Variation of Phenology of Flacourtia rukam in Two Different Habitats and Their Relation to Rainfall, Dry Days, and the Plant Water Status
Article Sidebar
Issue
Vol. 30 No. 1 (2024)
Accepted
7 February 2024
Published
1 April 2024
Keywords:
-
phenologycal shift, rukam, RWC, climate
Abstract
Phenological shifts in the emergence of vegetative and generative parts, occur due to the response of plants to water received due to climate change. The rukam tree (Flacourtia rukam (Zoll & Moritzi)) is a local Indonesian plant with potential as an edible fruit and antioxidant agent, but its existence is increasingly rare. F. rukam can be found in Pasuruan, East Java, including Purwodadi Botanical Garden (PBG) as collected plants and Sekarmojo Village as cultivated plants. These populations show a shift in phenology, but this has never been studied. This study aimed to analyze the spatial variation of the phenology of two rukam populations and its relation to plant water status, rainfall quantity (RQ), and drought days (DD). This research was conducted on two individual trees at each location, was conducted from August 2020 to October 2022 using secondary data from BMKG, such as daily rainfall and the number of days without rain. Phenology was directly observed every week with an estimated abundance of numbers 1-4; plant water status was observed by calculating relative water content (RWC); soil physical analysis was carried out in mid-season. Data were analyzed by Mann-Whitney test and SEM WarpPLS. The results showed differences in phenology in the phases of leaf fall, flower buds, young fruit, and ripe fruit on the trees in the different locations. The decreased RQ in the past month significantly reduced the RWC value of F. rukam in both places, while the number of DD contributed to a decrease in the RWC value in PBG only, not in Sekarmojo. In both sites, decreasing the RWC of the rukam increased the abundance of fallen leaves and the chances of flowering. Rainfall and drought days affected plant phenology directly or indirectly through RWC mediation. In both places, RQ had a direct positive and significant effect on blooming flowers and new leaves but had negative effect on fallen leaves. While DD had a positive effect on leaf fall, flower formation, and fruit ripening, but had a negative effect on the appearance of young fruit (in PBG). Indirectly, RQ mainly affected several phenological parameters, while DD did not affect all phenological parameters.
References
Almeida, A. A. F. D., & Valle, R. R. (2007). Ecophysiology of the cacao tree. Brazilian Journal of Plant Physiology, 19, 425–448. https://doi.org/10.1590/S1677-04202007000400011
Andriani, C. (2020). Aktivitas antibakteri ekstrak etanol akar dan daun rukam (Flacourtia rukam Zoll. & Mor) terhadap bakteri mulut (Streptococcus mutans) penyebab karies pada gigi [dissertation]. Bangka: Universitas Bangka Belitung.
Arisoesilaningsih, E., Soejono, A. Widyati, I. Palupi, & Kiswojo. (2001). Aktivitas reproduktif tiga spesies pohon langka tahan kering di Kebun Raya Purwodadi. In E. Arisoesilaningsih, B. Yanuwiadi, S. Indriyani, T. Yulistyarini, E. E. Ariyanti, N. D. Yulia, & Soejono (Eds.), Prosiding seminar nasional konservasi dan pendayagunaan kenekaragaman tumbuhan lahan kering. LIPI-KRP dan MIPA Universitas Brawijaya, Purwodadi, East Java.
Bandurska, H. (2022). Drought stress responses: Coping strategy and resistance. Plants, 11(7), 922–938. https://doi.org/10.3390/plants11070922
Barrs, H. D. & Weatherley, P. E. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australia Journal Biological Science. 15, 413–428. https://doi.org/10.1071/BI9620413
Bijalwan, P. Sharma, M. Kaushik, P. (2022). Review of the effects of drought stress on plants: A systematic approach. Preprints, 2022, 2022020014. https://doi.org/10.20944/preprints202202.0014.v1
[BMKG] Badan Meteorologi, Klimatologi, dan Geofisika (2023). Data harian Jawa Timur. Retrieved from https://dataonline.bmkg.go.id/data_iklim
Borchert, R., Rivera, G., & Haugner, W. (2002). Modification of vegetative phenology in a tropical semi-deciduous forest by abnormal drought and rain. Biotropica, 34(1), 27–39. https://doi.org/10.1111/j.1744-7429.2002.tb00239.x
Buckley, T. N. (2019). How do stomata respond to water status? New Phytologist, 224(1), 21–36. https://doi.org/10.1111/nph.15899
Budiharta, S., & Solikin. (2010). Potensi and konservasi buah-buahan lokal Jawa Timur. Jakarta: LIPI Press.
