Seasonal effects on bacterial community between intestine of Collichthys lucidus and water environment from Pearl River Estuary
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摘要:
棘头梅童鱼 (Collichthys lucidus) 是珠江口常见的优势种和经济鱼类物种。为揭示棘头梅童鱼的生物生态学特征,利用16S rRNA基因的高通量测序技术,探究了季节变化对珠江口棘头梅童鱼肠道和水体中细菌群落结构的影响。结果表明,鱼类肠道细菌以变形菌门居多 (78.89%),其次为厚壁菌门 (6.70%) 和拟杆菌门 (5.45%);水体细菌以变形菌门 (40.32%) 和拟杆菌门 (37.97%) 为主。棘头梅童鱼肠道中的优势菌属存在明显季节变化,春、夏季鱼类肠道中优势细菌为嗜冷杆菌 (Psychrobacter),秋季为发光杆菌 (Photobacterium),而冬季为假单胞菌(Pseudomonas)、Sva0996_marine_group、弧菌 (Vibrio)和甲基杆菌 (Methylobacterium)。冬季棘头梅童鱼肠道菌群的α多样性指数最高,秋季最低。春季和夏季鱼类肠道细菌组成无显著性差异 (p>0.05),而其余季节间存在显著性差异 (p<0.05)。水体细菌群落组成的季节变化与鱼类肠道菌群变化相似。水环境中黄杆菌 (Tenacibaculum)、嗜冷杆菌 (Psychrobacter)、Candidatus_Actinomarina、Salinimonas和OM60NOR5_clade共5个菌属与鱼类肠道细菌组成之间存在显著相关性 (r>0.4, p<0.01)。细菌共现网络分析显示冬季鱼类肠道和水环境的共有菌群比例最低,而夏季最高。研究表明,季节变化对珠江口棘头梅童鱼的肠道菌群和水体细菌群落组成均存在影响。
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关键词:
- 棘头梅童鱼 /
- 肠道菌群 /
- 共现网络 /
- 16S rRNA基因 /
- 珠江口
Abstract:Collichthys lucidus is a common dominant and economically important fish species in the Pearl River Estuary. To reveal the ecological characteristics of C. lucidus, we applied high-throughput sequencing technology of 16S rRNA gene to investigate the effects of seasonal changes on the bacterial community structure in the intestines and water body of the Pearl River Estuary. The bacterial community in the fish intestines was predominantly composed of members of Proteobacteria (78.89%), followed by Firmicutes (6.70%) and Bacteroidota (5.45%), while Proteobacteria (40.32%) and Bacteroidota (37.97%) dominated the surrounding water. Besides, we observed the seasonal changes in the dominant bacterial genera in the intestine of C. lucidus. The relative abundance of Psychrobacter was significantly higher in spring and summer, whereas Photobacterium predominated in autumn. However, Pseudomonas, Sva0996 marine group, Vibrio and Methylobacterium were more abundant in winter. The α-diversity index values of the intestinal bacteria of C. lucidus were highest in winter but lowest in autumn. PCoA and ANOSIM analyses reveal no significant differences in the intestinal bacterial composition between spring and summer (p>0.05), whereas significant differences were observed in the other seasons (p<0.05). The seasonal changes in the bacterial composition of surrounding water were similar to those in the fish intestinal bacteria. Mantel test analysis finds out that five bacterial genera (Tenacibaculum, Psychrobacter, Candidatus_Actinomarina, Salinimonas, OM60NOR5_clade) in water environment showed a significantly positive correlation with the intestinal bacteria of C. lucidus (r>0.4, p<0.01). Bacterial co-occurrence network analysis shows that the proportion of shared bacterial communities between the fish intestines and the water environment was lowest in winter but highest in summer. The results indicate that seasonal changes can impact both the intestinal bacterial communities of C. lucidus from the Pearl River Estuary and bacterial communities in water body.
