Sains Malaysiana 48(3)(2019): 561–570

http://dx.doi.org/10.17576/jsm-2019-4803-08

The Effects of Plant Secondary Metabolites from Coniferous Needle Leaf Litter on the Leaf Litter Decomposition of Betula albo-sinensis Burk

(Kesan Metabolit Tumbuhan Sekunder daripada Sampah Daun bak Jarum Konifer pada Penguraian Sampah Dedaun Betula albo-sinensis Burk)

XIAOXI ZHANG^1,2, HUI LIU¹, WENXING ZHOU¹, JIAJIA LI¹, HANGYU LEI¹, YONGKANG JI¹, BOYA WANG³ & ZENGWEN LIU^3*

¹Shaanxi Engineering and Technological Research Center for Conservation and Utilization of Regional, Biological Resources, College of Life Sciences, Yan’an University, Yan’an, Shaanxi, 716000, China

²Institute of Soil and Water Conservation, Northwest A&F University, Yangling, Shaanxi, 712100, China

³College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi, 712100, China

Received: 28 July 2018/Accepted: 4 January 2019

ABSTRACT

In this study, leaf litters of Betula albo-sinensis and 5 coniferous species were used as samples. The B. albo-sinensis leaf litter was buried in soil and termly treated with the water extracts of five types of coniferous leaf litter for a 6-month simulation decomposition experiment. The dynamics of mass loss and nutrients (C, N, P, and K) content of leaf litter and the soil enzymatic activities were measured to investigate the effects of plant secondary metabolites (PSM) from coniferous leaf litters on the decomposition processes of B. albo-sinensis leaf litter. The results indicated that the extracts of Pinus tabuliformis, Platycladus orientalis, P. armandii and Larix principis-rupprechtii leaf litters significantly inhibited the whole decomposition process and overall nutrients release of B. albo-sinensis leaf litter, while the extracts of Picea asperata leaf litter exhibited no significant influence. The general suppression of PSM on the soil sucrase, carboxymethyl cellulase and β-glucosidase activities might be the main reason leading to the inhibitory effects of the extracts of P. tabuliformis, P. orientalis, P. armandii and L. principis-rupprechtii leaf litter. The species causing inhibitory effects, especially L. principis-rupprechtii, was not recommended to be planted mixed with B. albo-sinensis, or their planting density should be lower in the mixed forests.

Keywords: Leaf litter decomposition; nutrient release; secondary metabolites; soil enzymatic activities

ABSTRAK

Dalam kajian ini, sampah dedaun bagi Betula albo-sinensis dan lima spesies konifer telah digunakan sebagai sampel. Sampah dedaun B. albo-sinensis telah ditanam di dalam tanah dan dirawat dengan ekstrak air daripada lima jenis sampah dedaun konifer untuk uji kaji penguraian simulasi selama 6 bulan. Dinamik kehilangan jisim dan kandungan nutrien (C, N, P dan K) sampah dedaun dan aktiviti enzim tanah diukur untuk mengkaji kesan metabolit sekunder tumbuhan (PSM) daripada sampah dedaun konifer dalam proses penguraian sampah dedaun B. albo-sinensis. Hasilnya menunjukkan bahawa ekstrak sampah dedaun Pinus tabuliformis, Platycladus orientalis, P. armandii dan Larix principis-rupprechtii menghalang proses penguraian keseluruhan dan penyebaran nutrien keseluruhan B. albo-sinensis secara signifikan, manakala ekstrak sampah dedaun Picea asperata tidak menunjukkan kesan yang signifikan. Penekanan umum PSM ke atas aktiviti sukrase, karboksimetil selulase dan aktiviti β-glucosidase tanah mungkin menjadi sebab utama yang membawa kepada kesan perencatan ekstrak sampah dedaun P. tabuliformis, P. orientalis, P. armandii dan L. principis-rupprechtii. Spesies yang menyebabkan kesan perencatan, terutamanya L. principis-rupprechtii adalah tidak disarankan untuk ditanam bercampur dengan B. albo-sinensis atau ketumpatan penanamannya harus lebih rendah di dalam hutan bercampur.