Calle, Z., Schlumpberger, B. O., Piedrahita, L., Leftin, A., Hammer, S. A., Tye, A., & Borchert, R. (2010). Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics. Trees, 24, 865–877. https://doi.org/10.1007/s00468-010-0456-3
Chapman, C. A., Chapman, L. J., Struhsaker, T. T., Zanne, A. E., Clark, C. J., & Poulsen, J. R. (2005). A long-term evaluation of fruiting phenology: Importance of climate change. Journal of Tropical Ecology, 21(1), 31–45. https://doi.org/10.1017/S0266467404001993
Comita, L. S., & Engelbrecht, B. M. (2009). Seasonal and spatial variation in water availability drives habitat associations in a tropical forest. Ecology, 90(10), 2755–2765. https://doi.org/10.1890/08-1482.1
Darmayanti, A. S., Ariffin, Waluyo, B., & Arisoesilaningsih, E. (2023). Study on the phenology of three fruit trees species in Purwodadi Botanical Gardens, East Java, and its relationship with mesoclimates. Jurnal Manajemen Hutan Tropika, 29(1), 88–98. https://doi.org/10.7226/jtfm.29.1.88
Dobra, J., Motyka, V., Dobrev, P., Malbeck, J., Prasil, I.T., Haisel, D., Gaudinova, A., Havlova, M., Gubis, J. & Vankova, R. (2010). Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology, 167(16), 1360–1370. https://doi.org/10.1016/j.jplph.2010.05.013
Dunham, A. E., Razafindratsima, O. H., Rakotonirina, P., & Wright, P. C. (2018). Fruiting phenology is linked to rainfall variability in a tropical rain forest. Biotropica, 50(3), 396–404. https://doi.org/10.1111/btp.12564
Ewusie, J. Y. (1986). Elements of tropical ecology. ELBS/Heinemann Educational Books.
Fadiyah, I., Lestari, I., Victory, S., & Mahardika, R. G. (2019). Uji aktivitas antioksidan ekstrak buah rukam (Flacourtia rukam) menggunakan metode maserasi. Proceedings of National Colloquium Research and Community Service, 3, 64–68. https://doi.org/10.33019/snppm.v3i0.1316
Flaigt, W., Beutelspacher, H., & Rietz, E. (1975). Chemical composition and physical properties of humic substances. In J. E. Gieseking (Ed.), Soil components: Organic components (pp 1–211). New York: Springer-Verlag
Gene Albrigo, L., & Galán Saúco, V. (2002). Flower bud induction, flowering, and fruit set of some tropical and subtropical fruit tree crops with special reference to citrus. Acta Hortic, 632, 81–90. https://doi.org/10.17660/ActaHortic.2004.632.10
Gordo, O., & Sanz, J. J. (2010). Impact of climate change on plant phenology in Mediterranean ecosystems. Global Change Biology, 16(3), 1082–1106. https://doi.org/10.1111/j.1365-2486.2009.02084.x
Griffiths, C. A., Gaff, D. F., & Neale, A. D. (2014). Drying without senescence in resurrection plants. Frontiers in Plant Science, 5, 36. https://doi.org/10.3389/fpls.2014.00036
Gu, L., Pallardy, S.G., Hosman, K.P., Sun Y. (2016). Impacts of precipitation variability on plant species and community water stress in a temperate deciduous forest in the central U.S. Agricultural and Forest Meteorology, 217, 120–136. https://doi.org/10.1016/j.agrformet.2015.11.014
Haberman, A., Bakhshian, O., Cerezo‐Medina, S., Paltiel, J., Adler, C., Ben‐Ari, G., Mercado, J. A, Pliego‐Alfaro, F., Lavee, S., & Samach, A. (2017). A possible role for flowering locus T‐encoding genes in interpreting environmental and internal cues affecting olive (Olea europaea L) flower induction. Plant, Cell & Environment, 40(8), 1263–1280. https://doi.org/10.1111/pce.12922
Hair, J. F., Ringle, C. M., & Sarstedt, M. (2013). Partial least squares structural equation modeling: Rigorous applications, better results and higher acceptance. Long Range Planning, 46(1–2), 1–12. https://doi.org/10.1016/j.lrp.2013.01.001
Hair, J. F., Matthews, L. M., Matthews, R. L., & Sarstedt, M. (2017). PLS-SEM or CB-SEM: Updated guidelines on which method to use. International Journal of Multivariate Data Analysis, 1(2), 107–123. https://doi.org/10.1504/IJMDA.2017.10008574
Harrington, R., Woiwood, I., & Sparks, T. H. (1999). Climate change and trophic interactions. Tree Ecology Evolution, 14, 146–150. https://doi.org/10.1016/s0169-5347(99)01604-3
Hatta, H., Gumilang, A. R., Fijridiyanto, I. A., Hashiba, K. & Darnaedi, D. (2005). Phenology and growth habits of tropical trees long-term observations in the Bogor and Cibodas Botanic Gardens, Indonesia. Bogor: National Science Museum.
