基于分子生物学技术的黄渤海沿岸两种常见桡足类的现场食物研究
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摘要
作为海洋浮游动物的重要组成部分，桡足类是海洋初级生产力和高营养级之间物质和能量传递的重要媒介，在海洋生态系统中起着重要的作用。作为海洋食物网中主要的摄食者，其与浮游植物等的相互作用关系到整个海洋生态系统功能的运转。桡足类在自然海区中的食物组成是其摄食研究的核心内容之一，是深入了解其在海洋食物网所处生态地位的关键。以往诸多研究方法受限于各自的局限性，在获取桡足类准确现场摄食信息方面尚存一些缺陷。基于分子生物学原理，以桡足类肠道内食物DNA为标记的研究方法具有普遍性、特异性、稳定性、不受食物形态限制、容易获取现场信息等优点，已开始应用于桡足类的摄食研究中。
本文利用分子生物学方法，对黄渤海沿岸中华哲水蚤（Calanus sinicusBrodsky）和太平洋纺锤水蚤（Acartia pacifica Steuer）的现场食物进行了分析，并通过开展室内摄食实验对分子分析的结果进行了部分验证。结果表明，这两种桡足类的现场食物组成较传统观点更为广泛和多样化，该结果突破了一些传统认识，具有新的发现。该研究也为深入开展海洋生态系统食物网结构和功能等研究提供了新的思路和研究手段。
1.桡足类现场食物的分子生物学检测
为了探索建立研究桡足类现场摄食的方法，研究自然海区中桡足类的食物组成信息，我们以核糖体小亚基基因（18S rDNA）为目标序列，研究了包括胶州湾太平洋纺锤水蚤（现场采集固定样品标记为JZB-I_Oct）、青岛近海中华哲水蚤（两个现场样品：QD-I_Jan和QD-I_Jun）及黄河口邻近水域中华哲水蚤（现场样品：YRE-I_May）在内的黄渤海沿岸两种常见桡足类的现场食物组成。对现场桡足类样品中出现的一些主要生物种类和类群进行了分析与探讨。主要结果和结论如下：
（1）丰富多样的潜在食物组成：对所有现场桡足类样品（自然海区中采集后立即固定）基于非桡足类（non-copepod）引物的分析显示，共有包括硅藻（Diatoms）、甲藻（Dinoflagellates）、颌鞭目藻类（Choanoflagellida）、隐藻（Cryptophyta）、金藻（Chrysophyceae）、绿藻（Chlorophyta）、褐藻（Phaeophyta）、轮藻（Streptophyta）、不等鞭毛类（Stramenopiles）、海洋真菌类（Marine fungi）、有孔虫（Rhizaria）、水螅水母类（Hydrozoa）、栉水母类（Ctenophora）、软体动物（Mollusca）、毛颚动物（Chaetognatha）、被囊类（Tunicata）、陆源松柏纲（Coniferopsida）与百合纲（Liliopsida）植物等近二十个门类的生物被检测出，另外还有若干序列仅辨认到真核生物（Eukaryota）水平上，表明可能有未被鉴定识别的种类也包含在桡足类的食物类群中。高度多样化生物类群的检出显示了基于non-copepod引物的分子生物学手段在测定桡足类食物种类和范围上的强大效用和优势。
（2）对硅藻和甲藻摄食的差别：硅藻来源序列所占比例很小。对于中华哲水蚤来说，QD‐I_Jan中只有一条硅藻来源的序列，YRE‐I_May中硅藻比例稍高，也只占到12.0%。太平洋纺锤水蚤（JZB‐I_Oct）中，硅藻来源序列所占比例（3.8%）明显小于其在对应水体样品中的比例（21.7%）。中华哲水蚤的一个（QD‐I_Jun）样品中没有检测到硅藻来源的序列，尽管其对应水体样品中有出现。以上结果表明，硅藻类群不是中华哲水蚤或太平洋纺锤水蚤的喜食性食物。与此相反的是，甲藻在QD‐I_Jun和JZB‐I_Oct中都较为丰富，特别是在JZB‐I_Oct中（26.9%），要远高于对应水体样品中的比例（13.0%），表明这两种桡足类可能对甲藻类群有一定的摄食选择性。