Kata kunci: Aktiviti enzimatik tanah; metabolit sekunder; pelepasan nutrien; penguraian sampah dedaun

REFERENCES

Adamczyk, B., Karonen, M., Adamczyk, S., Engström, M.T., Laakso, T., Saranpää, P., Kitunen, V., Smolander, A. & Simon, J. 2017. Tannins can slow-down but also speed-up soil enzymatic activity in boreal forest. Soil Biology and Biochemistry 89: 60-67.

Adamczyk, S., Adamczyk, B., Kitunen, V. & Smolander, A. 2015. Monoterpenes and higher terpenes may inhibit enzyme activities in boreal forest soil. Soil Biology and Biochemistry 87: 59-66.

Adamczyk, S., Kiikkilä, O., Kitunen, V. & Smolander, A. 2013. Potential response of soil processes to diterpenes, triterpenes and tannins: Nitrification, growth of microorganisms and precipitation of proteins. Applied Soil Ecology 67: 47-52.

Aderiye, B.I., Ogundana, S.K., Adesanya, S.A. & Roberts, M.F. 1989. The effect of β-sitosterol on spore germination and germ-tube elongation of Aspergillus niger and Botryodiplodia theobromae. International Journal of Food Microbiology 8(1): 73-78.

Asensio, D., Yuste, J.C., Mattana, S., Ribas, À., Llusià, J. & Peñuelas, J. 2012. Leaf litter VOCs induce changes in soil microbial biomass C and N and largely increase soil CO2 efflux. Plant and Soil 360(1-2): 163-174.

Cañas, A.I., Alcalde, M., Plou, F., Martínez, M.J., Martínez, Á.T. & Camarero, S. 2007. Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environmental Science & Technology 41(8): 2964-2971.

Chapman, S.K., Newman, G.S., Hart, S.C., Schweitzer, J.A. & Koch, G.W. 2013. Leaf litter mixtures alter microbial community development: Mechanisms for non-additive effects in leaf litter decomposition. PloS ONE 8(4): e62671.

Chen, W., Vermaak, I. & Viljoen, A. 2013. Camphor-a fumigant during the black death and a coveted fragrant wood in ancient Egypt and Babylon-a review. Molecules (Basel, Switzerland) 18(5): 5434-5454.

Chomel, M., Guittonny-Larchevêque, M., Fernandez, C., Gallet, C., DesRochers, A., Paré, D., Jackson, B.G. & Baldy, V. 2016. Plant secondary metabolites: A key driver of litter decomposition and soil nutrient cycling. Journal of Ecology 104(6): 1527-1541.

Coq, S., Souquet, J.M., Meudec, E., Cheynier, V. & Hättenschwiler, S. 2010. Interspecific variation in litter tannins drives decomposition in a tropical rain forest of French Guiana. Ecology 91(7): 2080-2091.

Cox, S., Mann, C., Markham, J., Bell, H., Gustafson, J., Warmington, J. & Wyllie, S. 2000. The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). Journal of Applied Microbiology 88(1): 170-175.

De Marco, A., Meola, A., Maisto, G., Giordano, M. & De Santo, A.V. 2011. Non-additive effects of leaf litter mixtures on decomposition of leaf litters in a Mediterranean maquis. Plant and Soil 344(1-2): 305-317.

Duan, J., Wang, S., Zhang, Z., Xu, G., Luo, C., Chang, X., Zhu, X., Cui, S., Zhao, X. & Wang, W. 2013. Non-additive effect of species diversity and temperature sensitivity of mixed litter decomposition in the alpine meadow on Tibetan Plateau. Soil Biology and Biochemistry 57: 841-847.