Ibanez, I., Primack, R. B., Miller-Rushing, A. J., Ellwood, E., Higuchi, H., Lee, S. D., Kobori, H., Silander, & J. A. (2010). Forecasting phenology under global warming. Philosophical Transactions of the Royal Society B. Biological Sciences, 365(1555), 3247–3260. https://doi.org/10.1098/rstb.2010.0120
Jabro, J. D., Evans, R. G., Kim, Y., & Iversen, W. M. (2009). Estimating in situ soil–water retention and field water capacity in two contrasting soil textures. Irrigation Science, 27, 223–229. https://doi.org/10.1007/s00271-008-0137-9
Jajo, A., Rahim, M. A., Serra, S., Gagliardi, F., Jajo, N. K., Musacchi, S., Costa, G., Bonghi, C., & Trainotti, L. (2014). Impact of the tree training system, branch type, and position in the canopy on the ripening homogeneity of 'Abbé Fétel'pear fruit. Tree Genetics & Genomes, 10, 1477–1488. https://doi.org/10.1007/s11295-014-0777-2
Kalra, G., & Lal, M. A. (2018). Physiology of flowering. In S. C. Bhatla, & M. A. Lal (Eds.), Plant physiology, development and metabolism (pp. 797–819). Springer. https://doi.org/10.1007/978-981-13-2023-1_25
Kobayashi, M. J., Takeuchi, Y., Kenta, T., Kume, T., Diway, B., & Shimizu, K. K. (2013). Mass flowering of the tropical tree Shorea beccariana was preceded by expression changes in flowering and drought‐responsive genes. Molecular Ecology, 22(18), 4767–4782. https://doi.org/10.1111/mec.12344
Kondo, T., & Morizono, H. (2022). Effects of drought stress on flower number in 'summer queen'passion fruit. The Horticulture Journal, 91(4), 448–452. https://doi.org/10.2503/hortj.QH-006
Landi, P., Sanguineti, M. C., Liu, C., Li, Y., Wang, T. Y., Giuliani, S., Bellotti, M., Salvi, S., & Tuberosa, R. (2007). Root-ABA1 QTL affects root lodging, grain yield, and other agronomic traits in maize grown under well-watered and water-stressed conditions. Journal of Experimental Botany, 58(2), 319–326. https://doi.org/10.1093/jxb/erl161
Laxa, M., Liebthal, M., Telman, W., Chibani, K., Dietz, K.-J. (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants, 8, 94. https://doi.org/10.3390/antiox8040094
Lee, S.-D. (2017). Global warming leading to phenological responses in the process of urbanization, South Korea. Sustainability, 9(12), 2203. https://doi.org/10.3390/su9122203
Liu, Y.-H., Offler, C. E., & Ruan, Y.-L. (2013). Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Frontiers in Plant Science, 4, 282. https://doi.org/10.3389/fpls.2013.00282
Maxwell, B. (2011). Arctic climate: Potential for change under global warming. In F. S. Chapin, R. L. Jefferies, J. F. Reynolds, G. R. Shaver, & J. Svoboda (Eds.), Artic ecosystems in a changing climate: An ecophysiological perspective. Academic Press. Cambridge, MA.
Mullan, D & Pietragalla, J. (2012). Leaf relative water content. In A. J. D. Pask, J. Pietragalla, D. M. Mullan, & M. P. Reynolds (Eds.), Physiological breeding II: A field guide to wheat phenotyping. Mexico.
Munoz-Fambuena, N., Mesejo, C., González-Mas, M. C., Primo-Millo, E., Agustí, M., & Iglesias, D. J. (2012). Fruit load modulates flowering-related gene expression in buds of alternate-bearing "Moncada" mandarin. Annals of Botany, 110(6), 1109–1118. https://doi.org/10.1093/aob/mcs190
Myneni, R. B., Yang, W., Nemani, R. R., Huete, A. R., Dickinson, R. E., Knyazikhin, Y., Didan, K., Fu, R., Negron Juarez, R. I., Saatchi, S. S., Hashimoto, H., Ichii, K., Shabanov, N. V., Tan, B., Ratana, P., Privette, J. L., Morisette, J. T., Vermote, E. F., Roy, D. P., Wolfe, R. E., Friedl, M. A., Running, S. W., Votava, P., El-Saleous, N., Devadiga, S., Su, Y., Salomonson, V. V. (2007). Large seasonal swings in leaf area of Amazon rainforests. Proceedings of the National Academy of Sciences, 104(12), 4820–4823. https://doi.org/10.1073/pnas.0611338104
Ovaskainen, O., Skorokhodova, S., Yakovleva, M., Sukhov, A., Kutenkov, A., Kutenkova, N., Shcherbakov, A., Meyke, E., & Delgado, M. D. M. (2013) Community-level phenological response to climate change. Proceedings of the National Academy of Sciences USA, 110, 13434–13439. https://doi.org/10.1073/pnas.130553311
Penuelas, J., Filella, I., & Comas, P. (2002). Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean Region. Global Change Biology, 8(6), 531–544. https://doi.org/10.1046/j.1365-2486.2002.00489.x
Piao, S., Liu, Q., Chen, A., Janssens, I.A., Fu, Y.H., Dai, J., Liu, L., Lian, X., Shen, M., & Zhu, X. (2019). Plant phenology and global climate change: Current progresses and challenges. Global Change Biology, 25(6), 1922–1940. https://doi.org/10.1111/gcb.14619
Pingping, W., Chubin, W., & Biyan, Z. (2017). Drought stress induces flowering and enhances carbohydrate accumulation in Averrhoa carambola. Horticultural Plant Journal, 3(2), 60–66. https://doi.org/10.1016/j.hpj.2017.07.008
Polansky, L. & C. Boesch. (2013). Long-term fruit phenology changes in a West African lowland tropical rainforests are not explained by rainfall. Biotropica, 45(4), 434–40. https://doi.org/10.1111/btp.12033
Prevey, J. S., Parker, L. E., & Harrington, C. A. (2020). Projected impacts of climate change on the range and phenology of three culturally-important shrub species. PLoS ONE, 15, e0232537. https://doi.org/10.1371/journal.pone.0232537
Rahayu, R. S., Poerwanto, R., Efendi, D., & Widodo, W. D. (2020). Appropriate duration of drought stress for Madura tangerine flower induction. Jurnal Hortikultura Indonesia, 11(2), 82–90. https://doi.org/10.29244/jhi.11.2.82-90
Riboni, M., Galbiati, M., Tonelli, C., & Conti, L. (2013). Gigantea enables drought escape response via abscisic acid-dependent activation of the florigens and suppressor of overexpression of constans. Plant Physiolog, 162(3), 1706–1719. https://doi.org/10.1104/pp.113.217729
Sambatti, J. B., & Caylor, K. K. (2007). When is breeding for drought tolerance optimal if is drought random? New Phytologist, 175(1), 70–80. https://doi.org/10.1111/j.1469-8137.2007.02067.x
Sandip, M., Makwana, A. N., Barad, A. V., & Nawade, B. D. (2015). Physiology of flowering-the case of mango. International Journal of Applied Research, 1(11), 1008–1012.