（3）水螅水母和栉水母中某些类群的普遍出现和优势地位：水螅水母和栉水母中某些类群的序列在所有现场桡足类样品中均出现，且均在各自样品中占优势地位。QD‐I_Jan中为花水母（Anthomedusae）来源的序列，最可能为八斑芮氏水母（Rathkea octopunctata），占到总样品的40%以上；QD‐I_Jun中为软水母（Leptomedusae）来源，最可能为其中的半球美螅水母（Clytiahemisphaerica），所占比例也在40%以上；JZB‐I_Oct和YRE‐I_May中均包含栉水母类和水螅水母类来源的序列，且都以前者为多，主要是触手纲（Tentaculata）环体腔亚纲（Cyclocoela）球栉水母目（Cydippida）中的类群，很可能为球形侧腕水母（Pleurobrachia globosa），所占比例分别为42.3%和32.0%；水螅水母次之，分别来源于软水母和花水母，最可能是软水母中的和平水母（Eirene）与花水母中的八斑芮氏水母，分别占23.1%和20.0%；水母类总计占各自样品的比例分别达65.4%和52.0%。我们对于水母类的大量出现进行了分析和探讨，认为中华哲水蚤和太平洋纺锤水蚤对这两类水母的摄食与海区中其分布和丰度密切相关，基于大小关系等考虑推测很可能是摄食其卵或浮浪幼虫。
（4）海洋真菌及Syndiniales类甲藻在桡足类食物中的出现：主要在QD‐I_Jun中出现丰富的海洋真菌，以茎点霉（Phoma）、Filobasidium和马拉色菌（Malassezia）三个属来源的序列为主，占总样品的比例大于20%。QD‐I_Jan和YRE‐I_May中甲藻均以寄生性甲藻Syndiniales为主，包括Euduboscquella、Hematodinium和Ichthyodinium三个属。桡足类可与许多生物形成共生体系统，较传统方法，分子生物学方法的使用发现了更多与桡足类相关的生物类群，海洋真菌和Syndiniales类甲藻便是其中的两个类群。它们均与桡足类有着复杂的营养关系，虽然我们以研究桡足类的摄食为目的，但认为基于序列分析检出的海洋真菌和Syndiniales甲藻与桡足类真实的营养关系尚不能判定为简单的摄食与被摄食的关系，而需要借助其它手段进行更加深入的研究。
（5）对水体中一些稀有类群的摄食：有许多从来不被认为是桡足类食物的种类出现在non-copepod引物扩增出的序列中，有些还占有较高比例。例如，QD‐I_Jun中陆生松科植物松树（Pinus）和黑麦草（Lolium）（占总样品的7.4%）。另外，两个现场中华哲水蚤样品中均出现了大型藻类，QD‐I_Jan中为褐藻中的萱藻（Scytosiphon），YRE‐I_May中为绿藻中的石莼（Ulva）。我们推测这两类生物分别以花粉、孢子细胞或未被完全降解的碎屑的形式被中华哲水蚤所摄食。
2.室内摄食实验验证
除了分析现场样品外，我们还对胶州湾太平洋纺锤水蚤和青岛近海中华哲水蚤活体进行了饥饿处理及室内摄食实验。鉴于现场桡足类样品中发现的现象，进行了部分室内摄食实验，除球等鞭金藻（Isochrysis galbana Parke8701）、青岛大扁藻（Platymonas helgolandica Kylin var. tsingtaoensis）、绿色巴夫藻（Pavlova viridis）和三角褐指藻（Phaeodactylum tricornutum）四种单胞藻外，还给两种桡足类提供动物性饵料，如强壮箭虫（Sagitta crassa）的卵和咸水丰年虫（Artemia salina）的无节幼虫。基于分子生物学的检测结果显示太平洋纺锤水蚤对咸水丰年虫有摄食，没有检测到中华哲水蚤对强壮箭虫的摄食。用non-copepod引物分析摄食后桡足类的基因组DNA，结果显示，三角褐指藻和绿色巴夫藻在检测到的食物类群中占绝对优势地位。这在一定程度上反映了室内摄食实验中容易出现的偏差：仅给予一种或数种饵料的摄食实验结果会掩盖桡足类真实的摄食情况。
Marine pelagic copepods are conventionally considered as the key linkagebetween primary production and higher trophic levels in marine food webs.Information of copepods in situ diets has pivotal impact on the understanding ofstructure and function of the marine food web, and yet remains obscure. PCR-baseddietary analysis, in which prey DNA as biomarkers, has advantages with highuniversality, specificity and stability. Unrestricted to the morphology of prey, DNAand PCR based method could get more accurate results efficiently.
