Spatio-temporal variability of periphytic protozoa related to environment in the Niyang River, Tibet, China

  • Haiping Liu (刘海平)
  • Shaowen Ye (叶少文)
  • Xuefeng Yang (杨学峰)
  • Chuanbo Guo (郭传波)
  • Huijuan Zhang (张惠娟)
  • Liqing Fan (范丽卿)
  • Liangsong Zhang (张良松)
  • Lek Sovan
  • Zhongjie Li (李钟杰)


The Niyang River, a main tributary of the Yarlung Zangbo River, is an important and typical plateau river ecosystem in Tibet, China. At present, few studies have focused on its aquatic living resources and river ecology. In this study, the composition, abundance, and diversity of periphytic protozoa were investigated across four seasons from 2008 to 2009 to better understand their spatio-temporal patterns and relationship to the environment. Our investigation shows that periphytic protozoa in the Niyang River contained 15 genera, belonged to Tubulinea, Alveolata, Discosea and Rhizaria, Alveolata possessed most genera, up to nine, with highest share in abundance, exceeding 50%, Difflugia and Glaucoma were dominant genera. Moreover, four diversity indices of periphytic protozoa, including species richness, total abundance, Shannon-Wiener diversity index and Pielou’s evenness index, displayed a significant descending trend as the seasons continued, in the order of winter, spring, summer and autumn; with a significant difference existing between winter and summer (or autumn) for Shannon-Wiener diversity index and species richness (P<0.05). Four of these diversity indices also presented a V-shaped pattern between the upper middle course of the Niyang River and the confluence of the Niyang River and Yarlung Zangbo River, with the lowest value occurred in the middle course of the Niyang River. However, no significant variation was found through the Niyang River (P>0.05). In addition, canonical correlation analysis (CCA) shows that the densities of Difflugia, Glaucomais, Enchelydium, Cyphoderia, and Enchelys correlate with water temperature, alkalinity, hardness, pH, and dissolved oxygen, respectively. Lastly, the relationship between periphytic protozoa diversity and the environmental factors of the Niyang River can be predicted using classification and regression trees (CART) annalysis, which suggests that the total abundance and Shannon-Wiener diversity index would be higher when the elevation is above 3 308 m. On the other hand, the Shannon-Wiener diversity index and Pielou’s evenness index would be lower when pH and ammoniacal nitrogen have lower or higher values. Finally yet importantly, close attention should be paid to periphytic protozoa and its environment to ensure sustainable development of the Niyang River ecosystem.


Tibetan Plateau Niyang River periphytic protozoa environment spatio-temporal dynamic 


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Thanks are given to YAN Hongwei, YIXI Quyun, LIU Jinfeng, DANZENG Pingcuo for their fi eld sampling. Thanks also go to the Editor Roger Z. YU and anonymous reviewers for their helpful comments and constructive suggestions.