Satake, A., Chen, Y. Y., Fletcher, C., & Kosugi, Y. (2019). Drought and cool temperature cue general flowering synergistically in the aseasonal tropical forests of Southeast Asia. Ecological Research, 34(1), 40–49. https://doi.org/10.1111/1440-1703.1012
Schwartz, M. D. (1998). Green-wave phenology. Nature, 394(6696), 839–840. https://doi.org/10.1038/29670
Sharafatmandrad, M., Bahremand, A., Mesdaghi, M., & Barani, H. (2010). The role of rainfall and light interception by litter on maintenance of surface soil water content in an arid rangeland (Khabr National Park, Southeast of Iran). Desert, 15(1), 53–60. https://doi.org/10.22059/jdesert.2010.21680
Shalom, L., Samuels, S., Zur, N., Shlizerman, L., Zemach, H., Weissberg, M., Ophir, R., Blumwald, E., & Sadka, A. (2012). Alternate bearing in citrus: changes in the expression of flowering control genes and in global gene expression in on- versus off-crop trees, PLoS ONE, 7(10), e46930. https://doi.org/10.1371/journal.pone.0046930
Sharp, R. E., Poroyko, V., Hejlek, L. G., Spollen, W. G., Springer, G. K., Bohnert, H. J., & Nguyen, H. T. (2004). Root growth maintenance during water deficits: Physiology to functional genomics. Journal of Experimental Botany, 55(407), 2343–2351. https://doi.org/10.1093/jxb/erh276
Smithers, B. V., North, M. P., Millar, C. I., & Latimer, A. M. (2018). Leap frog in slow motion: Divergent responses of tree species and life stages to climatic warming in Great Basin subalpine forests. Global Change Biology, 24(2), e442-e457. https://doi.org/10.1111/gcb.13881
Takeno, K. (2016). Stress-induced flowering: the third category of flowering response, Journal of Experimental Botany, 67(17), 4925–4934. https://doi.org/10.1093/jxb/erw272
Verreynne, J. S. & Lovatt, C. J. (2009). The effect of crop load on budbreak influences return nbloom in alternate bearing "Pixie" mandarin. Journal American Society for Horticultural Science, 134, 299–307. https://doi.org/10.21273/JASHS.134.3.299
Wasaya, A., Zhang, X., Fang, Q. & Yan, Z. (2018). Root phenotyping for drought tolerance: A review. Agronomy, 8(11), 241. https://doi.org/10.3390/agronomy8110241
Wright, S. J., & Calderón, O. (2018). Solar irradiance as the proximate cue for flowering in a tropical moist forest. Biotropica, 50, 374–383. https://doi.org/10.1111/btp.12522
Yang, J., & Zhang, J. (2006). Grain filling of cereals under soil drying. New Phytologist, 169(2), 223–236. https://doi.org/10.2307/3694603
Yang, M., Wu, Y., Jin, S., Hou, J., Mao, Y., Liu, W., Shen, Y., & Wu, L. (2015). Flower bud transcriptome analysis of Sapium sebiferum (Linn.) Roxb. and primary investigation of drought-induced flowering: Pathway construction and G-quadruplex prediction based on the transcriptome. PloS One, 10(3), e0118479. https://doi.org/10.1371/journal.pone.0118479
Yang, X., Lu, M., Wang, Y., Wang, Y., Liu, Z., & Chen, S. (2021). Response mechanism of plants to drought stress. Horticulturae, 7(3), 50. https://doi.org/10.3390/horticulturae7030050
Xu, Q., Liu, S., Wan, X., Jiang, C., Song, X., & Wang, J. (2012). Effects of rainfall on soil moisture and water movement in a subalpine dark coniferous forest in southwestern China. Hydrological Processes, 26(25), 3800–3809. https://doi.org/10.1002/hyp.8400
Xu, Z., Shimizu, H., Yagasaki, Y., Ito, S., Zheng, Y., & Zhou, G. (2013). Interactive effects of elevated CO2, drought, and warming on plants. Journal of Plant Growth Regulation, 32, 692–707. https://doi.org/10.1007/s00344-013-9337-5
Yu, L., T. Liu, K. Bu, F. Yan, J. Yang, L. Chang, & S. Zhang. (2015). Monitoring the long-term vegetation phenology change in Northeast China from 1982 to 2015. Scientific Reports, 7, 14770. https://doi.org/10.1038/s41598-017-14918-4
Zhang, J., Zhang, Y., Song, S., Su, W., Hao, Y., & Liu, H. (2020). Supplementary red light results in the earlier ripening of tomato fruit depending on ethylene production. Environmental and Experimental Botany, 175, 104044. https://doi.org/10.1016/j.envexpbot.2020.104044
Andriani, C. (2020). Aktivitas antibakteri ekstrak etanol akar dan daun rukam (Flacourtia rukam Zoll. & Mor) terhadap bakteri mulut (Streptococcus mutans) penyebab karies pada gigi [dissertation]. Bangka: Universitas Bangka Belitung.