In this study, we applied molecular analysis to determine the in situ diets ofCalanus sinicus and Acartia pacifica along coastal waters of Bohai Sea and YellowSea. Besides, laboratory-controlled feeding experiments were conducted for somepotential prey to verify molecular method-based results. Results showed that the twocopepods had very diverse in situ diets, including some groups that never suspectedto be copepods prey before. As new potential prey detected, what we found enlargedour knowledge about copepods in situ dietary compostion. Moreover, our researchinformed alternative and promising way to better understanding the strcture andfunction of marine food webs.
1. Molecular detection of copepods in situ diets
To explore the application of PCR based method in copepod feeding research, asa case study, natural diets of two common and dominant copepods, Calanus sinicusBrodsky and Acartia pacifica Steuer in Jiaozhou Bay, Qingdao coastal waters, andYellow River estuary adjacent waters were investigated. Using a18S rDNA basedmolecular approach, as many lineages of eukaryotes as possible were amplified, butC. sinicus, A. pacifica and related copepods were excluded. In situ diet compositionand occurance of some species/lineages were discussed. The main results and conclusions are listed below.
(1) Abundant and diverse potential diets: non-copepod18S rDNA-basedanalysis of all in situ fixed copepod samples showed that there are totally near20lineages were discovered. They are Diatoms, Dinoflagellates, Choanoflagellida,Cryptophyta, Chrysophyceae, Chlorophyta, Phaeophyta, Streptophyta, Stramenopiles,Marine fungi, Rhizaria, Hydrozoa, Ctenophora, Mollusca, Chaetognatha, Tunicata,Coniferopsida, Liliopsida. Besides, several sequences were clustered to unkowngroups, which indicated the unidentified species/lineages were included in the dietsof copepods. Discovery of the highly diverse plankton community resulted fromintrinsic advantages of PCR based analysis and the non-copepod primers.
(2) Difference in feeding diatoms and dinoflagellates: diatoms are minorityin all in situ fixed copepod samples. For C. sinicus, in QD-I_Jan, only1sequencebelonged to Thalassiosiraceae was detected, the proportion of diatom was a littlehigher in YRE-I_May (12.0%). For A. pacifica, proportion of diatom in JZB-I_Oct ismuch smaller (3.8%) than that (21.7%) in corresponding water sample. Diatomoriginated sequences even didn’t detected in QD-I_Jun while the proportion in watersample is10.4%. All the results showed that, maybe diatoms are not favorite foodfor both C. sinicus and A. pacifica. On the contrary, dinoflagellates were abundant inQD-I_Jun and JZB-I_Oct, especially in JZB-I_Oct, much more abundant (26.9%)than that in corresponding water sample (13.0%). These results maybe showed apositive feeding selectivity of the2copepods to dinoflagellates.
(3) Universality and dominace of some lineages in Hydrozoa andCtenophora: some lineages of Hydrozoa and Ctenophora emerged in all in situfixed copepod samples with much abundant proportion in each samples.Anthomedusae (Rathkea octopunctata, most likely) dominanted QD-I_Jan by aproportion higher than40%, similar proportion of Leptomedusae (Clytiahemisphaerica, most likely) dominated QD-I_Jun. Both Ctenophora and Hydrozoaoriginated sequences were discovered in JZB-I_Oct and YRE-I_May respectively,and Ctenophora was the first dominated jellyfish, represented by lineages inTentaculata, Cydippida (Pleurobrachia globosa, most likely). Hydrozoa was the second dominated lineages, represented by Rathkea octopunctata and Eirene. In all,jellyfish related sequences are very abundant in these2samples, with a proportion of65.4%and52.0%respectively. Occurance of some lineages in Hydrozoa andCtenophora were discussed, we think feeding of the2copepods to jellyfish is highlyrelated to their distribution and abundance in seas. Based on the results, we inferredthat the eggs or planula larva fmighte be captured by C. snicus and A. pacifica.
