  20. Fassnacht KS, Gower ST (1999) Comparison of the litterfall and forest floor organic matter and nitrogen dynamics of upland forest ecosystems in north central Wisconsin. Biogeochemistry 45:265–284Google Scholar
  21. Fioretto A, Papa S, Fuggi A (2003) Litter-fall and litter decomposition in a low Mediterranean shrubland. Biol Fertil Soils 39:37–44CrossRefGoogle Scholar
  22. Gallardo A, Rodríguez-Saucedo JJ, Covelo F, Fernández-Alés R (2000) Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil 222:71–82CrossRefGoogle Scholar
  23. Garnier E, Aronson J (1998) Nitrogen-use efficiency from leaf to stand level: clarifying the concept. In: Lambers H, Poorter H, Van Vuuren MMU (eds) Inherent variation in plant growth. Physiological mechanisms and ecological consequences. Backhuys, Leiden, pp 515–538Google Scholar
  24. Hamilton EW III, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing-tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  25. Hiremath AJ (1998) Nutrient use efficiency in simplified tropical ecosystems. PhD dissertation. University of Florida, Gainesville, Fla.Google Scholar
  26. Hiremath AJ, Ewel JJ (2001) Ecosystem nutrient use efficiency, productivity, and nutrient accrual in model tropical communities. Ecosystems 4:669–682CrossRefGoogle Scholar
  27. Hiremath AJ, Ewel JJ, Cole TG (2002) Nutrient use efficiency in three fast-growing tropical trees. For Sci 48:662–672Google Scholar
  28. Iversen CM (2004) Effects of increased nitrogen and phosphorus availability on plant productivity and nutrient use at multiple ecological scales in northern peatlands. MSc thesis. University of Nortre Dame, Ind.Google Scholar
  29. Knops JMH, Koenig WD, Nash TH III (1997) On the relationship between nutrient use efficiency and fertility in forest ecosystems. Oecologia 110:550–556CrossRefGoogle Scholar
  30. Ledgard SF, Jarvis SC, Hatch DJ (1998) Short-term N fluxes in grassland soils under different long-term N managements. Soil Biol Biochem 30:1233–1241CrossRefGoogle Scholar
  31. Li MF, Dong YS, Geng YB, Qi YC (2004) Analyses of the correlation between the fluxes of CO2 and the distribution of C & N in grassland soils. Environ Sci 25:7–11Google Scholar
  32. Liu QY, Tong YP, Li JY, Sun JH (2000) Factors influencing the availability of nutrients in the soil of Duolun County in mixed area of agriculture and pasturing. Acta Ecol Sin 20:1034–1037Google Scholar
  33. Mazzarino MJ, Bertiller MB, Sain CL, Satti P, Coronato FR (1998) Soil nitrogen dynamics in northeastern Patagonia steppe under different precipitation regimes. Plant Soil 202:125–131CrossRefGoogle Scholar
  34. Nakamura T, Uemura S, Yabe K (2002) Variation in nitrogen use traits within and between five Carex species growing in the lowland mires of northern Japan. Funct Ecol 16:67–72CrossRefGoogle Scholar
  35. Norby RJ, Iversen CM (2006) Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87:5–14PubMedCrossRefGoogle Scholar
  36. Paoli GD, Curran LM, Zak DR (2005) Phosphorus efficiency of aboveground productivity along a nutrient gradient in Bornean lowland rainforest: a test of the unimodel nutrient response efficiency hypothesis. Ecology 86:1548–1561CrossRefGoogle Scholar
  37. Pastor JP, Aber JD, McClaugherty CA, Melillo JM (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:256–268CrossRefGoogle Scholar
  38. Pastor J, Bridgham SD (1999) Nutrient efficiency along nutrient availability gradients. Oecologia 118:50–58CrossRefPubMedGoogle Scholar