Arisoesilaningsih, E., Soejono, A. Widyati, I. Palupi, & Kiswojo. (2001). Aktivitas reproduktif tiga spesies pohon langka tahan kering di Kebun Raya Purwodadi. In E. Arisoesilaningsih, B. Yanuwiadi, S. Indriyani, T. Yulistyarini, E. E. Ariyanti, N. D. Yulia, & Soejono (Eds.), Prosiding seminar nasional konservasi dan pendayagunaan kenekaragaman tumbuhan lahan kering. LIPI-KRP dan MIPA Universitas Brawijaya, Purwodadi, East Java.
Bandurska, H. (2022). Drought stress responses: Coping strategy and resistance. Plants, 11(7), 922–938. https://doi.org/10.3390/plants11070922
Barrs, H. D. & Weatherley, P. E. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australia Journal Biological Science. 15, 413–428. https://doi.org/10.1071/BI9620413
Bijalwan, P. Sharma, M. Kaushik, P. (2022). Review of the effects of drought stress on plants: A systematic approach. Preprints, 2022, 2022020014. https://doi.org/10.20944/preprints202202.0014.v1
[BMKG] Badan Meteorologi, Klimatologi, dan Geofisika (2023). Data harian Jawa Timur. Retrieved from https://dataonline.bmkg.go.id/data_iklim
Borchert, R., Rivera, G., & Haugner, W. (2002). Modification of vegetative phenology in a tropical semi-deciduous forest by abnormal drought and rain. Biotropica, 34(1), 27–39. https://doi.org/10.1111/j.1744-7429.2002.tb00239.x
Buckley, T. N. (2019). How do stomata respond to water status? New Phytologist, 224(1), 21–36. https://doi.org/10.1111/nph.15899
Budiharta, S., & Solikin. (2010). Potensi and konservasi buah-buahan lokal Jawa Timur. Jakarta: LIPI Press.
Calle, Z., Schlumpberger, B. O., Piedrahita, L., Leftin, A., Hammer, S. A., Tye, A., & Borchert, R. (2010). Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics. Trees, 24, 865–877. https://doi.org/10.1007/s00468-010-0456-3
Chapman, C. A., Chapman, L. J., Struhsaker, T. T., Zanne, A. E., Clark, C. J., & Poulsen, J. R. (2005). A long-term evaluation of fruiting phenology: Importance of climate change. Journal of Tropical Ecology, 21(1), 31–45. https://doi.org/10.1017/S0266467404001993
Comita, L. S., & Engelbrecht, B. M. (2009). Seasonal and spatial variation in water availability drives habitat associations in a tropical forest. Ecology, 90(10), 2755–2765. https://doi.org/10.1890/08-1482.1
Darmayanti, A. S., Ariffin, Waluyo, B., & Arisoesilaningsih, E. (2023). Study on the phenology of three fruit trees species in Purwodadi Botanical Gardens, East Java, and its relationship with mesoclimates. Jurnal Manajemen Hutan Tropika, 29(1), 88–98. https://doi.org/10.7226/jtfm.29.1.88
Dobra, J., Motyka, V., Dobrev, P., Malbeck, J., Prasil, I.T., Haisel, D., Gaudinova, A., Havlova, M., Gubis, J. & Vankova, R. (2010). Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology, 167(16), 1360–1370. https://doi.org/10.1016/j.jplph.2010.05.013
Dunham, A. E., Razafindratsima, O. H., Rakotonirina, P., & Wright, P. C. (2018). Fruiting phenology is linked to rainfall variability in a tropical rain forest. Biotropica, 50(3), 396–404. https://doi.org/10.1111/btp.12564
Ewusie, J. Y. (1986). Elements of tropical ecology. ELBS/Heinemann Educational Books.
