Population Ecology of Marine Cladocerans in Tolo Harbour, Hong Kong LI, Cheuk Yan Vivian a Thesis Submitted
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Population Ecology of Marine Cladocerans in Tolo Harbour, Hong Kong LI, Cheuk Yan Vivian A Thesis Submitted irt ~~rt~al? .P!+lfilm~pt'-r , -e.. ' Of the Requirements for the Degree of Master of Philosophy 1n Biology The Chinese University of Hong Kong January 2010 Thesis/Assessment Committee Professor Ka Hou CHU (Chair) Professor Chong Kim WONG (Thesis Supervisor) Professor Put 0 ANG, Jr (Committee Member) Professor Charles RAMCHARAN (External Examiner) Abstract of thesis entitled: Population Ecology of Marine Cladocerans in Tolo Harbour, Hong Kong Submitted by Ll, Cheuk Yan Vivian for the degree of Master of Philosophy in Biology at The Chinese University of Hong Kong in July 2009 Abstract This thesis provides a one year study on the population ecology of four marine cladocerans (Penilia avirostris, Pseudevadne tergestina, Pleopis polyphemoides and P. schmackeri) in Tolo Harbour, Hong Kong. Samples were obtained from November 2005 to October 2006 in Tolo Harbour and Tolo Channel. P. avirostris and P. tergestina occurred throughout most of the studied period, while P. polyphemoides and P. schmackeri occurred only from February to June 2006. Gamogenic individuals of P. tergestina and P. polyphemoides were recorded sporadically. Population dynamics of the marine cladocerans were studied and were used to infer when food, predators or temperature became the limiting factor of the growth of the populations. Birth rates were quantified based on a previous egg-ratio model of Edmondson and Paloheimo, whereas the growth rate was determined from successive population densities. Environmental factors such as temperature, dissolved oxygen content and salinity were found to limit the population growth at different times of ~he year. Fish predation played an important role in regulating the populations during February to April. Predation by chaetognaths also helped in regulating the marine cladocerans population. Feeding ecology of marine cladocerans is still meager. As food could be a limiting factor on population growth, investigation of the marine cladoceran diet would provide more information to understand their ecological role and population growth. We applied molecular technique to investigate the diet of P. tergestina. 18S RNA genes were amplified by PCR with universal eukaryotic primers using crude DNA extracted from P. tergestina. A total of 149 transformed colonies were assessed by restriction fragment length polymorphism using restriction enzyme Hae/11 and 23 unique RFLP patterns were obtained and sequenced on an ABI PRISM 3700 DNA Analyzer. Ciliates appeared to be an important prey item for P. tergestina. Picobiliphytes were also detected and had widened the size range of prey items which pod on ids can feed on. This study provides new information on what might be consumed by marine podonids apart from diatoms and dinoflagellates. II 摘要 本論文對香港吐露港海域四種海洋枝角類(鳥喙尖頭潭、肥胖僧帽潰、多型圓囊 滋及史氏圓囊道)的生態進行了一年的研究。樣本採樣自 2005 年十一月至 2006 年十月 在吐露港內及赤門海峽的兩採樣站。採樣結果發現鳥喙尖頭海和肥胖僧帽搔皆是全年 性發生，多型圓囊搔及史氏圓囊搔則發生於 2006 年二月至六月期間.採樣期間偶爾發 現肥胖僧帽法和多型圓囊淺的有性個體。 本論文透過所計算得的四種海洋枝角類的族群資料來推論海洋枝角類族群生長的 限制因素。出生率的計算方法是依從 Edmondson 和 Paloheimo 的卵比率模型，而增長 率則由鄰近族群密度所算而得。