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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 FACULTY OF ENGINEERING, SCIENCE & MATHEMATICS School of Ocean and Earth Sciences The physiological ecology of the specialist lagoon amphipod, Gammarus insensibilis By Andrew Russell Gates Thesis for the degree of Doctor of Philosophy December 2006 Graduate School of the National Oceanography Centre, Southampton This PhD. dissertation by Andrew Russell Gates has been produced under the supervision of the following persons Supervisors Dr. Martin Sheader Dr. John Williams Dr. Roger Bamber Chairs of Advisory Panel Prof. Paul Tyler Dr. Lawrence Hawkins i University of Southampton ABSTRACT FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS SCHOOL OF OCEAN AND EARTH SCIENCES Doctor of Philosophy THE PHYSIOLOGICAL ECOLOGY OF THE SPECIALIST LAGOON AMPHIPOD, GAMMARUS INSENSIBILIS By Andrew Russell Gates Coastal lagoons are habitats of conservation importance. The characteristic fauna of lagoons includes a number of specialist species, some of which are scheduled for protection. Work on the conservation of coastal lagoons has suggested that detailed information on the ecology of lagoon specialist species is essential to ensure management strategies are relevant to the lagoonal species. This study addresses this issue by providing information about the monthly reproductive investment and energy-balance as well as interactions with parasites for the specialist lagoon amphipod, Gammarus insensibilis (Stock). For comparison information is also presented on the reproductive investment of the lagoonal isopod Idotea chelipes (Pallas). Gilkicker lagoon on the south coast of England, UK, from which the majority of samples were taken, demonstrated environmental variability characteristic of coastal lagoons. Annually, temperature varied between 2 and 28 °C and salinity fluctuated between extremes of 24 and 39. The Lymington-Keyhaven lagoons, also on the south coast of England, demonstrated similar variation. This has implications for Gammarus insensibilis, and effects on reproductive investment were evident. The amphipod was shown to employ a continuous reproductive strategy but while the overall investment, expressed as clutch volume, remained relatively stable over the course of the year, the individual components varied. In the summer, when weight-specific embryo number was at its highest with a mean of 13 embryos mg dry wt.-1 the mean size of the individual embryos was small (0.032 mm3). The opposite was true in the winter months, with mean brood sizes as low as 6 embryos mg dry wt.-1 while mean embryo volume was larger, at 0.04 mm3. Idotea chelipes demonstrated a more seasonal reproductive strategy in which winter reproductive output was low. The environmental variability also had effects on the metabolic rates of individual amphipods with temperature related increases in feeding and respiration rates in the summer months. Scope For Growth (SFG), a measure of net energy availability to the organism, was variable during the year and was unrelated to temperature and salinity. Lowest SFG occurred in spring in conjunction with peak reproductive output. This suggested that the amphipods were well adapted to the environmental variation of the lagoon and that it was reproductive investment that represented an important cost to the organism. Eighty four percent of G. insensibilis from Gilkicker were shown to be infected by microphallid trematode parasites. Reproductive investment was negatively affected, with a 36.6 % reduction in weight-specific brood size associated with higher degrees of infection. Respiration rates were also reduced in the infected organisms. The high prevalence of the parasites and the related effects on the host suggest that trematode infection should be considered, alongside the characteristic habitat variability, as an important aspect of the ecology of lagoons. ii Table of Contents Chapter 1 General Introduction 1 1.1 Brief introduction 1 1.2 Lagoons 1 1.2.1 The coastal lagoon environment 2 1.2.2 Lagoon organisms 4 1.2.3 Adaptations to the lagoon environment 6 1.3 Study organisms 8 1.3.1 Gammarus insensibilis 9 1.3.2 Idotea chelipes 10 1.4 Reproductive biology of peracarids 11 1.4.1 Physico-chemical effects 11 1.4.2 Geographic effects 12 1.4.3 Parasitism 13 1.5 Stress 14 1.5.1 Stress resistance and the stress response 15 1.5.1.1 Behavioural