RIVER-LAKE DISCONNECTION ON FISH TAXONOMIC DISTINCTNESS IN LAKES FROM MIDDLE AND LOWER REACHES OF THE YANGTZE RIVER
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摘要: 基于1950s以来的长江中下游湖泊鱼类调查数据, 分析通江湖泊与阻隔湖泊的鱼类分类多样性差异, 以及通江和阻隔湖泊鱼类分类多样性的时间序列变化, 探讨江湖阻隔对鱼类多样性的影响。结果显示, 阻隔湖泊鱼类物种数、平均分类差异指数(Δ+)和分类差异变异指数(Λ+)平均值分别为48.47±14.64、74.02±3.09和736.89±33.80; 通江湖泊为76.22±14.40、78.31±0.98和697.31±25.53。阻隔湖泊物种数和Δ+值显著低于通江湖泊(P<0.001), 而阻隔湖泊Λ+值显著高于通江湖泊(P=0.002), 表明阻隔湖泊物种间亲缘关系更近, 均匀度下降, 即物种分类单元减少, 且集中分布于某几个分类阶元, 稳定性变差。典型通江与阻隔湖泊鱼类群落分类多样性的时间变化分析发现, 两种类型湖泊的鱼类物种数和Δ+值均随时间推移整体呈现下降趋势, Λ+值整体呈现升高趋势; 并且阻隔湖泊的Λ+值随阻隔时间增加而大幅上升, Δ+和Λ+值随时间变化多在95%置信区间之外。这表明通江湖泊也受到各种扰动影响, 导致鱼类资源整体衰退, 分类多样性下降; 但阻隔湖泊影响更显著, 稳定性更差。基于上述结果, 建议恢复阻隔湖泊与长江的连通性; 通过水环境治理改善鱼类栖息地质量; 科学调整阻隔湖泊鱼类群落结构, 放流江湖洄游型鱼类, 增加物种多样性。Abstract: In the middle-lower reach of the Yangtze River, there are many lakes with intensive fish biodiversity, which are connected with the Yangtze mainstream historically. Since the 1950s, most of these lakes have experienced river-lake disconnection by anthropogenic impacts, leading to remarkable biodiversity decline of fish in these lakes. Based on the published literatures about fish assemblages in lakes, the taxonomic distinctness and temporal changes of fish communities in the connected lakes and disconnected lakes were examined by using two taxonomic diversity indices (average taxonomic distinctness, Δ+ and variation in taxonomic distinctness, Λ+), to assess the impact of river-lake disconnection. The results indicated that disconnected lakes showed significantly lower species richness and Δ+ values (average values of 48.47±14.64 and 74.02±3.093, respectively) than connected lakes (average values of 76.22±14.40 and 78.31±0.98, respectively; P<0.001), indicating the loss of fish diversity. On the contrary, the disconnected lakes showed significantly higher Λ+ values (average values 736.89±33.80) than connected lakes (average values of 697.31±25.53; P=0.002), indicating the increasing unevenness of taxonomic distinctness. Our analysis of temporal changes showed that species richness and Δ+ generally declined, and Λ+ generally increased through time within representative connected and disconnected lakes. However, the species richness, Δ+ and Λ+ values of the connected lake fluctuated over time, and the Λ+ increased significantly over time. These mean that connected lakes were also affected by various disturbances, which led to the decline of taxonomic diversity and the distribution of fish in disconnected lakes was more concentrated in some taxa resulting high unevenness and low stability in the community. Based on our results, we suggested to restore the fish diversity in the middle and lower reaches of the Yangtze River by recovering the connection between the lakes and the Yangtze mainstream, improving the quality of fish habitat through water environment management, and scientifically adjusting the fish community structure.