(4) Occurance and abundant of marine fungi and Syndiniales (parasiticdinoflagellates) in detected diets: among all samples, abundant marine fungi weremostly discovered in QD-I_Jun, represented by Phoma, Filobasidium andMalassezia, they account for more than20%of the sample. Sequences belonged toSyndiniales were detected in QD-I_Jan and YRE-I_May, they are main part ofdinoflagellates in these two samples, represented by Euduboscquella, Hematodiniumand Ichthyodinium. Compared to traditional methods, application of PCR-basedmethod facilitated the discovery of more copepods-related organisms. Marine fungiand Syndiniales are two lineages of them. Copepods are always connected withfungi in the form of copepods-fungi symbiont system, where complex trophicrelationship existed. Similar condition may existed in the Syndiniales-copepodssystems. Although we discovered these two lineages by non-copepod primers, itwould be arbitrary to designate their relationship as predator-prey system. Newmethods should be jointed to further study their complicated trophic relationship.
(5) Feeding to some scarce lineages in ambient waters: some lineages whichnever suspected to be prey of copepods were discovered in diets by molecularanalysis. Among these lineages, some even had substaintial proportion. Taketerrestrial plants Pinus and Lolium for example, they account for7.4%in QD-I_Jun.Besides, macroalage were detected in diets of C. sinicus, Scytosiphon (Phaeophyceae)and Ulva (Chlorophyta) were detected in QD-I_Jan and YRE-I_May respectively,although they were scarce in ambient waters. We speculated that the feeding of C.sinicus to these seemingly ambient water-scarce species most likely in the form oftheir pollens and swarmers.
2. Experiments to verify the feeding of some organisms
Besides the in situ fixed copepod samples, live A. pacifica and C. sinicus werecollected to conduct gut evacuation processing and the following feedingexperiments in laboratory to verify the feeding of some organisms. According towhat we found in in situ fixed copepod samples, an attempt was made to verify thefeeding of copepods to some unexpected species.4lab-cultured algae (Isochrysisgalbana Parke8701, Platymonas helgolandica Kylin var. tsingtaoensis, Pavlovaviridis and Phaeodactylum tricornutum), eggs of Sagitta crassa and larva of Artemiasalina were supplied as food in two series laboratory-controlled feeding experiments,for C. sinicus and A. pacifica respectively. Molecular detection showed that Artemia.salina was detected in diet of A. pacifica, while S. crassa wasn’t detected in the dietof C. sinicus after feeding experiments. The mostly discovered dietary species werePhaeodactylum tricornutum and Pavlova viridis. To some degree, the results showedthe bias of laboratory-controlled feeding experiments: when only one or limitedkinds of food were supplied, the real feeding habit of copepods would be masked bythe man-supplied food.
本文利用分子生物学方法，对黄渤海沿岸中华哲水蚤（Calanus sinicusBrodsky）和太平洋纺锤水蚤（Acartia pacifica Steuer）的现场食物进行了分析，并通过开展室内摄食实验对分子分析的结果进行了部分验证。结果表明，这两种桡足类的现场食物组成较传统观点更为广泛和多样化，该结果突破了一些传统认识，具有新的发现。该研究也为深入开展海洋生态系统食物网结构和功能等研究提供了新的思路和研究手段。