Enguita, F.J. & Leitão, A.L. 2013. Hydroquinone: Environmental pollution, toxicity, and microbial answers. BioMed Research International 2013: e542168.

Gartner, T.B. & Cardon, Z.G. 2004. Decomposition dynamics in mixed-species leaf litter. Oikos 104(2): 230-246.

Ghasemi-Aghbash, F., Hosseini, V. & Poureza, M. 2015. Nutrient dynamics and early decomposition rates of Picea abies needles in combination with Fagus orientalis leaf litter in an exogenous ecosystem. Annals of Forest Research 59(1): 21-32.

Hättenschwiler, S. & Jørgensen, H.B. 2010. Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. Journal of Ecology 98(4): 754-763.

Hättenschwiler, S., Tiunov, A.V. & Scheu, S. 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 36: 191-218.

Iqbal, J., Siegrist, J.A., Nelson, J.A. & McCulley, R.L. 2012. Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biology and Biochemistry 44(1): 81-92.

Joanisse, G., Bradley, R., Preston, C. & Munson, A. 2007. Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: The case of Kalmia angustifolia. New Phytologist 175(3): 535-546.

Li, Q. & Liu, Z. 2013. Effects of decomposed leaf litter mixtures from Platycladus orientalis and broadleaf tree species on soil properties. Scandinavian Journal of Forest Research 28(7): 642-650.

Li, Q., Liu, P., Tang, Z., Zhao, H., Wang, J., Song, X., Yang, L. & Wan, S. 2016a. Effects of two phenolic acids on root zone soil nutrients, soil enzyme activities and pod yield of peanut. Chinese Journal of Applied Ecology 27(4): 1189-1195.

Li, Q., Zhao, G., Cao, G. & Liu, Z. 2016b. Soil effects of six different two-species litter mixtures that include Ulmus pumila. Chemistry and Ecology 32(8): 707-721.

Li, Y., Ying, Y.X., Zhao, D.Y. & Ding, W.L. 2014. Influence of allelochemicals on microbial community in ginseng cultivating soil. Chinese Herbal Medicines 6(4): 313-318.

Liu, P., Huang, J., Sun, O.J. & Han, X. 2010. Litter decomposition and nutrient release as affected by soil nitrogen availability and litter quality in a semiarid grassland ecosystem. Oecologia 162(3): 771-780.

Liu, P., Liu, Z., Wang, C., Guo, F., Wang, M., Zhang, Y., Dong, L. & Wan, S. 2012. Effects of three long-chain fatty acids present in peanut (Arachis hypogaea L.) root exudates on its own growth and the soil enzymes activities. Allelopathy Journal 29(1): 13-24.

Madritch, M., Donaldson, J.R. & Lindroth, R.L. 2006. Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9(4): 528-537.

Mao, B., Yu, Z.Y. & Zeng, D.H. 2015. Non-additive effects of species mixing on litter mass loss and chemical properties in a Mongolian pine plantation of Northeast China. Plant and Soil 396(1-2): 339-351.

Mierziak, J., Kostyn, K. & Kulma, A. 2014. Flavonoids as important molecules of plant interactions with the environment. Molecules (Basel, Switzerland) 19(10): 16240- 16265.

Naseby, D., Pascual, J. & Lynch, J. 2000. Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. Journal of Applied Microbiology 88(1): 161-169.

Ormeno, E., Baldy, V., Ballini, C., Larchevêque, M., Périssol, C. & Fernandez, C. 2006. Effects of environmental factors and leaf chemistry on leaf litter colonization by fungi in a Mediterranean shrubland. Pedobiologia 50(1): 1-10.

Osono, T. 2007. Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecological Research 22(6): 955-974.

Purahong, W., Kapturska, D., Pecyna, M.J., Schulz, E., Schloter, M., Buscot, F., Hofrichter, M. & Krüger, D. 2014. Influence of different forest system management practices on leaf litter decomposition rates, nutrient dynamics and the activity of ligninolytic enzymes: A case study from Central European forests. PloS ONE 9(4): e93700.

