Advertisement

Plant Ecology

, Volume 216, Issue 6, pp 809–822 | Cite as

Ecological stoichiometry of C, N, and P of invasive Phragmites australis and native Cyperus malaccensis species in the Minjiang River tidal estuarine wetlands of China

  • Wei Qi WangEmail author
  • Jordi SardansEmail author
  • Chun Wang
  • Cong Sheng Zeng
  • Chuan Tong
  • Dolores Asensio
  • Josep Peñuelas
Article

Abstract

Tidal estuarine wetlands of China are rich in plant diversity, but several global change drivers, such as species invasion, are currently affecting the biogeochemical cycles of these ecosystems. We seasonally analyzed the carbon (C), nitrogen (N), and phosphorus (P) concentrations in litters and soils and in leaves, stems, and roots of the C3 invasive species Phragmites australis (Cav.) Trin. ex Steud. and of the C4 native species Cyperus malaccensis var. brevifolius Boeckeler to investigate the effect of C3 plant invasion on C, N, and P stoichiometry in the C4 plant-dominated tidal wetlands of the Minjiang River. When averaged across seasons, the invasive species P. australis had higher N concentrations and lower P concentrations in leaves than the native species C. malaccensis. N and P concentrations were lower in litter (stem and leaf), whereas C concentrations in leaf litter were higher in P. australis than in C. malaccensis. The C, N, and P concentrations of the soil also did not differ, but plants had a lower C:N and much higher N:P ratios than soils. Root C:P and N:P ratios were lower in the growing season both in the invasive and the native species. The leaf C:N, C:P and N:P ratios peaked in summer. The invasive species had lower C:N ratio in leaves and roots, and higher N:P ratios in all biomass organs and litter than the native species, an effect related with the higher N-resorption capacity of the invasive species. Interspecific differences in C:N, C:P, and N:P ratios may likely reflect the differences in plant morphology, nutrient-use efficiency, and photosynthetic capacity between the C3 (P. australis) and C4 (C. malaccensis) plants. Our results generally suggested that the success of P. australis in these wetlands was related to its slow growth and higher resorption capacity of N and P. This implies a more conservative use of limited nutrients, particularly N, by P. australis, and to higher N concentration in its biomass thus potentially contributing to its invasiveness in these estuarine wetlands.

Keywords

Carbon Nitrogen N:P ratio N resorption Phosphorus Plant 

Notes

Acknowledgments

This work was supported by grants from the National Science Foundation of China (41371127), the Fujian Provincial Department of Education Foundation (JA13081), the Program for Innovative Research Team at Fujian Normal University (IRTL1205), the Key Sciences and Technology Project of Fujian Province (2014R1034-1), and by the European Research Council Synergy Grant ERC-2013-SyG-610028 IMBALANCE-P, the Spanish Government grant CGL2013-48074-P and the Catalan Government Grant SGR 2014-274.

Supplementary material

11258_2015_469_MOESM1_ESM.doc (11.7 mb)
Supplementary material 1 (DOC 11939 kb)