1.桡足类现场食物的分子生物学检测
为了探索建立研究桡足类现场摄食的方法，研究自然海区中桡足类的食物组成信息，我们以核糖体小亚基基因（18S rDNA）为目标序列，研究了包括胶州湾太平洋纺锤水蚤（现场采集固定样品标记为JZB-I_Oct）、青岛近海中华哲水蚤（两个现场样品：QD-I_Jan和QD-I_Jun）及黄河口邻近水域中华哲水蚤（现场样品：YRE-I_May）在内的黄渤海沿岸两种常见桡足类的现场食物组成。对现场桡足类样品中出现的一些主要生物种类和类群进行了分析与探讨。主要结果和结论如下：
（1）丰富多样的潜在食物组成：对所有现场桡足类样品（自然海区中采集后立即固定）基于非桡足类（non-copepod）引物的分析显示，共有包括硅藻（Diatoms）、甲藻（Dinoflagellates）、颌鞭目藻类（Choanoflagellida）、隐藻（Cryptophyta）、金藻（Chrysophyceae）、绿藻（Chlorophyta）、褐藻（Phaeophyta）、轮藻（Streptophyta）、不等鞭毛类（Stramenopiles）、海洋真菌类（Marine fungi）、有孔虫（Rhizaria）、水螅水母类（Hydrozoa）、栉水母类（Ctenophora）、软体动物（Mollusca）、毛颚动物（Chaetognatha）、被囊类（Tunicata）、陆源松柏纲（Coniferopsida）与百合纲（Liliopsida）植物等近二十个门类的生物被检测出，另外还有若干序列仅辨认到真核生物（Eukaryota）水平上，表明可能有未被鉴定识别的种类也包含在桡足类的食物类群中。高度多样化生物类群的检出显示了基于non-copepod引物的分子生物学手段在测定桡足类食物种类和范围上的强大效用和优势。
（2）对硅藻和甲藻摄食的差别：硅藻来源序列所占比例很小。对于中华哲水蚤来说，QD‐I_Jan中只有一条硅藻来源的序列，YRE‐I_May中硅藻比例稍高，也只占到12.0%。太平洋纺锤水蚤（JZB‐I_Oct）中，硅藻来源序列所占比例（3.8%）明显小于其在对应水体样品中的比例（21.7%）。中华哲水蚤的一个（QD‐I_Jun）样品中没有检测到硅藻来源的序列，尽管其对应水体样品中有出现。以上结果表明，硅藻类群不是中华哲水蚤或太平洋纺锤水蚤的喜食性食物。与此相反的是，甲藻在QD‐I_Jun和JZB‐I_Oct中都较为丰富，特别是在JZB‐I_Oct中（26.9%），要远高于对应水体样品中的比例（13.0%），表明这两种桡足类可能对甲藻类群有一定的摄食选择性。
（3）水螅水母和栉水母中某些类群的普遍出现和优势地位：水螅水母和栉水母中某些类群的序列在所有现场桡足类样品中均出现，且均在各自样品中占优势地位。QD‐I_Jan中为花水母（Anthomedusae）来源的序列，最可能为八斑芮氏水母（Rathkea octopunctata），占到总样品的40%以上；QD‐I_Jun中为软水母（Leptomedusae）来源，最可能为其中的半球美螅水母（Clytiahemisphaerica），所占比例也在40%以上；JZB‐I_Oct和YRE‐I_May中均包含栉水母类和水螅水母类来源的序列，且都以前者为多，主要是触手纲（Tentaculata）环体腔亚纲（Cyclocoela）球栉水母目（Cydippida）中的类群，很可能为球形侧腕水母（Pleurobrachia globosa），所占比例分别为42.3%和32.0%；水螅水母次之，分别来源于软水母和花水母，最可能是软水母中的和平水母（Eirene）与花水母中的八斑芮氏水母，分别占23.1%和20.0%；水母类总计占各自样品的比例分别达65.4%和52.0%。我们对于水母类的大量出现进行了分析和探讨，认为中华哲水蚤和太平洋纺锤水蚤对这两类水母的摄食与海区中其分布和丰度密切相关，基于大小关系等考虑推测很可能是摄食其卵或浮浪幼虫。
（4）海洋真菌及Syndiniales类甲藻在桡足类食物中的出现：主要在QD‐I_Jun中出现丰富的海洋真菌，以茎点霉（Phoma）、Filobasidium和马拉色菌（Malassezia）三个属来源的序列为主，占总样品的比例大于20%。QD‐I_Jan和YRE‐I_May中甲藻均以寄生性甲藻Syndiniales为主，包括Euduboscquella、Hematodinium和Ichthyodinium三个属。桡足类可与许多生物形成共生体系统，较传统方法，分子生物学方法的使用发现了更多与桡足类相关的生物类群，海洋真菌和Syndiniales类甲藻便是其中的两个类群。它们均与桡足类有着复杂的营养关系，虽然我们以研究桡足类的摄食为目的，但认为基于序列分析检出的海洋真菌和Syndiniales甲藻与桡足类真实的营养关系尚不能判定为简单的摄食与被摄食的关系，而需要借助其它手段进行更加深入的研究。
（5）对水体中一些稀有类群的摄食：有许多从来不被认为是桡足类食物的种类出现在non-copepod引物扩增出的序列中，有些还占有较高比例。例如，QD‐I_Jun中陆生松科植物松树（Pinus）和黑麦草（Lolium）（占总样品的7.4%）。另外，两个现场中华哲水蚤样品中均出现了大型藻类，QD‐I_Jan中为褐藻中的萱藻（Scytosiphon），YRE‐I_May中为绿藻中的石莼（Ulva）。我们推测这两类生物分别以花粉、孢子细胞或未被完全降解的碎屑的形式被中华哲水蚤所摄食。
2.室内摄食实验验证
除了分析现场样品外，我们还对胶州湾太平洋纺锤水蚤和青岛近海中华哲水蚤活体进行了饥饿处理及室内摄食实验。鉴于现场桡足类样品中发现的现象，进行了部分室内摄食实验，除球等鞭金藻（Isochrysis galbana Parke8701）、青岛大扁藻（Platymonas helgolandica Kylin var. tsingtaoensis）、绿色巴夫藻（Pavlova viridis）和三角褐指藻（Phaeodactylum tricornutum）四种单胞藻外，还给两种桡足类提供动物性饵料，如强壮箭虫（Sagitta crassa）的卵和咸水丰年虫（Artemia salina）的无节幼虫。基于分子生物学的检测结果显示太平洋纺锤水蚤对咸水丰年虫有摄食，没有检测到中华哲水蚤对强壮箭虫的摄食。用non-copepod引物分析摄食后桡足类的基因组DNA，结果显示，三角褐指藻和绿色巴夫藻在检测到的食物类群中占绝对优势地位。这在一定程度上反映了室内摄食实验中容易出现的偏差：仅给予一种或数种饵料的摄食实验结果会掩盖桡足类真实的摄食情况。
Marine pelagic copepods are conventionally considered as the key linkagebetween primary production and higher trophic levels in marine food webs.Information of copepods in situ diets has pivotal impact on the understanding ofstructure and function of the marine food web, and yet remains obscure. PCR-baseddietary analysis, in which prey DNA as biomarkers, has advantages with highuniversality, specificity and stability. Unrestricted to the morphology of prey, DNAand PCR based method could get more accurate results efficiently.
