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Calanus Helgolandicus in the Western English Channel: Population Dynamics and the Role of Mortality

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Calanus Helgolandicus in the Western English Channel: Population Dynamics and the Role of Mortality Calanus helgolandicus in the western English Channel: population dynamics and the role of mortality Thesis submitted in accordance of the requirements of Queen Mary, University of London for the degree of Doctor in Philosophy by Jacqueline Lesley Maud March 2017 1 Statement of Originality I, Jacqueline Lesley Maud, confirm that the research included within this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original, and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other Intellectual Property Right, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. Signature: Date: 29th March 2017 2 Collaborations: All chapters: L4 mesozooplankton and microplankton weekly time series sampling and identification were undertaken by Plymouth Marine Laboratory (PML) technicians and plankton analysts. Weekly egg production experiments were collected and analysed by Andrea McEvoy, who also made the ongoing time series data since 1992 available. Routine CTD and water sampling data (temperature, salinity, O2, turbidity, chlorophyll- a) were produced by PML scientists. Chapter Two: Egg hatch success and abnormal nauplii data were collected throughout 2013 by J. L. Maud (JLM). All data analysis was performed by JLM. Chapter Three: C. helgolandicus egg hatch success and naupliar abnormalities data were collected by J. L. Maud during 2013 and 2016; 2015 data collected by N. Djeghri, PML (ND). C. helgolandicus eggs were collected for fatty acid analysis by JLM; chemical fatty acid analysis undertaken by D. White, PML (DW). Mesozooplankton biomass conversions were performed by A. Atkinson, PML (AA) and M. Lilley, QMUL (ML). Mortality rate estimations and all data analyses were performed by JLM. Chapter Four: C. helgolandicus stage composition 2002-2004 was undertaken by D. Bonnet and A. G. Hirst, QMUL (AGH); 2012-2013 stage composition was undertaken by JLM. The collection and neutral red staining of mesozooplankton, sample processing and identification was undertaken by JLM. Mesozooplankton biomass conversions were performed by AA and ML. Young fish trawl abundance data from L4 were provided by N. Halliday, MBA (NH). Mortality rate estimations and all data analyses were performed by JLM. Chapter Five: Gelatinous zooplankton collection, DNA extraction, PCR amplification and visualisation using gel electrophoresis gel and cleaning of PCR products was undertaken by JLM. Sequencing data processing was undertaken by MR DNA. Bioinformatic processing and species analysis was performed by JLM. 3 Publications: Maud, J. L., A. Atkinson, A. G. Hirst, P. K. Lindeque, C. E. Widdicombe, R. A. Harmer, A. J. McEvoy and D. G. Cummings. 2015. How does Calanus helgolandicus maintain its population in a variable environment? Analysis of a 25-year time series from the English Channel. Progress in Oceanography 137, Part B: 513-523 (Chapter Two) Maud, J. L., A. G. Hirst, A. Atkinson, P. K. Lindeque and A. J. McEvoy. (In review). Mortality of Calanus helgolandicus: sources, differences between the sexes and consumptive and non-consumptive processes. Limnology and Oceanography (Chapter Four). Maud, J. L., A. Atkinson, A. G. Hirst, D. White, P. K. Lindeque, C. E. Widdicombe and A. J. McEvoy. (In preparation). Calanus helgolandicus egg mortality; egg hatch success, naupliar abnormalities and the impact of predators (Chapter Three). Atkinson, A., R. A. Harmer, C. E. Widdicombe, A. J. McEvoy, T. J. Smyth, D. G. Cummings, P. J. Somerfield, J. L. Maud and K. McConville. 2015. Questioning the role of phenology shifts and trophic mismatching in a planktonic food web. Progress in Oceanography 137: 498-512 (Chapter Two). White, D. A., C. E. Widdicombe, P. J. Somerfield, R. L. Airs, G. A. Tarran, J. L. Maud and A. Atkinson. 2015. The combined effects of seasonal community succession and adaptive algal physiology on lipid profiles of coastal phytoplankton in the Western English Channel. Marine Chemistry 177, Part 4: 638-652 (Chapter Three). 4 ABSTRACT Calanus helgolandicus is a key copepod species occurring in the North East Atlantic that is responding to oceanic warming through an expansion of its geographic range. This range extension has led to concerns about how this may affect ecosystem trophodynamics. Here I investigate the interannual variability and seasonality of C. helgolandicus, using a ~28 year time-series from the western English Channel (station L4). I focus specifically on the role of mortality, as a key life history process that is challenging to quantify and historically has received little attention. C. helgolandicus abundance remained within a narrow ~four-fold interannual envelope, which was a consequence of multiple losses that removed ~99% of the potential population. Loss of early life stages occurred through the incidence of non-viable eggs and abnormal nauplii (both higher in spring), and via predation; egg mortality rates were positively correlated with C. helgolandicus copepodite abundance and total copepod biomass, indicative of intraguild predation and cannibalism. By contrast, late-stage copepodite mortality rates were highest in autumn, and were positively related to gelatinous predator abundance and biomass (medusae, ctenophores and chaetognaths). Molecular gut-content analyses revealed that two abundant jellyfish species present during 2015 (Pleurobrachia pileus and Leuckartiara octona) both preyed on C. helgolandicus. Adult male consumptive mortality rates were ~6 times higher than that of adult females; whereas male non-consumptive rates were only ~1.5 times that of females, providing evidence that predation was the primary mortality source in males. Non-consumptive mortality rates contributed 0-54% (median of 4.5%) to total mortality and were positively related to the 72-hour maximum wind speed, implying that turbulence created during extreme weather events may increase zooplankton mortality. I conclude that C. helgolandicus population control is modulated via a series of mortality-related losses occurring through the different development stages; from reduced egg viability to predation of copepodites by gelatinous carnivores. Although I find little evidence for changing ecosystem trophodynamics at L4, my results contribute to the knowledge of C. helgolandicus population dynamics at a site near the centre of its distribution, and suggest that a future expanding population may be a valuable food source for a variety of predators. 5 TABLE OF CONTENTS STATEMENT OF ORIGINALITY ..................................................................................... 2 COLLABORATIONS ..................................................................................................... 3 PUBLICATIONS ........................................................................................................... 4 ABSTRACT .................................................................................................................. 5 ACKNOWLEDGEMENTS ............................................................................................ 14 CHAPTER ONE .......................................................................................................... 15 GENERAL INTRODUCTION................................................................................................... 15 CHAPTER TWO ......................................................................................................... 24 HOW DOES CALANUS HELGOLANDICUS MAINTAIN ITS POPULATION IN A VARIABLE ENVIRONMENT? ANALYSIS OF A 25-YEAR TIME SERIES FROM THE ENGLISH CHANNEL .......................................... 24 2.1 Introduction .................................................................................................. 26 2.2 Materials and methods ................................................................................. 27 2.2.1 Mesozooplankton data collection ............................................................. 27 2.2.2 Egg production rate ................................................................................... 29 2.2.3 Egg hatching success and naupliar abnormalities .................................... 29 2.2.4 Phyto- and microzooplankton ................................................................... 30 2.2.5 Chlorophyll-a ............................................................................................. 31 2.2.6 Temperature and Stratification Index ....................................................... 31 2.2.7 Phenological indices .................................................................................. 32 2.2.8 Numerical and statistical analyses ............................................................ 33 2.3 Results ........................................................................................................... 34 2.3.1 Overview of average seasonality at L4 ....................................................
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