水溫、溶氧及鹽度等環境因素於採樣年度的不同時問 內限制著族群的生長。於 2006 二 月至四月期間，魚類的捕食對控制海洋枝角類族群的 生長擔當著重要角色 。 此外，海洋枝角類的另一捕食者一箭蟲'也協助限制海洋枝角 類族群的生長。 食物可是族群生長的限制因素之一，探討海洋枝角類的攝食資料有助進一步了解 牠們於生態環境中擔演的角色及其族群生長情況。由於海洋枝角類的覓食生態資料缺 乏，第二章以利用分子技術來對肥胖僧帽潰的覓食生態進行研究。 我們從肥胖僧帽淺中抽取出 DNA ，然後以引子對 185 RNA 進行聚合酵素鏈鎖反應擴 增。取得共 149 個殖株後，使用 HaeIII 限制晦切割進行限制晦片段度多型分析，並取 得 23 個獨特的限制晦片段長度多型性形態，再利用 ABI PRISM 3700 DNAAnalyzer 對 每個限制晦片段長度多型性形態進行基因排列分析 。 研究結果顯示纖毛蟲是肥胖僧帽潰的主要食物 。 此外，微藻類的發現擴闊了圓囊 蚤可攝的食物大小的範圍。是次研究為海洋圓囊蚤提供了新的覓食資料。 III Acknowledgements I would like to express my greatest gratitude to my supervisor Professor C. K. Wong for his guidance and patience throughout my M. Phil study. I would also like to thank Professor K.H. Chu and Professor P.O. Ang for their valuable opinions. I appreciated the assistance from all the staff and labmates in MSL. Special thanks to Mr. Y. H. Yung for his assistance in the weekly field samplings, Mr. M. K. Cheung for his guidance and help in completing the molecular part, and Mr. K. M. Chau for his support. I would also like to thank Miss M. Fung for her support in times of frustration and exhaustion. IV Table of Contents Page Abstract (in English) I Abstract (in Chinese) III Acknowledgements IV Table of contents v List of figures VIII List of tables XII List of plates XIII Chapter 1 Population Dynamics of Marine Cladocerans in Tolo Harbour 1.1 Introduction 1 1.1.1 Study site 1.1.2 Species description and distribution 2 1.1.3 Population dynamics of marine cladocerans 4 1.1.3.1 Reproduction 5 1.1.3.2 Fecundity of marine cladocerans 6 1.1.3.3 Embryonic development time 7 1.1.3.4 Food 7 1.1.3.5 Predation 8 v 1.2 Objective 9 1.3 Materials and method IO 1.3.1 Field sampling 10 1.3.2 Hydrographical parameters and chlorophyll a concentration 10 1.3.3 Zooplankton sampling II 1.3.4 Zooplankton analysis 11 1.3.5 Calculation of Population Parameters 12 1.4 Results 16 1.4.1 Hydrographical parameters I6 1.4.1.1 Temperature I6 1.4.1.2 Salinity 16 1.4.1.3 Dissolved Oxygen content 17 1.4.2 Chlorophyll a concentration I7 1.4.3 Seasonal occurrence of marine cladocerans in Tolo Harbour 26 1.4.4 Parameters of the marine cladocerans populations 32 1.4.5 Occurrence of gamogenic individuals of marine cladocerans 51 1.4.6 Occurrence of chaetognaths 51 1.5 Discussion 57 1.6 Conclusion 66 VI Chapter 2 Molecular detection of the diet of the marine cladocerans, Pseudevadne tergestina 2.1 Introduction 68 2.1.1 The importance of marine cladocerans 68 2.1.2 Previous findings on cladoceran diet 69 2.1.2.1 Sidid cladocerans 69 2.1.2.2 Podonid cladocerans 69 2.1.3 Methods to investigate the feeding habit of animals 71 2.1.4 Application of molecular detection 72 2.2 Objectives 73 2.3 Materials and method 74 2.3.1 Zooplankton sampling and preparation 74 2.3.2 DNA extraction 74 2.3.3 18S rRNA gene amplification 75 2.3.4 18S rRNA Cloning 76 2.3.5 Clone screening by RFLP 76 2.3.6 Sequencing and phylogenetic analysis 77 2.4 Results 78 2.4.1 Alveolata 78 2.4.2 Other lineages 79 2.5 Discussion and conclusion 85 2.5.1 Errors and improvements 87 Reference 89 VII List of Figures Figure Page Figure 1.1 14 Location of sampling stations, TH and TC, in Tolo Harbour, Hong Kong SAR. Figure 2.1 19 Averaged water temperature at the two sampling stations, Tolo Harbour (TH) and Tolo Channel {TC). Figure 