Ecological stoichiometry of two common hemiparasite plants and their relationship with host trees in Ailao Mountain, Yunnan, China

TANG Dan-Dan1,2 WU Yi1,2 LIU Wen-Yao1 HU Tao1,2 HUANG Jun-Biao1,2 ZHANG Ting-Ting1,2

(1.CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, China 666303)
(2.University of Chinese Academy of Sciences, Beijing, China 100049)

【Abstract】Aims The objectives of this study were to characterize the carbon (C):nitrogen (N):phosphorus (P) stoichiometry of the “host branches–haustorias–parasitic branches–parasitic leaves” continuum and to better understand the nutrient relationship between hemiparasite plants and their hosts. Methods The study site is located in the Xujiaba area of Ailao Mountain, Yunnan Province. Two common hemiparasite plants Loranthus delavayi and Taxillus delavayi were selected, and the C, N and P concentrations of host branches, haustorias, parasitic branches and parasitic leaves were measured. Important findings The results showed that, the tendencies of C, N, P stoichiometry characteristics of host branches–haustorias–parasitic branches–parasitic leaves were species specific, and were not identical between the two hemiparasites. The host branches of the same parasitic plant had similar C, N, and P stoichiometry characteristics, and the host species had no significant effect on the stoichiometry of hemiparasites. There was a close coupling relationship between the C, N, P stoichiometry characteristics in the host branches, and the haustorias was weaker than the host branch, the parasitic branch was weaker than the haustorias, and there was no significant correlation between the N and P concentrations in the parasitic leaf. There was significant negative correlation between the host branches and the parasitic leaves of C concentration. The C, N, P stoichiometry characteristics of the haustorias were more similar to the parasitic branches, and it had very significant positive correlation with the host branches. As a key part of the host and parasitic plants, the haustorias had significant correlation with the host branches, which reflected the importance of the host branch nutrients to the parasitic plants. The element stoichiometry and their relationship of the haustorias were more similar to those of the parasitic branches, which embodied that haustorias as a parasitic plant organ had physiological functions similar to those of the parasitic branches. These results provided important data for in-depth study of nutrient utilization strategies and ecological adaptability of hemiparasitic plants.

【Keywords】 hemiparasite; ecological stoichiometry; branch; haustoria; leaf;

【DOI】

【Funds】 National Natural Science Foundation of China (31770496 and 41471050) Biodiversity Conservation Strategy Program of Chinese Academy of Sciences (ZSSD-016), and “135 Program” of Chinese Academy of Sciences (2017XTBG-T01)

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    References

    Bell TL, Adams MA (2011). Attack on all fronts: Functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiology, 31, 3–15.

    Chen L, Huang L, Li X, You S, Yang S, Zhang Y, Wang W (2013). Water and nutrient relationships between a mistletoe and its mangrove host under saline conditions. Functional Plant Biology, 40, 475–483.

    Cleveland CC, Liptzin D (2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass. Biogeochemistry, 85, 235–252.

    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, 12–19.

    Cui GY, Cao Y, Chen YM (2015). Characteristics of nitrogen and phosphorus stoichiometry across components of forest ecosystem in Shaanxi Province. Chinese Journal of Plant Ecology, 39, 1146–1155.

    Demey A, de Frenne P, Baeten L, Verstraeten G, Hermy M, Boeckx P, Verheyen K (2015). The effects of hemiparasitic plant removal on community structure and seedling establishment in semi-natural grasslands. Journal of Vegetation Science, 26, 409–420.

    Demey A, Rütting T, Huygens D, Staelens J, Hermy M, Verheyen K, Boeckx P (2014). Hemiparasitic litter additions alter gross nitrogen turnover in temperate semi-natural grassland soils. Soil Biology & Biochemistry, 68, 419–428.

    Duarte CM (1992). Nutrient concentration of aquatic plants: Patterns across species. Limnology and Oceanography, 37, 882–889.

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

    Garten CT (1976). Correlations between concentrations of elements in plants. Nature, 261, 686–688.

    Gebauer R, Volařík D, Urban J (2012). Quercus pubescens and its hemiparasite Loranthus europaeus: Nutrient dynamics of leaves and twigs. Acta Physiologiae Plantarum, 34, 1801–1809.

    Gebauer R, Volařík D, Urban J (2018). Seasonal variations of sulphur, phosphorus and magnesium in the leaves and current-year twigs of hemiparasitic mistletoe Loranthus europaeus Jacq. and its host Quercus pubescens Willd. Journal of Forest Science, 66–73.

