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Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in southwest China

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Abstract

Background and aims

Nitrogen (N) and/or phosphorus (P) limitation to primary productivity and other biological processes can change in a variety of ways as ecosystems develop. How N limitation and P limitation change from the early to the late stages of a secondary succession following farmland abandonment remains unclear in karst ecosystems in southwest China.

Methods

We used community foliar N:P ratio, soil alkaline phosphatase activity (APA) and other indicators of nutrient status (soil organic carbon [SOC], total soil N [TN], and total soil P [TP], Alkali-hydrolyzable N [AN], and available soil phosphorus [AP] concentrations) to examine changes in N and P status during secondary vegetation succession. Four types of plant communities (grasslands, shrublands, secondary forest, and primary forest) represented the early, middle, late, and very late successional stages, respectively.

Results

Community foliar N:P ratio, APA, and APA per unit SOC increased as succession proceeded from the grassland to the secondary and primary forest communities. Moreover, community foliar N:P ratios in the grassland were positively correlated with soil TN, while community foliar N:P ratios in the secondary forest and primary forest were negatively correlated with soil TP, but were not correlated with soil TN. Community foliar N:P ratios in the shrubland were not correlated with either soil TN or TP.

Conclusions

Our results suggest that the grassland in the karst region of southwest China is N limited, that the secondary and primary forests are P limited, and that the shrubland is constrained by N and P together or by other nutrients.

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Abbreviations

APA:

Alkaline phosphatase activity

SOC:

Soil organic carbon

References

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    CAS  Google Scholar 

  • Amatangelo KL, Vitousek PM (2008) Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia 157:619–627

    Article  PubMed  Google Scholar 

  • Bormann BT, Sidle RC (1990) Changes in productivity and distribution of nutrients in a chronosequence at glacier Bay national-park, Alaska. J Ecol 78:561–578

    Article  Google Scholar 

  • Broadbent EN, Zambrano AMA, Asner GP, Soriano M, Field CB, de Souza HR, Pena-Claros M, Adams RI, Dirzo R, Giles L (2014) Integrating stand and soil properties to understand foliar nutrient dynamics during forest succession following slash-and-burn agriculture in the Bolivian Amazon. Plos One 9

  • Castle SC, Neff JC (2009) Plant response to nutrient availability across variable bedrock geologies. Ecosystems 12:101–113

    Article  CAS  Google Scholar 

  • Cech PG, Kuster T, Edwards PJ, Olde Venterink H (2008) Effects of herbivory, fire and N(2)-fixation on nutrient limitation in a humid African savanna. Ecosystems 11:991–1004

    Article  CAS  Google Scholar 

  • Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497

    Article  CAS  Google Scholar 

  • Davidson EA, de Carvalho CJ, Figueira AM, Ishida FY, Ometto JP, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira IC, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–998

    Article  CAS  PubMed  Google Scholar 

  • Du Y, Pan G, Li L, Hu Z, Wang X (2011) Leaf N/P ratio and nutrient reuse between dominant species and stands: predicting phosphorus deficiencies in Karst ecosystems, southwestern China. Environ Earth Sci 64:299–309

    Article  CAS  Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    Article  CAS  PubMed  Google Scholar 

  • Göransson H, Edwards PJ, Perreijn K, Smittenberg RH, Olde Venterink H (2014) Rocks create nitrogen hotspots and N:P heterogeneity by funnelling rain. Biogeochemistry 121:329–338

    Article  Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Güsewell S, Koerselman W, Verhoeven JTA (2003) Biomass N:P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecol Appl 13:372–384

    Article  Google Scholar 

  • Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385

    Article  CAS  PubMed  Google Scholar 

  • He JS, Wang L, Flynn DFB, Wang X, Ma W, Fang J (2008a) Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155:301–310

  • He XY, Wang KL, Zhang W, Chen ZH, Zhu YG, Chen HS (2008b) Positive correlation between soil bacterial metabolic and plant species diversity and bacterial and fungal diversity in a vegetation succession on Karst. Plant Soil 307:123–134

    Article  CAS  Google Scholar 

  • Hedin LO, Armesto JJ, Johnson AH (1995) Patterns of nutrient loss from unpolluted, old-growth temperate forests–evaluation of biogeochemical theory. Ecology 76:493–509

    Article  Google Scholar 

  • Hedin LO, Vitousek PM, Matson PA (2003) Nutrient losses over four million years of tropical forest development. Ecology 84:2231–2255

    Article  Google Scholar 

  • Herbert D, Fownes J (1995) Phosphorus limitation of forest leaf area and net primary production on a highly weathered soil. Biogeochemistry 29:223–235

    Article  CAS  Google Scholar 

  • Hofmeister J, Mihaljevic M, Hosek J, Sadlo J (2002) Eutrophication of deciduous forests in the Bohemian Karst (Czech Republic): the role of nitrogen and phosphorus. For Ecol Manag 169:213–230

    Article  Google Scholar 

  • Huang W, Liu J, Wang Y, Zhou G, Han T, Li Y (2013) Increasing phosphorus limitation along three successional forests in southern China. Plant Soil 364:181–191

    Article  CAS  Google Scholar 

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J-M (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16

    Google Scholar 

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Kramer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32:179–188

    Article  CAS  Google Scholar 

  • Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll K-H, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–642