Fadiyah, I., Lestari, I., Victory, S., & Mahardika, R. G. (2019). Uji aktivitas antioksidan ekstrak buah rukam (Flacourtia rukam) menggunakan metode maserasi. Proceedings of National Colloquium Research and Community Service, 3, 64–68. https://doi.org/10.33019/snppm.v3i0.1316
Flaigt, W., Beutelspacher, H., & Rietz, E. (1975). Chemical composition and physical properties of humic substances. In J. E. Gieseking (Ed.), Soil components: Organic components (pp 1–211). New York: Springer-Verlag
Gene Albrigo, L., & Galán Saúco, V. (2002). Flower bud induction, flowering, and fruit set of some tropical and subtropical fruit tree crops with special reference to citrus. Acta Hortic, 632, 81–90. https://doi.org/10.17660/ActaHortic.2004.632.10
Gordo, O., & Sanz, J. J. (2010). Impact of climate change on plant phenology in Mediterranean ecosystems. Global Change Biology, 16(3), 1082–1106. https://doi.org/10.1111/j.1365-2486.2009.02084.x
Griffiths, C. A., Gaff, D. F., & Neale, A. D. (2014). Drying without senescence in resurrection plants. Frontiers in Plant Science, 5, 36. https://doi.org/10.3389/fpls.2014.00036
Gu, L., Pallardy, S.G., Hosman, K.P., Sun Y. (2016). Impacts of precipitation variability on plant species and community water stress in a temperate deciduous forest in the central U.S. Agricultural and Forest Meteorology, 217, 120–136. https://doi.org/10.1016/j.agrformet.2015.11.014
Haberman, A., Bakhshian, O., Cerezo‐Medina, S., Paltiel, J., Adler, C., Ben‐Ari, G., Mercado, J. A, Pliego‐Alfaro, F., Lavee, S., & Samach, A. (2017). A possible role for flowering locus T‐encoding genes in interpreting environmental and internal cues affecting olive (Olea europaea L) flower induction. Plant, Cell & Environment, 40(8), 1263–1280. https://doi.org/10.1111/pce.12922
Hair, J. F., Ringle, C. M., & Sarstedt, M. (2013). Partial least squares structural equation modeling: Rigorous applications, better results and higher acceptance. Long Range Planning, 46(1–2), 1–12. https://doi.org/10.1016/j.lrp.2013.01.001
Hair, J. F., Matthews, L. M., Matthews, R. L., & Sarstedt, M. (2017). PLS-SEM or CB-SEM: Updated guidelines on which method to use. International Journal of Multivariate Data Analysis, 1(2), 107–123. https://doi.org/10.1504/IJMDA.2017.10008574
Harrington, R., Woiwood, I., & Sparks, T. H. (1999). Climate change and trophic interactions. Tree Ecology Evolution, 14, 146–150. https://doi.org/10.1016/s0169-5347(99)01604-3
Hatta, H., Gumilang, A. R., Fijridiyanto, I. A., Hashiba, K. & Darnaedi, D. (2005). Phenology and growth habits of tropical trees long-term observations in the Bogor and Cibodas Botanic Gardens, Indonesia. Bogor: National Science Museum.
Ibanez, I., Primack, R. B., Miller-Rushing, A. J., Ellwood, E., Higuchi, H., Lee, S. D., Kobori, H., Silander, & J. A. (2010). Forecasting phenology under global warming. Philosophical Transactions of the Royal Society B. Biological Sciences, 365(1555), 3247–3260. https://doi.org/10.1098/rstb.2010.0120
Jabro, J. D., Evans, R. G., Kim, Y., & Iversen, W. M. (2009). Estimating in situ soil–water retention and field water capacity in two contrasting soil textures. Irrigation Science, 27, 223–229. https://doi.org/10.1007/s00271-008-0137-9
Jajo, A., Rahim, M. A., Serra, S., Gagliardi, F., Jajo, N. K., Musacchi, S., Costa, G., Bonghi, C., & Trainotti, L. (2014). Impact of the tree training system, branch type, and position in the canopy on the ripening homogeneity of 'Abbé Fétel'pear fruit. Tree Genetics & Genomes, 10, 1477–1488. https://doi.org/10.1007/s11295-014-0777-2
Kalra, G., & Lal, M. A. (2018). Physiology of flowering. In S. C. Bhatla, & M. A. Lal (Eds.), Plant physiology, development and metabolism (pp. 797–819). Springer. https://doi.org/10.1007/978-981-13-2023-1_25
Kobayashi, M. J., Takeuchi, Y., Kenta, T., Kume, T., Diway, B., & Shimizu, K. K. (2013). Mass flowering of the tropical tree Shorea beccariana was preceded by expression changes in flowering and drought‐responsive genes. Molecular Ecology, 22(18), 4767–4782. https://doi.org/10.1111/mec.12344
Kondo, T., & Morizono, H. (2022). Effects of drought stress on flower number in 'summer queen'passion fruit. The Horticulture Journal, 91(4), 448–452. https://doi.org/10.2503/hortj.QH-006
Landi, P., Sanguineti, M. C., Liu, C., Li, Y., Wang, T. Y., Giuliani, S., Bellotti, M., Salvi, S., & Tuberosa, R. (2007). Root-ABA1 QTL affects root lodging, grain yield, and other agronomic traits in maize grown under well-watered and water-stressed conditions. Journal of Experimental Botany, 58(2), 319–326. https://doi.org/10.1093/jxb/erl161
Laxa, M., Liebthal, M., Telman, W., Chibani, K., Dietz, K.-J. (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants, 8, 94. https://doi.org/10.3390/antiox8040094
Lee, S.-D. (2017). Global warming leading to phenological responses in the process of urbanization, South Korea. Sustainability, 9(12), 2203. https://doi.org/10.3390/su9122203
Liu, Y.-H., Offler, C. E., & Ruan, Y.-L. (2013). Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Frontiers in Plant Science, 4, 282. https://doi.org/10.3389/fpls.2013.00282
Maxwell, B. (2011). Arctic climate: Potential for change under global warming. In F. S. Chapin, R. L. Jefferies, J. F. Reynolds, G. R. Shaver, & J. Svoboda (Eds.), Artic ecosystems in a changing climate: An ecophysiological perspective. Academic Press. Cambridge, MA.
