Abstract
Despite being the world's largest single-flower, Rafflesia’s biology and life history are still poorly understood due to its cryptic growth strategy on Tetrastigma vines. Previous studies have been mostly short-term, contrary to Rafflesia’s long development period before blooming. Bud development and flower phenology of R. cantleyi was studied in a dipterocarp forest in Lata Jarum, Peninsular Malaysia. Seven populations, consisting of 247 buds, were monitored fortnightly for 65 months in two discrete studies between 2009 and 2018. The bud size distribution of R. cantleyi is dynamic, progressively changing from small flower buds to larger buds before flowering. Buds < 5.0 cm across had the slowest growth and highest mortality rates, while those > 15.0 cm across demonstrated accelerated growth. The bud growth profiles of the same site clustered distinctively regardless of sex with successful blooming rate that varied greatly between sites, prompting speculation about their relatedness to the sites’ physical attributes. We reported the first female-dominated population in Rafflesia’s life history. Rafflesia cantleyi’s blooming rate at Lata Jarum is moderate to high, with non-seasonal flowering phenology as evident by the lack of synchronisation and consistency between flowering and local rainfall patterns. Based on the field data of the present study and the published information of other Rafflesia species, R. cantleyi’s life cycle was estimated between 4.0 and 5.3 years. Our findings further explain Rafflesia’s biology and life history and highlight the gap in knowledge of the natural habitats on the endoparasite’s growth and fate potentially for future conservation and study.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Amini S, Rosli K, Abu-Bakar MF, Alias H, Mat-Isa MN, Juhari MA, Haji-Adam J, Goh HH, Wan KL (2019) Transcriptome landscape of Rafflesia cantleyi floral buds reveals insights into the roles of transcription factors and phytohormones in flower development. PLoS ONE 14:e0226338. https://doi.org/10.1371/journal.pone.0226338
Bänziger H (1991) Stench and fragrance: unique pollination lure of Thailand’s largest flower, Rafflesia kerrii Meijer. Nat Hist Bull Siam Soc 39:19–52
Bänziger H (1995) Ecological, morphological and taxonomic studies on Thailand’s fifth species of Rafflesiaceae: Rhizanthes zippelii (Blume) Spach. Nat Hist Bull Siam Soc 43:337–365
Bänziger H, Hansen B, Kreetiyutanont K (2000) A new form of the hermit’s spittoon, Sapria himalayana Griffith f. albovinosa Bänziger & Hansen f. nov. (Rafflesiaceae), with notes on its ecology. Nat Hist Bull Siam Soc 48:213–219
Barcelona JF, Pelser PB, Balete DS, Co LL (2009) Toxonomy, ecology and conservation status of Philippine Rafflesia. Blumea 54:77–93. https://doi.org/10.3767/000651909x474122
Barkman TJ, Lim S-H, Salleh KM, Nais J (2004) Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world’s largest flower. Proc Natl Acad Sci USA 101:787–792
Barkman TJ, Klooster MR, Gaddis KD, Franzone B, Calhoun S, Manickam S, Vessabutr S, Sasirat S, Davis CC (2017) Reading between the vines: hosts as islands for extreme holoparasitic plants. Am J Bot 104:1382–1389. https://doi.org/10.3732/ajb.1700117
Bascos EMA, Fernando ES, Duya MV, Rodriguez LJV (2021) Beginnings of a plant parasite: early development of Rafflesia consueloae inside its Tetrastigma host. Planta 254:61. https://doi.org/10.1007/s00425-021-03710-4
Beaman JH, Adam J (1984) Observations on Rafflesia in Sabah. Sabah Soc J 7:208–212
Beaman RS, Decker PJ, Beaman JH (1988) Pollination of Rafflesia (Rafflesiaceae). Am J Bot 75:1148–1162. https://doi.org/10.1002/j.1537-2197.1988.tb08828.x
Bouman F, Meijer W (1994) Comparative structure of ovules and seeds in Rafflesiaceae. Plant Syst Evol 193:187–212
Carranca C, Brunetto G, Tagliavini M (2018) Nitrogen nutrition of fruit frees to reconcile productivity and environmental concerns. Plants 7:4. https://doi.org/10.3390/plants7010004