    Glatzel G (1983). Mineral nutrition and water relations of hemiparasitic mistletoes: A question of partitioning. Experiments with Loranthus europaeus on Quercus petraea and Quercus robur. Oecologia, 56, 193–201.

    Glatzel G, Geils BW (2009). Mistletoe ecophysiology: Hostparasite interactions. Botany, 87, 10–15.

    Gong L, Li HL, Liu YT, An SQ (2017). Effects of nitrogen and phosphorus fertilizers on carbon, nitrogen, and phosphorus stoichiometry of oasis cotton in the upper reaches of Tarim River, Xinjiang, China. Acta Ecologica Sinica, 37, 7689–7697 (in Chinese).

    Güsewell S, Koerselman W (2002). Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology Evolution and Systematics, 5, 37–61.

    Han WX, Fang JY, Guo DL, Zhang Y (2005). Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytologist, 168, 377–385.

    Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (2011). Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecology Letters, 14, 788–796.

    Hatcher M, Dick JTA, Dunn AM (2012). Diverse effects of parasites in ecosystems: Linking interdependent processes. Frontiers in Ecology and the Environment, 10, 186–194.

    He HL, Yang XC, Wang D, Sun YY, Yin CY, Li T, Li YX, Zhou GY, Zhang L, Liu Q (2017). Ecological stoichiometric characteristics of soil carbon, nitrogen and phosphorus of Sibiraea angustata shrub in eastern Qinghai-Tibetan Plateau. Chinese Journal of Applied and Environmental Biology, 21, 1128–1135 (in Chinese).

    He M, Chen H, Pan CD, Hu Y, Xiao ZZ, Wang B (2015). Seasonal variation and correlation of mineral element concentrations between Juglans regia ‘Xinwen 185’ leaves and fruits. Xinjiang Agricultural Sciences, 52, 1399–1406 (in Chinese).

    Hedin LO (2004). Global organization of terrestrial plant nutrient interactions. Proceedings of the National Academy of Sciences of the United States of America, 101, 10849–10850.

    Hidaka A, Kitayama K (2015). Physiological linkage in co-variation of foliar nitrogen and phosphorus in tropical tree species along a gradient of soil phosphorus availability. Journal of Tropical Ecology, 31, 221–229.

    Hu F, Kong CH (2004). Selectivity and influence of parasite plants on their hosts. Chinese Journal of Applied Ecology, 15, 905–908 (in Chinese).

    Hu YS, Yao XY, Liu YH (2014). N and P stoichiometric traits of plant and soil in different forest succession stages in Changbai Mountains. Chinese Journal of Applied Ecology, 25, 632–638 (in Chinese).

    Huang XY, Guan KY, Li AR (2011). Biological traits and their ecological significances of parasitic plants: A review. Chinese Journal of Ecology, 30, 1838–1844 (in Chinese).

    Jiang LL, He S, Wu LF, Yan YF, Weng SF, Liu J, Wang WQ, Zeng CS (2014). Characteristics of stoichiometric homeostasis of three plant species in wetlands in Minjiang estuary. Wetland Science, 12, 293–298 (in Chinese).

    Jiang PP, Cao Y, Chen YM, Zhao YP (2017). N and P stoichiometric characteristics of leaves, litter, and soil for three dominant tree species in the Shaanxi Province. Acta Ecologica Sinica, 37, 443–454 (in Chinese).

    Kerkhoff AJ, Fagan WF, Else JJ, Enquist BJ (2006). Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. The American Naturalist, 168, 103–122.

    Koerselman W, Meuleman AFM (1996). The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33, 1441–1450.

    Lepš J, Těšitel J (2015). Root hemiparasites in productive communities should attack competitive host, and harm them to make regeneration gaps. Journal of Vegetation Science, 26, 407–408.

    Li S, Liu WY, Wang LS, Yang GP, Li DW (2007). Species diversity and distribution of epiphytic lichens in the primary and secondary forests in Ailao Mountain, Yunnan. Biodiversity Science, 15, 445–455 (in Chinese).

    Li W (2016). Global pattern of plant ecological stoichiometrics characteristics. Journal of Nanchang Institute of Technology, 35 (6), 6–10 (in Chinese).

    Li XW, Sun K, Li FY (2014). Variation in leaf nitrogen and phosphorus stoichiometry in the nitrogen-fixing Chinese sea-buckthorn (Hippophae rhamnoides L. subsp. sinensis Rousi) across northern China. Ecological Research, 29, 723–731.

    Li YH, Chen SL, Lu D, Zhu KX, Zhao MH, Pei HH, Ruan JL (2009). Study on the contents of total flavonoids of herbataxilli from different host-plants. Lishizhen Medicine and Materia Medicare Research, 20, 3009–3010 (in Chinese).