Mullan, D & Pietragalla, J. (2012). Leaf relative water content. In A. J. D. Pask, J. Pietragalla, D. M. Mullan, & M. P. Reynolds (Eds.), Physiological breeding II: A field guide to wheat phenotyping. Mexico.
Munoz-Fambuena, N., Mesejo, C., González-Mas, M. C., Primo-Millo, E., Agustí, M., & Iglesias, D. J. (2012). Fruit load modulates flowering-related gene expression in buds of alternate-bearing "Moncada" mandarin. Annals of Botany, 110(6), 1109–1118. https://doi.org/10.1093/aob/mcs190
Myneni, R. B., Yang, W., Nemani, R. R., Huete, A. R., Dickinson, R. E., Knyazikhin, Y., Didan, K., Fu, R., Negron Juarez, R. I., Saatchi, S. S., Hashimoto, H., Ichii, K., Shabanov, N. V., Tan, B., Ratana, P., Privette, J. L., Morisette, J. T., Vermote, E. F., Roy, D. P., Wolfe, R. E., Friedl, M. A., Running, S. W., Votava, P., El-Saleous, N., Devadiga, S., Su, Y., Salomonson, V. V. (2007). Large seasonal swings in leaf area of Amazon rainforests. Proceedings of the National Academy of Sciences, 104(12), 4820–4823. https://doi.org/10.1073/pnas.0611338104
Ovaskainen, O., Skorokhodova, S., Yakovleva, M., Sukhov, A., Kutenkov, A., Kutenkova, N., Shcherbakov, A., Meyke, E., & Delgado, M. D. M. (2013) Community-level phenological response to climate change. Proceedings of the National Academy of Sciences USA, 110, 13434–13439. https://doi.org/10.1073/pnas.130553311
Penuelas, J., Filella, I., & Comas, P. (2002). Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean Region. Global Change Biology, 8(6), 531–544. https://doi.org/10.1046/j.1365-2486.2002.00489.x
Piao, S., Liu, Q., Chen, A., Janssens, I.A., Fu, Y.H., Dai, J., Liu, L., Lian, X., Shen, M., & Zhu, X. (2019). Plant phenology and global climate change: Current progresses and challenges. Global Change Biology, 25(6), 1922–1940. https://doi.org/10.1111/gcb.14619
Pingping, W., Chubin, W., & Biyan, Z. (2017). Drought stress induces flowering and enhances carbohydrate accumulation in Averrhoa carambola. Horticultural Plant Journal, 3(2), 60–66. https://doi.org/10.1016/j.hpj.2017.07.008
Polansky, L. & C. Boesch. (2013). Long-term fruit phenology changes in a West African lowland tropical rainforests are not explained by rainfall. Biotropica, 45(4), 434–40. https://doi.org/10.1111/btp.12033
Prevey, J. S., Parker, L. E., & Harrington, C. A. (2020). Projected impacts of climate change on the range and phenology of three culturally-important shrub species. PLoS ONE, 15, e0232537. https://doi.org/10.1371/journal.pone.0232537
Rahayu, R. S., Poerwanto, R., Efendi, D., & Widodo, W. D. (2020). Appropriate duration of drought stress for Madura tangerine flower induction. Jurnal Hortikultura Indonesia, 11(2), 82–90. https://doi.org/10.29244/jhi.11.2.82-90
Riboni, M., Galbiati, M., Tonelli, C., & Conti, L. (2013). Gigantea enables drought escape response via abscisic acid-dependent activation of the florigens and suppressor of overexpression of constans. Plant Physiolog, 162(3), 1706–1719. https://doi.org/10.1104/pp.113.217729
Sambatti, J. B., & Caylor, K. K. (2007). When is breeding for drought tolerance optimal if is drought random? New Phytologist, 175(1), 70–80. https://doi.org/10.1111/j.1469-8137.2007.02067.x
Sandip, M., Makwana, A. N., Barad, A. V., & Nawade, B. D. (2015). Physiology of flowering-the case of mango. International Journal of Applied Research, 1(11), 1008–1012.
