Unique mixture vegetation in and around a Crescentic Lake in the Tsangpo River

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1 Annual Report of Research Institute for Biological Function 13: (2012) 108 Field Survey Report Unique mixture vegetation in and around a Crescentic Lake in the Tsangpo River Basin on the Southeastern Tibetan Plateau, China Motoyasu MINAMI 1), Tetsuo MURAKAMI 2), Junbo WANG 3), Liping ZHU 3), Yasuhiro IZUTSU 4), Tetsuya MATSUNAKA 4), Mitsugu NISHIMURA 4) 1) College of Bioscience & Biotechnology, Chubu University 2) Faculty of Domestic Science, Nagoya Women's University 3) Institute of Tibetan Plateau Research, Chinese Academy of Sciences 4) Graduate School of Marine Science and Technology, Tokai University 1. Introduction The distribution of plants and vegetation on the Tibetan Plateau is markedly influenced by local climate and topology. Indeed, the changes in topology associated with the geological uplifting of the Himalaya and Tibetan plateau were responsible for the development and subsequent strengthening of the humid southwestern summer monsoon (Chang, 1983). Especially, the southeastern Tibetan Plateau lies within the humid southwestern summer monsoon region and receives abundant rainfall (Chang, 1981). Of particular importance to the climate of the region is the influence of the humid southwestern summer monsoon from the Indian Ocean, which passes over the mountains of western Yunnan before moving into the southeastern region of the Tibetan Plateau in summer (Chang, 1983). The humid southwestern summer monsoon then changes direction and moves northwest along the Tsangpo River basin, which is drained by the Niyan, Yegongqu and Polong-Tsangpo tributaries of the Tsangpo River, as well as the Nu, Lancang and Jinsha rivers in the southeastern Tibetan Plateau (Chang, 1983). Together the humid southwestern summer monsoon systems produce abundant summer rainfall, also called plum rains, which are important for supplying the subtropical forest zone on the southeastern Tibetan Plateau (Chang, 1983). Hence, it becomes wetter than the west as the east in the Tsangpo River basin, because the humid southwestern summer monsoon blows westward along this basin. From these reasons, the Tsangpo River basin, which is situated at a crossroads of various vegetations, is central to understanding the geographic zonality and regionalism of Sino-Himalayas vegetation (Yoshida, 2005). However, restricted access to the area for political and military Photo. 1 Pond along the Niyan River where Azolla sp. and Ranunculus bungei grow sympatrically. Pond dimensions: length: ca. 300 m, width at shortest point: ca m, depth: < 0.8 m. (29 43'57.7''N, 94 05'09.3''E, 3,120m above sea level)

2 Unique mixture vegetation on the Southeastern Tibetan Plateau, China reasons has meant that relatively limited information is currently available on the flora of the Tsangpo River basin. Since the vegetation in the Tsangpo River basin is situated at a crossroads of various vegetations, it is believed that the area supports a variety of unique plant species. During July 2-6 in 2009, we surveyed the flora from Lhasa to Bomi in the southeastern Tibet along National Road No. 318 to obtain baseline data for assessing the relationships between vegetation and the humid southwestern summer monsoon. On July 6, we discovered a pond (Photo. 1) along the Niyan River that had been colonized by genus Azolla Lam. (Photo. 2) and Ranunculus bungei Steud. (Photo. 3). In this survey, the discovered Azolla genus was supposed A. cristata or interspecific hybrid between A. cristata and A. filiculoides by morphological characters. However, Watanabe (2006) reported that Azolla genus has many interspecific hybrids and it is impossible to distinguish their hybrids from their parent species by morphological characters. Recently, DNA analysis is effective for solution to above taxonomic issues. Accordingly, we were going to perform identification of species and judgment whether the discovered Azolla genus is hybrid by DNA analysis. However, we were not able to analyze DNA sequences of discovered Azolla genus, because these samples were damaged when we took our laboratory. From reasons, we defined the discovered Azolla genus as Azolla sp. in this report. On the other hands, the separation of the genus Batrachium from the genus Ranunculus is well defined in the Flora of China (Wang and Tamura, 2001). However, Horandl et al. (2005) reported the former genus to be identified within latter, using molecular phylogenetic analysis. Thus, our taxonomic interpretation is based on the opinion of Horandl et al. (2005). These two aquatic plants usually inhabit habitats Photo. 