  1. Aberle N, Bauer B, Lewandowska A, Gaedke U, Sommer U. 2012. Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production. Marine Biology, 159 (11): 441–2453.CrossRefGoogle Scholar
  2. Adl S M, Simpson A G B, Lane C E, Lukeš J, Bass D, Bowser S S, Brown M W, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, le Gall L, Lynn D H, McManus H, Mitchell E A D, Mozley-Stanridge S E, Parfrey L W, Pawlowski J, Rueckert S, Shadwick L, Schoch C L, Smirnov A, Spiegel F W. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology, 59 (5): 29–514.CrossRefGoogle Scholar
  3. Bai J H, Cui B S, Chen B, Zhang K J, Deng W, Gao H F, Xiao R. 2009. Spatial distribution and ecological risk assessment of heavy metals in surface sediments from a typical plateau lake wetland, China. Ecological Modelling, 222 (2): 01–306.Google Scholar
  4. Biswas S N, Godhantaraman N, Rakshit D, Sarkar S K. 2013. Community composition, abundance, biomass and production rates of Tintinnids (Ciliata: Protozoa) in the coastal regions of Sundarban Mangrove wetland, India. Indian Journal of Geo -Marine Sciences, 42 (2): 63–173.Google Scholar
  5. Camargo J C, Velho L F M. 2011. Longitudinal variation of attributes from flagellate protozoan community in tropical streams. Acta Scientiarum Biological Sciences, 33 (2): 61–169.CrossRefGoogle Scholar
  6. Camargo J C, Vieira L C G, Velho L F M. 2012. The role of limnological variables and habitat complexity in impacted tropical streams as regulatory factors on the flagellate protozoa community. Acta Limnologica Brasiliensia, 24 (2): 93–206.CrossRefGoogle Scholar
  7. Canals O, Serrano-Suárez A, Salvadó H et al. 2015. effect of chlorine and temperature on free-living protozoa in operational man-made water systems (cooling towers and hot sanitary water systems) in Catalonia. Environmental Science and Pollution Research, 22 (9): 610–6618.CrossRefGoogle Scholar
  8. Corrêa L V A, Hardoim E L, Zeilhofer P. 2015. Is the periphytic structure of testaceans (protozoa: rhizopoda) related to water quality: a case study in the Cuiabá River, Brazil. Applied Ecology and Environmental Research, 13 (1): 5–97.Google Scholar
  9. Dorgham M M, El-Tohamy W S, Aziz N E A, El-Ghobashi A, Qin J G. 2013. Protozoa in a stressed area of the Egyptian Mediterranean coast of Damietta, Egypt. Oceanologia, 55 (3): 33–750.CrossRefGoogle Scholar
  10. Dray S, Dufour A B. 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software, 22 (4): 1–20.CrossRefGoogle Scholar
  11. Duan S Q, Wang J, Feng S H, Li J, Han S F. 2011). Research on the assessment of water resources vulnerability of lakes in Yunnan Plateau. China Rural Water and Hydropower, (9): 55–59. (in Chinese with English abstract)Google Scholar
  12. Gong J, Song W B, Warren A. 2005. Periphytic ciliate colonization: annual cycle and responses to environmental conditions. Aquatic Microbial Ecology, 39 (2): 59–170.Google Scholar
  13. Guan Z H, Chen C Y, Qu Y X et al. 1984. Rivers and Lakes in Tibet. Science Press, Beijing. (in Chinese)Google Scholar
  14. He G Q. 2007. Alpine Wetland Ecosystem Service Valuation and Wetland Protection Countermeasures in Tibet. Northwest Agriculture & Forestry University, Xi’an, China. (in Chinese)Google Scholar
  15. Hu Y L, Zheng W. 2011. Research on sustainable development in plateau lake basins. Ecological Economy, 3: 168–171, 183. (in Chinese with English abstract)Google Scholar
  16. Huang Q. 2012. The influence about Human Activities and Ecological Environment Change around Sanjiangyuan Region based on GIS. Minzu University of China, Beijing, China. (in Chinese with English abstract)Google Scholar