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近年来,由于持续的过度捕捞和环境污染使得澄海莱芜海域渔业资源衰退、海洋环境恶化。人工鱼礁是人为设置在海中的构造物,可为海底生物提供一个人工的栖息场所,为鱼类等水生生物的生长、繁育营造适宜的环境,达到修复海洋生态环境、增殖和养护渔业资源的目的。建设人工鱼礁是修复海洋生态环境和恢复渔业资源的重要措施之一。
澄海莱芜人工鱼礁区位于广东省汕头市东部莱芜半岛东南约2 n mile的海域,礁区东南方面向广阔的南海,东北方毗连南澳岛,西南方为达濠岛和汕头港。礁区底质坚实,以沙、沙泥为主。礁区水深在6~9 m之间,礁区内有水深小于5 m的浅滩,礁区的西南方至正北方,分布有多个港口和多条入海河流。该礁区于2004年完成了人工鱼礁建设。
2003年5月和2007年8月分别进行了澄海莱芜人工鱼礁区投礁前的本底调查和投礁后的跟踪调查,文章根据2次调查结果初步评估了人工鱼礁建设的集鱼效果,以期为该礁区的科学管理和进一步建设提供依据,为广东省乃至全国人工鱼礁的建设和研究提供参考资料。
1. 材料与方法
1.1 调查时间和调查站位
本底调查和跟踪调查均设礁区站和对比站2个调查站位。投礁前的本底调查于2003年5月6日进行,在礁区的中心位置设置礁区站,在距礁区边缘2~3 n mile的海域设置对比区站。投礁后的跟踪调查于2007年8月24日进行,由于投礁后礁区中心不能拖网,紧贴礁区边设一站位作为礁区站,对比区站的位置同本底调查。
1.2 调查网具和调查方法
本底调查租用主机功率为36 kW的“粤澄海91202”虾拖船进行,调查使用的网具为虾拖网,网口宽度为12 m,网全长20 m,袖网网目为60 mm,网囊网目为20 mm。跟踪调查租用主机功率为48 kW的“粤澄海91204”虾拖船进行,调查使用的网具为虾拖网,网口宽度为8 m,网全长35 m,袖网网目为60 mm,网囊网目为20 mm。
本底调查和跟踪调查,均在礁区站和对比区站进行拖网试捕,每站拖15 min,拖速约为3 kn。
1.3 渔获处理和结果统计方法
游泳生物的采样和分析均按《海洋监测规范》(GB17378-1998)和《海洋调查规范-海洋生物调查》(GB12763.6-91)中规定的方法进行。现场对全部渔获物进行种类鉴定和计量。
采用资源密度指数(D)[1]、Margalef种类丰度指数(R)和Shannon-Winener多样性指数(H′)来研究生物群落多样性[2-6]。
游泳生物资源密度指数(D)采用底拖网扫海面积法[7-9]估算。计算公式为:
$$ D=\frac{y}{v l} \cdot \frac{1}{(1-E)} $$ (1) 式中y为拖网渔获率;v为平均拖速;l为网口宽度;E为逃逸率(取0.5)。
Margalef种类丰富度指数计算公式为:
$$ R=(S-1) / \ln N $$ (2) Shannon-Winener多样性指数计算公式为:
$$ H^{\prime}=-\sum\limits_{i=1}^S P_i \ln P_i $$ (3) 生产效益估算公式为:
$$ Y_v=\sum\limits_{i=1}^S V_i D $$ (4) (2) ~ (4)式中,S为各站的总渔获种数,N为各站总渔获尾数,Pi为第i种渔获尾数占该站总渔获尾数的比例,Vi为第i种种类在跟踪调查时的市场价格。
2. 结果
2.1 资源密度变动情况
调查结果显示,投礁后礁区海域各类资源的资源密度都显著比投礁前高,总资源密度由111.16 kg · km-2增加到2 960.359 kg · km-2(表 1),增加了25.63倍。其中,蟹类、虾类、鱼类、虾蛄类和头足类分别比投礁前增加了77.09、44.88、16.75、5.42和4.70倍。在跟踪调查中,蟹类资源密度增加最显著,并且多数蟹种在本底调查中未曾出现。在本底调查和跟踪调查中,同时出现的游泳生物种类为9种,其资源密度在跟踪调查时均有较大增幅,其中口虾蛄增幅最大,比投礁前约增加了144倍。
表 1 礁区及对比区游泳生物各类群渔获资源密度Table 1 Biomass density of nekton groups in artificial reefs area and control area in background and tracking survey调查时间
survey time调查站位
survey stations资源密度/kg·km-2 biomass density 鱼类
fish蟹类
crab虾蛄类
squilla头足类
cephalopod虾类
shrimp合计
total本底调查
background survey礁区 artificial reefs area 51.160 20.944 19.744 14.835 4.472 111.155 对比区 control area 51.093 41.919 51.441 11.844 2.206 158.503 跟踪调查