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动物肠道内生活着大量的微生物, 包括真核微生物、细菌、古菌和病毒等[1]。在肠道微生态系统中, 各种微生物与宿主经过长期的协同进化, 在调节宿主生理生化反应、促进消化吸收、介导宿主免疫应答和抵制宿主疾病发生等方面发挥着重要的作用, 以至于被认为是动物额外的器官[2—5]。这些与肠道联系紧密的共生菌群, 与宿主相互作用, 共同维系整个肠道生态系统平衡与稳定。然而, 肠道正常菌群不是一成不变的, 可因环境、饵料、宿主行为和基因型等的不同有所差异, 但总体上处于相对稳定状态[6—9]。
有研究表明, 有些肠道微生物只是随机进入肠道或暂时生活于此, 而某些病原微生物入侵肠道微环境, 可直接或间接影响肠道正常菌群的平衡与稳定[10]。Li等[11]研究发现, 患有疖病的圆口铜鱼肠道菌群多样性显著低于健康圆口铜鱼, 且肠道菌群在患病个体间的差异也远大于健康个体间差异。对患有“红鳃病”的鲫与健康鲫肠道菌群进行对比分析, 也得出相似的结论[12], 这表明病原入侵会导致肠道菌群发生紊乱。
草鱼(Ctenopharyngodon idellus)是我国最为重要的淡水养殖鱼类, 在长江、珠江流域养殖量极大[13]。草鱼幼苗容易感染病原发病, 其中威胁最大的是草鱼出血病(Grass carp hemorrhage)。草鱼呼肠孤病毒(Grass carp reovirus, GCRV)是草鱼出血病的主要病原, 其致病类型主要有3种: “红肌肉型”、“红鳍红鳃盖型”、“肠炎型”[14]。其中, 患肠炎型(由GCRV感染草鱼引起的肠道炎症)出血病会导致草鱼肠道微生态环境发生剧烈变化[15]。目前有关草鱼肠道菌群的研究多局限于从成年草鱼消化道内分离培养与纤维素水解相关的微生物, 研究不同饵料饲喂下草鱼消化道微生物的群落结构, 以及影响草鱼消化道微生物群落结构的因素等[9, 16—18], 关于GCRV感染对草鱼肠道菌群的影响研究还鲜见报道。对此, 本研究运用高通量测序技术, 对健康草鱼和人工感染GCRV草鱼肠道菌群进行了比较研究, 以期为该病的防治提供肠道微生物方面的依据和参考。
1. 材料与方法
1.1 实验材料与样品采集
实验草鱼(体重20—30 g/尾)来自于中国科学院水生生物研究所官桥养殖基地, 采样前1周转移至中国科学院水生生物研究所室内养殖系统, 水温控制在24—28℃, 期间投喂人工配合饲料。室内驯化1周后选规格相同的草鱼随机分成病毒感染组和对照组。病毒感染组草鱼通过浸泡在GCRV水溶液中10min, 对照组草鱼则浸泡在不含GCRV的水溶液中10min作对照处理。分别于感染GCRV后第2、第4、第6天(从处理组开始有草鱼表现出不适到因感染病毒导致死亡过程)分别随机各取3尾感染组和对照组草鱼进行后续分析。在第6天实验组增加3尾死亡草鱼样品的分析(因此对照组共9尾, 感染病毒处理组12尾)。由于草鱼个体较小, 肠道样品取整个肠道用来提取菌群DNA, 样品的具体采集和处理方法参照文献[19]进行。
1.2 草鱼肠道菌群16S rRNA基因高通量测序分析
草鱼肠道菌群DNA采用MoBio PowerFecal试剂盒参照说明书提取, 基因组DNA保存在–20℃; 首先, 用NanoDrop检测DNA样品的浓度, 将所有DNA样品浓度稀释到2 ng/μL用于PCR扩增。16S rRNA基因PCR扩增参照Wu等[20], 步骤如下: 25 μL反应体系中包含1×Buffer II, 正、反向引物(515F、806R)各0.8 μmol/L, 0.5U的AccuPrimeTM Taq酶和10 ng模板DNA序列, 每个样品平行做3个重复, 并设阴性对照; PCR扩增程序如下: 94℃ 1min, 后接10个循环(94℃ 20s, 53℃ 25s, 68℃ 45s)之后68℃ 10min。PCR产物经Agencourt Ampure XP纯化后再次作为模板进行第二次PCR扩增, 扩增条件和第一轮PCR一致, 但是所使用的反向引物加了barcode标记, 并进行20个循环, 此两步法PCR能很好地降低barcode引物的扩增偏好性[20]。最后, PCR产物用1%琼脂糖胶进行检测。在所有样品都成功扩增后, 各样品PCR产物用PicoGreen (Molecular Probes)进行定量。300 ng样品的PCR产物等量混合, 并用琼脂糖凝胶在90 V下电泳2h, 目的片段使用DNA纯化试剂盒(Qiagen)纯化后再次进行PicoGreen定量, 建库后使用MiSeq测序平台进行测序。所得到DNA序列分析参照Wu等[20]的方法进行分析, 并通过RDP (Ribosomal Database Project)数据库进行比对和OTU分类。
1.3 数据分析
分析过程使用R语言环境和PAST 2.0软件, 其中, R语言使用了vegan、VennDiagram、ggplot 2和ggfority程序包。进行的分析主要包括: (A)每个肠道样品做OTU稀释性曲线; (B)计算每个样品的Alpha多样性, 参数包括: 香农指数(Shannon-Wienner index)、辛普森指数(Inverse Simpson index)、皮鲁均匀度指数(Pielou evenness index)、辛普森均匀度指数(Simpson evenness index); (C)计算了Beta多样性, 包括非参数检验: 基于Bray-Curits距离的MRPP (Multiple-Response Permutation Procedure)、Anosim (Analysis of Similarity)、Adonis分析。同时也进行了主成分分析(Principal component analysis, PCA); (D)通过维恩图(Venn diagram)统计两组样品共有(shared)和特有(Unique)OTU; (E)用SPSS 24.0对实验组和对照组Alpha多样性指数进行独立样本t检验(Independent samples t-test)、对肠道菌群在处理组和对照组组内两两个体间距离均值进行威尔科克森检验(Wilcoxon test)以及对两组样品肠道优势OTU (relative abundance>1%)进行t检验(t-test)。
2. 结果
2.1 肠道菌群Alpha多样性分析
Alpha多样性分析结果表明, 除辛普森均匀度指数外, 感染组的香农指数、辛普森指数、皮鲁均匀度指数均显著低于对照组(t-test, P<0.05), 表明GCRV感染使草鱼肠道菌群的物种多样性和均匀度明显降低(图 1)。对每个样品进行OTU稀释性曲线的分析中, 也发现了相似的规律, 感染组样品OTU数普遍低于对照组(图 2)。