2 Azolla sp. Azolla sp. inhabited stagnant area at the northern bank of the pond that was not affected directly by spring water. Photo. 3 Ranunculus bungei R. bungei revealed that the area of spring water from floor at the northeastern bank of the pond. with very different climates. To our knowledge, no studies on the vegetation of the Tibetan Plateau have reported instances of these species having a sympatric distribution (Institute of Tibetan Plateau Research; ITPR, 1988). Since this area is considered to be a unique mixture vegetation zone, we recorded the vascular plants in and around the pond and analyzed the water quality of each aquatic plant habitat in the pond. 2. Field survey The pond (length: ca. 300 m, width at shortest

3 110- Minami et al. point: ca m, depth: < 0.8 m) (29 43'57.7''.N, 94 05'09.3''E, 3,120 m above sea level) was located on the shore of the Niyan River, the largest tributary of the Tsangpo River, in Nyingchi Prefecture on the southeastern Tibetan Plateau in China. The pond is the crescentic lake, which was formed of the Niyan River mender, and no inflow was found. The pond was divided to two by National Road No We collected specimens from the vascular plant species growing in and around the pond and identified them based on the classifications of Wu (1983, 1985a, 1985b, 1986, 1987), ITPR (1988), Kadono (1994) and Yoshida (2005). The five water quality parameters examined in the Azolla sp. and R. bungei habitats included water temperature ( C), dissolved oxygen (DO; mg/l), electric conductivity (EC; ms/m), ph and turbidity (NTU). 3. Results and discussion 3.1 Riparian vegetation around the pond We confirmed 24 terrestrial plants species (including one identified species) belonging to 14 families (Appendix). The dominant families were Rosaceae (5 spp.), Ranunculaceae (4 spp.), Cyperaceae (2 spp.), Plantaginaceae (2 spp.) and Polygonaceae (2 spp.), with all of the remaining families represented by less than one species. Previous studies classified the vegetation zone and plant communities of the survey area as subtropical montane coniferous forest (Chang, 1981). The dominant vegetation around the pond was the same as that described in previous reports; for example, Amygdalus mira (Koehne) Ricker (Lu, 2003) and Sorbaria arborea C. K. Schneid. (Gu and Alexander, 2003), which dominated the tree layer. Both of these species originally grew in the mixed forests, mountain valleys and ravines of the more temperate and subtropical monsoon zone in Sichuan, Xizang and Yunnan (Lu, 2003; Gu and Alexander, 2003). However, in the shrub layer of this deciduous forest zone, common species were Berberis franchetiana C. K. Schneid. (Ying and Ying, 2011) and Aconitum tongolense Ulbr. (Liangqian and Kadota, 2001). Generally, on the Tibetan Plateau, members of these genera (Berberis and Aconitum) grow in the mountain valleys and ravines of the high-altitude and cold zone area (Ying and Ying, 2011; Liangqian and Kadota, 2001). The riparian vegetation around the pond consisted of a mixture of temperate and subtropical monsoon species, as well as species typical of the high-altitude and cold zones. 3.2 Aquatic plants in the pond We confirmed six aquatic plant species (including one identified species) belonging to five families (Appendix). Except for Azolla sp., five of these species are mentioned in Flora Xizangica (Wu, 1985a, 1986, 1987) and Vegetation Xizang (ITPR, 1988). Although the family of Azollaceae (Synonym of Salviniaceae) are mentioned in the Flora of China (Lin, 1990), no reports have been published to date listing the genus Azolla (Wu, 1983) as being growth to Tibet with the exception of this survey. Generally, it has been reported that the genus Azolla was widely distributed in rice paddies, ponds and ditches of tropical, subtropical and warm temperate regions, such as the areas around the Yangtze River and in southern China (Lin, 1990). In addition to being utilized as a biofertilizer for a variety of crops, Azolla genera (A. imbricata and A. filiculoides) (Lin, 1990) can also be used as the production of hydrogen fuel, biogas, control of weeds and mosquitoes, and for reducing the volatilization of ammonia associated with the application of chemical nitrogen fertilizer (Wagner, 1997). This variety of applications means that the Azolla sp. discovered in this survey may have been intentionally introduced to areas on the southeastern Tibetan Plateau. On the other hand, eight species belonging to the genus Batrachium (Synonym