Cheang B-K (1993) Interannual variability of monsoons in Malaysia and its relationship with ENSO. Proc Indian Acad Sci, Earth Planet Sci 102:219–239. https://doi.org/10.1007/BF02839192
Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678. https://doi.org/10.1126/science.1100671
Emmons LH, Nais J, Briun A (1991) The fruit and consumers of Rafflesia keithii (Rafflesiaceae). Biotropica 23:197–199. https://doi.org/10.2307/2388307
Er AC, Rosniza Aznie CR, Novel L, Mohd Azlan A, Adam JH (2012) Ekopelancongan dan analisis sosioekonomi komuniti Ulu Dong. Geografia Malays J Soc Space 8:46–52
Galang R (2007) Population study of Rafflesia lobate in the northern section of the central Panay Island mountain ranges, Philippines. Folia Malaysiana 8:87–98
Galindon JMM, Ong PS, Fernando ES (2016) Rafflesia consueloae (Rafflesiaceae), the smallest among giants; a new species from Luzon island, Philippines. Phytokeys 61:37–46. https://doi.org/10.3897/phytokeys.61.7295
Hidayati SN, Meijer W, Baskin JM, Walck JL (2000) A contribution to the life history of the rare Indonesian holoparasite Rafflesia patma (Rafflesiaceae). Biotropica 32:404–414. https://doi.org/10.1111/j.1744-7429.2000.tb00487.x
Irish EE, Nelson T (1989) Sex determination in monoecious and dioecious in plants. Plant Cell 1:737–744
Justesen PT (1922) Morphological and biological notes on Rafflesia flowers, observed in the highlands of mid-Sumatra. Ann Jard Bot Buitenzorg 32:64–87
Kusuma YWC, Noerwana O, Isagi Y (2018) New evidence of flower predation on three parasitic Rafflesia species from Java. Trop Conserv Sci 11:1–6. https://doi.org/10.1177/1940082918796011
Lee XW, Mat-Isa MN, Mohd-Elias NA, Aizat-Juhari MA, Goh HH, Dear PH, Chow KS, Haji Adam J, Mohamed R, Firdaus-Raih M, Wan KL (2016) Perigone lobe transcriptome analysis provides insights into Rafflesia cantleyi flower development. PLoS ONE 11:e0167958. https://doi.org/10.1371/journal.pone.0167958
Lestari D, Hikmat A, Zuhud EAM (2014) Conservation strategy of Rafflesia zollingeriana Koord in Meru Betiri National Park, East Java. J Man Hut Trop 20:9–16. https://doi.org/10.7226/jmht.20.1
Loehwing WF (1938) Physiological aspects of sex in angiosperms. Bot Rev IV 11:581–625
Meijer W (1958) A contribution to the taxonomy and biology of Rafflesia arnoldii in West Sumatra. Ann Bogor 3:33–44
Meijer W (1985) Saving the world’s largest flower. Natl Geogr Mag 168:136–139
Meijer W (1997) Rafflesiaceae. Fl Males 13:1–42
Meijer W, Elliot S (1990) Taxonomy, ecology, and conservation of Rafflesia kerrii Meijer in southern Thailand. Nat Hist Bull Siam Soc 38:117–133
Milewicz M, Sawicki J (2012) Mechanisms of sex determination in plants. Čas Slez Muz Opava 61:123–129
Mursidawati S, Irawati N (2014) Rafflesia patma (Rafflesiaceae): notes on its field study, cultivation, seed germination, and anatomy. Bull Kebun Raya 17:9–14
Mursidawati S, Wicaksono A (2020) Tissue differentiation of the early and the late flower buds of Rafflesia patma Blume. J Plant Dev 27:19–32
Mursidawati S, Wicaksono A (2021) A preliminary study of in vivo injection of auxin and cytokinin into Rafflesia patma Blume flower bud. Buletin Kebun Raya. https://doi.org/10.14203/bkr.v24i2.670
Mursidawati S, Wicaksono A, da Silva T (2019) Development of the endophytic parasite, Rafflesia patma Blume, among host plant (Tetrastigma leucostaphylum (Dennst.) Alston) vascular cambium tissue. S Afr J Bot 123:382–386
Nais J (1997) Distribution, reproductive ecology and conservation of Rafflesia in Sabah. Dissertation, University of Aberdeen, Malaysia
Nais J (2001) Rafflesia of the world. Sabah Parks, Kota Kinabalu, Malaysia
Nikolov LA, Tomlison PB, Manickam S, Endress PK, Kramer EM, Davis CC (2014a) Holoparasitic Rafflesiaceae possess the most reduced endophytes and yet give rise to the world’s largest flowers. Ann Bot 114:233–242. https://doi.org/10.1093/aob/mcu114
Nikolov LA, Staedler YM, Manickam S, Schönenberger J, Endress PK, Kramer EM, Davis CC (2014b) Floral structure and development in Rafflesiaceae with emphasis on their exceptional gynoecia. Am J Bot 101:225–243. https://doi.org/10.3732/ajb.1400009
