e-ISSN 2231-8542
ISSN 1511-3701
Zar Ni Zaw, Piyanut Musigapong, Rawee Chiarawipa, Surachart Pechkeo and Amonrat Chantanaorrapint
Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 1, February 2023
DOI: https://doi.org/10.47836/pjtas.46.1.07
Keywords: Agroforestry, Arecaceae, ecophysiological adaptation, Hevea brasiliensis, tropical palm species
Published on: 22 Febuary 2023
Hevea rubber farm is viable for agroforestry systems since its canopy lessens extreme weather conditions and contributes to the adaptation of shade-tolerant plants. However, some limitations in the availability of soil water and shades vary with the age of rubber trees and affect the understorey plants’ acclimatization. Tropical palms are potentially associated plants for the rubber-based agroforestry systems because they are rainforest species adaptable to understorey environments. Two rubber farms, ages 12 and 25 years, intercropped with tropical palms were selected to investigate the acclimatization of the palms to the seasonal abiotic variations in the mature rubber farms. The studied palm species were Chrysalidocarpus lutescens and Rhapis excelsa in the 12-year-old rubber farm and Livistona speciosa and Licuala spinosa in the 25-year-old rubber farm, respectively. Leaf area, stomatal conductance, photosynthesis pigments, and leaf nitrogen content were identified as the palms’ morpho-physiological traits. The 12-year-old rubber farm had a marked soil water deficit in all soil depths at the beginning of the rainy season, reaching around 200 kPa at the 80 cm soil depth, while the 25-year-old rubber farm received greater light transmissions, ranging between 37 and 46% in the late dry season. All palms adjusted leaf area to balance the photosynthetic capacity. The Rhapis palm had greater acclimatization with significant responses of stomatal conductance. Other than the Licuala palm, all palms exhibited the allocation of chlorophyll pigments and nitrogen content significantly in their leaves in response to the different intensities of abiotic stresses in the understorey of the rubber farms.
Aasamaa, K., Sober, A., & Rahi, M. (2001). Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal of Plant Physiology, 28(8), 765-774. https://doi.org/10.1071/PP00157
Ahrends, A., Hollingsworth, P. M., Ziegler, A. D., Fox, J. M., Chen, H., Su, Y., & Xu, J. (2015). Current trends of rubber plantation expansion may threaten biodiversity and livelihoods. Global Environmental Change, 34, 48-58. https://doi.org/10.1016/j.gloenvcha.2015.06.002
Association of Natural Rubber Producing Countries. (2021). Natural rubber statistics March 2021. ANRPC. http://www.anrpc.org/html/nrts.aspx?ID1=57&ID=58&PID=59
Awal, M. A., Wan Ishak, Endan, J., & Haniff, M. (2004). Determination of specific leaf area and leaf area-leaf mass relationship in oil palm plantation. Asian Journal of Plant Sciences, 3(3), 264-268. https://doi.org/10.3923/AJPS.2004.264.268
Bertolino, L. T., Caine, R. S., & Gray, J. E. (2019). Impact of stomatal density and morphology on water-use efficiency in a changing world. Frontiers in Plant Science, 10, 225.
Bojović, B., & Marković, A. (2009). Correlation between nitrogen and chlorophyll content in wheat (Triticum aestivum L.). Kragujevac Journal of Sciences, 31, 69-74.