  17. Ju J T, Zhu L P, Feng J L, Wang J B, Wang Y, Xie M P, Peng P, Zhen X L, Lü X M. 2012. Hydrodynamic process of Tibetan Plateau lake revealed by grain size: case study of Pumayum Co. Chinese Science Bulletin, 57 (19): 433–2441.CrossRefGoogle Scholar
  18. Ju L H, Yang J, Liu L M, Wilkinson D M. 2014. Diversity and distribution of freshwater testate amoebae (protozoa) along latitudinal and trophic gradients in China. Microbial Ecology, 68 (4): 57–670.CrossRefGoogle Scholar
  19. Lisi P J, Schindler D E, Cline T J, Scheuerell M D, Walsh P B. 2015. Watershed geomorphology and snowmelt control stream thermal sensitivity to air temperature. Geophysical Research Letters, 42 (9): 380–3388.CrossRefGoogle Scholar
  20. Liu H P, Ye S W, Yang X F, Zhang L S, Zhang H J, Fan L Q, Li Z J. 2016. Spatio-temporal characteristics of aquatic organism community and their relationship to environment in Niyang River, the branch of Yarlung Zangbo River, Tibet: 4. zooplankton. Journal of Lake Sciences, 28 (2): 70–378. (in Chinese with English abstract)Google Scholar
  21. Liu H P, Ye S W, Yang X F, Zhang L S, Zhong G H, He Y P, Li Z J. 2014. Spatio-temporal dynamics of aquatic organism community and their relationships to environment in Niyang River, Tibet: 3. macrozoobenthos. Journal of Lake Sciences, 26 (1): 54–160. (in Chinese with English abstract)Google Scholar
  22. Liu H P, Ye S W, Yang X F, Zhang L S, Zhong G H, He Y P, Li Z J. 2013b. Spatio-temporal dynamics of aquatic organism community and their relationships to environment in Niyang River, Tibet: 2. Periphytic algae. Journal of Lake Sciences, 25 (6): 07–915. (in Chinese with English abstract)Google Scholar
  23. Liu H P, Ye S W, Yang X F, Zhang L S, Zhong G H, Li Z J. 2013a. Spatial-temporal dynamics of aquatic organism community and their relationships to environment in Niyang River, Tibet: 1. Phytoplankton. Journal of Lake Sciences, 25 (5): 95–706. (in Chinese with English abstract)Google Scholar
  24. Liu H P, Zhong G H, Ye S W, Zhang L S, Zhang H J, Fan L Q, Basang, Li Z J. 2015. Multivariate statistical analysis of water environment for Niyang River, the branch of the Yarlung Zangbo River, Tibet. Journal of Lake Sciences, 27 (6): 187–1196. (in Chinese with English abstract)Google Scholar
  25. Liu J K. 1999. Advanced Hydrobiology. Science Press, Beijing. (in Chinese)Google Scholar
  26. Luosang L Z D J. 2005. Utilization and protection of water resources in the Qinghai-Tibet Plateau. Resources Science, 27 (2): 3–27. (in Chinese with English abstract)Google Scholar
  27. Ma X F, Liu D Q, Xiong B X, Wang W M. 2005. Studies on the attached protozoan community structure in the Daoguanhe reservoir. Reservoir Fisheries, 25 (5): 1–64. (in Chinese with English abstract)Google Scholar
  28. Ministry of Environmental Protection of the People’s Republic of China. 2002. Standard methods for the examination of water and wastewater. Environmental Science Press, Beijing. (in Chinese)Google Scholar
  29. Neto E V S. 2001. Índices ecológicos de comunidades de Testacea (Protozoa: Rhizopoda) no Rio Cuiabá-perímetro urbano de Rosário Oeste, Mato Grosso. Universidade Federal do Mato Grosso, Cuiabá.Google Scholar
  30. Pepin N, Bradley R S, Diaz H F et al. 2015. Elevationdependent warming in mountain regions of the world. Nature Climate Change, 5 (5): 24–430.CrossRefGoogle Scholar
  31. Pielou E C. 1975. Ecological Diversity. Wiley, New York. 165p.Google Scholar
  32. Puigagut J, Maltais-Landry G, Gagnon V, Brisson J. 2012. Are ciliated protozoa communities affected by macrophyte species, date of sampling and location in horizontal subsurface flow constructed wetlands? Water Research, 46 (9): 005–3013.CrossRefGoogle Scholar