responses 16 1.5.1.2 Heat shock proteins 16 1.5.1.3 Endocrine responses 17 1.5.2 Differential susceptibility to stress 17 1.5.3 The energetic costs of stress and trade-offs 18 1.6 Bioenergetics, energy balance and the energy equation 20 1.6.1 “Scope For Growth” and stress 21 1.6.2 Factors affecting “Scope For Growth” 21 1.7 Parasites associated with lagoon species 25 1.8 Aims and objectives of the study 27 Chapter 2 Site descriptions 28 2.1 Study sites 28 2.1.1 Gilkicker 28 2.1.1.1 Salinity 31 2.1.1.2 Temperature 32 2.1.1.3 Dissolved oxygen 32 2.1.1.4 pH 32 2.1.1.5 Nutrients 33 2.1.1.6 Sediment total organic matter 33 2.1.2 Lymington-Keyhaven lagoons 34 2.1.3 Moulton Marsh lagoons 34 iii 2.2 Temperature and salinity records for the present study 34 2.2.1 Gilkicker 35 2.2.1.1 Temperature 35 2.2.1.2 Salinity 36 2.2.2 Lymington-Keyhaven 37 2.2.3 Moulton Marsh 37 2.3 Discussion 38 Chapter 3 Methods 40 3.1 Sample collection 40 3.2 Population dynamics and reproductive investment 43 3.2.1 Population structure 43 3.2.2 Size of individual embryos 46 3.2.3 Brood size 48 3.2.4 Brood mass 52 3.2.5 Clutch volume 53 3.3 Bioenergetics 56 3.3.1 Energy loss (respiration and excretion) 56 3.3.1.1 Respiration rate 56 3.3.1.2 Excretion rate 56 3.3.2 Energy gain (Feeding and assimilation) 57 3.3.2.1 Feeding rate 57 3.3.2.2 Assimilation efficiency 57 3.3.2.3 Assimilation rate 57 3.4 Statistical analysis 58 Chapter 4 The annual variation in the population dynamics of Gammarus insensibilis 59 4.1 Introduction 59 4.2 Methods 62 4.3 Results 63 4.3.1 Summary of reproductive factors 63 4.3.2 Monthly brood sizes 65 4.3.3 Monthly embryo sizes 67 4.3.4 Clutch volumes and brood sizes 69 4.3.5 Juvenile size 71 4.3.6 Loss of embryos and brood parasitism 72 4.3.7 Sex ratio 74 4.3.8 Population structure 75 4.4 Discussion 79 4.4.1 Reproductive biology of gammarid amphipods 79 4.4.2 Reproductive investment 79 4.4.3 Population structure 84 iv Chapter 5 Seasonal variation in the energy balance of G. insensibilis 87 5.1 Introduction 87 5.1.1 Energy loss 88 5.1.2 Energy uptake 89 5.2 Methods 91 5.3 Results 92 5.3.1 Feeding and assimilation rate 92 5.3.2 Respiration rate 103 5.3.3 Excretion rate 105 5.4 Discussion 110 Chapter 6 SFG, reproduction and links between levels of biological organisation 118 Chapter 7 The physiological tolerances of G. insensibilis 127 7.1 Introduction 127 7.2 Methods 130 7.3 Results 133 7.4 Discussion 140 Chapter 8 The effects of trematodes on the biology of G. insensibilis 147 8.1 Introduction 147 8.2 Materials and methods 151 8.3 Results 153 8.3.1 Respiration rate 156 8.3.2 Feeding rate 160 8.3.3 Effects on reproduction 161 8.4 Discussion 166 v Chapter 9 The reproductive biology of Idotea chelipes 176 9.1 Introduction 176 9.2 Methods 178 9.3 Results 179 9.4 Discussion 186 Chapter 10 Summary and general discussion 191 Chapter 11 References 200 vi List of Figures Chapter 1 1.1 Chaetomorpha linum and its inhabitants 9 1.2 The complex life cycle of trematodes 26 Chapter 2 2.1 The location of Gilkicker and the Lymington-Keyhaven lagoons 30 2.2 The temperature and salinity of Gilkicker and the adjacent Solent 35 2.3 The temperature difference between Gilkicker lagoon and The Solent 36 2.4 The salinity difference between Gilkicker lagoon and The Solent 36 2.5 The temperature and salinity of 8-Acre Pond and Salterns lagoons 37 Chapter 3 3.1 Gilkicker lagoon viewed from the barrier with to The Solent 41 3.2 Chaetomorpha linum in near shore shallow water at Gilkicker lagoon 42 3.3 The water outlet from Gilkicker lagoon at low tide 43 3.4 The length measurements taken on the Gammarus insensibilis specimens 44 3.5 Oöstegite development in female Gammarus insensibilis 45 3.6 The relationship between female Gammarus insensibilis head length and dry 46 weight on brood size 3.7 The relationship between female Gammarus insensibilis size and embryo size 47 3.8 The changes in Gammarus insensibilis embryo volume with developmental 48 stage 3.9 The effect of female Gammarus insensibilis size on brood size 49 3.10 The effect of female Gammarus insensibilis dry weight on weight-specific 50 brood size 3.11 Changes in the weight-specific brood size with developmental stage in broods 51 of Gammarus insensibilis 3.12 Seasonal changes in the weight-specific brood size of Gammarus insensibilis 51 with developmental stage 3.13 The relationship between
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