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图 2 处理组和对照组样品物种丰度的稀释曲线Figure 2. Rarefaction curves between treated and control groups based on sequencing results![]()
图 1 处理组(右边)和对照组(左边)草鱼肠道菌群Alpha多样性指数比较槽口图包括四分位间距(IQR), 第一、第三和第四分位数, 内侧粗线代表中位数; *表示显著性水平P<0.05, n.s.表示差异不显著Figure 1. Comparing alpha-diversity index between treated (right) and control (left) groupsThe notch boxes include the interquartile range (IQR), from the first, third and fourth quartiles, and the inside bold line represents the median. *indicate P<0.05, n.s., not significant2.2 肠道菌群Beta多样性分析
图 3显示对照组草鱼肠道内总共有646个OTUs, 而病毒处理组则检测到了498个OTUs, 相比对照组减少了148个OTUs。此外, 对照组中特有的OTUs为394个, 而GCRV感染后草鱼特有OTUs为246个; 2组草鱼共有OTUs数为252个。
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图 3 处理组和对照组OTU数量对比维恩图Figure 3. Venn diagram representing shared OTUs between treated and control groups对所有样品进行基于Bray-Curits距离的差异分析(表 1), 结果表明GCRV感染组草鱼和对照组草鱼肠道菌群差异显著(MRPP, Anosim, Adonis, P<0.01)。
表 1 基于Bray-Curits距离的差异显著性检验Table 1. Comparing the results of dissimilarity test between the treated and control groups based on Bray-Curtis dissimilarity指标
Item实验组 vs. 对照组
Treatment vs. ControlMRPP. Delta 0.527 MRPP. P-value 0.002** Anosim. R-value 0.192 Anosim. P-value 0.020** Adonis. F-value 2.976 Adonis. P-value 0.007** 注: ** 表示显著性水平P<0.01Note: The double asterisk indicates a significant difference withP<0.01 对所有草鱼样品肠道菌群进行PCA排序(图 4A), 对照组各样点聚集较为紧密, 说明肠道菌群在个体之间的差异较小。处理组草鱼各样点相距较远, 说明肠道菌群在个体之间的差异较大。此外, 第一轴(PC1)的解释变异量为63.73%, 第二轴(PC2)的解释变异量为21.67%, 2个轴解释变异量累计高达85.4%。对处理组和对照组肠道菌群在组内个体间Bray-Curtis距离进行比较, 发现肠道菌群在病毒感染组不同个体间的平均距离要显著高于对照组草鱼(Wilcoxon test, P<0.05,图 4B)。
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图 4 PCA排序图(A)及处理组和对照组(B)组内个体间距离差异比较* 表示显著性水平P<0.05Figure 4. Comparing beta-diversity index between the GCRV-infected and healthy grass carps A. The treated and control samples were visualized by PCA. B. Comparing Bray-Curtis dissimilarities between individuals in the GCRV-infected and control groups* indicate P<0.052.3 肠道菌群组成
在门水平进行分析比较发现(图 5), 对照组样品中共检测到18个菌门, 分别为脱铁杆菌门(Deferribacteres)、芽单胞菌门(Gemmatimonadetes)、装甲菌门(Armatimonadetes)、泉古菌门(Crenarchaeota)、衣原体门(Chlamydiae)、柔膜菌门(Tenericutes)、浮霉菌门(Planctomycetes)、绿弯菌门(Chloroflexi)、蓝藻门(Cyanobacteria)、疣微菌门(Verrucomicrobia)、酸杆菌门(Acidobacteria)、放线菌门(Actinobacteria)、螺旋体门(Spirochaetes)、拟杆菌门(Bacteroidetes)、厚壁菌门(Firmicutes)、变形菌门(Proteobacteria)、梭杆菌门(Fusobacteria)和其他未被分类的细菌。而实验组样品中则总共检测到15个菌门, 与对照组相比少了脱铁杆菌门、芽单胞菌门、装甲菌门、泉古菌门, 但新增了栖热菌门(Deinococcus-Thermus)。在所有的菌门中, 处理组与对照组共有优势菌门为变形菌门、梭杆菌门、厚壁菌门、拟杆菌门, 4个优势菌门在GCRV感染组和对照组草鱼肠道菌群中所占得比例分别为98.3%和97.4%。