  33. Qin D H, Chen Y Y. 2005a. China’s Climate and Environmental Evolution (Volume 1): The Evolution and Forecast of China’s Climate and Environment. Science Press, Beijing. p.389–390. (in Chinese)Google Scholar
  34. Qin D H, Chen Y Y. 2005b. China’s Climate and Environmental Evolution (Volume 2): The Influence, Adaptation and Mitigation Strategy of Climate and Environment Changes. Science Press, Beijing. p.98–109. (in Chinese)Google Scholar
  35. Rakshit D, Biswas S N, Sarkar S K, Bhattacharya B D, Godhantaraman N, Satpathy K K. 2014. Seasonal variations in species composition, abundance, biomass and production rate of tintinnids (Ciliata: Protozoa) along the Hooghly (Ganges) River Estuary, India: a multivariate approach. Environmental Monitoring and Assessment, 186 (5): 063–3078.CrossRefGoogle Scholar
  36. Sarah E N, Joshua H V, Michael L D, et al. 2013. Stream temperature sensitivity to climate warming in California’s Sierra Nevada: impacts to coldwater habitat. Climatic Change, 116 (S1): 149–170.Google Scholar
  37. Segura C, Caldwell P, Sun G, McNulty S, Zhang Y. 2015. A model to predict stream water temperature across the conterminous USA. Hydrological Processes, 29 (9): 178–2195.CrossRefGoogle Scholar
  38. Shannon E E, Wiener W. 1949. The Mathematical Theory of Communication. University Illinois Press, London. 125p.Google Scholar
  39. Shen H B, Guo L. 2008. Survey and analysis on fish composition of Niyang River in Tibet. Hebei Fisheries, 5): 51–54, 60. (in Chinese with English abstract)Google Scholar
  40. Shen Y F. 1980. Ecological studies on the periphytic protozoa in Lake Dong Hu, Wuhan. Acta Hydrobiologica Sinica, 7 (1): 8–40. (in Chinese with English abstract)Google Scholar
  41. Shen Y F. 1990. New technology for microbial monitoring. China Building Industry Press, Beijing. (in Chinese)Google Scholar
  42. Shen Y P, Wang G X, Wu Q B, Liu S Y. 2002. The Impact of future climate change on ecology and environments in the Changjiang -Yellow Rivers source region. Journal of Glaciol o gy and Geocryology, 24 (3): 08–314. (in Chinese with English abstract)Google Scholar
  43. Shi X L, Liu X J, Liu G J, Sun Z Q, Xu H L. 2012. An approach to analyzing spatial patterns of protozoan communities for assessing water quality in the Hangzhou section of Jing-Hang Grand Canal in China. Environmental Science and Pollution Research, 19 (3): 39–747.CrossRefGoogle Scholar
  44. Sickman J O, Melack J M. 1998. Nitrogen and sulfate export from high elevation catchments of the Sierra Nevada, California. Water, Air, and Soil Pollution, 105 (1-2): 217–226.CrossRefGoogle Scholar
  45. Slemmons K E H, Saros J E, Simon K. 2013. The influence of glacial meltwater on alpine aquatic ecosystems: a review. Environmental Science: Processes & Impacts, 15 (10): 794–1806.Google Scholar
  46. Tan X L, Shi X L, Liu G J, Xu H L, Nie P. 2009. An approach to analyzing taxonomic patterns of protozoan communities for monitoring water quality in Songhua River, northeast China. Hydrobiologia, 638 (1): 93–201.Google Scholar
  47. Therneau T M, Atkinson B, Ripley B. 2010. rpart: Recursive Partitioning. R Package Version 3. p.1–46.Google Scholar
  48. Vaerewijck M J M, Sabbe K, Baré J, Houf K. 2011. Occurrence and diversity of free-living protozoa on butterhead lettuce. International Journal of Food Microbiology, 147 (2): 05–111.CrossRefGoogle Scholar
  49. Wang P, Huang C L, Liu Z D. 1988. Snow and ice chemical characteristic for Xixiabangma Mountain area, Tibet. Environmental Science, 9 (1): 3–26. (in Chinese)Google Scholar
  50. Wey J K, Jürgens K, Weitere M. 2012. Seasonal and successional influences on bacterial community composition exceed that of protozoan grazing in river biofilms. Applied and Environmental Microbiology, 78 (6): 013–2024.CrossRefGoogle Scholar