    Article  Google Scholar 

  • Li DJ, Niu SL, Luo YQ (2012) Global patterns of the dynamics of soil carbon and nitrogen stocks following afforestation: a meta-analysis. New Phytol 195:172–181

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Lang Y, Li S, Piao H, Tu C, Liu Z, Zhang W, Zhu S (2009) Researches on biogeochemical processes and nutrient cycling in karstic ecological systems, southwest China: a review. Earth Sci Front 16:1–12

    Google Scholar 

  • Ludwig F, de Kroon H, Prins HHT, Berendse F (2001) Effects of nutrients and shade on tree-grass interactions in an East African savanna. J Veg Sci 12:579–588

    Article  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • McGroddy ME, Baisden WT, Hedin LO (2008) Stoichiometry of hydrological C, N, and P losses across climate and geology: an environmental matrix approach across New Zealand primary forests. Glob Biogeochem Cycles 22

  • Mendes ID, Fernandes MF, Chaer GM, dos Reis FB (2012) Biological functioning of Brazilian Cerrado soils under different vegetation types. Plant Soil 359:183–195

    Article  CAS  Google Scholar 

  • Menge DNL, Hedin LO, Pacala SW (2012) Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. PLoS ONE 7:e42045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niinemets U, Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecol Int J Ecol 28:345–356

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    Article  CAS  Google Scholar 

  • Olde Venterink H (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant Soil 347:137–146

    Article  CAS  Google Scholar 

  • Olde Venterink H, van der Vliet RE, Wassen MJ (2001) Nutrient limitation along a productivity gradient in wet meadows. Plant Soil 234:171–179

    Article  CAS  Google Scholar 

  • Olde Venterink H, Wassen MJ, Verkroost AWM, de Ruiter PC (2003) Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84:2191–2199

    Article  Google Scholar 

  • Perakis SS, Hedin LO (2002) Nitrogen loss from unpolluted South American forests mainly via dissolved organic compounds. Nature 415:416–419

    Article  PubMed  Google Scholar 

  • Piao H, Liu C, Zhu S, Zhu J (2005) Variations fo C4 and C3 plant N:P ratios influenced by nutrient stoichiometry in limestone and sandstone areas of Guizhou. Quat Sci 25:552–560

    Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Richardson S, Peltzer D, Allen R, McGlone M, Parfitt R (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139:267–276

    Article  PubMed  Google Scholar 

  • Rivera LW, Aide TM (1998) Forest recovery in the karst region of Puerto Rico. For Ecol Manag 108:63–75

    Article  Google Scholar 

  • Selmants PC, Hart SC (2008) Substrate age and tree islands influence carbon and nitrogen dynamics across a retrogressive semiarid chronosequence. Glob Biogeochem Cycles 22

  • Selmants PC, Hart SC (2010) Phosphorus and soil development: does the Walker and Syers model apply to semiarid ecosystems? Ecology 91:474–484

    Article  PubMed  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    PubMed  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534

    Article  CAS  Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118

    Article  PubMed  Google Scholar 

  • Turner BL, Baxter R, Whitton BA (2002) Seasonal phosphatase activity in three characteristic soils of the English uplands polluted by long-term atmospheric nitrogen deposition. Environ Pollut 120:313–317

    Article  CAS  PubMed  Google Scholar 

  • Uliassi DD, Ruess RW (2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83:88–103

    Article  Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    Article  CAS  Google Scholar 

  • Vitousek P, Walker L, Whiteaker L, Matson P (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23:197–215

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Zhang W, Chen H, Wang K, Zhang J, Hou Y (2007) Effects of planting pattern and bare rock ratio on spatial distribution of soil nutrients in Karst depression area. Chin J Appl Ecol 1459–1463

  • Zhu H, He X, Wang K, Su Y, Wu J (2012) Interactions of vegetation succession, soil bio-chemical properties and microbial communities in a Karst ecosystem. Eur J Soil Biol 51:1–7

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Basic Research Program of China (2015CB452703), the Chinese Academy of Sciences through its Hundred Talent Program to Dejun Li, two grants from the National Natural Science Foundation of China (31270555 and 31300448), and a grant from the Western Light Program from CAS to Wei Zhang. We appreciate Dr. Harry Olde Venterink and the anonymous reviewers for their time and constructive comments and suggestions.

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    Authors and Affiliations

    1. Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, 410125, China

      Wei Zhang, Jie Zhao, Fujing Pan, Dejun Li, Hongsong Chen & Kelin Wang

    2. Huanjiang Observation and Research Station for Karst Ecosystems, Chinese Academy of Sciences, Huanjiang, Guangxi, 547100, China

      Wei Zhang, Jie Zhao, Fujing Pan, Dejun Li, Hongsong Chen & Kelin Wang

    3. Graduate School of the Chinese Academy of Sciences, Beijing, 100039, China

      Fujing Pan

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    1. Wei Zhang
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    3. Fujing Pan
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    Correspondence to Wei Zhang.

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    Responsible Editor: Harry Olde Venterink.

    Wei Zhang and Jie Zhao contributed equally to this work.

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    Zhang, W., Zhao, J., Pan, F. et al. Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in southwest China. Plant Soil 391, 77–91 (2015). https://doi.org/10.1007/s11104-015-2406-8

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