Pannell JR (2017) Plant sex determination. Curr Biol 27:191–197
Pelser PB, Nickrent DL, Callado JRC, Barcelona JF (2013) Mt. Banahaw reveals: the resurrection and neotypification of the name Rafflesia lagascae (Rafflesiacea) and clues to the dispersal of Rafflesia seeds. Phytotaxa 1311:35–40. https://doi.org/10.11646/phytotaxa.131.1.6
Refaei J, Jones EBG, Sakayaroj J, Santhanam J (2011) Endophytic fungi from Rafflesia cantleyi: species diversity and antimicrobial activity. Mycosphere 2:429–447
Sumaia MMB, Wan AY, Jumaat HA, Nzalina I (2015) Effects of acqueous extract of Rafflesia cantleyi bud on aphrodisiac activity in male Sprague dawley rats. Int J Pharmacol 11:938–943. https://doi.org/10.3923/1jp.2015.938.943
Susatya A (2020) The growth of flower bud, life history, and population structure of Rafflesia arnoldii (Rafflesiaceae) in Bengkulu, Sumatra, Indonesia. Biodiversitas 21:792–798. https://doi.org/10.13057/biodiv/d210247
Susatya A, Prndeka F, Saprinurdin S, Rahman N (2017) Population attributes of the very rare Rafflesia bengkiluensis at Kaur Regency, Southern Bengkulu. Bull Kebun Raya 20:43–50
Susatya A (2007) Taxonomy and ecology of Rafflesia in Bengkulu, Indonesia. Dissertation, Universiti Kebangsaan Malaysia.
Tolod JR, Galindon JMM, Atienza RR, Duya MV, Fernando ES, Ong PS (2021) Flower and fruit development and life history of Rafflesia consueloae (Rafflesiaceae). Philippine J Sci 150:321–324. https://doi.org/10.56899/150.s1.23
van de Jong Lier Q (2014) Water availability to plants. In: Teixeira W, Ceddia M, Ottoni M, Donnagema G (eds) Application of soil physics in environmental analyses. Progress in soil science. Springer, Cham
Whitten TRE, Soeriatmadia ASA (1996) The ecology of Java and Bali. Periplus Editions, Republic of Singapore
Wicaksono A, Mursidawati S, Sukamto LA, da Teixeira Silva JA (2016) Rafflesia spp.: propogation and conservation. Planta 244:286–296. https://doi.org/10.1007/s00425-016-2512-8
Wicaksono A, Mursidawati S, Molina J (2021) A plant within a plant: insights on the development of the Rafflesia endophyte within its host. Bot Rev 87:233–242. https://doi.org/10.1007/s12229-020-09236-w
Wong M, Latiff AM (1994) Rafflesia of Peninsula Malaysia. Nat Malaysiana 19:84–88
Yahya AF, Hyun JO, Lee JH, Choi TB, Sun BY, Lapitan PG (2010) Distribution pattern, reproductive biology, cytotaxonomic study and conservation of Rafflesia manillana in Mt. Makiling, Laguna. Philippines J Trop Forest Sci 22:118–126
Acknowledgements
We gratefully acknowledge Mohd Shukri M.A. (District Forest Office, Raub and Cameron Highland, Pahang) and Nur Syazwani M.B. for field assistance in study period I and II, respectively, and Norbet Simon for help in constructing the topographical map of the study sites. We also thank the anonymous reviewers for constructive comments to improve the quality of the manuscript. Research permissions granted by the Department of Forestry of Peninsular Malaysia, Ministry of Natural Resources and Environment, Malaysia and Pahang State Forestry Department, Malaysia, are greatly appreciated
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This research was supported by the Fundamental Research Grant Scheme: FRGS/1/2015/ST03/UKM/02/1 and UKM-ST-06-FRGS015-2010 by Ministry of Higher Education Malaysia, and Malaysian Toray Science Foundation (Science & Technology Research Grant STGL-011-2008) awarded to SLW.
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SLW conceived and designed research; SLW, SBT and SHT collected the data; SLW and BKBT analysed the data; SLW wrote the manuscript with input from all authors. All authors read and gave final approval for publication.
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Wee, S.L., Tan, S.B., Tan, S.H. et al. Bud development, flower phenology and life history of holoparasitic Rafflesia cantleyi. J Plant Res (2024). https://doi.org/10.1007/s10265-024-01522-7
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DOI: https://doi.org/10.1007/s10265-024-01522-7