Spatial distribution characteristics and driving factors of benthic ciliates in northern China
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摘要: 为深入了解不同地理尺度因素对驱动微型生物群落空间结构的相对影响,本研究于2020年10月调查了中国北方14个砂质潮间带的砂栖纤毛虫群落。研究结果如下:(1)检获纤毛虫105种,隶属26目65属,按丰度优势依次为帆口目、小胸目和环毛目;(2)黄海、渤海两区域的环境因子存在显著差异,但纤毛虫群落组成趋于相似;(3)偏Mental分析显示,环境条件较空间距离在纤毛虫群落组成的驱动中更为重要,其中盐度、粒度和海滩坡度是解释纤毛虫空间分布的最优环境因子组合,而潮差和溶解无机氮含量是次要影响因子;(4)沿海区域微型生物的强扩散效应在一定程度上掩盖了环境异质性影响。综上,由于沿海生态系统中微型生物受到更少扩散限制,在空间分布格局的形成上,环境条件的影响比空间距离更重要。本研究为海洋微型生物地理学提供了基础数据,有助于在全球变化背景下制定沙滩管理和保护规划。Abstract: In October 2020, we sampled the benthic ciliate communities in 14 sandy intertidal zones in northern China to gain insight into the relative influence of diverse geographical scale parameters on driving the spatial pattern of microbial communities. The main findings were as follow: (1) 105 ciliates were identified belonging to 65 genera and 26 orders, and Pleuronematida, Microthoracida, and Cyclotrichida were the dominant groups; (2) although significant differences in environmental conditions were detected between the Yellow Sea and the Bohai Sea, the community composition of ciliates did not show significant difference; (3) partial Mental test revealed that environmental factors were more important than spatial distance in determining ciliate community composition, with salinity, grain size, and beach slope were the most important environmental factors in explaining ciliate spatial distribution, while tidal range and dissolved inorganic nitrogen content were less important; (4) in coastal areas, the mass effect of microorganisms somewhat hided the effects of environmental heterogeneity. In conclusion, because microorganisms in coastal environments were less restricted by dispersal, environmental variables played a larger role in the establishment of spatial distribution patterns than spatial distance. This research gives basic information on marine microbial biogeography, which can aid beach management and conservation planning in the face of global change.
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Key words:
- protozoa /
- community structure /
- intertidal zone /
- local environment /
- mass effect
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图 1 研究站位分布及海滩坡度计算示意图
1. 长兴岛海滨公园;2. 鲅鱼圈沙滩;3. 兴海沙滩;4. 山海关老龙头海水浴场;5. 唐山碧海浴场;6. 金脉广场沙滩;7. 大连金石滩;8. 烟台第一海水浴场;9. 爱莲湾;10. 大辛家沙滩;11. 石老人海水浴场;12. 青岛银沙滩;13. 日照荷兰假日海滩;14. 连云港东西连岛海滩
Fig. 1 Schematic illustration of study station distribution and beach slope computation
1. Changxingdao Seashore Park; 2. Bayuquan Beach; 3. Xinghai Beach; 4. the Old Dragon’s Head Bathing Beach; 5. Bihai Bathing Beach of Tangshan; 6. Jinmai-Square Beach; 7. Jinshi Beach of Dalian; 8. the First Bathing Beach of Yantai; 9. Ailian Bay; 10. Daxinjia Beach; 11. Shilaoren Bathing Beach; 12. Qingdao Silver Beach; 13. Rizhao Dutch Holiday Beach; 14. Lianyungang East and West Liandao Beach
表 1 砂栖纤毛虫群落丰度优势物种在黄海、渤海的组成及分布
Tab. 1 Composition and distribution of benthic ciliates abundance-dominant species in the Yellow Sea and Bohai Sea