Roy, R., Laskar, S. & Sen, S. 2006. Dibutyl phthalate, the bioactive compound produced by Streptomyces albidoflavus 321.2. Microbiological Research 161(2): 121-126.

Schimel, J.P. & Hättenschwiler, S. 2007. Nitrogen transfer between decomposing leaves of different N status. Soil Biology and Biochemistry 39(7): 1428-1436.

Schweitzer, J.A., Bailey, J.K., Rehill, B.J., Martinsen, G.D., Hart, S.C., Lindroth, R.L., Keim, P. & Whitham, T.G. 2004. Genetically based trait in a dominant tree affects ecosystem processes. Ecology Letters 7(2): 127-134.

Shi, B., Luan, D., Wang, S., Zhao, L., Tao, L., Yuan, Q. & Wang, X. 2015. Borneol-grafted cellulose for antifungal adhesion and fungal growth inhibition. RSC Advances 5: 51947-51952.

Triebwasser, D.J., Tharayil, N., Preston, C.M. & Gerard, P.D. 2012. The susceptibility of soil enzymes to inhibition by leaf litter tannins is dependent on the tannin chemistry, enzyme class and vegetation history. New Phytologist 196(4): 1122- 1132.

Ushio, M., Balser, T.C. & Kitayama, K. 2013. Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest. Plant and Soil 365(1-2): 157-170.

Uusitalo, M., Kitunen, V. & Smolander, A. 2008. Response of C and N transformations in birch soil to coniferous resin volatiles. Soil Biology and Biochemistry 40(10): 2643-2649.

Wang, J., Wang, D., Yu, F., Shen, W., Zou, C., Zhang, R. & Hou, P. 2014. Enzyme activity in rhizosphere soil of Cryptomeria fortunei seedlings with simulated acid rain and litter. Journal of Zhejiang Forestry College 31(3): 373-379.

Wang, Z., Zhao, X., Xu, W., Su, Y., You, Y., Liu, S., Hu, Y., Yang, Y. & Zhang, Y. 2015. Response of microbial biomass and enzyme activities in black soil to din-butyl phthalate contamination. Asian Journal of Ecotoxicology 10(6): 199- 205.

Zhang, F., Guo, A., Li, Q., Li, H., Hu, M. & Wang, F. 2013. The allelopathic effects of five volatiles released from Eupatorium adenophora on Trichoderma harzianum and Botrytis cinerea. Acta Phytophylacica Sinica 40(2): 191-192.

Zhang, X., Liu, Z., Tian, N., Luc, N.T., Zhu, B. & Bing, Y. 2015. Allelopathic effects of decomposed leaf litter from intercropped trees on rape. Turkish Journal of Agriculture and Forestry 39(6): 898-908.

Zhang, X., Liu, Z. & Hu, W. 2016. Response of nutrient release of Periploca sepium litter to soil petroleum contamination. CLEAN-Soil, Air, Water 44(12): 1709-1716.

Zheng, Y. 2008. Antibitic functions and volatile organic compounds from Pinus tabulaeformis Var. Mukdensis Uyeki and Betula Platyphlla Suk. Northeast Forestry University.

Zhou, B., Han, L., Yin, Y., Wu, J., Sun, C., Ye, X. & Bai, L. 2010. Effects of allelochemicals hexadecanoic acid on soil microbial composition and biomass in rhizosphere of eggplant. Journal of Shenyang Agricultural University 41(3): 275-278.

Zhou, B., Kong, C.H., Li, Y.H., Wang, P. & Xu, X.H. 2013. Crabgrass (Digitaria sanguinalis) allelochemicals that interfere with crop growth and the soil microbial community. Journal of Agricultural and Food Chemistry 61(22): 5310- 5317.

*Corresponding author; email: zengwenliu2003@aliyun.com