tracking survey礁区 artificial reefs area 908.327 1 635.469 126.790 84.593 205.180 2 960.359 对比区 control area 940.507 343.609 289.286 36.652 141.700 1 751.754 投礁后对比区海域各类游泳生物的资源密度同样都比投礁前有显著增加,但增加的幅度不如礁区海域,总资源密度由158.503 kg · km-2增加到1 751.754 kg · km-2,增加了10.05倍。其中虾类资源密度增加最显著,由2.206 kg · km-2增加到141.700 kg · km-2,增加了63.23倍。
投礁前礁区海域游泳生物资源密度低于对比区,投礁后礁区海域游泳生物资源密度为2 960.359 kg · km-2,比同期对比区增加了0.69倍。
综上所述,投礁后该礁区海域各生物种类资源密度增加显著,显示出明显的集鱼效果。
2.2 总渔获种类变动情况
2003年本底调查,整个调查海域出现游泳生物10目26科50种。其中鱼类6目17科26种,虾类1目2科7种,蟹类4科10种,虾蛄类1目1科4种,头足类2目2科3种。
2007年跟踪调查,整个调查海域出现游泳生物14目34科63种。其中鱼类8目21科29种,虾类2目4科16种,蟹类5科12种,虾蛄类1目1科3种,头足类3目3科3种。
在礁区海域,投礁后各类资源种类均比投礁前丰富,总种类数由投礁前的23种增加至41种,比投礁前本底调查增加了0.78倍。其中,蟹类增加最多,由投礁前的4种增加至11种,增加了1.75倍;虾类由投礁前的3种增加至8种,增加了1.67倍;虾蛄类和头足类增幅较小。
对比区海域,投礁后游泳生物的总种类也比投礁前丰富,但增幅不如礁区海域明显。总种类数由投礁前的23种增加至32种,比投礁前本底调查增加了0.39倍。其中虾类增加明显,由投礁前的3种增加至10种,增加了2.33倍;鱼类由8种增加至13种,增加了0.63倍。
投礁前,礁区和对比区总种类数相同,投礁后,礁区种类比对比区丰富,增加了0.28倍(表 2)。尤其是蟹类种类丰富多样,比同期调查对比区增加了0.83倍。
表 2 本底调查和跟踪调查时礁区及对比区游泳生物各类群渔获种数Table 2 Number of species caught in artificial reefs area and control area in background and tracking survey调查时间
survey time调查站位
survey stations渔获种数 species number 鱼类
fish蟹类
crab虾蛄类
squilla头足类
cephalopod虾类
shrimp合计
total本底调查
background survey礁区 artificial reefs area 12 4 2 2 3 23 对比区 control area 8 6 3 3 3 23 跟踪调查
tracking survey礁区 artificial reefs area 17 11 2 3 8 41 对比区 control area 13 6 2 1 10 32 在礁区海域,投礁前和投礁后出现的相同种类数为9种(表 3),投礁后新出现的种类数为32种,其中鱼类和蟹类的种类数增加明显,分别增加了14种和8种。
表 3 投礁后礁区游泳生物各类群种数增加情况Table 3 Increment of species number caught in artificial reefs area in tracking survey项目
item渔获种数 species number 鱼类
fish蟹类
crab虾蛄类
squilla头足类
cephalopod虾类
shrimp合计
total跟踪调查时新增的种类
new species occured in tracking survey14 8 1 2 7 32 本底调查和跟踪调查出现的相同种类
the species occurred in both background and tracking survey3 3 1 1 1 9 仅在本底调查时出现的种类
species only occurred in tracking survey9 1 1 1 2 14 莱芜礁区及邻近海域游泳生物种类分布的上述变化情况表明,礁体投放后,礁区海域新型的人工生境已初步形成,对游泳生物(特别是鱼类和虾蟹类)显示出了明显的诱集效果。
2.3 优势种变动情况
投礁前和投礁后,礁区和对比区游泳生物的优势类群和主要优势种都发生了明显的变化,投礁前礁区主要优势类群为虾蛄类、鱼类、蟹类和头足类,断脊口虾蛄Oratosquilla interrupa的资源密度为19.089 kg · km-2(表 4),为第一优势种,对比区主要优势类群为虾蛄类、鱼类和蟹类,口虾蛄的资源密度为27.869 kg · km-2,为第一优势种。
表 4 本底调查和跟踪调查时礁区及对比区游泳生物主要优势种及资源密度Table 4 The dominant species and biomass density in artificial reefs area and control area in background and tracking survey调查时间