References

  1. Adame MF, Virdi B, Lovelock CE (2010) Effect of geomorphological setting and rainfall on nutrient exchange in mangroves during tidal inundation. Mar Fresh Res 61:1197–1206CrossRefGoogle Scholar
  2. Amlin NA, Rood SB (2001) Inundation tolerances of riparian willows and cottonwoods. J Am Water Res Assoc 37:1709–1720CrossRefGoogle Scholar
  3. Bai JH, Yang HO, Deng W, Zhu YM, Zhang XL, Wang QG (2005) Spatial distribution characteristics of organic matter and total nitrogen of marsh soils in river marginal wetlands. Geoderma 124:181–192CrossRefGoogle Scholar
  4. Bridgham SD, Pastor J, McClaugherty CA, Richard CJ (1995) Nutrient-use efficiency: a litterfall index, a model, and a test along a nutrient-availability gradient in North Carolina peatlands. Am Nat 145:1–21CrossRefGoogle Scholar
  5. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2004) Phylogenetic variation in the shoot mineral concentration of angiosperms. J Exp Bot 55:321–336PubMedCrossRefGoogle Scholar
  6. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468PubMedCrossRefGoogle Scholar
  7. Cebrian J, Lartigue J (2004) Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecol Monogr 74:237–259CrossRefGoogle Scholar
  8. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  9. Demars BOL, Edwards AC (2007) Tissue nutrient concentrations in freshwater aquatic macrophytes: high inter-taxon differences and low phenotypic response to nutrient supply. Fresh Biol 52:2073–2086CrossRefGoogle Scholar
  10. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Res 30:75–115CrossRefGoogle Scholar
  11. Elser JJ, Fagan WF, Denno RF et al (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580PubMedCrossRefGoogle Scholar
  12. Elser JJ, Acharya K, Kyle M et al (2003) Growth rate- stoichiometry couplings in diverse biota. Ecol Lett 6:936–943CrossRefGoogle Scholar
  13. Elser JJ, Peace AL, Kyle M, Wojewodzic M, McCrackin ML, Andersen T, Hessen DO (2010) Atmospheric nitrogen deposition is associated with elevated phosphorus limitation of lake zooplankton. Ecol Lett 13:1256–1261PubMedCrossRefGoogle Scholar
  14. Feng YL (2008) Photosynthesis, nitrogen allocation and specific leaf area in invasive Eupatorium adenophorum and native Eupatorium japonicum grown at different irradiances. Physiol Plant 133:318–326PubMedCrossRefGoogle Scholar
  15. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081PubMedCrossRefGoogle Scholar
  16. Geider R, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17CrossRefGoogle Scholar
  17. González AL, Kominoski JS, Danger M, Ishida S, Iwai N, Rubach A (2010) Can ecological stoichiometry help explain patterns of biological invasion? Oikos 119:779–790CrossRefGoogle Scholar
  18. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol Evol Syst 5:37–61CrossRefGoogle Scholar
  19. Güsewell S, Verhoeven JTA (2006) Litter N:P ratios indicate whether N or P limits the decomposability of graminoid leaf litter. Plant Soil 287:131–143CrossRefGoogle Scholar
  20. Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci USA 107:15505–15507CrossRefGoogle Scholar
  21. Huang GL, He P, Hou M (2006) Present status and prospects of estuarine wetland research in China. Chin J Appl Ecol 17:1751–1756Google Scholar
  22. Huang JY, Zhu XG, Yuan ZY, Song SH, Li X, Li LH (2008) Changes in nitrogen resorption traits of six temperate grassland species along a multi-level N addition gradient. Plant Soil 306:149–158CrossRefGoogle Scholar
  23. Jia RX, Tong C, Wang WQ, Zeng CS (2008) Organic carbon concentrations and storages in the salt marsh sediments in the Min River estuary. Wetl Sci 6:492–499Google Scholar
  24. Jobbágy EG, Jackson R (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51–77CrossRefGoogle Scholar
  25. Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 68:E103–E122CrossRefGoogle Scholar
  26. Kirwan ML, Guntenspergen GR (2012) Feedbacks between inundation, root production, and shoot growth in a rapidly submerging brackish marsh. J Ecol 100:764–770CrossRefGoogle Scholar
  27. Knecht MF, Göransson A (2004) Terrestrial plants require nutrients in similar proportions. Tree Physiol 24:447–460PubMedCrossRefGoogle Scholar