Satake, A., Chen, Y. Y., Fletcher, C., & Kosugi, Y. (2019). Drought and cool temperature cue general flowering synergistically in the aseasonal tropical forests of Southeast Asia. Ecological Research, 34(1), 40–49. https://doi.org/10.1111/1440-1703.1012
Schwartz, M. D. (1998). Green-wave phenology. Nature, 394(6696), 839–840. https://doi.org/10.1038/29670
Sharafatmandrad, M., Bahremand, A., Mesdaghi, M., & Barani, H. (2010). The role of rainfall and light interception by litter on maintenance of surface soil water content in an arid rangeland (Khabr National Park, Southeast of Iran). Desert, 15(1), 53–60. https://doi.org/10.22059/jdesert.2010.21680
Shalom, L., Samuels, S., Zur, N., Shlizerman, L., Zemach, H., Weissberg, M., Ophir, R., Blumwald, E., & Sadka, A. (2012). Alternate bearing in citrus: changes in the expression of flowering control genes and in global gene expression in on- versus off-crop trees, PLoS ONE, 7(10), e46930. https://doi.org/10.1371/journal.pone.0046930
Sharp, R. E., Poroyko, V., Hejlek, L. G., Spollen, W. G., Springer, G. K., Bohnert, H. J., & Nguyen, H. T. (2004). Root growth maintenance during water deficits: Physiology to functional genomics. Journal of Experimental Botany, 55(407), 2343–2351. https://doi.org/10.1093/jxb/erh276
Smithers, B. V., North, M. P., Millar, C. I., & Latimer, A. M. (2018). Leap frog in slow motion: Divergent responses of tree species and life stages to climatic warming in Great Basin subalpine forests. Global Change Biology, 24(2), e442-e457. https://doi.org/10.1111/gcb.13881
Takeno, K. (2016). Stress-induced flowering: the third category of flowering response, Journal of Experimental Botany, 67(17), 4925–4934. https://doi.org/10.1093/jxb/erw272
Verreynne, J. S. & Lovatt, C. J. (2009). The effect of crop load on budbreak influences return nbloom in alternate bearing "Pixie" mandarin. Journal American Society for Horticultural Science, 134, 299–307. https://doi.org/10.21273/JASHS.134.3.299
Wasaya, A., Zhang, X., Fang, Q. & Yan, Z. (2018). Root phenotyping for drought tolerance: A review. Agronomy, 8(11), 241. https://doi.org/10.3390/agronomy8110241
Wright, S. J., & Calderón, O. (2018). Solar irradiance as the proximate cue for flowering in a tropical moist forest. Biotropica, 50, 374–383. https://doi.org/10.1111/btp.12522
Yang, J., & Zhang, J. (2006). Grain filling of cereals under soil drying. New Phytologist, 169(2), 223–236. https://doi.org/10.2307/3694603
Yang, M., Wu, Y., Jin, S., Hou, J., Mao, Y., Liu, W., Shen, Y., & Wu, L. (2015). Flower bud transcriptome analysis of Sapium sebiferum (Linn.) Roxb. and primary investigation of drought-induced flowering: Pathway construction and G-quadruplex prediction based on the transcriptome. PloS One, 10(3), e0118479. https://doi.org/10.1371/journal.pone.0118479
Yang, X., Lu, M., Wang, Y., Wang, Y., Liu, Z., & Chen, S. (2021). Response mechanism of plants to drought stress. Horticulturae, 7(3), 50. https://doi.org/10.3390/horticulturae7030050
Xu, Q., Liu, S., Wan, X., Jiang, C., Song, X., & Wang, J. (2012). Effects of rainfall on soil moisture and water movement in a subalpine dark coniferous forest in southwestern China. Hydrological Processes, 26(25), 3800–3809. https://doi.org/10.1002/hyp.8400
Xu, Z., Shimizu, H., Yagasaki, Y., Ito, S., Zheng, Y., & Zhou, G. (2013). Interactive effects of elevated CO2, drought, and warming on plants. Journal of Plant Growth Regulation, 32, 692–707. https://doi.org/10.1007/s00344-013-9337-5
Yu, L., T. Liu, K. Bu, F. Yan, J. Yang, L. Chang, & S. Zhang. (2015). Monitoring the long-term vegetation phenology change in Northeast China from 1982 to 2015. Scientific Reports, 7, 14770. https://doi.org/10.1038/s41598-017-14918-4
Zhang, J., Zhang, Y., Song, S., Su, W., Hao, Y., & Liu, H. (2020). Supplementary red light results in the earlier ripening of tomato fruit depending on ethylene production. Environmental and Experimental Botany, 175, 104044. https://doi.org/10.1016/j.envexpbot.2020.104044
Authors
DarmayantiA. S., Ariffin, WaluyoB., & AriesoesilaningsihE. (2024). Variation of Phenology of Flacourtia rukam in Two Different Habitats and Their Relation to Rainfall, Dry Days, and the Plant Water Status. Jurnal Manajemen Hutan Tropika, 30(1), 118. https://doi.org/10.7226/jtfm.30.1.118
This work is licensed under a Creative Commons Attribution 4.0 International License.
Jurnal Manajemen Hutan Tropika is an open access journal which means that all contents is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the Budapest Open Access Initiative (BOAI) definition of open access.Article Details