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图 5 实验组与对照组肠道微生物在门水平相对丰度比较‘trt_’和‘ctr_’分别表示处理组、对照组, trt_和ctr_之后的数字表示样品编号Figure 5. Relative abundance of the phyla in the treated and control groups‘trt_’ and ‘ctr_’ represent treated and control grass carp, respectively. The numbers indicate sample ID将相对丰度大于1%的OTU进行比较发现, 对照组草鱼样品优势OTUs有17个, 而GCRV感染的草鱼样品优势OTUs有10个(表 2)。处理组草鱼肠道内OTU_504 (Comamonadaceae, 丛毛单胞菌科)、OTU_69 (Pasteurellaceae, 巴斯德氏菌科)、OTU_1898 (Cetobacteriu, 鲸杆菌属)和OTU_822 (Uliginosibacterium)相对丰度显著低于对照组(t-test, P<0.05)。OTU_504 (丛毛单胞菌科)在健康草鱼体内相对丰度为5.4%, 而在处理组草鱼肠道内则仅为1.5%。OTU_1898 (鲸杆菌属)和OTU_1357 (Gammaproteobacteria, γ变形菌纲)在对照组草鱼肠道样品的相对丰度分别为3.5%和10.5%, 而在处理组则下降为1.1%和8.8%。其他OTU感染GCRV后也有不同程度的下降, OTU_66 (Neisseriacea, 奈瑟氏球菌科)、OTU_98 (Shewanella, 希瓦氏菌属)、OTU_163 (Chitinophagaceae)、OTU_471 (Clostridiales, 梭菌目)和OTU_94 (Neisseriacea, 奈瑟氏球菌科)等在病毒处理组相对丰度降至1%以下。然而, 也有部分OTU相对丰度在感染GCRV后反而增加了, 其中增加幅度最为明显的是OTU_434 (Cetobacteriu, 鲸杆菌属), 该OTU的相对丰度在感染病毒的草鱼肠道内急剧上升, 由29.3%上升至46%。同样, OTU_1154 (Vibrionaceae, 弧菌科)上升幅度较大, 由1.5%增至12.3%。此外, 处理组中新增加一优势OTU, 即OTU_48 (Vibrio, 弧菌属)。OTU_893 (Aeromonas, 气单胞菌属)在两组肠道样品中相对丰度差别不大。
表 2 相对丰度大于1%的OTU对比分析Table 2. OTU with relative abundance greater than 1% in treated and control groups实验组Treatment 对照组Control 分类单元OTU 相对丰度Abundance (%) 分类Classification 分类单元OTU 相对丰度Abundance (%) 分类Classification OTU_434 46.0 Cetobacterium OTU_434 29.3 Cetobacterium OTU_1154 12.3 Vibrionaceae OTU_1357 10.5 Gammaproteobacteria OTU_1357 8.8 Gammaproteobacteria OTU_822* 5.4 Uliginosibacterium OTU_806 4.1 Leuconostoc OTU_504* 4.8 Comamonadaceae OTU_893 3.0 Aeromonas OTU_806 4.4 Leuconostoc OTU_48 2.0 Vibrio OTU_1898* 3.5 Cetobacterium OTU_504 1.5 Comamonadaceae OTU_893 3.1 Aeromonas OTU_1832 1.3 Lactococcus OTU_69* 2.8 Pasteurellaceae OTU_1898 1.1 Cetobacterium OTU_436 1.6 Neisseriaceae OTU_822 1.0 Uliginosibacterium OTU_1154 1.5 Vibrionaceae OTU_66 1.4 Neisseriaceae OTU_98 1.3 Shewanella OTU_163 1.2 Chitinophagaceae OTU_471 1.2 Clostridiales OTU_94 1.1 Neisseriaceae OTU_1832 1.0 Lactococcus OTU_26 1.0 Pelomonas 注: *显著性水平为P<0.05Note: * indicateP-values significant at 0.05 level 3. 讨论
鱼类肠道内定植着种类丰富、数量庞大的菌群[21, 22]。在正常情况下, 肠道菌群之间、菌群与宿主之间处于动态平衡, 从而维持着鱼类肠道正常生理功能[5]。但当受到病原微生物感染时, 肠道菌群的平衡状态受到干扰后可能被打破[11, 12]。肠道菌群结构失衡可能使得宿主的免疫系统受到影响, 某些条件致病菌还有可能会转移或危及宿主其他组织器官, 导致细菌性疾病爆发[23, 24]。因此, 肠道微生态的相对稳定对于宿主的健康有着重要的意义。
中国水产养殖占世界水产养殖总量的近70%[25], 其中草鱼是我国最重要的淡水养殖鱼类。在草鱼养殖常见的疾病中, 草鱼呼肠孤病毒导致的出血病常常给养殖业造成了严重的经济损失。感染该病毒的草鱼, 其肠腔内黏液减少, 上皮细胞大量坏死脱落[15], 肠道微生态环境的急剧恶化, 因此肠道菌群很有可能失去原有的平衡状态而变得紊乱。虽然以往的研究表明病原感染可引起水生动物肠道群菌紊乱[11, 26], 但GCRV感染对草鱼肠道菌群的影响尚不清楚。
本研究利用MiSeq高通量测序研究了GCRV感染对草鱼肠道菌群的影响, 结果表明GCRV感染使得草鱼肠道的微生物群落结构发生了显著变化(MRPP, Anosim, Adonis, P<0.01), 李东亮等[27]用嗜水气单胞菌(Aeromonas hydrophila)感染草鱼得到类似的结果。肠道作为一个小型生态系统, 众多的微生物栖息于此并形成复杂的生态群落[28]。肠道正常菌群及肠道生态系统的稳定性与肠道功能密切相关[29]。本研究发现, GCRV感染组草鱼肠道菌群Alpha多样性显著低于对照组草鱼(Independent samples t-test, P<0.05), 说明肠道微生态系统发生了紊乱。在正常情况下, 肠道正常菌群牢固地附着于肠黏膜和肠上皮细胞表面。但感染GCRV后, 其肠腔内黏液减少、上皮细胞成片脱落[15], 正常菌群因失去附着位点而极易随排泄物排出体外。此外, 发生肠炎的草鱼摄食减弱, 导致肠道正常菌群赖以生存的资源减少, 也可能是部分肠道正常菌群数量减少的原因之一[30]。
