海洋生态与环境科学重点实验室知识库

在人类活动及全球变化的影响下，海洋生态系统的结构与功能发生了很大转变，水母作为胶质类浮游动物的重要代表，在全球很多海洋生态系统中数量急剧增多，我国近海水域同样出现水母种群暴发现象。水母暴发的原因及暴发后对海洋生态系统产生的影响已成为国际浮游生态学研究的热点之一。我国近海以海月水母、白色霞水母、沙海蜇暴发范围最广、致灾最为严重。水母暴发的危害之一就是对海洋食物网产生的重要影响，然而，我国对于这三种水母食性的定量研究，以及三者与其他浮游动物及鱼类营养关系的研究基础相对较弱。本文以中国近海三种大型致灾水母为研究对象，对此开展定量化的食性研究，分析三者对不同浮游动物及鱼类的摄食选择与营养关系，有助于我们了解三种水母在中国近海海洋食物网中的营养地位与营养策略。此外，我国学者已经开始关注水母暴发对浮游动物种群及鱼类产生的影响，但这需要定量化的食性与摄食率等营养生态学参数作为基础，本研究为合理分析水母与其他浮游动物及鱼类之间的营养关系，准确评估三种大型水母暴发对海洋食物网的影响提供了重要参数与理论支撑。

本研究以海月水母、白色霞水母、沙海蜇为研究对象，分别选取胶州湾、长江口附近海域、黄东海交界海域作为重点研究区域，通过室内实验（清除率实验）、野外调查（胃含物分析）、稳定同位素分析的手段，开展三种水母的食性研究，测定三者的摄食率，分析三种水母对不同饵料生物的摄食选择性与营养关系；基于所得参量，结合野外调查的水母数量、伞径大小、浮游动物丰度信息、以及环境条件等，定量评估水母暴发对中国近海海洋食物网所产生的影响。本研究主要得出以下结论：

1. 室内清除率实验结果表明：海月水母、霞水母水母体对仔稚鱼及胶质类水螅水母具有较高的摄食选择性，对于桡足类、毛颚类选择性较低；此外，霞水母表现出对海月水母的贪婪性摄食；沙海蜇同样表现出对仔稚鱼具有较高的摄食选择性，然而不能捕食胶质类水螅水母，这表明根口目沙海蜇与旗口目海月水母、霞水母的摄食特性有很大不同。水母体大小对清除率具有显著影响，三者均表现出清除率随伞径圆盘面积增加而呈现线性增加趋势。

2. 海月水母水螅体胃含物解剖结果表明，水螅体食性广泛，主要由浮游动物碎屑、小型桡足类（平均前体长485 μm）、桡足类幼体及纤毛虫等组成；小型桡足类是胶州湾海月水母水螅体主要的能量来源（碳贡献比例：60.61% ± 18.05%）。水螅体摄食率具有很大的季节波动（0.04-0.372 μg C μg C^-1 d^-1）。水螅体广布于沿岸生态系统，其数量急剧增多会对浮游-底栖生物耦合产生重要影响。

3. 利用同位素方法对长江口附近海域白色霞水母的食性及与其他生物之间的营养关系研究发现，随霞水母伞径增加，其同位素δ¹³C（~1.93‰）与δ¹⁵N（~2.23‰）值呈线性增加。MixSIAR模型表明，霞水母在生长过程中发生了明显的食性组成上的改变，以悬浮物（seston）为主转移到以浮游动物为主；桡足类是霞水母生长发育过程中重要的能量供给者，食性占比较为稳定（31.03%–38.63%）。胶质类生物是霞水母食性中不可或缺的一部分，随霞水母伞径增加，胶质类生物在其食性中的占比由15.74%增加到35.18%，这表明个体较大的霞水母需要消耗更多的胶质类生物；沙海蜇在霞水母食性中的占比最高可达9.43%，表明霞水母对沙海蜇存在较强的同质捕食现象。

4. 对2009年5-8月份胶州湾海月水母种群研究表明，海月水母暴发对浮游动物种群会产生重要影响，且具有一定的季节波动；其中6-7月海月水母对湾内水体的清除次数可达0.3倍以上，桡足类在湾内平均滞留时间不足6天，最小只有2天左右，对浮游动物产生巨大的摄食压力；而其他月份影响较小。胶州湾浮游动物数量的年际变化进行对比发现，海月水母暴发年（2009）湾内浮游动物数量较未暴发年（2008、2010）显著下降。海月水母大量出现对胶州湾浮游动物产生很大的摄食压力，会对湾内浮游动物种群产生很强的调控作用。