  28. Kobayashi T, Ryder DS, Gordon G, Shannon I, Ingleton T, Carpenter M, Jacobs SJ (2009) Short-term response of nutrients, carbon and planktonic microbial communities to floodplain wetland inundation. Aquat Ecol 43:843–858CrossRefGoogle Scholar
  29. Kocacinar F, Sage RF (2003) Photosynthetic pathway alters xylem structure and hydraulic function in herbaceous plants. Plant, Cell Environ 26:2015–2026CrossRefGoogle Scholar
  30. Laungani R, Knops JMH (2009) Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions. Proc Natl Acad Sci USA 106:12400–12405PubMedCentralPubMedCrossRefGoogle Scholar
  31. Liu JQ, Zeng CS, Chen N (2006) Research of Minjiang River estuary wetland. Science Press, BeijingGoogle Scholar
  32. Lu RK (1999) Analysis methods of soil science and agricultural chemistry. Agricultural Science and Technology Press, BeijingGoogle Scholar
  33. Luo WT, Jiang Y, Lu XT, Wang X, Li MH, Bai E, Han XG, Xu ZW (2013) Patterns of plant biomass allocation in temperate grasslands across a 2500-km transect in Northern China. PLOS One 8(8):e71749PubMedCentralPubMedCrossRefGoogle Scholar
  34. Malone SL, Starr G, Staudhammer CL, Ryan MG (2013) Effects of simulated drought on the carbon balance of Everglades short-hydroperiod marsh. Glob Change Biol 19:2511–2523CrossRefGoogle Scholar
  35. Matzek V (2011) Superior performance and nutrient-use efficiency of invasive plants over non-invasive congeners in a resource-limited environment. Biol Invasions 13:3005–3014CrossRefGoogle Scholar
  36. McClaugherty CA, Pastor J, Aber JD, Melillo JM (1985) Forest litter decomposition in relation to soil nitrogen dynamics and litter quality. Ecology 66:266–275CrossRefGoogle Scholar
  37. Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. Proc Natl Acad Sci USA 105:19780–19785PubMedCentralPubMedCrossRefGoogle Scholar
  38. Mulder C, Ahrestani FS, Bahn M, Bohan DA, Bonkowski M, Griffiths BS, Guicharnaud RA, Kattge J, Krogh PH, Lavorel S, Lewis OT, Mancinelli H, Naeem S, Peñuelas J, Poorter H, Reich PB, Rossi L, Rusch GM, Sardans J, Wright IJ (2013) Connecting the green and brown worlds: allometric and stoichiometric predictability of above- and below-ground networks. Adv Ecol Res 49:69–175Google Scholar
  39. Neves JP, Simões MP, Ferreira LF, Madeira M, Gazarini LC (2010) Comparison of biomass and nutrient dynamics between an invasive and a native species in a Mediterranean saltmarsh. Wetlands 30:817–826CrossRefGoogle Scholar
  40. Noe GB, Hupp CR (2007) Seasonal variation in nutrient retention during inundation of a short-hydroperiod floodplain. River Res Appl 23:1088–1101CrossRefGoogle Scholar
  41. Northup RR, Dahlgren RA, Mccoll JG (1998) Polyphenols as regulators of plant-litter-soil interactions in northern California’s pygmy forest: a positive feedback? Biogeochemistry 421:89–220Google Scholar
  42. Olde Venterink H, Wassen MJ, Buiter Verkroost AWM, Ruiter PCD (2003) Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84:2191–2199CrossRefGoogle Scholar
  43. Peñuelas J, Sardans J, Llusia J, Owen S, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on ‘leaf economics’ and different biogeochemical niche in invasive compared with native plant species. Glob Change Biol 16:2171–2185CrossRefGoogle Scholar
  44. Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hisinger R, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013) Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934PubMedGoogle Scholar
  45. Sardans J, Peñuelas J (2012) The role of plants in the effects of Global Change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761PubMedCentralPubMedCrossRefGoogle Scholar
  46. Sardans J, Peñuelas J (2013) Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Glob Ecol and Biogeogr 22:494–507Google Scholar
  47. Sardans J, Peñuelas J (2014) Climate and taxonomy underlie different elemental concentrations and stoichiometries of forest species: the optimum “biogeochemical niche”. Plant Ecol 215:441–455PubMedCentralPubMedCrossRefGoogle Scholar
  48. Sardans J, Rivas-Ubach A, Peñuelas J (2012) The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111:1–39CrossRefGoogle Scholar