已有基于DGGE[19]、纯培养[16]和高通量测序[31, 32]的结果表明, Proteobacteria、Firmicutes、Bacteroidetes、Fusobacteria为草鱼肠道的主要类群, 本研究结果与之相符。然而与健康草鱼相比, 感染GCRV的草鱼肠道内Proteobacteria、Firmicutes、Bacteroidetes相对丰度均有不同程度的下降, 而Fusobacteria则有较大幅度增加。其他非优势菌门如Deferribacteres、Gemmatimonadetes、Armatimonadetes、Crenarchaeota在病毒感染组中消失。这些变化, 一方面, 可能与患病草鱼摄食减少导致肠道中可利用的资源减少有关[33]。另一方面, 可能与感染病毒后肠道微生态环境恶化存在关联[15]。此外, 有研究表明免疫系统对肠道菌群有着重要的影响[34, 35]。而GCRV对草鱼免疫系统有着重要的影响[36], 因此, GCRV病毒也有可能通过干扰草鱼免疫系统间接影响肠道菌群组成, 但还有待进一步证实。
研究表明感染GCRV的草鱼肠上皮细胞会大量脱落[15], OTU_434相对丰度在感染组明显升高, 该OTU在Cetobacteriu丰度占比极高(96%) , 可能与Cetobacteriu能合成的维生素B12 (Vitamin B12)促进肠道细胞修复有关[36, 37]。感染GCRV后OTU_98 (Shewanella)在肠道中相对丰度有所下降。有研究表明饥饿能够改变肠道菌群[38, 39]。在本实验中, Shewanella(OTU_98)相对丰度降低可能与患病草鱼摄食减少, 肠道营养贫乏有关[40]。
综上所述, GCRV感染会导致草鱼肠道正常菌群紊乱。肠道菌群发生紊乱往往伴随着致病菌过度增殖, 引起肠道微生态失衡和机体的炎症反应, 导致疾病的发生或病情的加重[41]。健康宿主肠道微生物可通过与致病菌竞争黏附位点、介导调节肠道免疫应答等方式抑制病原菌的增殖, 来缓解或防止肠道炎症[5]。因此, 如果能从草鱼肠道内分离出这些有益微生物并制成微生态制剂投喂草鱼, 或许能使已发生紊乱的肠道菌群恢复至正常状态, 从而为缓解或防止草鱼出血病提供帮助。本研究从草鱼肠道菌群入手, 能为草鱼病毒性出血病的防治和深化研究提供依据和参考。
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图 1 长江中下游通江湖泊与阻隔湖泊物种数、Δ+和Λ+对比及t检验
Figure 1. Species richness, Δ+ and Λ+ of the river -connected lakes and river -disconnected lakes in the middle and lower reaches of Yangtze River; the result of independent-samples t-test are also shown
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图 2 长江中下游湖泊Δ+和Λ+对应物种数的95%置信区间漏斗图
Figure 2. Funnel plots showing Δ+ and Λ+ versus the number of species observed for the fish fauna in the freshwater lake in the middle and lower reaches of Yangtze River; the lines showing mean value and 95% confidence intervals are determined via random selection from the total master species lists
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图 3 鄱阳湖、洞庭湖平均分类差异指数(Δ+)和分类差异变异指数(Λ+)随时间变化图
Figure 3. Temporal variations in average taxonomic distinctness index, Δ+ and variation in taxonomic distinctness index, Λ+ of fish assemblages in Poyang Lake and Dongting Lake
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图 4 鄱阳湖、洞庭湖不同时期Δ+和Λ+对应物种数的95%置信区间漏斗图
A、B. 鄱阳湖; C、D. 洞庭湖
Figure 4. Funnel plots showing Δ+ and Λ+ versus the number of species observed for the fish fauna in Poyang Lake and Dongting Lake in different periods; the lines showing mean value and 95% confidence intervals were determined via random selection from the total master species lists
A and B. Poyang Lake; C and D. Dongting Lake
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图 5 梁子湖、洪泽湖、洪湖平均分类差异指数(Δ+)和分类差异变异指数(Λ+)随时间变化图
Figure 5. Temporal variations in average taxonomic distinctness index, Δ+ and variation in taxonomic distinctness index, Λ+ of fish assemblages in Liangzi Lake, Hongze Lake and Honghu Lake
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图 6 梁子湖、洪泽湖、洪湖不同时期Δ+和Λ+对应物种数的95%置信区间漏斗图
A、B. 梁子湖; C、D. 洪泽湖; E、F. 洪湖
Figure 6. Funnel plots showing Δ+ and Λ+ versus the number of species observed for the fish fauna in Liangzi Lake, Hongze Lake and Honghu Lake in different periods. The lines showing mean value and 95% confidence intervals are determined via random selection from the total master species lists