survey time调查站位
survey stations主要优势种及资源密度/kg·km-2
dominant species and biomass density本底调查background survey 礁区
artificial reefs area断脊口虾蛄
Oratosquilla interrupa鹿斑鲾
Leiognathus ruconius三疣梭子蟹
Portunus trituberculatus杜氏枪乌贼
Loligo duvaucelii Orbigny短吻鲾
Leiognathus brevirostris19.089 16.580 13.090 11.999 8.945 对比区
control area口虾蛄
O.oratoria银牙NFDAB
Otolithes argenteus断脊口虾蛄
O.interrupa阿氏强蟹
Eucrate alcocki Serene银鲳
Pampus argenteus27.869 26.708 17.418 14.515 10.683 跟踪调查
tracking survey礁区
artificial reefs area鳞斑蟹
Demania scaberrima龙头鱼
Harpodon nehereus红星梭子蟹
P.sanguinolentus疣面关公蟹
Dorippe frascone纤手梭子蟹
P.gracilimanus459.963 345.172 344.372 255.980 201.584 对比区control area 白姑鱼
Argyrosomus argentatus叫姑鱼
Johnius dussumieri口虾蛄
O.oratoria疣面关公蟹
D.frascone龙头鱼
H.nehereus379.606 261.797 248.707 163.623 128.281 投礁后,礁区主要优势类群为蟹类和鱼类,5个优势种中有4个种是蟹类,蟹类成为绝对优势种。鳞斑蟹Demania scaberrima、龙头鱼Harpodon nehereus和红星梭子蟹Portunus sanguinolentus为礁区新增优势种,在本底调查中未曾出现,这说明礁体可以把礁区邻近海域的游泳生物聚集到礁区内,初步表明礁体的投放对聚集鱼类和蟹类非常有效。经济种类资源密度的增加,也一定程度说明鱼礁的投放产生良好的生态效益和经济效益。
2.4 生物多样性
为进一步评估人工鱼礁投放后的生态效果,对2次调查的物种多样性指数进行了计算分析。结果表明,投礁前对比区资源种类丰富度高于礁区,投礁后礁区海域游泳生物的丰富度明显高于投礁前,比投礁前增加了0.22倍(表 5),并且高于同期调查的对比区,投礁后Shannon-Wienver多样性指数(H′)在礁区和对比区均比投礁前有所增加,且在礁区增加较多。这说明投礁后鱼礁区游泳生物丰富度有所改善,群落结构优于投礁前和对比区。
表 5 礁区及对比区种类数和多样性指数Table 5 Species and diversity index in artificial reefs and control area in background survey and tracking survey调查时间
survey time调查站位
survey stations总渔获种数
species number种类丰富度指数(R)
species abundance index多样性指数(H′)
diversity index本底调查
background survey礁区 artificial reefs area 23 4.39 2.30 对比区 control area 23 4.63 2.71 跟踪调查
tracking survey礁区 artificial reefs area 41 5.38 2.53 对比区 control area 32 4.50 2.86 2.5 投礁后礁区生产效益估算
为评价投放人工鱼礁所产生的经济价值,笔者把水产市场上出售的鱼种定义为经济鱼种,投礁后,经济鱼种的种类数为29种(表 6),比投礁前增加了9种;经济鱼种的渔获尾数比投礁前约增加了7.9倍,经济鱼种的总资源密度比投礁前约增长17倍。笔者于2007年8月通过询问调查的方法,统计当地经济鱼种的市场价格,以此价格作为基础,用生产效益评估公式,计算投礁前后礁区经济鱼种的总生产效益。结果表明,投礁后经济鱼种的总生产效益比投礁前增加了15倍。说明了人工鱼礁的投放能够丰富礁区海域经济鱼种的种类、数量以及资源密度。投礁后经济鱼种资源量的显著增加,使总生产效益明显增加,表明投放人工鱼礁所产生的经济效益明显。
表 6 投礁后礁区生产效益估算Table 6 Estimation of the production profit in artificial reefs area in tracking survey调查时间
survey time经济种类数/种
the species number of commercial species经济种总渔获尾数/尾
the individual quantity of commercial species经济种总资源密度/kg·km-2