种名 渤海 黄海 尖梭刺膜袋虫(Acucyclidium atractodes) +++ ++ 棕色楯纤虫(Aspidisca fusca) + 斯坦楯纤虫(Aspidisca steini) + ++ 三角齿管虫(Chlamydodon triquetrus) + ++ 德氏篷体虫(Chlamydonella derouxi) ++ + 中型发袋虫(Cristigera media) + 瞬闪膜袋虫(Cyclidium glaucoma) ++ ++ 针毛双眉虫(Diophrys hystrix) + + 盾圆双眉虫(Diophrys scutum) ++ 乳突盘毛虫(Discotricha papillifera) +++ ++ 坚实表叶虫(Epiphyllum soliforme) + + 柠檬镰膜袋虫(Falcicyclidium citriforme) +++ ++ 方氏镰膜袋虫(Falcicyclidium fangi) ++ ++ 细纤刺叶虫(Kentrophyllum fibrillatum) ++ ++ 刚毛刺叶虫(Kentrophyllum setigerum) ++ ++ 有肋薄咽虫(Leptopharynx costatus) ++ ++ 拟迟钝洛佩虫(Lopezoterenia paratorpens) + 蠕状斜叶虫(Loxophyllum verrucosum) + 蚤状中缢虫(Mesodinium pulex) + +++ 简单小胸虫(Microthorax simplex) ++ +++ 装饰异偏体虫(Mirodysteria decora) + 长拟盘头虫(Paradiscocephalus elongatus) ++ 佛氏环须虫(Peritromus faurei) + 冠帆口虫(Pleuronema coronatum) + 少毛帆口虫(Pleuronema paucisaetosum) ++ ++ 刚毛帆口虫(Pleuronema setigerum) ++ + 维氏帆口虫(Pleuronema wiackowskii) ++ ++ 活泼拟小胸虫(Pseudomicrothorax agilis) + 邓氏伪扁丝虫(Pseudoplatynematum dengi) + 具齿伪扁丝虫(Pseudoplatynematum denticulatum) ++ 侯氏柔页虫(Sathrophilus holtae) ++ ++ 扁柔页虫(Sathrophilus planus) ++ 艾氏裂纱虫(Schizocalyptra aeschtae) ++ 小冠须虫(Stephanopogon minuta) ++ 弓形腹梭虫(Trachelocerca sagitta) ++ ++ 注:+表示个体数量占总体数量1%以下;++表示个体数量占总体数量的1%~10%;+++表示个体数量占总体数量的10%以上。 表 2 砂栖纤毛虫多样性指数与环境因子的皮尔逊相关分析
Tab. 2 Correlation investigation of benthic ciliate diversity indices with environmental conditions using Pearson’s correlation analysis
环境因子 s N J ' ORP −0.07 −0.06 −0.50 S −0.14 −0.23 −0.15 ${ {\rm{SiO} }_3^{2-} }$含量 −0.40 0.10 −0.21 ${{\rm{NO} }_2^- }$含量 0.25 0.28 −0.03 ${{\rm{NH} }_4^+ }$含量 0.32 0.51 −0.18 ${{\rm{PO} }_4^{3-}}$含量 −0.07 0.37 0.09 ${{\rm{NO} }_3^-}$含量 −0.17 −0.30 0.23 DIN含量 0.09 0.47 −0.27 TOC含量 0.60** 0.36 −0.10 Chl a含量 0.63* 0.55* −0.03 SED −0.68** −0.40 0.39 Slope −0.52 −0.10 0.32 maxTR 0.43 −0.20 0.19 注:*在0.05级别(双尾),相关性显著;**在0.01级别(双尾),相关性极显著。 表 3 与群落结构相关性最密切的环境因子组合
Tab. 3 The most closely connected environmental parameters with community structure
变量个数 相关系数 组合因子 3 0.613 S、SED、Slope 2 0.590 S、SED 4 0.574 S、DIN含量、SED、Slope 4 0.556 S、SED、Slope、maxTR 4 0.546 S、${\rm{NH} }_4^+$含量、SED、Slope 表 4 纤毛虫群落的非相似性与环境和空间距离间的Mantel检验和偏Mantel检验
Tab. 4 Mantel test and partial Mantel test for non-similarity between ciliate communities and environmental and spatial variables
距离矩阵 R p 环境距离矩阵 0.626 0.001 环境距离矩阵 | 空间距离矩阵 0.628 0.001 空间距离矩阵 0.167 0.074 空间距离矩阵 | 环境距离矩阵 0.177 0.073 -
[1] Cottenie K. Integrating environmental and spatial processes in ecological community dynamics[J]. Ecology Letters, 2005, 8(11): 1175−1182. doi: 10.1111/j.1461-0248.2005.00820.x [2] Erős T, Sály P, Takács P, et al. Temporal variability in the spatial and environmental determinants of functional metacommunity organization-stream fish in a human-modified landscape[J]. Freshwater Biology, 2012, 57(9): 1914−1928. doi: 10.1111/j.1365-2427.2012.02842.x [3] Mellin C, Bradshaw C J A, Meekan M G, et al. Environmental and spatial predictors of species richness and abundance in coral reef fishes[J]. Global Ecology and Biogeography, 2010, 19(2): 212−222. doi: 10.1111/j.1466-8238.2009.00513.x [4] de Maçaneiro J P, Oliveira L Z, Seubert R C, et al. More than environmental control at local scales: do spatial processes play an important role in floristic variation in subtropical forests?