    Li YH, Su BW, Zhang XJ, Zhu KX, Pei HH, Zhao MH, Lu D (2012). Influence of host plant on the volatile components of taxilli herba. Lishizhen Medicine and Materia Medicare Research, 23, 574–578 (in Chinese).

    Liao ZW, Mao XY, Liu KX (2014). Effect of organic Carbon fertilizer on nutrient balance—Analysis of carbon, a short board, in plant nutrition. Acta Pedologica Sinica, 51, 656–659 (in Chinese).

    Liu WT, Wei ZJ, LüSJ, Sun SX (2015). Research advances in stoichiometry of grassland in China. Acta Agrestia Sinica, 23, 914–926 (in Chinese).

    Lu ZY, Song L, Wang X, Li YW, Zhang YP, Sha LQ (2017). Ecological stoichiometry characteristics of the litterfall–humus–soil continuum systems under different successional stages of the subtropical forest in SW China. Mountain Reseach, 35, 274–282 (in Chinese).

    Luo Y, Gong L, Zhu ML, An SQ (2017). Stoichiometry characteristics of leaves and soil of four shrubs in the upper reaches of the Tarim River Desert. Acta Ecologica Sinica, 37, 8326–8335 (in Chinese).

    Michaels AF (2003). The ratios of life. Science, 300, 906–907.

    Minden V, Kleyer M (2015). Internal and external regulation of plant organ stoichiometry. Plant Biology, 16, 897–907.

    Nave LE, Heckman KA, Muñoz AB, Swanston CW (2017). Radiocarbon suggests the hemiparasitic annual Melampyrum lineare Desr. may acquire carbon from stressed hosts. Radiocarbon, 60, 1–13.

    Nickrent DL, Duff RJ, Colwell AE, Wolfe AD, Young ND, Steiner KE, de Pamphilis CW (1998). Molecular phylogenetic and evolutionary studies of parasitic plants. Molecular Systematics of Plants II. Springer, New York. 211–241.

    Niklas KJ (2006). Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. Annals of Botany, 97, 155–163.

    Niklas KJ, Cobb ED (2005). N, P, and C stoichiometry of Eranthis hyemalis (Ranunculaceae) and the allometry of plant growth. American Journal of Botany, 92, 1256–1263.

    Norton DA, Lange PJD (1999). Host specificity in Parasitic mistletoes (Loranthaceae) in New Zealand. Functional Ecology, 13, 552–559.

    Phoenix GK, Press MC (2010). Linking physiological traits to impacts on community structure and function: The role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). Journal of Ecology, 93, 67–78.

    Press MC, Phoenix GK (2010). Impacts of parasitic plants on natural communities. New Phytologist, 166, 737–751.

    Qiu XZ, Xie SC (1998). Studies on the Forest Ecosystem in Ailao Mountains, Yunnan, China. Yunnan Science and Technology Press, Kunming (in Chinese).

    Quested HM, Callaghan TV, Cornelissen JHC, Press MC (2010). The impact of hemiparasitic plant litter on decomposition: Direct, seasonal and litter mixing effects. Journal of Ecology, 93, 87–98.

    Reich PB, Oleksyn J (2004). Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of National Academy of Sciences of the United States of America, 101, 11001–11006.

    Reich PB, Oleksyn J, Wright IJ, Niklas KJ, Hedin L, Elser JJ (2010). Evidence of a General 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. Proceedings of the Royal Society B, 277, 877–883.

    Ren SJ, Yu GR, Tao B, Wang SQ (2007). Leaf nitrogen and phosphorus stoichiometry across 643 terrestrial plant species in NSTEC. Environmental Science, 28, 2665–2673 (in Chinese).

    Selosse MA, Charpin M, Not F (2017). Mixotrophy everywhere on land and in water: The grandécart hypothesis. Ecology Letters, 20, 246.

    Sterner RW, Elser JJ (2002). Ecological Stoichiometry: The Biology of Elements From Molecules to the Biosphere. Princeton University Press, Princeton. 225–226.

    Suriyagoda LDB, Rajapaksha R, Pushpakumara G, Lambers H (2017). Nutrient resorption from senescing leaves of epiphytes, hemiparasites and their hosts in tropical forests of Sri Lanka. Journal of Plant Ecology, 11, 815–826.

    SvětlíkováP, Blažek P, Mühlsteinová R, Těšitel J (2016). Tracing nitrogen flow in a root-hemiparasitic association by foliar stable-isotope labelling. Plant Ecology and Evolution, 149, 39–44.