Casson S. A., & Hetherington, A. M. (2010). Environmental regulation of stomatal development. Current Opinion Plant Biology, 13(1), 90-95. https://doi.org/10.1016/j.pbi.2009.08.005
Chaves, M. M., Morocco, J. P., & Pereira, J. S. (2003). Understanding plant responses to drought – From genes to the whole plant. Functional Plant Biology, 30(3), 239-264. https://doi.org/10.1071/fp02076
Chen, J. M., Rich, P. M., Gower, S.T., Norman, J. M., & Plummer, S. (1997). Leaf area index of boreal forests: Theory, techniques, and measurements. Journal of Geophysical Research: Atmospheres, 102(D24), 29429-29443. https://doi.org/10.1029/97JD01107
Cornelissen, J. H. C., Werger, M. J. A., Castro-Diez, P., van Rheenen, J. W. A., & Rowland, A. P. (1997). Foliar nutrients in relation to growth, allocation and leaf traits in seedlings of a wide range of woody plant species and types. Oecologia, 111, 460-469. https://doi.org/10.1007/s004420050259
d’Auzac, J., Jacob, J. L., Prevot, J. C., Clement, A., Gallois, R., Cretin, H., Lecote, R., Pujade-Renaud, V., & Gohet, E. (1997). The regulation of cis-polyisoprene production (natural rubber) from Hevea brasiliensis. ResearchGate. https://www.researchgate.net/publication/235908218_The_regulation_of_cis-polyisoprene_production_natural_rubber_from_Hevea_brasiliensis
Dijkstra, P. (1990). Causes and effect of differences in specific leaf area. In H. Lambers, M. L. Cambridge, H. Konings, & T. L. Pons (Eds.), Causes and consequences of variation in growth rate and productivity of higher plants (pp. 125-140). SPB Academic Publishing.
Dransfield, J., Barfod, A. S., & Pongsattayapipat, R. (2004). A preliminary checklist to Thai palms. Thai Forest Bulletin, 32, 32-72.
Evans, J. R., (1989). Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 78, 9-19. https://doi.org/10.1007/bf00377192
Fan, Y., Chen, J., Cheng, Y., Raza, M. A., Mu, X., Wang, Z., Liu, Q., Wang, R., Wang, X., Yong, T., Liu, W., Liu, J., Du, J., Shu, K., Yang, W., & Feng, Y. (2018). Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize-soybean relay-strip intercropping system. PLOS One, 13(5), e0198159. https://doi.org/10.1371/journal.pone.0198159
Farquhar, G. D., & Sharkey, T. D. (1982). Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33, 317-345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Feng, L., Raza, M. A., Li, Z., Chen, Y., Khalid, M. H. B., Du, J., Liu, W., Wu, X., Song, C., Yu, L., Zhang, Z., Yuan, S., Yang, W., & Yang, F. (2019). The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean. Frontiers in Plant Science, 9, 1952. https://doi.org/10.3389/fpls.2018.01952
Field, C., & Mooney, H. A. (1986). The photosynthesis-nitrogen relationship in wild plants. In T. Givnish (Ed.), On the economy of plant form and function (pp. 25-55). Cambridge University Press.
Fox, J., & Castella, J. C. (2013). Expansion of rubber (Hevea brasiliensis) in mainland Southeast Asia: What are the prospects for smallholders?. Journal of Peasant Studies, 40(1), 155-170. https://doi.org/10.1080/03066150.2012.750605
Franks, P. J., & Beerling, D. J. (2009). Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of National Academy of Sciences of the United States of America, 106(25), 10343-10347. https://doi.org/10.1073/pnas.0904209106
Galhidy, L., Mihok, B., Hagyo, A., Rajkai, K., & Standovar, T. (2005). Effects of gap size and associated changes in light and soil moisture on the understorey vegetation of a Hungarian beech forest. Plant Ecology, 183, 133-145. https://doi.org/10.1007/s11258-005-9012-4
Givnish, T. J. (1988). Adaptation to sun and shade: A whole-plant perspective. Australian Journal of Plant Physiology, 15(2), 63-92. https://doi.org/10.1071/PP9880063
Hamanishi, E. T., Thomas, B. R., & Campbell, M. M. (2012). Drought induces alterations in the stomatal development program in Populus. Journal of Experimental Botany, 63(13), 4959-4971. http://doi.org/10.1093/jxb/ers177
