Seasonal variation and ecological importance of tannin and nutrient concentrations in Casuarina equisetifolia branchlets and fine roots

Lihua Zhang , Shangju Zhang , Gongfu Ye , Xiaochun Qin

Journal of Forestry Research ›› 2019, Vol. 31 ›› Issue (5) : 1499 -1508.

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Journal of Forestry Research ›› 2019, Vol. 31 ›› Issue (5) : 1499 -1508. DOI: 10.1007/s11676-019-00991-0
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Seasonal variation and ecological importance of tannin and nutrient concentrations in Casuarina equisetifolia branchlets and fine roots

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Abstract

In this study, we investigated the effects of environmental factors on plant phenolic variability, seasonal dynamics of total phenolic content (TP), extractable condensed tannins (ECT), protein-bound condensed tannins (PBCT), fiber-bound condensed tannins (FBCT), total condensed tannins (TCT), protein precipitation capacity (PPC) and nutrient content in the branchlets and fine roots of Casuarina equisetifolia. TP and TCT concentrations in branchlets were lowest in the spring, then increased in summer and autumn, similar to the seasonal dynamics in air temperature. TP and TCT concentrations in fine roots were highest in summer, coinciding with heavy precipitation. In general, TP and TCT concentrations were higher in branchlets than in fine roots. No significant difference was found in C concentration among various seasons for either branchlets or fine roots. Branchlets had significantly higher N and P concentrations than fine roots in most seasons. The C/N and N/P ratios in branchlets were significantly lower than in fine roots in all seasons, except summer. The relationship between branchlets and fine roots was significant for C, P and FBCT, but no significant relationships were found for N, TP, ECT, PBCT and TCT. Additionally, TP and TCT content were each significantly correlated with PPC in branchlets and in fine roots. Both TP/N and TCT/N ratios were highest in the autumn for the branchlets and in the summer for fine roots. The results indicate that high temperatures lead to increased tannin production in branchlets, but that the tannin content in fine roots is mainly affected by precipitation. Tannin content was greater in branchlets than in fine roots, which may indicate that selective pressure is greater on branchlets than on fine roots.

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Lihua Zhang, Shangju Zhang, Gongfu Ye, Xiaochun Qin. Seasonal variation and ecological importance of tannin and nutrient concentrations in Casuarina equisetifolia branchlets and fine roots. Journal of Forestry Research, 2019, 31(5): 1499-1508 DOI:10.1007/s11676-019-00991-0

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References

[1]

Aerts RJ, Barry TN, McNabb WC. Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agr Ecosyst Environ, 1999, 75(1–2): 1-12.

[2]

Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B. Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L.. Acta Physiol Plant, 2011, 33(4): 1103-1111.

[3]

Bryant JP, Chapin FS, Klein DR. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 1983, 40(3): 357-368.

[4]

Bucchetti B, Matthews MA, Falginella L, Peterlunger E, Castellarin SD. Effect of water deficit on Merlot grape tannins and anthocyanins across four seasons. Sci Hortic, 2011, 128(3): 297-305.

[5]

Chen JZ, Zhang HY, Han ZP, Ye JY, Liu ZL. The influence of aquatic macrophytes on Microcystis aeruginosa growth. Ecol Eng, 2012, 42: 130-133.

[6]

Chomel M, Fernandez C, Bousquet-Melou A, Gers C, Monnier Y, Santonja M, Gauquelin T, Gros R, Lecareux C, Baldy V. Secondary metabolites of Pinus halepensis alter decomposer organisms and litter decomposition during afforestation of abandoned agricultural zones. J Ecol, 2014, 102(2): 411-424.

[7]

Clemensen AK, Provenza FD, Lee ST, Gardner DR, Rottinghaus GE, Villalba JJ. Plant secondary metabolites in alfalfa, birdsfoot trefoil, reed canarygrass, and tall fescue unaffected by two different nitrogen sources. Crop Sci, 2017, 57(2): 964-970.