    Tennakoon KU, Chak WH, Bolin JF (2011). Nutritional and isotopic relationships of selected Bornean tropical mistletoehost associations in Brunei Darussalam. Functional Plant Biology, 38, 505–513.

    Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD (2015). Integrating ecology and physiology of root-hemiparasitic interaction: Interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytologist, 205, 350–360.

    Tian D, Yan ZB, Niklas KJ, Han WX, Kattge J, Reich PB, Luo YK, Chen YH, Tang ZY, Hu HF, Wright IJ, Schmid B, Fang JY (2018). Global leaf nitrogen and phosphorus stoichiometry and their scaling exponent. National Science Review, 5, 728–739.

    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, 22, 327–346.

    Vitousek PM (1998). Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems, 1, 401–407.

    Wang T, Yang YH, Ma WH (2008). Storage, patterns and environmental controls of soil phosphorus in China. Acta Scientiarum Naturalium Universitatis Pekinensis, 44, 945–952 (in Chinese).

    Wang XN, Zhang L (2017). Species diversity and distribution of mistletoes and hosts in four different habitats in Xishuangbanna, Southwest China. Chinese Journal of Plant Ecology, 39, 701–711 (in Chinese).

    Watson DM (2010). Parasitic plants as facilitators: More dryad than dracula? Journal of Ecology, 97, 1151–1159.

    Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002). Plant ecological strategies: Some leading dimensions of variation between species. Annual Review of Ecology and Systematics, 33, 125–159.

    Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005). Assessing the generality of global leaf trait relationships. New Phytologist, 166, 485–496.

    Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, 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.

    Yan ZB, Li XP, Tian D, Han WX, Hou XH, Shen HS, Guo YL, Fang JY (2018). Nutrient addition affects scaling relationship of leaf nitrogen to phosphorus in Arabidopsis thaliana. Functional Ecology, 32, 2689–2698.

    Yang M, Wang CQ, Yuan DG, Li QQ, Zeng J, Luo Q, Lan XM, Tang J (2015). C, N, P stoichiometry traits of different flue-cured tobacco organs at different growth stages. Chinese Journal of Eco-Agriculture, 23, 686–693 (in Chinese).

    You CX (1983). Classification of Vegetation in Xujiaba Region in Ailao Mts. Research of Forest Ecosystems on Ailao Mountains Yunnan. Yunnan Science and Technology Press, Kunming (in Chinese).

    Young SS, Herwitz SR (1995). Floristic diversity and co-occurrences in a subtropical broad-leaved forest and two contrasting regrowth stands in central-west Yunnan Province, China. Vegetatio, 119, 1–13.

    Zeng DH, Chen GS (2005). Ecological stoichiometry: A science to explore the complexity of living systems. Acta Phytoecologica Sinica, 29, 1007–1019 (in Chinese).

    Zeng DP, Jiang LL, Zeng CS, Wang WQ, Wang C (2013). Reviews on the ecological stoichiometry characteristics and its applications. Acta Ecologica Sinica, 33, 5484–5492 (in Chinese).

    Zeng ZX, Wang KL, Liu XL, Zeng FP, Song TQ, Peng WX, Zhang H, Du H (2015). Stoichiometric characteristics of plants, litter and soils in karst plant communities of Northwest Guangxi. Chinese Journal of Plant Ecology, 39, 682–693 (in Chinese).

    Zhang K, He MZ, Li XR, Tan HJ, Gao YH, Li G, Han GJ, Wu YY (2014). Foliar carbon, nitrogen and phosphorus stoichiometry of typical desert plants across the Alashan Desert. Acta Ecologica Sinica, 34, 6538–6547 (in Chinese).

    Zhao YP, Cao Y, Chen YM, Peng SZ (2007). Ecological stoichiometry in a forest in the hilly-gully of Loess Plateau. Acta Ecologica Sinica, 37, 5451–5460 (in Chinese).

    Zhou HH, Liu XL, Qian HB, Wang SQ, Zhou C (2013). Comparative study on toxicities of Taxillus sutchuenensis from different host plants. Chinese Journal of Experimental Traditional Medical Formulae, 19, 274–277 (in Chinese).

    Zhu H, Yan LC (2009). List of Seed Plants in the Ailao Mts. of Yunnan Province, China. Yunnan Science and Technology Press, Kunming (in Chinese).

This Article

ISSN:1005-264X

CN:11-3397/Q

Vol 43, No. 03, Pages 245-257

March 2019

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Article Outline

Abstract

  • 1 Materials and methods
  • 2 Results and analysis
  • 3 Discussion
  • 4 Conclusions
  • References