[J]. Acta Botanica Brasilica, 2016, 30(2): 183−192. doi: 10.1590/0102-33062015abb0294 [5] Ribeiro K F, da Rocha C M, de Castro D, et al. Distribution and coexistence patterns of phytoplankton in subtropical shallow lakes and the role of niche-based and spatial processes[J]. Hydrobiologia, 2018, 814(1): 233−246. doi: 10.1007/s10750-018-3539-6 [6] Soininen J. Macroecology of unicellular organisms-patterns and processes[J]. Environmental Microbiology Reports, 2012, 4(1): 10−22. doi: 10.1111/j.1758-2229.2011.00308.x [7] Chu Haiyan, Sun Haobo, Tripathi B M, et al. Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau[J]. Environmental Microbiology, 2016, 18(5): 1523−1533. doi: 10.1111/1462-2920.13236 [8] Plante C J, Hill-Spanik K, Cook M, et al. Environmental and spatial influences on biogeography and community structure of saltmarsh benthic diatoms[J]. Estuaries and Coasts, 2021, 44(1): 147−161. doi: 10.1007/s12237-020-00779-0 [9] Xu Y, Soininen J. Spatial patterns of functional diversity and composition in marine benthic ciliates along the coast of China[J]. Marine Ecology Progress Series, 2019, 627: 49−60. doi: 10.3354/meps13086 [10] Passy S I. A distinct latitudinal gradient of diatom diversity is linked to resource supply[J]. Ecology, 2010, 91(1): 36−41. doi: 10.1890/09-0545.1 [11] Zhou Zhenghu, Wang Chuankuan, Luo Yiqi. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality[J]. Nature Communications, 2020, 11(1): 3072. doi: 10.1038/s41467-020-16881-7 [12] Heino J, Melo A S, Siqueira T, et al. Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects[J]. Freshwater Biology, 2015, 60(5): 845−869. doi: 10.1111/fwb.12533 [13] Hua Er, Zhang Zhinan, Zhou Hong, et al. Meiofauna distribution in intertidal sandy beaches along China shoreline (18°–40°N)[J]. Journal of Ocean University of China, 2016, 15(1): 19−27. doi: 10.1007/s11802-016-2740-3 [14] Nel R, Campbell E E, Harris L, et al. The status of sandy beach science: past trends, progress, and possible futures[J]. Estuarine, Coastal and Shelf Science, 2014, 150: 1−10. doi: 10.1016/j.ecss.2014.07.016 [15] Tarragô L D, Ferreira P M A, Utz L R P. Benthic marine ciliate assemblages from southern Brazil and their relationship with seasonality and urbanization level[J]. Diversity, 2020, 12(1): 16. [16] Wickham S, Gieseke A, Berninger U G. Benthic ciliate identification and enumeration: an improved methodology and its application[J]. Aquatic Microbial Ecology, 2000, 22(1): 79−91. [17] Fenchel T. The ecology of marine microbenthos I. The quantitative importance of ciliates as compared with metazoans in various types of sediments[J]. Ophelia, 1967, 4(2): 121−137. doi: 10.1080/00785326.1967.10409616 [18] 徐奎栋. 海洋微型底栖生物的多样性与地理分布[J]. 生物多样性, 2011, 19(6): 661−675.Xu Kuidong. Biodiversity and biogeography of marine microbenthos: progress and prospect[J]. Biodiversity Science, 2011, 19(6): 661−675. [19] Huang H, Yang Jinpeng, Huang Shixiang, et al. Spatial distribution of planktonic ciliates in the western Pacific Ocean: along the transect from Shenzhen (China) to Pohnpei (Micronesia)[J]. Marine Life Science & Technology, 2021, 3(1): 103−115. [20] Lynn D H. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature[M]. 