5. 对2019年5月份在黄海南部、东海北部海域采集的沙海蜇样品，利用胃含物解剖的方法进行食性分析发现，沙海蜇食物类型主要包含小型桡足类（体长< 1000 μm）、大型桡足类（体长> 1000 μm）、桡足类幼体及磷虾类四种；其中小型桡足类（66.1%）与桡足类幼体（32.6%）占据了沙海蜇食物的绝大部分，磷虾数量极少；据此推测，小型桡足类及桡足类幼体应为沙海蜇的主要食物来源。同时本研究评估了该区域沙海蜇的摄食率以及对桡足类的摄食压力，结果表明，2019年5月份在研究海域单位水体沙海蜇的摄食率在9.3-93.3 g C km^-2 d^-1之间；沙海蜇对调查站位的大型桡足类、小型桡足类及桡足类幼体的平均摄食压力最大分别为0.012%、0.102%、0.081%；据此，本研究认为2019年5月份沙海蜇对黄海南部及东海北部海域桡足类的摄食并不会造成其数量的下降，这主要是由于5月份沙海蜇在该海域处于发生初期，丰度较低、伞径较小，对浮游动物种群产生较低的摄食压力。

6. 三种水母形态结构上的差异决定了捕食机制的不同。海月水母主要通过调整伞径收缩频率来适应不同的饵料环境；而霞水母具有长而密集的触手丝，成为其捕食的有利武器，它主要依靠调整触手丝的伸缩来适应不同的饵料环境，饵料生物对于霞水母伞径收缩频率却没有刺激作用。沙海蜇发育过程中中央口腕愈合，肩板及口腕末端的细小通路成为食物的主要通路；另外，在其伞径下方同样有辐射状食物通路，最终与沙海蜇胃部相通；因此，饵料生物的宽度决定了是否能够被成功捕食；本研究认为，位于沙海蜇肩板及口腕处的食物通路应在2 mm以上。

In recent years, human activities and climate changes have greatly affected the structure and function of marine ecosystem. The number of gelatinous zooplankton especially jellyfish in the marine ecosystem has globally increased. There are many reports about the blooms of jellyfish, and usually the jellyfish blooms caused enormous ecological, economic and societal problems. Jellyfish ecology research has become one of the hot spots in marine ecology. The frequent occurrence of Aurelia coerulea, Nemopilema nomurai, and Cyanea nozakii. blooms in the bay, the offshore and the continental shelf in China have caused serious problems to the tourism, coastal industry and fishery. The vast majority of previous researches have concerned about the life cycle, growth rate and bloom mechanisms of the jellyfish, but the quantitative study on the feeding of these three jellyfish and their trophic relationship with zooplankton and fish populations are relatively scarce in China. Jellyfish are usually considered as voracious predators, which play important roles in the material cycling and energy flow in marine ecosystems. A quantitative study on the diets of these three jellyfish was carried out; their feeding selection and trophic relationship with different prey organisms were analyzed. This research enhanced our understanding to the trophic position and strategy of these three jellyfish in the coastal waters.

In the present study, the three main blooming jellyfish in the Chinese coastal waters A. coerulea, N. nomurai, and C. nozakii were taken as our target species; the main research areas included Jiaozhou Bay, Yellow sea and East China Sea, and the Yangtze estuary, respectively. Feeding activities, gut content analysis, and stable isotope δ¹³C and δ¹⁵N were used to quantitatively investigate the diet model of three species of jellyfish; prey selection and predation mechanisms were analysed simultaneously. Based on these parameters, the effects of jellyfish feeding on marine food web were quantitatively evaluated. The main conclusions of this study are as follows：

1. Clearance rates widely varied with the type of prey organisms. Hydromedusae and fish larvae were captured by A. coerulea and C. nozakii in considerably high efficiency, followed by copepods and chaetognath. Moreover, C. nozakii could greedily prey on A. coerulea. N. nomurai also could efficiently prey on fish larvae, but could bot prey on small medusae, e.g., hydromedusae. Predator size has a significant effect on clearance; clearance rate linearly increased with the cross-sectional area.

2. The diet of A. coerulea polyps was determined using gut content analysis. Digestion time was measured in situ. Ingestion rates, based on gut contents and digestion time, were assessed monthly. A. coerulea polyps had a varied diet, including zooplankton prey detritus, copepods adult and nauplii, and protozoa. Prey detritus represented the bulk of total prey intake in number, followed by copepods, protozoa and nauplii. Copepods (mean body length = 485 μm) accounted for 60.61% ± 18.05% of the carbon ingested by the polyps, while zooplankton prey detritus accounted for 37.75% ± 18.89%. Small copepods should be an important source of nutrition for the polyp stage during jellyfish blooms. Polyps have a large seasonal variation in carbon weight-specific ingestion rates (I_w, range 0.040 to 0.372 μg C μg C^-1 d^-1). Scyphopolyps are widely distributed predators in littoral ecosystems and may play an important role in plankton-benthos coupling. Massive scyphopolyp blooms may influence pelagic ecosystems.