  39. Pavón NP, Briones O, Flores-Rivas J (2005) Litterfall production and nitrogen content in an intertropical semi-arid Mexican scrub. J Arid Environ 60:1–13CrossRefGoogle Scholar
  40. Pérez CA, Armesto JJ, Torrealba C, Carmona MR (2003) Litterfall dynamics and nitrogen use efficiency in two evergreen temperate rainforests of southern Chile. Austral Ecol 28:591–600CrossRefGoogle Scholar
  41. Prescott CE, Corbin JP, Parkinson D (1989) Biomass, productivity, and nutrient-use efficiency of aboveground vegetation in four Rocky Mountain coniferous forests. Can J For Res 19:309–317CrossRefGoogle Scholar
  42. Pugnaire FI, Chapin FS III (1992) Environmental and physiological factors governing nutrient resorption efficiency in barley. Oecologia 90:120–126CrossRefGoogle Scholar
  43. Reich PD, Grigal D, Aber JD, Gower ST (1997) Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78:335–347Google Scholar
  44. Sala OE, Golluscio RA, Lauenroth WK, Soriano A (1989) Resource partitioning between shrubs and grasses in the Patagonian steppe. Oecologia 81:501–505CrossRefGoogle Scholar
  45. Sankaran M, Hanan NP, Scholes RJ et al (2005) Determinants of woody cover in African savannas. Nature 438:846–849PubMedCrossRefGoogle Scholar
  46. Shaver GR, Melillo JM (1984) Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65:1491–1510CrossRefGoogle Scholar
  47. Silla F, Escudero A (2004) Nitrogen-use efficiency: trade-offs between N productivity and mean residence time at organ, plant and population levels. Funct Ecol 18:511–521CrossRefGoogle Scholar
  48. Silver WL (1994) Is nutrient availability related to plant nutrient use in humid tropical forests? Oecologia 98:336–343CrossRefGoogle Scholar
  49. van Staalduiden M, Anten NPR (2005) Difference in the capacity for compensatory growth of two co-occurring grass species in relation to water availability. Oecologia 146:190–199CrossRefGoogle Scholar
  50. Vázquez de Aldana BR, Berendse F (1997) Nitrogen-use efficiency in six perennial grasses from contrasting habitats. Funct Ecol 11:619–626CrossRefGoogle Scholar
  51. Vitousek PM (1982) Nutrient cycling and nitrogen use efficiency. Am Nat 119:553–572CrossRefGoogle Scholar
  52. Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitations in tropical forests. Ecology 65:285–298CrossRefGoogle Scholar
  53. Vitousek PM (1997) On regression and residuals: response to Knops et al. Oecologia 110:557–559CrossRefGoogle Scholar
  54. Vitousek PM, Howarth RH (1991) Nitrogen limitation on land and in the sea, how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  55. Yasumura Y, Hikosaka K, Matsui K, Hirose T (2002) Leaf-level nitrogen-use efficiency of canopy and understorey species in a beech forest. Funct Ecol 16:826–834CrossRefGoogle Scholar
  56. Yuan ZY, Li LH, Huang JH (2003) On plant nutrient use efficiency. I. Some aspects in reassessing plant nutrient use efficiency. In: Li CS (ed) Advances in plant sciences. Higher Education Press, Bejing, pp 187–200Google Scholar
  57. Yuan ZY, Li LH, Han XG, Wan SQ, Zhang WH (2005) Variation in nitrogen economy of two Stipa species in the semiarid region of northern China. J Arid Environ 61:13–25CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Zhi-You Yuan
    • 1
  • Ling-Hao Li
    • 1
  • Xing-Guo Han
    • 1
  • Shi-Ping Chen
    • 1
  • Zheng-Wen Wang
    • 1
  • Quan-Sheng Chen
    • 1
  • Wen-Ming Bai
    • 1
  1. 1.Key Laboratory of Quantitative Vegetation Ecology, Institute of Botany Chinese Academy of SciencesBeijingPeople’s Republic of China

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