3rd ed. New York: Springer, 2008. [21] Xu Yuan, Stoeck T, Forster D, et al. Environmental status assessment using biological traits analyses and functional diversity indices of benthic ciliate communities[J]. Marine Pollution Bulletin, 2018, 131: 646−654. doi: 10.1016/j.marpolbul.2018.04.064 [22] Hamels I, Muylaert K, Sabbe K, et al. Contrasting dynamics of ciliate communities in sandy and silty sediments of an estuarine intertidal flat[J]. European Journal of Protistology, 2005, 41(4): 241−250. doi: 10.1016/j.ejop.2005.02.002 [23] Xu Yuan, Soininen J, Zhang Shukun, et al. Disentangling the relative roles of natural and anthropogenic-induced stressors in shaping benthic ciliate diversity in a heavily disturbed bay[J]. Science of the Total Environment, 2021, 801: 149683. doi: 10.1016/j.scitotenv.2021.149683 [24] Tirjaková E, Krajčovičová K, Illyová M, et al. Interaction of ciliate communities with cyanobacterial water bloom in a shallow, hypertrophic reservoir[J]. Acta Protozoologica, 2016, 55(3): 173−188. [25] Kosiba J, Krztoń W, Wilk-Woźniak E. Effect of microcystins on proto- and metazooplankton is more evident in artificial than in natural waterbodies[J]. Microbial Ecology, 2018, 75(2): 293−302. doi: 10.1007/s00248-017-1058-z [26] Barboza F R, Defeo O. Global diversity patterns in sandy beach macrofauna: a biogeographic analysis[J]. Scientific Reports, 2015, 5: 14515. doi: 10.1038/srep14515 [27] Azovsky A I, Mazei Y A, Saburova M A, et al. Patterns in diversity and composition of the microbenthos of subarctic intertidal beaches with different morphodynamics[J]. Marine Ecology Progress Series, 2020, 648: 19−38. doi: 10.3354/meps13419 [28] Li Guihao, Su Lei, Zhang Qianqian, et al. Molecular diversity and biogeography of benthic ciliates in the Bohai Sea and Yellow Sea[J]. Acta Oceanologica Sinica, 2019, 38(2): 78−86. doi: 10.1007/s13131-018-1236-y [29] Pan Yongbo, Yang Jun, McManus G B, et al. Insights into protist diversity and biogeography in intertidal sediments sampled across a range of spatial scales[J]. Limnology and Oceanography, 2020, 65(5): 1103−1115. doi: 10.1002/lno.11375 [30] Liu Weiwei, McManus G B, Lin Xiaofeng, et al. Distribution patterns of ciliate diversity in the South China Sea[J]. Frontiers in Microbiology, 2021, 12: 689688. doi: 10.3389/fmicb.2021.689688 [31] Zhao Feng, Filker S, Xu Kuidong, et al. Microeukaryote communities exhibit phyla-specific distance-decay patterns and an intimate link between seawater and sediment habitats in the western Pacific Ocean[J]. Deep-Sea Research Part I: Oceanographic Research Papers, 2020, 160: 103279. doi: 10.1016/j.dsr.2020.103279 [32] 刘世昊, 丰爱平, 夏东兴, 等. 辽东湾西岸典型岬湾海滩表层沉积物粒度分布特征及水动力条件浅析[J]. 沉积学报, 2014, 32(4): 700−709.Liu Shihao, Feng Aiping, Xia Dongxing, et al. Grain-size distribution of surface sediments of two typical headland-bay beaches on western Liaodong Bay, Bohai Sea and simply analysis of hydrodynamic conditions[J]. Acta Sedimentologica Sinica, 2014, 32(4): 700−709. [33] 岳保静, 廖晶, 高茂生, 等. 山东半岛砂质海滩动力地貌演化特征[J]. 海洋科学, 2017, 41(4): 118−127. doi: 10.11759/hykx20161107001Yue Baojing, Liao Jing, Gao Maosheng, et al. Evolutionary features of morphodynamics of sandy beaches on the Shandong Peninsula[J]. Marine Sciences, 2017, 41(4): 118−127. doi: 10.11759/hykx20161107001 [34] 刘宗宇, 杨丽中, 乔守文, 等. 山东省滨海沙滩现状调查[J]. 海洋科学, 2020, 44(9): 121−129.Liu Zongyu, Yang Lizhong, Qiao Shouwen, et al. Investigation of coastal beaches in Shandong Province[J]. Marine Sciences, 2020, 44(9): 121−129. [35] 宣俊, 李海波, 王超锋, 等. 黑潮及相邻海域表层砂壳纤毛虫分布模式: 以夏季黄海、东海至西太平洋断面为例[J]. 