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University of Southampton Research Repository Eprints Soton University of Southampton Research Repository ePrints Soton Copyright © and Moral Rights for this thesis are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given e.g. AUTHOR (year of submission) "Full thesis title", University of Southampton, name of the University School or Department, PhD Thesis, pagination http://eprints.soton.ac.uk UNIVERSITY OF SOUTHAMPTON NUTRITIONAL REGULATION OF EGG PRODUCTION OF CALANUS FINMARCHICUS IN THE NORTH ATLANTIC Daniel Justin Mayor A thesis presented for the degree of Doctor of Philosophy Faculty of Science School of Ocean and Earth Science Southampton Oceanography Centre March 2005 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF SCIENCE SCHOOL OF OCEAN AND EARTH SCIENCE Doctor of Philosophy NUTRITIONAL REGULATION OF EGG PRODUCTION OF CALANUS FINMARCHICUS IN THE NORTH ATLANTIC by Daniel Justin Mayor Ship-board experiments in the North Atlantic were used to study how food quality influences the egg production of Calanus finmarchicus feeding on natural planktonic diets. Food quality was expressed in terms of carbon (C), nitrogen (N), and the essential fatty acids eicosapentaenoic acid (EPA; 20:5(n-3)) and docosahexaenoic acid (DHA; 22:6(n-3)). Five consecutive 24 hr bottle incubations were conducted in April and July/August 2002 under in situ conditions to determine egg production rates and the ingested quantities of C, N, EPA and DHA. Biomass contributions towards growth were determined and the biochemical composition of the eggs was examined. In order to accurately determine ingestion rates, a method to account for microzooplankton grazing in particle removal experiments was developed. Balanced physiological budgets were compiled for C. finmarchicus in both seasons. The input terms of these budgets consisted of ingestion and the use of biomass, and the outputs were growth, respiration, excretion and egestion. Respiration and excretion were not determined experimentally, and were therefore determined by mass balance and compared to literature-derived values. In April, close agreement between literature- and mass balance-derived rates of respiration and excretion demonstrated that the experimentally determined components of the budget were accurate. Ingestion rates were low, and > 80 % of the C utilised was derived internally from somatic biomass. The absence of storage fatty acids and the low C:N ratio (~ 4 µg µg-1) of the biomass lost from the females indicated that these animals had been catabolising structural protein and were close to exhaustion. This suggests that when food is scarce, C. finmarchicus adopts a semelparous reproductive strategy. In July/August, the observed growth exceeded the estimated ingestion rates. This shortfall was possibly provided by cannibalising eggs. Assuming that EPA and DHA were used with high efficiency (0.9), the stoichiometric analysis predicted that these compounds were non-limiting in April. Using typical maximum growth efficiencies for C (< 0.6) and N (0.4), the former was predicted to be limiting because the biomass utilised was rich in N, EPA and DHA relative to the demand for C. Graduate School of the Southampton Oceanography Centre This PhD dissertation by Daniel Justin Mayor has been produced under the supervision of the following persons: Supervisors: Dr Thomas Anderson Dr David Pond Dr Xabier Irigoien Dr John Williams DECLARATION OF AUTHORSHIP I, Daniel Mayor, declare that the thesis entitled ‘Nutritional regulation of egg production of Calanus finmarchicus in the North Atlantic’ and the work presented in it are my own. I confirm that: • This work was done wholly while in candidature for a research degree at the University of Southampton; • Part of the work presented in chapter 3 has been submitted for publication in Marine Ecology-Progress Series. This paper is co-authored by Drs T. Anderson, X. Irigoien and D. Pond, although they only contributed by providing comments on the manuscript and scientific advice; • Where I have consulted the published work of others, this is always clearly attributed; • Where I have quoted from the work of others, the source is always given. With the exception of such quotations, this thesis is entirely my own work; • I have acknowledged all main sources of help. Contents Figure list I Table list VI 1. Introduction 1.1. Copepods in the