A and B. Liangzi Lake; C and D. Hongze Lake; E and F. Honghu Lake
表 1 长江中下游湖泊调查时间及江湖连通状况
Table 1 Investigation time and connected or disconnected status of lakes in the middle and lower reaches of Yangtze River
湖泊
Lake调查时间
Year of survey湖泊类型
Status of lake湖泊
Lake调查时间
Year of survey湖泊类型
Status of lake通江湖泊 五湖[75] 1974—1975 Connected 鄱阳湖1[46] 1980s Connected 保安湖[67] 1992—1994 Disconnected 鄱阳湖2[47] 1982—1990 Connected 澄湖[68] 2002—2003 Disconnected 鄱阳湖3[47] 1997—2000 Connected 东湖[69] 1992—1994 Disconnected 洞庭湖1[48] 1973—1979 Connected 北青菱湖[67] 1993—1996 Disconnected 洞庭湖2[49] 2002—2003 Connected 桥墩湖[67] 1993—1996 Disconnected 洞庭湖3[49] 2012—2014 Connected 扁担塘[70] 1993—1996 Disconnected 阻隔湖泊(历史通江湖泊) 牛山湖[71] 1996—1999 Disconnected 洪泽湖1[50] 1960—1982 Connected 东汤逊湖[71] 1996—1999 Disconnected 洪泽湖2[51] 1989—1990 Disconnected 黄湖[71] 1996—1999 Disconnected 洪泽湖3[52] 2010—2011 Disconnected 龙感湖[71] 1996—1999 Disconnected 洪泽湖4[53] 2014 Disconnected 固城湖[58] 1987—1988 Disconnected 洪泽湖5[54] 2017—2018 Disconnected 长湖[72] 2014 Disconnected 梁子湖1[55] 1955—1957 Connected 菜子湖[73] 2018 Disconnected 梁子湖2[55] 1974 Disconnected 陈瑶湖[74] 2000—2001 Disconnected 梁子湖3[55] 1981—1983 Disconnected 天鹅洲[66] 2015—2016 Disconnected 梁子湖4[55] 1997—1999 Disconnected 武昌湖[74] 2000—2001 Disconnected 洪湖1[56] 1959 Disconnected 白荡湖[74] 2000—2001 Disconnected 洪湖2[56] 1964 Disconnected 泊湖[74] 2000—2001 Disconnected 洪湖3[56] 1981 Disconnected 淀山湖[76] 2011 Disconnected 洪湖4[56] 1993 Disconnected 骆马湖[77] 2013—2015 Disconnected 洪湖5[57] 2004 Disconnected 滆湖[78] 2008 Disconnected 通江湖泊与阻隔湖泊比较 傀儡湖[79] 2010 Disconnected 鄱阳湖3[47] 1997—2000 Connected 何王庙[80] 2016 Disconnected 洞庭湖3[49] 2012—2014 Connected 武湖[81] 2006—2007 Disconnected 洪泽湖1[50] 1960—1982 Connected 大通湖[82] 2011—2012 Disconnected 洪泽湖5[54] 2017—2018 Disconnected 南湖 2020 Disconnected 梁子湖1[55] 1955—1957 Connected 洋圻湖[83] 1998 Disconnected 梁子湖4[55] 1997—1999 Disconnected 军山湖[84] 1993—1994 Disconnected 太湖1[58] 1951—1985 Connected 青岚湖[84] 1993—1994 Disconnected 太湖2[59, 60] 2002—2003 Disconnected 陈家湖[84] 1993—1994 Disconnected 巢湖1[61] 1959—1963 Connected 瑶岗湖[84] 1993—1994 Disconnected 巢湖2[62] 2002—2004 Disconnected 观溪湖[84] 1993—1994 Disconnected 五里湖1[63] 1950—1953 Connected 龙窝湖[85] 1979—1980 Disconnected 五里湖2[64] 2007—2008 Disconnected 黄大湖[74] 2000—2001 Disconnected 涨渡湖1[65] 1950s Connected 南青菱湖[67] 1993—1996 Disconnected 涨渡湖2[65] 2000s Disconnected 黄家湖[67] 1993—1996 Disconnected 洪湖5[57] 2004 Disconnected 
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附表 1 长江中下游湖泊鱼类主名录分类学组成
Appendix 1 Fish species composition in lakes in the middle and lower reaches of the Yangtze River