4 Unique mixture vegetation on the Southeastern Tibetan Plateau, China of Ranunculus) are listed in the Flora of China (Wang and Tamura, 2001). Two of these eight species, B. bungei and B. bungei (Steud.) L. Liou var. flavidum (Hand.-Mazz.) L. Liou. appear in Flora Xizangica (Liu, 1985). B. bungei (Synonym of Ranunculus bungei) inhabits the fast flowing water in rivers and springs in high-altitude and cold zone areas throughout China (Liu, 1985). These two species of aquatic plants, Azolla sp. and R. bungei, usually have markedly different climate preferences (Wagner, 1997; Wang and Tamura, 2001). Indeed, the reason why the vegetation of the pond is unique is because Azolla sp. and R. bungei had a sympatric distribution. This vegetation, with its unique microclimate, was not described in Vegetation Xizang (ITPR, 1988). 3.3 Water quality parameters The comparisons of water quality parameters between Azolla sp. and R. bungei habitats are shown in Table 1. The comparisons of the habitats between Azolla sp. and R. bungei revealed that the areas of spring water from the floor of the pond as well as areas of flowing water in the pond were only colonized by R. bungei. Conversely, Azolla sp. inhabited stagnant areas that were not affected directly by spring water. The water temperature preferences of the two species were also affected by the presence of spring water, which is relatively cold. At the time measurements were taken (Table 1), the water temperature preference of R. bungei (11.5 C) at the northeastern bank of the pond was the optimum temperature for aquatic types in this genus (Okubo and Oike, 2008). It is thus considered likely that the reason why R. bungei were able to grow at the subtropical montane coniferous forest area was due to the presence of cold-water springs at the survey site. On the other hand, the water temperature preference of Azolla sp. (13.6 C) was too low for the growth of this genus, because the optimum temperature for the genus Azolla is C (Wagner, 1997). As previous reports (Li, 1984), there is some species maintaining cold tolerant in the genus Azolla; for example A. filiculoides through the winter was no longer a problem and widely adapted in the Eastern China since introducing. In addition, A. filiculoides was widely distributed from the Southern South America to Alaska (Kannaiyan and Kumar, 2006). Therefore, it was possibility that the discovered Azolla sp. was interspecific hybrid between A. cristata and A. filiculoides by morphological and physiological characters. In order to solve the taxonomical issue of Azolla sp., we need to collect new samples and then analyze the DNA sequences. Comparing the DO characteristics (mg/l) (DO saturation level, %) of the Azolla sp. and R. bungei habitats in the pond, DO was lower in the R. bungei habitat (9.3 mg/l) than it was in the Azolla sp. habitat (16.8 mg/l). In addition to being slightly alkaline, the ph of the water in Azolla sp. habitat (ph 9.4) was higher than that measured in R. bungei habitat (ph 7.9), implying that the carbon dioxide had been used by the photosynthesis of alga and phytoplankton which inhabited in the stagnant water in Azolla sp. habitat. While the DO levels of the R. bungei habitat in this study were almost saturated (88%) by oxygen from the atmosphere and that produced by R. bungei photosynthesis, the Azolla sp. habitat was considered to be supersaturated with oxygen (167%) due to mainly photosynthesis of alga and phytoplankton in the stagnant water in Azolla sp. habitat. The EC levels in both the Azolla sp. (4.0 ms/m) and R. bungei (4.0 ms/m) habitats were same and relatively low, indicating that the inorganic salt concentrations were extremely low. The absence of strongly flowing water meant that the turbidities associated with both hydrosphere environments were low. As for these results, it was supposed that the water of this pond was supplied by only spring.