[8]

Covelo F, Gallardo A. Temporal variation in total leaf phenolics concentration of Quercus robur in forested and harvested stands in northwestern Spain. Can J Bot, 2001, 79(11): 1262-1269.

[9]

Duda SC, Mărghitaş LA, Dezmirean D, Duda M, Mărgăoan R, Bobiş O. Changes in major bioactive compounds with antioxidant activity of Agastache foeniculum, Lavandula angustifolia, Melissa officinalis and Nepeta cataria: Effect of harvest time and plant species. Ind Crops Prod, 2015, 77: 499-507.

[10]

Hagerman AE. Radial diffusion method for determining tannin in plant extracts. J Chem Ecol, 1987, 13(3): 437-449.

[11]

Hagerman AE (2011) The tannin handbook. https://www.users.muohio.edu/hagermae. Accessed 6 June 2019

[12]

Hattas D, Scogings PF, Julkunen-Tiitto R. Does the growth differentiation balance hypothesis explain allocation to secondary metabolites in Combretum apiculatum, an African savanna woody species?. J Chem Ecol, 2017, 43(2): 153-163.

[13]

Henneron L, Chauvat M, Archaux F, Akpa-Vinceslas M, Bureau F, Dumas Y, Mignot L, Ningre F, Perret S, Richter C. Plant interactions as biotic drivers of plasticity in leaf litter traits and decomposability of Quercus petraea. Ecol Monogr, 2017, 87(2): 321-340.

[14]

Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q Rev Biol, 1992, 67(3): 283-335.

[15]

Hernes PJ, Hedges JI. Determination of condensed tannin monomers in environmental samples by capillary gas chromatography of acid depolymerization extracts. Anal Chem, 2000, 72(20): 5115-5124.

[16]

Hernes PJ, Benner R, Cowie GL, Goni MA, Bergamaschi BA, Hedges JI. Tannin diagenesis in mangrove leaves from a tropical estuary: A novel molecular approach. Geochim Cosmochim Ac, 2001, 65(18): 3109-3122.

[17]

Institute of Soil Science, Chinese Academy of Sciences. Physico-chemical analysis of soils, 1978, Shanghai: Shanghai Science and Technology Press.

[18]

Izquierdo AM, Torres MPN, Jimenez GS, Sosa FC. Changes in biomass allocation and phenolic compounds accumulation due to the effect of light and nitrate supply in Cecropia peltata plants. Acta Physiol Plant, 2011, 33(6): 2135-2147.

[19]

Keinänen M, Julkunen-Tiitto R, Mutikainen P, Walls M, Ovaska J, Vapaavuori E. Trade-offs in phenolic metabolism of silver birch: effects of fertilization, defoliation, and genotype. Ecology, 1999, 80(6): 1970-1986.

[20]

Kim SM, Kang SW, Jeon JS, Jung YJ, Kim WR, Kim CY, Um BH. Determination of major phlorotannins in Eisenia bicyclis using hydrophilic interaction chromatography: seasonal variation and extraction characteristics. Food Chem, 2013, 138(4): 2399-2406.

[21]

Kleiner KW, Raffa KF, Dickson RE. Partitioning of 14C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia, 1999, 119(3): 408-418.

[22]

Koricheva J. Interpreting phenotypic variation in plant allelochemistry: problems with the use of contents. Oecologia, 1999, 119(4): 467-473.

[23]

Kosola KR, Parry D, Workmaster BAA. Responses of condensed tannins in poplar roots to fertilization and gypsy moth defoliation. Tree Physiol, 2006, 26(12): 1607-1611.

[24]

Kraus TEC, Dahlgren RA, Zasoski RJ. Tannins in nutrient dynamics of forest ecosystems: a review. Plant Soil, 2003, 256(1): 41-66.

[25]

Kraus TEC, Zasoski RJ, Dahlgren RA. Fertility and pH effects on polyphenol and condensed tannin concentrations in foliage and roots. Plant Soil, 2004, 262(1–2): 95-109.

[26]

Li CM, Wang Y, Yu WX. Dynamic changes of phenolic compound contents in leaf and bark of poplar during autumn temperature drop. J For Res, 2011, 22(3): 481-485.