Hartmut, K. L., Alexander, Ac., Michal, V. M., Jiri, K., & Urban, O. (2007). Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiology and Biochemistry, 45(8), 577-588. https://doi.org/10.1016/j.plaphy.2007.04.006
Hendry, G. A. F., & Price, A. H. (1993). Stress indicators: Chlorophylls and carotenoids. In G. A. F. Hendry & J. P. Grime (Eds.), Methods in comparative plant ecology (pp. 148-152). Springer. https://doi.org/10.1007/978-94-011-1494-3
Hollinger, D. Y. (1989). Canopy organization and foliage photosynthetic capacity in a broad-leaved evergreen montane forest. Functional Ecology, 3(1), 53-62. https://doi.org/10.2307/2389675
Houborg, R., McCabe, M., Cescatti, A., Gao, F., Schull, M., & Gitelson, A. (2015). Joint leaf chlorophyll content and leaf area index retrieval from Landsat data using a regularized model inversion system (REGFLEC). Remote Sensing of Environment, 159, 203-221. https://doi.org/10.1016/j.rse.2014.12.008
Inskeep, W. P., & Bloom, P. R. (1985). Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiology, 77(2), 483-485. https://doi.org/10.1104/pp.77.2.483
Jacob, J. L., Prévôt, J. C., Roussel, D., Lacote, R., Serres, E., d’Auzac, J., Eschback, J.-M., & Omont, H. (2018). Yield limiting factors, latex physiological parameters, latex diagnosis and clonal typology. In J. d’Auzac, J. L. Jacob, & H. Chrestin (Eds.), Physiology of rubber tree latex: The laticiferous cell and latex – A model of cytoplasm (pp. 345-382). CRC Press. https://doi.org/10.1201/9781351075695-16
Johnson, D. V. (2011). Tropical palms: 2010 revision. Food and Agriculture Organization of the Unite Nations. https://www.fao.org/3/i1590e/i1590e00.htm
Jongrungrot, V., Thungwa, S., & Snoeck, D. (2014). Diversification des cultures pérennes dans les plantations d’hévéa pour augmenter les revenus des petits producteurs de caoutchouc du sud de la Thaïlande [Tree-crop diversification in rubber plantations to diversify sources of income for small-scale rubber farmers in Southern Thailand]. Bios et Forets des Tropiques, 321, 21-32. http://doi.org/10.19182/bft2014.321.a31214
Kitajima, K., & Hogan, K. P. (2003). Increase of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant, Cell and Environment, 26(6), 857-865. https://doi.org/10.1046/j.1365-3040.2003.01017.x
Langenberger, G., Cadisch, G., Martin, K., Min, S., & Waibel, H. (2017). Rubber intercropping: A viable concept for the 21st century?. Agroforestry System, 91, 577-596. https://doi.org/10.1007/s10457-016-9961-8
Leakey, R. R. B. (2017). Definition of agroforestry revisited. In Multifunctional agriculture – Achieving sustainable development in Africa (pp. 5-6). Academic Press. https://doi.org/10.1016/B978-0-12-805356-0.00001-5
Lei, T. T., & Lechowicz, M. J. (1997). The photosynthetic response of eight species of Acer to simulated light regimes from the centre and edges of gaps. Functional Ecology, 11(1), 16-23.
Li, T., Liu, L., Jiang, C. D., Liu, Y. J., & Shi, L. (2014). Effects of mutual shading on the regulation of photosynthesis in field-grown sorghum. Journal of Photochemistry and Photobiology B: Biology, 137, 31-38. https://doi.org/10.1016/j.jphotobiol.2014.04.022
Li, Y., Lan, G., & Xia, Y. (2016). Rubber trees demonstrate a clear retranslocation under seasonal drought and cold stresses. Frontiers in Plant Science, 7, 1907. https://doi.org/10.3389/fpls.2016.01907
Lichtenthaler, H. K., Buschmann, C., Döll, M., Fietz, H. J., Bach, T., Koizel, U., Meir, D., & Rahmsdorf, U. (1981). Photosynthetic activity chloroplasts ultrastructure and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynthesis Research, 2, 115-141. https://doi.org/10.1007/BF00028752
Lin, X. H., Chen, Q. B., Hua, Y. G., Yang, L. F., & Wang, Z. H. (2011). Soil moisture content and fine root biomass of rubber tree (Hevea brasiliensis) plantations at different ages. Journal of Applied Ecology, 22(2), 331-336.
Liu, S., Liu, J., & Cao, J. (2006). Stomatal distribution and character analysis of leaf epidermis of jujube under drought stress. Journal of Anhui Agricultural Science, 34, 1315-1318.