5 112- Minami et al. Table 1 Comparisons water quality parameters between Azolla sp. and Ranunculus bungei habitats Habitat Time of measurement Water temperature ( ) Dissolved Oxygen (mg/l) Saturation level (%) Electric conductivity (ms/m) ph Turbidity (NTU) Azolla sp. 12:00 PM (167%) R. bungei 12:20 PM (88%) Unique mixture vegetation zone The vegetation in and around the pond consisted of a mix of temperate, subtropical, and monsoon zone species, as well as species from high-altitude and cold zone areas. R. bungei was considered to have originated from high-altitude and cold zone areas, and was capable of growing in the subtropical montane coniferous forest zone because the pond provided a favorable habitat with relatively colder and flowing water fed by spring. Of the terrestrial species that grew around the pond, most were alpine species that were typically associated with the forest floor environments of deciduous forests. The relatively cool characteristics of the forest floor environment have been considered to promote the growth of high-altitude and cold zone species in the subtropical montane coniferous forest zone in Nyingchi Prefecture on the southeastern Tibetan Plateau strongly influenced by the humid southwestern summer monsoon. We also confirmed that the Nyingchi area is a unique mixture vegetation zone, with vegetation ranging from temperate zone through to the subtropical monsoon zone and the high-altitude and cold zone. Future research will examine the relationship between the vegetational gradient in the Tsangpo River basin and the southeastern monsoon. Acknowledgements This study was supported by the research fund of the bilateral program-joint research projects with the National Natural Science Foundation of China (NSFC) by the Japan Society for the Promotion of Science (JSPS). References Chang, D.H.S. (1981) The vegetation zonation of the Tibetan Plateau, Mountain Research and Development 1: Chang, D.H.S. (1983) The Tibetan plateau in relation to the vegetation of China, Ann. Missouri Bot. Gard. 70: Gu, C. and Alexander, C. (2003) Sorbaria arborea, Wu, Y., Raven, H. and Hong, Y. (eds.), Flora of China Vol. 9, p.76, Science Press, Beijing and Missouri Botanical Garden Press, St. Louis. Horandl, E., Paun, O., Jan T. Johansson, J.T., Lehnebach, C., Armstrong, T., Chen, L, and Lockhart, P. (2005) Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Molecular Phylogenetics and Evolution 36: Institute of Tibetan Plateau Research. (1988) Vegetation of Xizang, Science Press, Beijing. (in Chinese) Kadono, Y. (1994) Aquatic plants of Japan, Bun-ichi Sogo Shuppan, Tokyo. (in Japanese)

6 Unique mixture vegetation on the Southeastern Tibetan Plateau, China Kannaiyan, S. and Kumar, K. (2006) Introduction, Biodiversity of Azolla and its algal symbiont Anabaena azollae, p.4, National Biodiversity Authority, Tamilnadu. Liangqian, L. and Kadota, Y. (2001) Aconitum tongolense, Wu, Y., Raven, H. and Hong, Y. (eds.), Flora of China Vol. 6, p.149, Science Press, Beijing and Missouri Botanical Garden Press, St. Louis. Lin, Y.X. (1990) Azollaceae, Wu, Y., Raven, H. and Hong, Y. (eds.), Flora of China Vol. 3, Science Press, Beijing and Missouri Botanical Garden Press, St. Louis. Li, S.Y. (1984) Azolla in the paddy fields of eastern China, Organic matter and rice, International Rice Research Institute, Manila. Liu, L. (1985) Batrachium, Flora Xizangica Vol.2, pp , Science Press, Beijing. (in Chinese) Lu, L. (2003) Amygdalus, Wu, Y., Raven, H. and Hong, Y. (eds.), Flora of China Vol. 9, p.391, Science Press, Beijing and Missouri Botanical Garden