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Title Significance of the Phosphorus-Use Strategies of Trees Significance of the phosphorus-use strategies of trees for the Title cycling of phosphorus in Bornean tropical rainforest ecosystems( Dissertation_全文 ) Author(s) Tsujii, Yuki Citation 京都大学 Issue Date 2018-03-26 URL https://doi.org/10.14989/doctor.k21147 学位規則第9条第2項により要約公開; 許諾条件により本文 Right は2020-07-02に公開; 許諾条件により要約は2019-03-20に 公開 Type Thesis or Dissertation Textversion ETD Kyoto University Significance of the phosphorus-use strategies of trees for the cycling of phosphorus in Bornean tropical rainforest ecosystems Yuki Tsujii 2018 Contents Acknowledgements p 1 Chapter 1. General introduction p 3 Chapter 2. Significance of the localization of phosphorus among tissues on a cross- section of leaf lamina of Bornean tree species for phosphorus-use efficiency p 33 Chapter 3. Phosphorus and nitrogen resorption from different chemical fractions in senescing leaves of tropical tree species on Mount Kinabalu, Borneo p 44 Chapter 4. Relationships of phosphorus concentration in reproductive organs with soil phosphorus availability for tropical rainforest tree species on Mount Kinabalu, Borneo p 78 Chapter 5. Significance of phosphorus allocation among tree organs for the residence time of phosphorus in tropical rainforest biomass p 103 Chapter 6. General discussion p 132 References p 142 Acknowledgements First and foremost, I express my sincere gratitude to my supervisor Prof. K. Kitayama for his guidance, patience and encouragement throughout my study. He gave me the precious opportunity to conduct an ecosystem ecological study on Mount Kinabalu, Borneo. The complex and diverse ecosystems on the mountain always stir my curiosity. Additionally, I thank my committee member Prof. Y. Honda, Prof. Y. Kosugi, and Prof. K. Kitajima for their comments and discussions. I thank Dr. Jamili Nais, Ms. Rimi Repin, Mr. Fred Tuh, Mr. Alim Biun, and all stuff of Sabah parks for giving me opportunities to study the ecosystems of Mount Kinabalu, and their kind support. I also thank Assoc. Prof. S. Aiba, Assist. Prof. Y. Onoda and Dr. A. Hidaka for their fruitful advice on field work and chemical analyses. Dr. M. Oikawa helped me examine a Micro-PIXE analysis with the staff members of NIRS, Japan. I would like to express my gratitude to the following persons: Assoc. Prof. N. Osawa, Prof. Y. Isagi, Prof. M. Takyu, Prof. J. Yanai, Assoc. Prof. N. Okada, Assist. Prof. M. Yamasaki, Dr. R. Wagai, Dr. K. Miyamoto, Assoc. Prof. T. Seino, Assoc. Prof. N. Imai, Dr. H. Samejima, Assist. Prof. A. Nakao, Ms. Luiza Majuakim, Dr. K. Fujii, Dr. M. Ushio, Dr. K. Okada, Dr. T. Mori, Dr. R. Aoyagi, Dr. H. Iidzuka, Dr. S. Fujiki, and Dr. R. Spake. Their comments helped me to improve my thesis. Ms. Rosnah Binti Molidin, Mr. Therence Richie Kimpong, Mr. Daniel James, Dr. A. Izuno, Dr. K. Ioki, Ms. L.J. Sun, Mr. S. Ando, Ms. C. Ikeda, Ms. Y. Ichitsuka, Mr. S. Nishio, Mr. K. Nakashima, Mr. Y. Nomura, Mr. D. Yokoyama, Ms. M. Mukai, Ms. M. Okano, Mr. T. Genroku, Ms. H. Nagano, Mr. T. Takehara, Ms. S. Yanou, Mr. M. Nakano, Mr. H. Taga, and Ms. K. Ohira assisted me in field work 1 and chemical analyses. Members in the laboratory of forest ecology, Kyoto University, commented to my work. I thank Ms. T. Norimoto, Ms. R. Fujiwara, and Ms. K. Taneda for their daily support. I would like to send my special thanks to all my Kadazan and Dusun friends. Had it not been for their help, I could not do this work. Finally, I thank my parents Mr. Sadahiko Tsujii and Ms. Etsuko Tsujii, my brothers Mr. Koki Tsujii and Mr. Haruki Tsujii, and my grandmother Ms. Matsue Shimodaira. This study was supported by JSPS KAKENHI Grant numbers JP16J11435 to Y. Tsujii, and JP22255002 to Prof. K. Kitayama, and ‘the MEXT Project for Creation of Research Platforms and Sharing of Advanced Research Infrastructure’. 2 Chapter 1. General introduction Phosphorus (P) is an essential element for all living organisms, and is used to build the molecules for genes (DNA and RNA), energy carriers (ATP and ADP), cellular membranes (phospholipids), and others (Westheimer 1987; Campbell & Farrell 2006; Alberts et al. 2013). Plants require P particularly for photosynthesis, because the substrates for binding carbon dioxides consist of P-containing compounds (i.e. sugar-phosphate) (Malkin & Niyogi 2000; Raven et al. 2005; Hawkesford et al. 2012). Therefore, P availability can be a selective pressure for plants by affecting photosynthesis (Shane et al. 2004; Thomas et al. 2006; Denton et al. 2007; Hidaka & Kitayama 2009, 2013), productivity (Vitousek 1984; Wardle et al. 2004; Elser et al. 2007; Cleveland et al. 2011; Harpole et al. 2011), reproduction (Lambers et al. 2010; Wright et al. 2011; Fujita et al. 2014; Kitayama et al. 2015; DiManno & Ostertag 2016), and others. P in terrestrial ecosystems is derived mostly from rock weathering (Walker & Syers 1976). Bioavailable P (i.e. inorganic P and labile organic P) in soils decreases with increasing