In this study, we applied molecular analysis to determine the in situ diets ofCalanus sinicus and Acartia pacifica along coastal waters of Bohai Sea and YellowSea. Besides, laboratory-controlled feeding experiments were conducted for somepotential prey to verify molecular method-based results. Results showed that the twocopepods had very diverse in situ diets, including some groups that never suspectedto be copepods prey before. As new potential prey detected, what we found enlargedour knowledge about copepods in situ dietary compostion. Moreover, our researchinformed alternative and promising way to better understanding the strcture andfunction of marine food webs.
1. Molecular detection of copepods in situ diets
To explore the application of PCR based method in copepod feeding research, asa case study, natural diets of two common and dominant copepods, Calanus sinicusBrodsky and Acartia pacifica Steuer in Jiaozhou Bay, Qingdao coastal waters, andYellow River estuary adjacent waters were investigated. Using a18S rDNA basedmolecular approach, as many lineages of eukaryotes as possible were amplified, butC. sinicus, A. pacifica and related copepods were excluded. In situ diet compositionand occurance of some species/lineages were discussed. The main results and conclusions are listed below.
(1) Abundant and diverse potential diets: non-copepod18S rDNA-basedanalysis of all in situ fixed copepod samples showed that there are totally near20lineages were discovered. They are Diatoms, Dinoflagellates, Choanoflagellida,Cryptophyta, Chrysophyceae, Chlorophyta, Phaeophyta, Streptophyta, Stramenopiles,Marine fungi, Rhizaria, Hydrozoa, Ctenophora, Mollusca, Chaetognatha, Tunicata,Coniferopsida, Liliopsida. Besides, several sequences were clustered to unkowngroups, which indicated the unidentified species/lineages were included in the dietsof copepods. Discovery of the highly diverse plankton community resulted fromintrinsic advantages of PCR based analysis and the non-copepod primers.
(2) Difference in feeding diatoms and dinoflagellates: diatoms are minorityin all in situ fixed copepod samples. For C. sinicus, in QD-I_Jan, only1sequencebelonged to Thalassiosiraceae was detected, the proportion of diatom was a littlehigher in YRE-I_May (12.0%). For A. pacifica, proportion of diatom in JZB-I_Oct ismuch smaller (3.8%) than that (21.7%) in corresponding water sample. Diatomoriginated sequences even didn’t detected in QD-I_Jun while the proportion in watersample is10.4%. All the results showed that, maybe diatoms are not favorite foodfor both C. sinicus and A. pacifica. On the contrary, dinoflagellates were abundant inQD-I_Jun and JZB-I_Oct, especially in JZB-I_Oct, much more abundant (26.9%)than that in corresponding water sample (13.0%). These results maybe showed apositive feeding selectivity of the2copepods to dinoflagellates.