the biomass densityof total commercial species经济种总生产效益/元·km-2
the production profit of commercial species本底调查
background survey20 138 103.30 1 448.24 跟踪调查
tracking survey29 1 228 1 870.85 23 778.30 3. 讨论
国内外学者对人工鱼礁的许多研究[10-15]表明,投放人工鱼礁可使大量生物聚集在鱼礁区,起到聚集、养护和增殖渔业资源的效果。对澄海莱芜人工鱼礁区的调查也得到相似的结果,投礁后礁区内生物种类(特别是蟹类)增加明显,总种类数比投礁前本底调查增加了0.78倍,对比区总种类数比投礁前本底调查增加了0.39倍。无论在礁区还是对比区,投礁后各类生物的资源密度明显比投礁前高,总资源密度比投礁前分别增加了25.63和10.05倍。这说明莱芜人工鱼礁建设使礁区和对比区总种类数和总资源密度均显著增加,确实起到了资源养护的效果。
人工鱼礁区海域生物多样性指数的分析显示,Margalef种类丰度指数(R)和多样性指数(H′)在2次调查中变化较大,投礁后礁区海域的游泳生物丰富度明显高于投礁前,比投礁前增加了0.22倍;Shannon-Wienver多样性指数(H′)也高于投礁前,生物群落多样性指数的变化反映了生物群落种类组成和结构的改善。以上调查结果在一定程度上说明投礁以后人工鱼礁区的渔业资源丰富度有所改善,群落结构变得复杂和多样,资源状况优于投礁前。
投礁后礁区优势种类群变动明显,蟹类逐渐成为绝对优势种类,且其资源量远大于投礁前。人工鱼礁为蟹类提供了良好的栖息和生长环境,有利于蟹类的聚集和生长。在本底调查中没有出现的经济种类龙头鱼在跟踪调查中也成为主要优势种,说明人工鱼礁作为优良的聚集地和产卵地对聚集鱼类等经济种类非常有效。
依据当地水产市场上出售的经济鱼类价格,对投礁前后在礁区海域捕获的经济鱼类进行了总生产价值的估算,计算得出投礁后经济鱼种的总生产效益比投礁前增加了15倍,每平方千米约增值2.23万元。表明投放人工鱼礁所产生的经济效益明显。
跟踪调查结果表明,投礁后礁区海域各类群资源总量显著增加,人工鱼礁表现出显著的集鱼效果。但由于跟踪调查是在休渔期过后的8月份进行,与5月份本底调查的调查时间不同。通常每年5月份是南海北部渔业资源种类的主要产卵期和索饵期,而休渔期限制捕捞,资源密度通常会有所增加,今后应开展人工鱼礁区不同季节资源状况的系统调查和分析,了解在不同时间调查时季节因素对聚鱼效果的影响,以期更准确地评价人工鱼礁的增殖效果。
人工鱼礁的聚鱼、养护和增殖效果受到礁区的水深、底质[16-17]、流场、资源环境状况以及布局、礁体设计[18]、投放时间[16]、投放规模[19]和礁区管理等诸多因素的影响。国内外的研究表明,鱼礁投放后的优良生态效应要经过长时间才能明显体现。此次调查采样次数有限,只能得出一个初步结果。但就此有限的资料已可看到,鱼礁聚集生物、改善局部区域群落结构和增加生物多样性的作用是显而易见的,人工鱼礁在恢复渔业资源方面已发挥了显著作用。随着礁区规模进一步扩大,加强礁区管理,将会使该礁区更好地发挥其改善海洋生态环境和恢复近海渔业资源的功能。今后的人工鱼礁研究课题应该围绕提高鱼礁区渔获质量、生物多样性、生态系统稳定性和摸清鱼礁水动力机制与集鱼之间的关系等方面作进一步的研究。
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图 1 门分类水平下棘头梅童鱼肠道和水环境中优势细菌的相对丰度
注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL和W分别代表棘头梅童鱼和水样;数字代表样品标号。
Figure 1. Relative abundance of dominant bacteria in intestine of C. lucidus and water environment on phyla level
Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal, and Win, respectively; CL and W represent C. lucidus and water samples, respectively; and the numbers represent sample labels.
图 2 属水平下棘头梅童鱼肠道和水环境中优势菌群结构
注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL和W分别代表棘头梅童鱼和水样;数字代表样品标号。
Figure 2. Composition of dominant bacterial genus in intestines of C. lucidus and water environment on genera level
Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal and Win, respectively; CL and W represent C. lucidus and water samples, respectively; and the numbers represent sample labels.
图 3 不同季节棘头梅童鱼肠道中菌属数量 (a) 和肠道特有及共有的属数量 (b)
注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL代表棘头梅童鱼。
Figure 3. Number of bacterial genera in intestines of C. lucidus in different seasons (a) and number of unique and common genera in intestines in different seasons (b)
Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal, and Win, respectively; CL represent C. lucidus.
图 4 棘头梅童鱼肠道和水体中的细菌群落多样性指数的季节变化
注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL和 W分别代表棘头梅童鱼和水样;不同字母表示存在显著性差异 (p<0.05)。
Figure 4. Seasonal variation of bacterial diversity in intestines of C. lucidus and water environment
Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal and Win, respectively; CL and W represent C. lucidus and water samples, respectively; Different letters represent significant differences (p<0.05).
图 5 基于Bray-Curtis距离的水体和肠道细菌群落的主坐标分析
注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL和W分别代表棘头梅童鱼和水样;* 表示存在显著性差异 (p<0.05)。
Figure 5. Principal coordinate analysis (PCoA) of bacterial composition in intestines of C. lucidus and water environment based on Bray-Curtis distance
Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal, and Win, respectively; CL and W represent C. lucidus and water samples, respectively; * represents significant differences (p<0.05).
表 1 不同季节棘头梅童鱼肠道与水体中的细菌组成差异分析
Table 1 Difference of bacterial composition between intestines of C. lucidus and water environment in different seasons
分组Group r2 p Spr_CL-vs-Sum_CL 0.939 0.154 Spr_CL-vs-Fal_CL 0.814 0.030* Spr_CL-vs-Win_CL 0.871 0.025* Sum_CL-vs-Fal_CL 0.766 0.032* Sum_CL-vs-Win_CL 0.818 0.041* Fal_CL-vs-Win_CL 0.923 0.028* Spr_CL-vs-Spr_W 0.854 0.018* Sum_CL-vs-Sum_W 0.929 0.022* Fal_CL-vs-Fal_W 0.740 0.025* Win_CL-vs-Win_W 0.029* 注:春季、夏季、秋季、冬季分别用Spr、Sum、Fal、Win表示;CL和W分别代表棘头梅童鱼和水样;* 表示存在显著性差异 (p<0.05)。 Note: Spring, summer, fall and winter are denoted by Spr, Sum, Fal, and Win, respectively; CL and W represent C. lucidus and water samples, respectively; * represents significant differences (p<0.05). -
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