[27]

Lim TY, Lim YY, Yule CM. Distribution and characterization of phenolic compounds in Macaranga pruinosa and associated soils in a tropical peat swamp forest. J Trop For Sci, 2017, 29(4): 509-518.

[28]

Lin YM, Liu JW, Xiang P, Lin P, Ye GF, Sternberg LdSL. Tannin dynamics of propagules and leaves of Kandelia candel and Bruguiera gymnorrhiza in the Jiulong River Estuary, Fujian, China. Biogeochemistry, 2006, 78(3): 343-359.

[29]

Makkar HPS, Dawra RK, Singh B. Protein precipitation assay for quantitation of tannins: determination of protein in tannin-protein complex. Anal Biochem, 1987, 166(2): 435-439.

[30]

Mannino AM Vaglica V Cammarata M Oddo E (2016) Effects of temperature on total phenolic compounds in Cystoseira amentacea (C. Agardh) Bory (Fucales, Phaeophyceae) from southern Mediterranean Sea Plant Biosyst 150 2 152 160

[31]

Mansfield JL, Curtis PS, Zak DR, Pregitzer KS. Genotypic variation for condensed tannin production in trembling aspen (Populs tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. Am J Bot, 1999, 86(8): 1154-1159.

[32]

Masbough A, Frankowski K, Hall KJ, Duff SJB. The effectiveness of constructed wetland for treatment of woodwaste leachate. Ecol Eng, 2005, 25(5): 552-566.

[33]

Massad TJ, Trumbore SE, Ganbat G, Reichelt M, Unsicker S, Boeckler A, Gleixner G, Gershenzon J, Ruehlow S. An optimal defense strategy for phenolic glycoside production in Populus trichocarpa-isotope labeling demonstrates secondary metabolite production in growing leaves. New Phytol, 2014, 203(2): 607-619.

[34]

Moore JA, Mika PG, Shaw TM. Root chemistry of mature Douglas-fir differs by habitat type in the interior northwestern United States. For Sci, 2000, 46(4): 531-536.

[35]

Naumann HD, Coope CE, Muir JP. Seasonality affects leaf nutrient and condensed tannin concentration in southern African savannah browse. Afr J Ecol, 2017, 55(2): 168-175.

[36]

Osborne NJT, McNeill DM. Characterisation of Leucaena condensed tannins by size and protein precipitation capacity. J Sci Food Agric, 2001, 81(11): 1113-1119.

[37]

Pacifico S, Galasso S, Piccolella S, Kretschmer N, Pan SP, Marciano S, Bauer R, Monaco P. Seasonal variation in phenolic composition and antioxidant and anti-inflammatory activities of Calamintha nepeta (L.) Savi. Food Res Int, 2015, 69: 121-132.

[38]

Penuelas J, Estiarte M. Can elevated CO2 affect secondary metabolism and ecosystem function?. Tree, 1998, 13: 20-24.

[39]

Pinyopusarerk K, Williams ER. Range-wide provenance variation in growth and morphological characteristics of Casuarina equisetifolia grown in Northern Australia. For Ecol Manag, 2000, 134(1–3): 219-232.

[40]

Randriamanana TR, Lavola A, Julkunen-Tiitto R. Interactive effects of supplemental UV-B radiation and temperature in European aspen seedlings: Implications for growth, leaf traits, phenolic defense and associated organisms. Plant Physiol Biochem, 2015, 93: 84-93.

[41]

Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K. Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth, and accumulation of phenolics?. Oecologia, 2002, 130(3): 380-390.

[42]

Scogings PF, Hjalten J, Skarpe C, Hattas D, Zobolo A, Dziba L, Rooke T. Nutrient and secondary metabolite concentrations in a savanna are independently affected by large herbivores and shoot growth rate. Plant Ecol, 2014, 215(1): 73-82.

[43]

Shan LP, Song CC, Zhang XH, Ren JS. Effects of long-term nitrogen and phosphorus addition on plant defense compounds in a freshwater wetland. Ecol Indic, 2018, 94(1): 1-6.