海洋科学, 2022, 46(2): 28−36.Xuan Jun, Li Haibo, Wang Chaofeng, et al. Summertime tintinnid community in the surface waters of the Kuroshio and adjacent waters: a case study along a transect from the Yellow Sea and East China Sea to the West Pacific[J]. Marine Sciences, 2022, 46(2): 28−36. [36] 于莹, 王宇, 张博伦, 等. 渤海湾浮游纤毛虫丰度和生物量的周年变化[J]. 生态学报, 2022, 42(9): 3822−3831.Yu Ying, Wang Yu, Zhang Bolun, et al. Annual variation of abundance and biomass of planktonic ciliates in the Bohai Bay, China[J]. Acta Ecologica Sinica, 2022, 42(9): 3822−3831. [37] 周百灵, 维妙, 李菊, 等. 黄海底栖纤毛虫的群落结构与时空变化[J]. 海洋与湖沼, 2016, 47(2): 336−345.Zhou Bailing, Wei Miao, Li Ju, et al. Community structure and spatiotemporal variation of benthic ciliates in the Yellow Sea[J]. Oceanologia et Limnologia Sinica, 2016, 47(2): 336−345. [38] Xu Kuidong, Du Yongfen, Lei Yanli, et al. A practical method of Ludox density gradient centrifugation combined with protargol staining for extracting and estimating ciliates in marine sediments[J]. European Journal of Protistology, 2010, 46(4): 263−270. doi: 10.1016/j.ejop.2010.04.005 [39] 宋微波, 沃伦A, 胡晓钟. 中国黄渤海的自由生纤毛虫[M]. 北京: 科学出版社, 2009.Song Weibo, Alan W, Hu Xiaozhong. Free-Living Ciliates in the Bohai and Yellow Seas, China[M]. Beijing: Science Press, 2009. [40] Pratt J R, Cairns Jr J. Functional groups in the protozoa: roles in differing ecosystems[J]. The Journal of Protozoology, 1985, 32(3): 415−423. doi: 10.1111/j.1550-7408.1985.tb04037.x [41] Fenchel T. The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna commuities with special reference to the ciliated protozoa[J]. Ophelia, 1969, 6(1): 1−182. doi: 10.1080/00785326.1969.10409647 [42] 韩永强, 夏嘉, 谭靖千, 等. 环雷州半岛近海表层沉积物有机碳分布及其控制因素分析[J]. 海洋科学, 2020, 44(3): 93−103. doi: 10.11759/hykx20191012002Han Yongqiang, Xia Jia, Tan Jingqian, et al. Distribution and controlling factors of organic carbon in surface sediments of the coastal region surrounding Leizhou Peninsula[J]. Marine Sciences, 2020, 44(3): 93−103. doi: 10.11759/hykx20191012002 [43] Hossain G M, Bhuiyan M A H. Spatial and temporal variations of organic matter contents and potential sediment nutrient index in the Sundarbans mangrove forest, Bangladesh[J]. KSCE Journal of Civil Engineering, 2016, 20(1): 163−174. doi: 10.1007/s12205-015-0333-0 [44] 顾福康. 原生动物学概论[M]. 北京: 高等教育出版社, 1991.Gu Fukang. Introduction to Protozoology[M]. Beijing: Higher Education Press, 1991. [45] Defeo O, Gomez J, Lercari D. Testing the swash exclusion hypothesis in sandy beach populations: the mole crab Emerita brasiliensis in Uruguay[J]. Marine Ecology Progress Series, 2001, 212: 159−170. doi: 10.3354/meps212159 [46] McLachlan A, Dorvlo A. Global patterns in sandy beach macrobenthic communities: biological factors[J]. Journal of Coastal Research, 2007, 23(5): 1081−1087. doi: 10.2112/04-0408.1 [47] Defeo O, McLachlan A. Global patterns in sandy beach macrofauna: species richness, abundance, biomass and body size[J]. Geomorphology, 2013, 199: 106−114. doi: 10.1016/j.geomorph.2013.04.013 [48] Mazei Y A, Burkovskii I V, Stolyarov A P. Salinity as a factor of forming ciliate community (Colonization Experiments)[J]. Zoologicheskiĭ Zhurnal, 2002, 81(4): 387−393. [49] Oren A. Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications[J]. Journal of Industrial Microbiology and Biotechnology, 2002, 28(1): 56−63. doi: 10.1038/sj/jim/7000176 [50] Finlay B J, Esteban G F, Brown S, et al. Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies[J]. Protist, 2006, 157(4): 377−390. doi: 10.1016/j.protis.2006.05.012 [51] Virta L, Soininen J, Norkko A. Diversity and distribution across a large environmental and spatial gradient: evaluating the taxonomic and functional turnover, transitions and environmental drivers of benthic diatom communities[J]. Global Ecology and Biogeography, 2020, 29(12): 2214−2228. doi: 10.1111/geb.13190 [52] Mo Yuanyuan, Peng Feng, Gao Xiaofei, et al. Low shifts in salinity determined assembly processes and network stability of microeukaryotic plankton communities in a subtropical urban reservoir[J]. Microbiome, 2021, 9(1): 128. doi: 10.1186/s40168-021-01079-w [53] Wang Yibo, Zhang Wenjing, Lin Yuanshao, et al. Phosphorus, nitrogen and chlorophyll a are significant factors controlling ciliate communities in summer in the northern Beibu Gulf, South China Sea[J]. PLoS One, 2014, 9(7): e101121. doi: 10.1371/journal.pone.0101121 [54] Xu Kuidong, Choi J K, Lei Yanli, et al. Marine ciliate community in relation to eutrophication of coastal waters in the Yellow Sea[J]. Chinese Journal of Oceanology and Limnology, 2011, 29(1): 118−127. doi: 10.1007/s00343-011-9106-x [55] Howarth R W, Marino R. Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades[J]. Limnology and Oceanography, 2006, 51(1part2): 364−376. doi: 10.4319/lo.2006.51.1_part_2.0364 [56] Azovsky A I, Chertoprud E S, Garlitska L A, et al. Does size really matter in biogeography? Patterns and drivers of global distribution of marine micro- and meiofauna[J]. Journal of Biogeography, 2020, 47(5): 1180−1192. doi: 10.1111/jbi.13771 [57] Vyverman W, Verleyen E, Sabbe K, et al. Historical processes constrain patterns in global diatom diversity[J]. Ecology, 2007, 88(8): 1924−1931. doi: 10.1890/06-1564.1 [58] Petz W, Valbonesi A, Schiftner U, et al. Ciliate biogeography in Antarctic and Arctic freshwater ecosystems: endemism or global distribution of species?[J]. FEMS Microbiology Ecology, 2007, 59(2): 396−408. doi: 10.1111/j.1574-6941.2006.00259.x [59] Hillebrand H, Azovsky A I. Body size determines the strength of the latitudinal diversity gradient[J]. Ecography, 2001, 24(3): 251−256. doi: 10.1034/j.1600-0587.2001.240302.x [60] Spalding M D, Fox H E, Allen G R, et al. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas[J]. BioScience, 2007, 57(7): 573−583. doi: 10.1641/B570707 [61] Bortolini J C, Pineda A, Rodrigues L C, et al. Environmental and spatial processes influencing phytoplankton biomass along a reservoirs-river-floodplain lakes gradient: a metacommunity approach[J]. Freshwater Biology, 2017, 62(10): 1756−1767. doi: 10.1111/fwb.12986 [62] Leibold M A, Holyoak M, Mouquet N, et al. The metacommunity concept: a framework for multi-scale community ecology[J]. Ecology Letters, 2004, 7(7): 601−613. doi: 10.1111/j.1461-0248.2004.00608.x [63] Heino J, Grönroos M, Ilmonen J, et al. Environmental heterogeneity and β diversity of stream macroinvertebrate communities at intermediate spatial scales[J]. Freshwater Science, 2013, 32(1): 142−154. doi: 10.1899/12-083.1 -