soil age by leaching and/or the conversion to unavailable forms (e.g. P adsorption by soils), and consequently P is impoverished in old soils (Fig. 1-1) (Walker & Syers 1976; Lajtha & Schlesinger 1988; Crews et al. 1995; Richardson et al. 2004; Vitousek 2004; Turner et al. 2007; Laliberté et al. 2012). Wardle et al. (2004) examined the change of tree basal area per area (a surrogate of tree biomass) in relation to the nitrogen (N):P ratios of fresh litter and humus, which increase with increasing P deficiency (Redfield 1958) along the following six pedogenesis chronosequences: the Cooloola dune sequence in eastern Australia, the Arjeplog lake island sequence in Sweden, the Glacier Bay sequence in Alaska, the 3 chronosequence of the Hawaiian Archipelagos, and the Franz Josef and Waitutu sequences in New Zealand. The tree basal area increased in the earlier stage, and then decreased in the later stage of pedogenesis across the sequences. The decline of the tree basal area was linked with the increases of the N:P ratios of fresh litter and humus at the final stage of pedogenesis. Therefore, Wardle et al. (2004) suggested that forest retrogression occurred due to P deficiency in the end of pedogenesis across biomes. Contrary to this hypothesis, Kitayama (2005) demonstrated that the biomass of Bornean tropical rainforests was maintained even on P-poor soils. He analyzed the relationship of tree aboveground biomass with the N:P ratio of fresh litter for Bornean tropical rainforests, and found that the biomass did not dramatically decline with the increase of the N:P ratio of leaf litter, which varied more widely than that in Wardle et al. (2004). Kitayama (2005, 2012) pointed out the extreme high species diversity in Bornean tropical rainforests compared with that in Wardle et al. (2004), and suggested that the high species diversity maintained forest biomass on P-poor soils by the increase of P-use efficient species in abundance with increasing P deficiency. 1.1. The questions, objectives and logical structure of this thesis Soils in the tropics are often highly weathered and contain little bioavailable P (Crews et al. 1995; Kitayama et al. 2000; Yang et al. 2014; Fujii et al. 2017). Bornean tropical rainforests on such soils are gigantic and highly productive (Kitayama 2005). This is thought to be because Bornean rainforest trees on P-poor soils have high P-use efficiency (PUE; net primary productivity per unit P absorbed from soils; Vitousek 1982) (Kitayama et al. 2000; Kitayama & Aiba 2002) with 4 adaptive mechanisms to P deficiency (Paoli et al. 2005; Hidaka & Kitayama 2011, 2013) (see section 1.2.). Previous studies have explored the underlying mechanism of high PUE by focusing on leaf, which is the primary photosynthetic organ of trees and requires a large amount of P, and have elucidated several mechanisms for high photosynthetic P-use efficiency and a long residence time of P in leaves (e.g. Paoli et al. 2005; Hidaka 2011; Hidaka & Kitayama 2009, 2011, 2013) (see section 1.3.). On the other hand, a substantial amount of P is allocated to other functions, such as P storage (Ichie & Nakagawa 2013; Sardans & Peñuelas 2013; Zavišić & Polle 2017), mechanical supporting (Tanner 1985; Meerts 2002; Chave et al. 2009; Imai et al. 2010; Sardans & Peñuelas 2013; Heineman et al. 2016), P acquisition (i.e. fine roots, Gordon & Jackson 2000; Yuan & Chen 2010; Yuan et al. 2011; Wurzburger & Wright 2015; Okada et al. 2017), and especially reproduction (Lambers et al. 2010; Ichie & Nakagawa 2013; Tully et al. 2013; Kitayama et al. 2015; Dimanno & Ostertag 2016). Reproduction requires much P for genes (DNA and RNA) and the investment for progenies (i.e. P storage in seeds) (Fenner et al. 1986; Lott et al. 2000; Fenner & Thompson 2005; Lambers et al. 2010) (see section 1.4). The investment of P to reproduction, which competes with that to photosynthesis and others (Obeso 2002), may influence PUE by affecting forest productivity. Therefore, the knowledge on the reproductive strategy of trees is required for understanding the maintenance of the biomass of forests on P-poor soils. However, the relationship of P with the reproduction of Bornean rainforest trees remains mostly unknown. This is because the reproduction is not easily observed due to the episodic occurrence of flowering/fruiting events, known as general flowering/fruiting (Ashton et al. 1988; Sakai 2002; Cannon et al. 2007). A continuous monitoring is required for the observation of the reproduction 5 of Bornean rainforest trees. Therefore, I aimed to answer my research questions by conducting a continuous monitoring of the forests. In this chapter, I explain the novelty and importance of this thesis by reviewing previous studies addressing the P-use strategies in production and reproduction for Bornean rainforest trees on P- poor soils. First, I introduce P-use efficiency (PUE), which is an essential concept to understand the P-use strategies of trees.
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