  49. Shen HT, Zhu JR (1999) The land and ocean interaction in the coastal zone of China. Mar Sci Bull 18:11–17Google Scholar
  50. Sorrell B, Brix H, Schierup HH, Lorenzen B (1997) Die-back of Phragmites australis: influence on the distribution and rate of sediment methanogenesis. Biogeochemistry 36:173–188CrossRefGoogle Scholar
  51. Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534CrossRefGoogle Scholar
  52. Tian HQ, Chen GS, Zhang C, Melillo JM, Hall CAS (2010) Pattern and variation of C:N:P ratios in China’s soils: a synthesis of observational data. Biogeochemistry 98:139–151CrossRefGoogle Scholar
  53. Tong C, Liu BG (2009) Litter decomposition and nutrient dynamics in different tidal water submergence environments of estuarine tidal wetland. Geogr Res 28:118–128Google Scholar
  54. Tong C, Wang WQ, Zeng CS, Marrs R (2010) Methane emission from a tidal marsh in the Min River estuary, southest China. J Environ Sci Health 45:506–516CrossRefGoogle Scholar
  55. Townsend A, Cleveland CC, Asner GP, Bustamante MC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118PubMedCrossRefGoogle Scholar
  56. Vitousek PM, Peter M (1984) Nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298CrossRefGoogle Scholar
  57. Wang SQ, Yu GR (2008) Ecological stoichiometry characteristics of ecosystem carbon, nitrogen and phosphorus elements. Acta Ecol Sin 28:3937–3947CrossRefGoogle Scholar
  58. Wang WQ, Tong C, Jia RX, Zeng CS (2010a) Ecological stoichiometry of characteristics of wetland soil carbon, nitrogen and phosphorus in different water-flooded frequency. J Soil Water Conserv 24:238–242Google Scholar
  59. Wang WQ, Tong C, Zeng CS (2010b) Stoichiometry characteristics of carbon, nitrogen, phosphorus and anaerobic carbon decomposition of wetland soil of different texture. China Environ Sci 30:1130–1134Google Scholar
  60. Wilson SD (2007) Competition, resources, and vegetation during 10 years in native grassland. Ecology 88:2951–2958PubMedCrossRefGoogle Scholar
  61. Windham L (2001) Comparison of biomass production and decomposition between Phragmites australis (common reed) and Spartina patens (salt hay grass) in brackish tidal marshes of New Jersey, USA. Wetlands 21:179–188CrossRefGoogle Scholar
  62. Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar
  63. Wurzburger N, Hendrick R (2009) Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J Ecol 97:528–536CrossRefGoogle Scholar
  64. Zand E, Soufizadeh S, Eskandari A (2006) Water stress and nitrogen limitation effects on corn (Zea mays L.) competition with a C3 and a C4 weed. Commun Agric Appl Biol Sci 71:753–760PubMedGoogle Scholar
  65. Zeng CS, Zhang LH, Tong C (2009a) Seasonal dynamics of nitrogen and phosphorus in Phragmites australis and Spartina alterniflora in the wetlands of Min River estuary. Wetl Sci 7:16–24Google Scholar
  66. Zeng CS, Zhang LH, Tong C (2009b) Seasonal variation of nitrogen and phosphorus concentrations and accumulation of Cyperus malaccensis in Minjiang River estuary. Chin J Ecol 28:788–794Google Scholar
  67. Zhang LH, Zeng CS, Tong C (2008) Study on biomass dynamics of Phragmites australis and Spartina alterniflora in the wetlands of Minjiang River estuary. J Subtrop Resour Environ 3:25–33Google Scholar
  68. Zheng CH, Zeng CS, Chen ZQ (2006) A study on the changes of landscape pattern of estuary wetlands of the Minjiang River. Wetl Sci 4:29–34Google Scholar
  69. Zhou LJ, Tu YY, Song YC (2006) The biodiversity of wetland and its prevention measures in Min River Estuary. Ecol Sci 25:330–334Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Wei Qi Wang
    • 1
    • 2
    Email author
  • Jordi Sardans
    • 3
    • 4
    Email author
  • Chun Wang
    • 1
    • 2
  • Cong Sheng Zeng
    • 1
    • 2
  • Chuan Tong
    • 1
    • 2
  • Dolores Asensio
    • 3
    • 4
  • Josep Peñuelas
    • 3
    • 4
  1. 1.Institute of GeographyFujian Normal UniversityFuzhouChina
  2. 2.Key Laboratory of Humid Subtropical Eco-geographical ProcessMinistry of Education, Fujian Normal UniversityFuzhouChina
  3. 3.CSICGlobal Ecology Unit CREAF-CSIC-UABCerdanyola del VallèsSpain
  4. 4.CREAFCerdanyola del VallèsSpain

Personalised recommendations