2.2 20 Thermoclines at the two sampling stations, TH and TC, from June-August 2006. Figure 2.3 21 Averaged salinity at the two sampling stations, Tolo Harbour (TH) and Tolo Channel (TC). Figure 2.4 22 Haloclines at the two sampling stations, TH and TC, from June-August 2006. Figure 2.5 23 Averaged dissolved oxygen at the two sampling station, Tolo Harbour {TH) and Tolo Channel (TC). Figure 2.6 24 Oxyclines at the two sampling stations, TH and TC, from June-August 2006. Figure 2.7 25 Chlorophyll a concentrations at the two sampling stations, TH and TC. Figure 2.8 28 Seasonal abundance of Penilia avirostris at two sampling stations, TH and TC. Figure 2.9 29 Seasonal abundance of Pseudevadne tergestina at two sampling stations, TH and TC. VIII Figure 2.10 30 Seasonal abundance of Pleopis polyphemoides at two sampling stations, TH and TC. Figure 2.11 31 Seasonal abundance of Pleopis schmackeri at two sampling stations, TH and TC. Figure 2.12a 35 Size distribution of Penilia avirostris in Tolo Harbour. Figure 2.12b 36 Size distribution of Penilia avirostris in Tolo Channel. Figure 2.13a 37 Frequency distributions of parthenogenetic females of Penilia avirostris with different brood size in Tolo Harbour. Figure 2.13b 38 Frequency distributions of parthenogenetic females of Penilia avirostris with different brood size in Tolo Channel. Figure 2.14 39 Population parameters of Penilia avirostris at two sampling stations, a) birth rate, b) growth rate and c) death rate Figure 2.15a 40 Size distribution of Pseudevadne tergestina in Tolo Harbour. Figure 2.15b 41 Size distribution of Pseudevadne tergestina in Tolo Channel. Figure 2.16a 42 Frequency distributions of parthenogenetic females of Pseudevadne tergestina with different brood size in Tolo Harbour. Figure 2.16b 43 Frequency distributions of parthenogenetic females of Pseudevadne tergestina with different brood size in Tolo Channel. IX Figure 2.17 44 Population parameters of Pseudevadne tergestina at two sampling stations, a) birth rate, b) growth rate and c) death rate. Figure 2.18 45 Size distribution of Pleopis polyphemoides in Tolo Harbour and Tolo Channel. Figure 2.19 46 Frequency distributions of parthenogenetic females of Pleopis polyphemoides with different brood size in Tolo Harbour and Tolo Channel. Figure 2.20 47 Population parameters of Pleopis polyphemoides at two sampling stations, a) birth rate, b) growth rate and c) death rate. Figure 2.21 48 Size distribution of Pleopis schmackeri in Tolo Harbour and Tolo Channel. Figure 2.22 49 Frequency distributions of parthenogenetic females of Pleopis schmackeri with different brood size in Tolo Harbour and Tolo Channel. Figure 2.23 50 Population parameters of Pleopis schmackeri at two sampling stations, a) birth rate, b) growth rate and c) death rate. Figure 2.24 52 Percentage of gameogenic individuals of Pseudevadne tergestina in Tolo Harbour and Tolo Channel. Figure 2.25 53 Percentage of gameGgenic individuals of Pleopis polyphemoides in Tolo Harbour and Tolo Channel. Figure 2.26 56 Seasonal abundance of chaetognaths in Tolo Harbour and Tolo Channel. X Figure 3.1 80 Gel photo showing all restriction fragment length polymorphism (RFLP) patterns in the current study. Figure 3.2 84 Neighbor-joining phylogenetic trees based on 18s rRNA sequences.