Loomis, R. S. (1997). On the utility of nitrogen in leaves. Proceedings of National Academy Sciences of the United States of America, 94(25), 13378-13379. https://doi.org/10.1073/pnas.94.25.13378
Mathur, S., Jain, L., & Jajoo, A. (2018). Photosynthetic efficiency in sun and shade plants. Photosynthetica, 56(1), 354-365. https://doi.org/10.1007/s11099-018-0767-y
Meng, L., Li, L., Chen, W., Xu, Z., & Liu, L. (1999). Effect of water stress on stomatal density, length, width and net photosynthetic rate I rice leaves. Journal of Shenyang Agricultural University, 30(5), 477-480.
Meziane, D., & Shipley, B. (2001). Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply. Annals of Botany, 88(5), 915-927. https://doi.org/10.1006/anbo.2001.1536
Moran, R., & Porath, D. (1980). Chlorophyll determination in intact tissues using N, N-dimethylformamide. Plant Physiology, 65(3), 478-479. https://doi.org/10.1104/pp.65.3.478
Munasinghe, E. S., & Rodrigo, V. H. L. (2017). Lifespan of rubber cultivation can be shortened for high returns: A financial assessment of stimulated conditions in Sri Lanka. Experimental Agriculture, 54(3), 323-335. https://doi.org/10.1017/S0014479717000011
Niinemets, Ü., & Tenhunen, J. D. (1997). A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell and Environment, 20(7), 845-866. https://doi.org/10.1046/j.1365-3040.1997.d01-133.x
Pathiratna, L. S. S. (2006). Management of intercrops under rubber: Implications of competition and possibilities for improvement. Bulletin of Rubber Research Institution of Sri Lanka, 47, 8-16.
Poorter, H. (1999). Growth responses of 15 rain-forest tree species to a light gradient: The relative importance of morphological and physiological traits. Functional Ecology, 13(3), 396-410. https://doi.org/10.1046/j.1365-2435.1999.00332.x
Powles, S. B. (1984). Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology, 35, 15-44. https://doi.org/10.1146/annurev.pp.35.060184.000311
Premakumari, D., & Saraswathyamma, C. K. (2000). The para rubber tree. In P. J. George & C. J. Kuruvilla (Eds.), Natura rubber: Agromanagement and crop processing (pp. 29-35). Rubber Research Institute of India.
Rappaport, D., & Montagnini, F. (2014). Tree species growth under a rubber (Hevea brasiliensis) plantation: Native restoration via enrichment planting in southern Bahia, Brazil. New Forests, 45, 715-732. https://doi.org/10.1007/s11056-014-9433-9
Sáez-Plaza, P., Navas, M. J., Wybraniec, S., Michalowski, T., & Asuero, A. G. (2013). An overview of the Kjeldahl method of nitrogen determination. Part II. Sample preparation, working scale, instrumental finish and quality control. Critical Reviews in Analytical Chemistry, 43(4), 224-272. https://doi.org/10.1080/10408347.2012.751787
Saraswathyamma, C. K., Licy, J., & Marattukalam, J. G. (2000). Planting materials. In P. J. Geroge & C. J. Kuruvilla (Eds.), Natural rubber: Agromanagement and crop processing (pp. 59-74). Rubber Research Institute of India.
Sarijeva, G., Knapp, M., & Lichtenthaler, H. K. (2007). Differences in photosynthetic activity, chlorophyll and carotenoid levels, and in chlorophyll fluorescence parameters in green sun and shade leaves of Ginkgo and Fagus. Journal of Plant Physiology, 164(7), 950-955. https://doi.org/10.1016/j.jplph.2006.09.002
Saw, L. G., Dransfield, J., & Keith-Lucas, D. M. (2003). Morphological diversity of the genus Licuala (Palmae). Telopea, 10(1), 187-206. https://doi.org/10.7751/telopea20035615
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675. https://doi.org/10.1038/nmeth.2089
Schroeder, J. I., Allen, G. J., Hugouvierx, V., Kwak, J. M., & Waner, D. (2001). Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 627-658. https://doi.org/10.1146/annurev.arplant.52.1.627
Somboonsuke, B., Wetayaprasit, P., Chernchom, P., & Pacheerat, K. (2011). Diversification of smallholding rubber agroforestry system (SRAS) Thailand. Kasetsart Journal of Social Sciences, 32, 327-339.