目Order 科Family 属Genus 种Species 拉丁名Latin name 鲟形目 鲟科 鲟属 中华鲟 Acipenser sinensis 匙吻鲟科 白鲟属 白鲟 Psephurus gladius 鲱形目 鳀科 鲚属 刀鲚 Coilia nasus 短颌鲚 Coilia brachygnathus 胡瓜鱼目 银鱼科 银鱼属 前额间银鱼 Salanx prognathus 大银鱼属 大银鱼 Protosalanx chinensis 间银鱼属 短吻间银鱼 Hemisalanx brachyrostralis 新银鱼属 寡齿新银鱼 Neosalanx oligodontis 太湖新银鱼 Neosalanx taihuensis 陈氏新银鱼 Neosalanx tangkahkeii 乔氏新银鱼 Neosalanx jordani 鳗鲡目 鳗鲡科 鳗鲡属 鳗鲡 Anguilla japonica 鲤形目 鲤科 鱲属 宽鳍鱲 Zacco platypus 马口鱼属 马口鱼 Opsariichthys bidens 鱥属 尖头鱥 Rhynchocypris oxycephalus 赤眼鳟属 赤眼鳟 Squaliobarbus curriculus 青鱼属 青鱼 Mylopharyngodon piceus 草鱼属 草鱼 Ctenopharyngodon idella 鳤属 鳤 Ochetobius elongatus 鳡属 鳡 Elopichthys bambusa 飘鱼属 飘鱼 Pseudolaubuca sinensis 寡鳞飘鱼 Pseudolaubuca engraulis 䱗属 䱗 Hemiculter leucisculus 贝氏䱗 Hemiculter bleekeri 似鱎属 似鱎 Toxabramis swinhonis 原鲌属 红鳍原鲌 Chanodichthys erythropterus 鲌属 拟尖头鲌 Culter oxycephaloides 翘嘴鲌 Culter alburnus 蒙古鲌 Culter mongolicus 达氏鲌 Culter dabryi 鳊属 鳊 Parabramis pekinensis 华鳊属 伍氏华鳊 Sinibrama wui 鲂属 鲂 Megalobrama skolkovii 团头鲂 Megalobrama amblycephala 鲴属 银鲴 Xenocypris macrolepis 黄尾鲴 Xenocypris davidi 细鳞鲴 Xenocypris microlepis 圆吻鲴属 圆吻鲴 Distoechodon tumirostris 湖北圆吻鲴 Distoechodon hupeinensis 似鳊属 似鳊 Pseudobrama simoni 鲢属 鲢 Hypophthalmichthys molitrix 鳙 Hypophthalmichthys nobilis 䱻属 唇䱻 Hemibarbus labeo 花䱻 Hemibarbus maculatus 似刺鳊 属 似刺鳊 Paracanthobrama guichenoti 麦穗鱼属 麦穗鱼 Pseudorasbora parva 长麦穗鱼 Pseudorasbora elongata 鳈属 华鳈 Sarcocheilichthys sinensis 小鳈 Sarcocheilichthys parvus 江西鳈 Sarcocheilichthys kiangsiensis 黑鳍鳈 Sarcocheilichthys nigripinnis 颌须属 短须颌须 Gnathopogon imberbis 银属 银 Squalidus argentatus 亮银 Squalidus nitens 点纹银 Squalidus wolterstorffi 铜鱼属 圆口铜鱼 Coreius guichenoti 铜鱼 Coreius heterodon 吻属 吻 Rhinogobio typus 圆筒吻 Rhinogobio cylindricus 似属 似 Pseudogobio vaillanti 棒花鱼属 棒花鱼 Abbottina rivularis 小鳔属 福建小鳔 Microphysogobio fukiensis 乐山小鳔 Microphysogobio kiatingensis 小口小鳔 Microphysogobio brevirostris 洞庭小鳔 Microphysogobio tungtingensis 蛇属 长蛇 Saurogobio dumerili 蛇 Saurogobio dabryi 光唇蛇 Saurogobio gymnocheilus 细尾蛇 Saurogobio gracilicaudatus 鳅鮀属 宜昌鳅鮀 Gobiobotia filifer 鱊属 大鳍鱊 Acheilognathus macropterus 越南鱊 Acheilognathus barbatus 须鱊 Acheilognathus barbatus 短须鱊 Acheilognathus barbatulus 无须鱊 Acheilognathus gracilis 兴凯鱊 Acheilognathus chankaensis 大口鱊 Acheilognathus tabira 多鳞鱊 Acheilognathus polylepis 白河鱊 Acheilognathus peihoensis 彩副鱊 Acheilognathus imberbis 田中鳑鲏属 革条田中鳑鲏 Tanakia himantegus 鳑鲏属 高体鳑鲏 Rhodeus ocellatus 中华鳑鲏 Rhodeus sinensis 方氏鳑鲏 Rhodeus fangi 倒刺鲃属 中华倒刺鲃 Spinibarbus sinensis 光倒刺鲃 Spinibarbus hollandi 华鲮属 湘华鲮 Bangana tungting 光唇鱼属 光唇鱼 Acrossocheilus fasciatus 白甲鱼属 白甲鱼 Onychostoma simum 鲤属 鲤 Cyprinus carpio 鲫属 鲫 Carassius auratus 细鲫属 中华细鲫 Aphyocypris chinensis 胭脂鱼科 胭脂鱼属 胭脂鱼 Myxocyprinus asiaticus 平鳍鳅科 犁头鳅属 犁头鳅 Lepturichthys fimbriata 后平鳅属 峨嵋后平鳅 Metahomaloptera omeiensis 鳅科 副沙鳅属 花斑副沙鳅 Parabotia fasciata 武昌副沙鳅 Parabotia banarescui 薄鳅属 长薄鳅 Leptobotia elongata 红唇薄鳅 Leptobotia rubrilabris 紫薄鳅 Leptobotia taeniops 花鳅属 中华沙鳅 Sinibotia superciliaris 泥鳅属 泥鳅 Misgurnus anguillicaudatus 鳅属 中华花鳅 Cobitis sinensis 大斑花鳅 Cobitis macrostigma 副泥鳅属 大鳞副泥鳅 Paramisgurnus