3. A significant change in stable isotope values was found during C. nozakii growth: δ¹³C values increased by ~1.93‰, and δ¹⁵N values increased by ~2.23‰. The MixSIAR model indicated that C. nozakii underwent a dietary shift during growth, from a seston-based diet in smaller medusae to a zooplankton-based diet in larger medusae. Copepods were an important food source for C. nozakii (31.03%–38.63%) irrespective of size. Gelatinous prey organisms represented 15.74% of the diet of smaller C. nozakii, and 35.18% of the diet of larger C. nozakii, suggesting that larger C. nozakii consumed more gelatinous prey. The diet of C. nozakii included 9.43% N. nomurai and 9.53% small medusae. The results suggested that intraguild predation among these species may be an important trophic relationship in the northern ECS.

4. The population burst of jellyfish Aurelia coerulea occurred in Jiaozhou Bay in 2009, and the potential predation impact of A. coerulea on zooplankton population was investigated. In June and July 2009, the population A. coerulea could potentially clear the volume of water in the Bay more than 0.3 times a day in July. Residence time for copepods was less than 6 d, the minimum residence time was only 2.15 d in June and July. Abundances of copepods, hydromedusae, and chaetognaths were extremely low in 2009 (jellyfish bloom year) as compared to 2008 and 2010 (jellyfish non-bloom years), particularly with respect to the populations of small copepods and hydromedusae. Large predation pressure of A. coerulea occurred to control zooplankton communities in Jiaozhou Bay, at least during June and July. A. coerulea perhaps should be considered as a keystone species in the control of the trophic structure when its massively appears in Jiaozhou Bay.

5. Gut content analysis was used to determine the diet of N. nomurai medusae; 21 N. nomurai individuals (diameter: 5-47 cm) collected in the Yellow Sea and the East China Sea in May 2019 were analysed. Small copepods (body length < 1000 μm), large copepods (body length > 1000 μm), copepods larvae and Euphausiacea were found in the guts of N. nomurai; small copepods (66.1%) and copepods larvae (32.6%) comprised the majority part of the prey in N. nomurai gut. We speculated that small copepods and copepods larvae provided the main energy of N. nomurai growth. The estimated ingestion rate of N. nomurai medusae in unit water in our study area ranged from 9.3 g C km^-2 d^-1 (the capture rate of the bottom trawl is 1) to 93.3 g C km^-2 d^-1 (the capture rate of the bottom trawl is 0.1). Basing on the ingestion rate, we estimated the feeding pressure of N. nomurai on the standing stock of copepods (large and small copepods, and copepods larvae). The results indicated that the mean feeding pressure of N. nomurai on standing stock of large copepods, small copepods and copepods larvae were 0.012%, 0.102%, 0.081%, respectively, in May 2019 (the capture rate of the bottom trawl is 0.1). This suggested that the population of N. nomurai have little effect on zooplankton population in May 2019. This was mainly due to the fact that N. nomurai population was in the early stage of its occurrence, with low abundance and small diameter in May 2019.

6. The differences in the morphology and structure of three jellyfish determined the various predation mechanisms. Predation process of A. coerulea based on the fluid motions created during swimming to entrain and capture prey, and we found that swimming propulsion of A. coerulea was adjusted to adapt to different feeding conditions, and swimming speeds of Aurelia and predator-prey encounter rates increase after initial contact with prey. However, C. nozakii medusae had long trailing tentacles, and food was obtained only by random contact with these. The responses of extension and contraction of C. nozakii tentacle were oscillated at different feeding conditions, but no significant difference of swimming propulsion. N. nomurai medusae without central mouths have developed complicated canal systems connecting the tip of tentacle and oral arm to the gut. Prey were gathered by tentacles, and entered into the gut via the canal system at oral arms and scapulets. In addition, there are also radial canal system following the umbrella path, which eventually connect with the gut of jellyfish. Hence, the width of prey determined whether it could be successfully preyed on. In this study, we firstly reported Euphausiacea (body length: 6.1 ± 0.8 mm; width: 2.1 ± 0.3 mm) remained in the medusa scapulet and oral arm, we also confirmed by predation experiments that N. nomurai could successfully capture Euphausiacea. This implied that the diameter of terminal pore is more than 2 mm, which is larger than the previous thought about 1 mm.

Keywords: Jellyfish blooms, Prey selection, Ingestion rate, Gut content analysis, Stable isotope analysis, Feeding pressure