(3) Universality and dominace of some lineages in Hydrozoa andCtenophora: some lineages of Hydrozoa and Ctenophora emerged in all in situfixed copepod samples with much abundant proportion in each samples.Anthomedusae (Rathkea octopunctata, most likely) dominanted QD-I_Jan by aproportion higher than40%, similar proportion of Leptomedusae (Clytiahemisphaerica, most likely) dominated QD-I_Jun. Both Ctenophora and Hydrozoaoriginated sequences were discovered in JZB-I_Oct and YRE-I_May respectively,and Ctenophora was the first dominated jellyfish, represented by lineages inTentaculata, Cydippida (Pleurobrachia globosa, most likely). Hydrozoa was the second dominated lineages, represented by Rathkea octopunctata and Eirene. In all,jellyfish related sequences are very abundant in these2samples, with a proportion of65.4%and52.0%respectively. Occurance of some lineages in Hydrozoa andCtenophora were discussed, we think feeding of the2copepods to jellyfish is highlyrelated to their distribution and abundance in seas. Based on the results, we inferredthat the eggs or planula larva fmighte be captured by C. snicus and A. pacifica.
(4) Occurance and abundant of marine fungi and Syndiniales (parasiticdinoflagellates) in detected diets: among all samples, abundant marine fungi weremostly discovered in QD-I_Jun, represented by Phoma, Filobasidium andMalassezia, they account for more than20%of the sample. Sequences belonged toSyndiniales were detected in QD-I_Jan and YRE-I_May, they are main part ofdinoflagellates in these two samples, represented by Euduboscquella, Hematodiniumand Ichthyodinium. Compared to traditional methods, application of PCR-basedmethod facilitated the discovery of more copepods-related organisms. Marine fungiand Syndiniales are two lineages of them. Copepods are always connected withfungi in the form of copepods-fungi symbiont system, where complex trophicrelationship existed. Similar condition may existed in the Syndiniales-copepodssystems. Although we discovered these two lineages by non-copepod primers, itwould be arbitrary to designate their relationship as predator-prey system. Newmethods should be jointed to further study their complicated trophic relationship.
(5) Feeding to some scarce lineages in ambient waters: some lineages whichnever suspected to be prey of copepods were discovered in diets by molecularanalysis. Among these lineages, some even had substaintial proportion. Taketerrestrial plants Pinus and Lolium for example, they account for7.4%in QD-I_Jun.Besides, macroalage were detected in diets of C. sinicus, Scytosiphon (Phaeophyceae)and Ulva (Chlorophyta) were detected in QD-I_Jan and YRE-I_May respectively,although they were scarce in ambient waters. We speculated that the feeding of C.sinicus to these seemingly ambient water-scarce species most likely in the form oftheir pollens and swarmers.
2. Experiments to verify the feeding of some organisms
Besides the in situ fixed copepod samples, live A. pacifica and C. sinicus werecollected to conduct gut evacuation processing and the following feedingexperiments in laboratory to verify the feeding of some organisms. According towhat we found in in situ fixed copepod samples, an attempt was made to verify thefeeding of copepods to some unexpected species.4lab-cultured algae (Isochrysisgalbana Parke8701, Platymonas helgolandica Kylin var. tsingtaoensis, Pavlovaviridis and Phaeodactylum tricornutum), eggs of Sagitta crassa and larva of Artemiasalina were supplied as food in two series laboratory-controlled feeding experiments,for C. sinicus and A. pacifica respectively. Molecular detection showed that Artemia.salina was detected in diet of A. pacifica, while S. crassa wasn’t detected in the dietof C. sinicus after feeding experiments. The mostly discovered dietary species werePhaeodactylum tricornutum and Pavlova viridis. To some degree, the results showedthe bias of laboratory-controlled feeding experiments: when only one or limitedkinds of food were supplied, the real feeding habit of copepods would be masked bythe man-supplied food.
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