North Atlantic 1 1.2. Understanding what limits copepod production 1 1.2.1. Elemental Stoichiometry 3 1.3. Lipids and fatty acids in Calanus 5 1.3.1. The life-cycle of C. finmarchicus 6 1.3.2. The lipid composition of C. finmarchicus 7 1.3.3. Essential fatty acids in Calanus 8 1.3.4. Extending stoichiometry theory to micronutrients 9 1.3.5. The origin of EPA and DHA in copepods 10 1.3.6. Homeostasis of EPA and DHA in Calanus 10 1.3.7. Homeostasis of essential fatty acids in the eggs of Calanus 11 1.4. Food and feeding selectivity 11 1.4.1. Calanus and detritus 14 1.5. The use of characteristic ‘biomarker’ fatty acids 15 1.6. Objectives of the thesis 18 1.7. Summary of the thesis 19 2. Experimental and analytical methods 2.1. Collection of samples 21 2.2. General procedure 21 2.3. Experimental protocol 21 2.3.1. Animals 21 2.3.2. Collection of water 24 2.3.3. Incubation protocol 24 2.3.4. Eggs 25 2.3.5. Particulate sampling 25 2.4. Microplankton analysis 26 2.4.1. Sample preparation 26 2.4.2. Cell counts 27 2.4.3. Reliability of the cell counts 27 2.4.4. Cell volume estimations 27 2.4.5. Volume:Carbon regression equations 28 2.4.6. Shrinkage effects of Lugol’s 28 2.5. Organic carbon and nitrogen analysis 30 2.5.1. Removal of inorganic carbon 30 2.5.2. Preparation of filters for analysis 31 Calibration and running procedures for Carlo Erba EA1108 31 2.5.3. C/N analyzer 2.6. Fatty acid analysis 33 2.6.1. Extraction 33 2.6.2. Alkaline hydrolysis (saponification) 33 2.6.3. Preparation of PFB esters (fatty acid derivatization) 34 2.6.4. Purification 34 2.6.5. Injection and identification of fatty acids 35 2.6.6. Quantification of fatty acids 35 2.7. Statistical analysis 35 3. Quantifying copepod grazing when using natural plankton assemblages 3.1. AIMS 37 3.2. INTRODUCTION 37 3.3. THEORY 39 3.4. METHODS 45 3.4.1. Estimating specific gross growth rates (r) with a simple 45 mathematical model 3.4.2. Maximal growth rates (µmax) 45 3.4.3. Nutrient limitation 47 3.4.4. Assigning trophic status to protists 53 3.4.5. Calculating copepod grazing and prey preferences 53 3.5. RESULTS 55 3.5.1. Microplankton dynamics in the control bottles 55 3.5.2. Selective removal of microzooplankton 62 3.5.3. Microplankton dynamics in the experimental bottles 62 3.5.4. Sensitivity analysis 70 3.6. DISCUSSION 70 3.6.1. Microplankton dynamics in the control bottles 70 3.5.2. Selective removal of microzooplankton 76 3.5.3. Microplankton dynamics in the experimental bottles 76 3.7. CONCLUSIONS 79 4. Nutritional quantity and quality of the particulate environment in April and July/August 4.1. AIMS 80 4.2. METHODS 80 4.2.1. Statistical methods 80 4.3. RESULTS 81 4.3.1. The particulate environment 81 4.3.1.1. April 83 4.3.1.2. July/August 83 4.3.2. Microplankton community composition and biomass 83 4.3.2.1. April 83 4.3.2.2. July/August 89 4.3.3. Quantitative comparison of the microplankton assemblages 89 observed in April and July/August: Multivariate approach 4.3.4. Particulate fatty acid composition and quantity 90 4.3.4.1. April 90 4.3.4.2. July/August 97 4.3.5. Quantitative comparison of individual fatty acids in the 97 particulates between April and July/August: Multivariate approach. 4.3.6. Correlation analysis 99 4.3.6.1. Particulate descriptors 99 4.3.6.2. Microplankton species assemblage and fatty acid 99 biomarkers 4.4. DISCUSSION 103 4.4.1. Environmental data 103 4.4.2. Particulate descriptors 103 4.4.3. Microplankton community composition 105 4.4.4. Availability of microplankton to adult C. finmarchicus 106 4.4.5. Understanding the contribution of detritus to the particulate 107 samples 108 4.4.6. Assessing the quantity of food available for C. finmarchicus 109 4.4.7. The quality of food available to C. finmarchicus 110 4.4.7.1. April 110 4.4.7.2. July/August 111 4.4.8. Evaluation of particular fatty acids as biomarkers for 111 individual microplankton groups 4.5. SUMMARY 112 5. Ingestion and food selection of Calanus finmarchicus feeding above the Reykjanes Ridge in April and July/August: examining the dynamics of incubation experiments 5.1. AIMS 115 5.2. METHODS 115 5.2.1. Statistical methods 115 5.3. RESULTS 116 5.3.1. Particulate dynamics 116 5.3.1.1. April 116 5.3.1.2. July/August 118 5.3.2. Clearance and ingestion 120 5.3.2.1. April 120 5.3.2.2. July/August 127 5.3.3. Particulate variables as predictors of copepod ingestion 129 5.3.4.
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