dabryanus 鲇形目 鲇科 鲇属 鲇 Silurus asotus 南方鲇 Silurus meridionalis 胡子鲇科 胡子鲇属 胡子鲇 Clarias fuscus 鲿科 黄颡鱼属 黄颡鱼 Pelteobagrus fulvidraco 长须黄颡鱼 Pelteobagrus eupogon 瓦氏黄颡鱼 Pelteobagrus vachellii 光泽黄颡鱼 Pelteobagrus nitidus 属 纵带 Leiocassis argentivittatus 长吻 Leiocassis longirostris 粗唇 Leiocassis crassilabris 拟鲿属 白边拟鲿 Pseudobagrus albomarginatus 圆尾拟鲿 Pseudobagrus tenuis 细体拟鲿 Pseudobagrus pratti 切尾拟鲿 Pseudobagrus truncatus 乌苏拟鲿 Pseudobagrus ussuriensis 鳠属 大鳍鳠 Mystus macropterus 钝头科 䱀属 黑尾䱀 Liobagrus nigricauda 白缘䱀 Liobagrus marginatus 司氏䱀 Liobagrus styani 鳗尾䱀 Liobagrus anguillicauda 拟缘䱀 Liobagrus marginatoides 科 纹胸属 中华纹胸 Glyptothorax sinensis 颌针鱼目 青鳉科 青鳉属 青鳉 Oryzias latipes 鱵科 下鱵属 间下鱵 Hyporhamphus intermedius 合鳃目 刺鳅科 刺楸属 刺鳅 Macrognathus aculeatus 中华刺鳅属 中华刺鳅 Sinobdella sinensis 合鳃鱼科 黄鳝属 黄鳝 Monopterus albus 鲈形目 鮨科 鳜属 鳜 Siniperca chuatsi 长身鳜 Siniperca roulei 大眼鳜 Siniperca knerii 斑鳜 Siniperca scherzeri 波纹鳜 Siniperca undulata 沙塘鳢科 黄䱂鱼属 小黄䱂鱼 Micropercops swinhonis 沙塘鳢属 河川沙塘鳢 Odontobutis potamophila 鰕虎鱼科 鲻鰕虎鱼属 粘皮鲻鰕虎鱼 Mugilogobius myxodermus 吻鰕虎鱼属 子陵吻虾虎鱼 Rhinogobius giurinus 波氏吻鰕虎鱼 Rhinogobius cliffordpopei 褐吻鰕虎鱼 Rhinogobius Brunneus 鳗鰕虎鱼属 须鳗虾虎鱼 Taenioides cirratus 狼鰕虎鱼属 红狼牙鰕虎鱼 Odontamblyopus rubicundus 拉氏狼牙鰕虎鱼 Odontamblyopus lacepedii 缟鰕虎鱼属 纹缟鰕虎鱼 Tridentiger trigonocephalus 丝足鲈科 斗鱼属 圆尾斗鱼 Macropodus chinensis 叉尾斗鱼 Macropodus opercularis 鳢科 鳢属 乌鳢 Channa argus 月鳢 Channa asiatica 鲽形目 舌鳎科 舌鳎属 三线舌鳎 Cynoglossus trigrammus 窄体舌鳎 Cynoglossus gracilis 鲀形目 鲀科 东方鲀属 弓斑多纪鲀 Takifugu ocellatus 暗纹东方鲀 Takifugu obscurus
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表 2 鄱阳湖、洞庭湖3个时期的鱼类分类阶元数目、Δ+和Λ+
Table 2 Number of taxa at each taxonomic resolution level of fishes, Δ+ and Λ+ in Poyang Lake and Dongting Lake for the three time periods
湖泊
Lake调查时间
Year of survey目
Order科
Family属
Genus种
SpeciesΔ+ Λ+ 鄱阳湖1 1980s 11 23 67 108 80.12 674.00 鄱阳湖2 1982—1990 10 22 64 100 79.61 676.93 鄱阳湖3 1997—2000 8 19 60 98 78.50 709.44 洞庭湖1 1973—1979 10 22 68 104 77.46 675.93 洞庭湖2 2002—2003 7 14 53 81 76.88 719.80 洞庭湖3 2012—2014 7 16 46 64 76.79 686.38
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表 3 梁子湖、洪泽湖、洪湖不同时期鱼类分类阶元数目、Δ+和Λ+
Table 3 Number of taxa at each taxonomic resolution level of fishes, Δ+ and Λ+ in Liangzi Lake, Hongze Lake and Honghu Lake in different periods
湖泊
Lake调查时间
Year of survey目
Order科
Family属
Genus种
SpeciesΔ+ Λ+ 梁子湖1 1955—1957 9 17 47 59 77.99 728.20 梁子湖2 1974 9 18 49 67 77.14 730.12 梁子湖3 1981—1983 7 14 42 56 74.06 754.18 梁子湖4 1997—1999 8 16 41 56 76.63 738.59 洪泽湖1 1960—1982 9 17 57 77 78.73 685.37 洪泽湖2 1989—1990 8 16 49 65 74.57 720.42 洪泽湖3 2010—2011 7 14 43 62 74.06 766.45 洪泽湖4 2014 7 13 34 41 77.09 748.61 洪泽湖5 2017—2018 8 15 40 50 76.76 747.85 洪湖1 1959 9 18 51 62 77.65 698.74 洪湖2 1964 9 18 53 71 77.84 708.10 洪湖3 1981 9 18 43 52 78.64 673.44 洪湖4 1993 7 15 43 56 74.41 755.00 洪湖5 2004 6 11 33 42 72.31 751.28
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