[44]

Sobuj N, Virjamo V, Zhang YD, Nybakken L, Julkunen-Tiitto R. Impacts of elevated temperature and CO2 concentration on growth and phenolics in the sexually dimorphic Populus tremula (L.). Environ Exp Bot, 2018, 146: 34-44.

[45]

Terrill T, Rowan A, Douglas G, Barry T. Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. J Sci Food Agric, 1992, 58(3): 321-329.

[46]

Top SM, Preston CM, Dukes JS, Tharayil N. Climate influences the content and chemical composition of foliar tannins in green and senesced tissues of Quercus rubra. Front Plant Sci, 2017, 8: 423.

[47]

Usami T, Lee J, Oikawa T. Interactive effects of increased temperature and CO2 on the growth of Quercus myrsinaefolia saplings. Plant Cell Environ, 2001, 24: 1007-1019.

[48]

Wam HK, Stolter C, Nybakken L. Compositional changes in foliage phenolics with plant age, a natural experiment in boreal forests. J Chem Ecol, 2017, 43(9): 920-928.

[49]

Wang WJ, Zu YG, Li XY. Seasonal change and organs difference of tannin content in Larix gmelinii. Chem Ind For Prod, 2007, 27(2): 81-84.

[50]

Wang WJ, Li WX, Xu HN, Zu YG, Wang Y. Characters of life cycle forms of Chelidonium majus populations indifferent habitats and their correlation to the contents of tannin, flavones and alkaloids in diffferent organs. Acta Ecol Sin, 2008, 28(11): 5228-5237.

[51]

Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Diaz S, Engelbrecht BMJ, Harms KE, Hubbell SP, Marks CO, Ruiz-Jaen MC, Salvador CM, Zanne AE. Functional traits and the growth-mortality trade-off in tropical trees. Ecology, 2010, 91(12): 3664-3674.

[52]

Wurzburger N, Hendrick RL. Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest. J Ecol, 2009, 97(3): 528-536.

[53]

Yang LG, Yin PP, Li K, Fan H, Xue Q, Li X, Sun LW, Liu YJ. Seasonal dynamics of constitutive levels of phenolic conponents lead to alterations of antioxidant capacities in Acer truncatum leaves. Arab J Chem, 2018, 11(1): 14-25.

[54]

Ye GF, Zhang SJ, Zhang LH, Lin YM, Wei SD, Liao MM, Lin GH. Age-related changes in nutrient resorption patterns and tannin concentration of Casuarina equisetifolia plantations. J Trop For Sci, 2012, 24(4): 546-556.

[55]

Zhang LH, Lin YM, Ye GF, Liu XW, Lin GH. Changes in the N and P concentrations, N: P ratios, and tannin content in Casuarina equisetifolia branchlets during development and senescence. J For Res, 2008, 13(5): 302-311.

[56]

Zhang LH, Ye GF, Lin YM, Zhou HC, Zeng Q. Seasonal changes in tannin and nitrogen contents of Casuarina equisetifolia branchlets. J Zhejiang Univ (Sc B), 2009, 10(2): 103-111.

[57]

Zhang LH, Shao HB, Ye GF, Lin YM. Effects of fertilization and drought stress on tannin biosynthesis of Casuarina equisetifolia seedlings branchlets. Acta Physiol Plant, 2012, 34(5): 1639-1649.

[58]

Zhang LH, Zhang SJ, Ye GF, Shao HB, Lin GH, Brestic M. Changes of tannin and nutrients during decomposition of branchlets of Casuarina equisetifolia plantation in subtropical coastal areas of China. Plant Soil Environ, 2013, 59(2): 74-79.

[59]

Zhou HC, Wei SD, Zeng Q, Zhang LH, Tam NF, Lin YM. Nutrient and caloric dynamics in Avicennia marina leaves at different developmental and decay stages in Zhangjiang River Estuary, China. Estuar Coast Shelf S, 2010, 87(1): 21-26.

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