Sun, Y., Ma, Y., Cao, K., Li, H., Shen, J., Liu, W., Di, L., & Mei, C. (2017). Temporal changes of ecosystem carbon stocks in rubber plantations in Xishuangbanna, Southwest China. Pedosphere, 27(4), 737-746. https://doi.org/10.1016/S1002-0160(17)60327-8
Supapvanich, S., Megia, R., & Ding, P. (2014). Salak (Salacca zalacca (Gaertner) Voss). In E. M. Yahia (Ed.), Postharvest biology and technology of tropical and subtropical fruits (pp. 334-352). Woodhead Publishing. https://doi.org/10.1533/9780857092618.334
Tan, Z. H., Zhang, Y. P., Song, Q. H., Liu, W. J., Deng, X. B., Tang, J. W., Zhou, W. J., Yang, L. Y., Yu, G. R., Sun, M. X., & Liang, N. S. (2011). Rubber plantations act as water pumps in tropical China. Geophysical Research Letters, 38(24), L24406. https://doi.org/10.1029/2011GL050006
Terashima, I., & Hikosaka, K. (1995). Comparative ecophysiology of leaf and canopy photosynthesis. Plant, Cell and Environment, 18(10), 1111-1128. https://doi.org/10.1111/j.1365-3040.1995.tb00623.x
Thai Meteorological Department. (2019). The climate of Thailand. https://www4.tmd.go.th/en/archive/thailand_climate.pdf
Valladares, F., Laanisto, L., Niinemets, Ü., & Zavala, M. A. (2016). Shedding light on shade: Ecological perspectives of understory plant life. Plant Ecology and Diversity, 9(3), 237-251. https://doi.org/10.1080/17550874.2016.1210262
Vaten, A., & Bergmann, D. C. (2012). Mechanisms of stomatal development: An evolutionary view. EvoDevo, 3, 11. https://doi.org/10.1186/2041-9139-3-11
Vincent, G. (2001). Leaf photosynthetic capacity and nitrogen content adjustment to canopy openness in tropical forest tree seedlings. Journal of Tropical Ecology, 17(4), 495-509. http://doi.org/10.1017/S0266467401001377
Wang, M., Shi, S., Lin, F., Hao, Z., Jiang, P., & Dai, G. (2012). Effects of soil water and nitrogen on growth and photosynthetic response of Manchurian ash (Fraxinus mandshurica) seedlings in Northeastern China. PLOS One, 7, e30754. https://doi.org/10.1371/journal.pone.0030754
Wellburn, A. R. (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 144(3), 307-313. https://doi.org/10.1016/S0176-1617(11)81192-2
Weyers, J. D. B., & Meidner, H. (1990). Methods in stomatal research. Longman.
Windsor-Collins, A., Cutler, D., & Atherton, M. (2006). The palm – A model for success?. WIT Transactions on State-of-the-art in Science and Engineering, 27, 303-326. https://doi.org/10.2495/978-1-85312-853-0/10
Wu, J., Liu, W., & Chem, C. (2016). Can intercropping with the world’s tree major beverage plants help improve the water use of rubber trees?. Journal of Applied Ecology, 53(6), 1787-1799. https://doi.org/10.1111/1365-2664.12730
Xu, Z. Z., & Zhou, G. S. (2005). Effects of water stress and nocturnal temperature on carbon allocation in the perennial grass, Leymus chinensis. Physiologia Plantarum, 123(3), 272-280. https://doi.org/10.1111/j.1399-3054.2005.00455.x
Zaw, Z. N., Sdoodee, S., & Lacote, R. (2017). Performances of low frequency tapping system with rainguard in high rainfall area in Myanmar. Australian Journal of Crop Science, 11(11), 1451-1456. https://doi.org/10.21475/ajcs.17.11.11.pne593
ISSN 1511-3701
e-ISSN 2231-8542