Press, St. Louis. Ohba, H. (2009) Syllabus of the vascular plants of Japan, Aboc-Sha, Inc., Kamakura. (in Japanese) Okubo, K. and Oike, S. (2008) Relationship between the aquatic plant distributions and environmental conditions in irrigation canals in Kamiina district, Nagano Prefecture, Journal of the Japanese Institute of Landscape Architecture 71: (in Japanese with English summary) Watanabe, I. (2006) Whither Azolla use goes? -Regulation by Invasive Alien Species Act, J. Weed Sci. Tech. 51: (in Japanese). Wagner, G. (1997) Azolla: A review of its biology and utilization, The Botanical Review 63: Wang, W. and Tamura, M. (2001) Batrachium, Wu, Y., Raven, H. and Hong, Y. (eds), Flora of China. Vol. 6, p.431, Science Press, Beijing and Missouri Botanical Garden Press. St. Louis. Wu, C.Y. (1983) Flora Xizangica Vol. 1, Science Press, Beijing. (in Chinese) Wu, C.Y. (1985a) Flora Xizangica Vol. 2, Science Press, Beijing. (in Chinese) Wu, C.Y. (1985b) Flora Xizangica Vol. 4, Science Press, Beijing. (in Chinese) Wu, C.Y. (1986) Flora Xizangica Vol. 3, Science Press, Beijing. (in Chinese) Wu, C.Y. (1987) Flora Xizangica Vol. 5, Science Press, Beijing. (in Chinese) Ying, J. and Ying, T. (2011) Berberis, Wu, Y., Raven, H. and Hong, Y. (eds), Flora of China Vol. 19, p.714, Science Press, Beijing and Missouri Botanical Garden Press. St. Louis. Yoshida, T. (2005) Himalayan plants illustrated, YAMA KEI, Tokyo. (in Japanese) Title : Unique mixture vegetation in and around a Crescentic Lake in the Tsangpo River Basin on the Southeastern Tibetan Plateau, China Authors: Motoyasu MINAMI 1), Tetsuo MURAKAMI 2), Junbo WANG 3), Liping ZHU 3), Yasuhiro IZUTSU 4), Tetsuya MATSUNAKA 4), Mitsugu NISHIMURA 4) Addresses: 1) College of Bioscience & Biotechnology, Chubu University, 2) Faculty of Domestic Science, Nagoya Women's University, 3) Institute of Tibetan Plateau Research, Chinese Academy of Sciences, 4) Graduate School of Marine Science and Technology, Tokai University Keywords: Tibetan Plateau, Crescentic Lake, Azolla, Ranunculus bungei

7 114- Minami et al. Appendix List of vascular plants found in and around a Crescentic Lake on the Niyan River in Nyingchi Prefecture on the southeastern Tibetan Plateau, China Growth form Family Species Aquatic plants Emergent Plantaginaceae Hippuris vulgaris L. Floating-leaved Potamogetonaceae Potamogeton natans L. Submerged Ranunculaceae Ranunculus bungei (Steud.) L. Liou Free-floating Salviniaceae Azolla Lam. Semiaquatic Ranunculaceae Halerpestes tricuspis (Maxim.) Hand.-Mazz. Ranunculus longicaulis C. A. Mey. var. nephelogense (Edgew.) L. Liou Terrestrial plants Pteridophytes Dennstaedtiaceae Pteridium aquilinum (L.) Kuhn var. latiusculum (Desv.) Underw. Spermatophyte Adoxaceae Sambucus adnata Wall. ex DC. Berberidaceae Crassulaceae Cyperaceae Berberis franchetiana C. K. Schneid. var. glabripes Ahrendt Sedum multicaule Wall. ex Lindl. Bulbostylis densa (Wall.) Hand. - Mazz. Eleocharis valleculosa Ohwi Fabaceae Phrymaceae Plantaginaceae Desmodium elegans DC. Lancea tibetica Hook.f et Thoms Veronica persica Poir. V. serpyllifolia L. Polygonaceae Polygonum kawagoeanum Makino Rumex nepalensis Spreng. Ranunculaceae Aconitum tongolense Ulbr. Anemone rivularis Buch.-Ham.ex DC. Ranunculus distans Wall. ex Royle Thalictrum atriplex Finet et Gagnep. Rhamnaceae Rosaceae Berchemia yunnanensis Franch. Potentilla indica (Andr.) Th. Wolf Potentilla anserina L. Amygdalus mira (Koehne) Ricker Rosa sericeae Lindl. Sorbaria arborea C. K. Schneid. Rubiaceae Salicaceae Galium hoffmeisteri (Klotzch) Ehrend.et Schönb.-Tem.ex R.R.Mill Salix sp. The classification referred to Ohba (2009).