  51. Wu W H, Xu S J, Lu H Y, Yang J D, Yin H W, Liu W. 2011. Mineralogy, major and trace element geochemistry of riverbed sediments in the headwaters of the Yangtze, Tongtian River and Jinsha River. Journal of Asian Earth Sciences, 40 (2): 11–621.CrossRefGoogle Scholar
  52. Wu W H, Zheng H B, Xu S J, Yang J D, Yin H W. 2012. Geochemistry and provenance of bed sediments of the large rivers in the Tibetan Plateau and Himalayan region. International Journal of Earth Sciences, 101 (5): 357–1370.CrossRefGoogle Scholar
  53. Xie H. 2012. The Evapotranspiation and Its Response to Climate Change on the Tibetan Plateau (1970-2010). Lanzhou University, Lanzhou, China. (in Chinese with English abstract)Google Scholar
  54. Xu H L, Min G S, Choi J K, Zhu M Z, Jiang Y, Al-Rasheid K A S. 2010. Temporal population dynamics of dinoflagellate Prorocentrum minimum in a semi-enclosed mariculture pond and its relationship to environmental factors and protozoan grazers. Chinese Journal of Oceanology and Limnology, 28 (1): 5–81.CrossRefGoogle Scholar
  55. Yang J P, Löder M G J, Gerdts G, Wiltshire K H. 2015. Structural composition and temporal variation of the ciliate community in relation to environmental factors at Helgoland Roads, North Sea. Journal of Sea Research, 101: 9–30.CrossRefGoogle Scholar
  56. Ye S W, Lin M L, Li L, Liu J S, Song L R, Li Z J. 2015. Abundance and spatial variability of invasive fishes related to environmental factors in a eutrophic Yunnan Plateau lake, Lake Dianchi, southwestern China. Environmental Biology of Fishes, 98 (1): 09–224.CrossRefGoogle Scholar
  57. Zhai H J. 2009. Study on the River Ecological Integrity under the Threat of Hydropower Development in LRGR. Beijing Normal University, Beijing, China. (in Chinese with English abstract)Google Scholar
  58. Zhang H P, Chen R H, Li F P, Chen L. 2015. Effect of flow rate on environmental variables and phytoplankton dynamics: results from field enclosures. Chinese Journal of Oceanology and Limnology, 33 (2): 30–438.Google Scholar
  59. Zhang J, Örmälä-Odegrip A M, Mappes J et al. 2014. Topdown effects of a lytic bacteriophage and protozoa on bacteria in aqueous and biofilm phases. Ecology and Evolution, 4 (23): 444–4453.CrossRefGoogle Scholar
  60. Zhang W, Xu H L. 2015. Seasonal shift in community pattern of periphytic ciliates and its environmental drivers in coastal waters of the Yellow Sea, northern China. Journal of the Marine Biological Association of the United Kingdom, 95 (2): 77–288.CrossRefGoogle Scholar
  61. Zhang Y H, Xu C J, Qi Q, Hou G L. 2011. Climate change and ecological effect on the Tibetan plateau. Journal of Qinghai University (Natural Science), 29 (4): 8–22. (in Chinese with English abstract)Google Scholar
  62. Zhou K X, Xu M Q, Cao H. 2003. Influence of protozoan grazing on aquatic bacteria. Acta Hydrobiologica Sinica, 27 (2): 90–195. (in Chinese with English abstract)Google Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Haiping Liu (刘海平)
    • 1
    • 2
    • 3
  • Shaowen Ye (叶少文)
    • 1
  • Xuefeng Yang (杨学峰)
    • 4
  • Chuanbo Guo (郭传波)
    • 1
  • Huijuan Zhang (张惠娟)
    • 3
  • Liqing Fan (范丽卿)
    • 3
  • Liangsong Zhang (张良松)
    • 5
  • Lek Sovan
    • 6
  • Zhongjie Li (李钟杰)
    • 1
  1. 1.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Agricultural and Animal Husbandry College of Tibet UniversityLinzhiChina
  4. 4.Xilinhot No.6 Middle SchoolXilinhotChina
  5. 5.Fujian Marine Products Technical Promotion StationFuzhouChina
  6. 6.UMR 5174 EDBCNRS-University Paul SabatierToulouseFrance

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