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(2011) Quantitative Analysis of the Fine Structure of the Fish Gill: Environmental Response and Relation to Welfare Jenjan, Hussein B.B. (2011) Quantitative analysis of the fine structure of the fish gill: environmental response and relation to welfare. PhD thesis. http://theses.gla.ac.uk/3033/ Copyright and moral rights for this thesis are retained by the author 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 Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] QUANTITATIVE ANALYSIS OF THE FINE STRUCTURE OF THE FISH GILL: ENVIRONMENTAL RESPONSE AND RELATION TO WELFARE. Fish Feeding by Hawaa Jenjan Hussein B.B. Jenjan Thesis submitted for degress of Doctor of Philosophy Institute of Biodiversity Animal Health and Comparative Medicine College of Medical, Veterinary and Life Sciences University of Glasgow September, 2011 Abstract • Methods were developed to quantify variation in gill size and microstructure and applied to three fish species: brown trout, Arctic charr and common carp. Measurements of arch length, number and length of gill rakers, number and length of gill filaments and number, length and spacing of the lamellae were taken for each gill arch and combined by principal component analyses to give length-independent scores of gill size. Levels of fluctuating asymmetry in gill arch length were also examined. Buccal and gill cavity volumes were measured from silicon moulds. Standard histological methods were used to examine gill microstructure • Benthic-feeding charr from a sample collected in Loch Awe, Scotland had relatively larger heads and buccal cavities than did sympatric pelagic-feeding fish Allowing for body size, they also had a more extensive respiratory surface, perhaps reflecting exposure to poorly oxygenated water while feeding on the loch bottom and/or a more active life style. Levels of asymmetry in gill arch length were higher in the pelagic-feeding form, which grow faster than the benthic-feeding form (Chapter 2). • Gill size and structure were compared in carp (Chapter 3) and trout (Chapter 4) classified by a standard test as having proactive, reactive or intermediate stress copping styles. Proactive carp and trout had more extensive respiratory surfaces and lower levels of hyperplasia than did reactive fish, intermediate fish lying in between. The opposite was the case for density of mucous cells, which was highest in reactive fish and lowest in proactive ones. These data suggest that maintaining a large respiratory surface may represent an unrecognised cost of a proactive coping style. • Common carp were held in mixed groups of proactive and reactive fish in one of 6 combinations of temperature (20oC and 25oC) and dissolved oxygen (3-4, 5-6 and 7-8 mg O2 L-¹) for 10 weeks. At the higher temperature fish had relatively larger heads and longer secondary lamellae, but had fewer mucous cells and a lower percentage of hyperplasia. At the lowest oxygen levels fish had relatively larger heads and a higher degree of hyperplasia than those held in normoxic and hyperoxic conditions. These results suggest that, over weeks, carp are able to “remodel” their respiratory structures in response to their current oxygen requirements. Few clear differences in response were found between proactive and reactive fish (Chapter 5). • In semi-extensively farmed carp sampled over their final production year. Short- term, acute husbandry stressors (grading and crowding) produced striking changes in 2 several potential welfare indicators, including reduced body condition, increased in plasma glucose, lactate and cortisol levels and higher level of body damage. Percentage hyperplasia and secondary lamella number and length also increased. Long-term acute stress (pre-harvest crowding in concrete tanks) was associated with increased levels of skin and fin damage and in hyperplasia and mucus cell number, reflecting high stress levels and/or poor water quality. Glucose, lactate and cortisol levels fell, suggesting either habituation to current conditions or differential mortality by physiological stress status (Chapter 6). • The results of Chapters 2-6 are synthesised in a general discussion (Chapter 7) and considered in the context of the existing literature on trophic polymorphism, on stress coping strategies, on the effects of environmental conditions of the welfare of cultured fish and on how gill structure and microstructure relate to other indicators of welfare. 3 To the soul of my late father and to my beloved mother To you my wife Asma To my daughters Hawaa and Azad. 4 Table of Contents List of Tables .........................................................................................................................9 List of Figures ......................................................................................................................16 Acknowledgements..............................................................................................................19 Author’s Declaration............................................................................................................20 CHAPTER 1 ........................................................................................................................21 1 General introduction....................................................................................................22 1.1 Introduction..........................................................................................................22 1.2 Gill structure and function .........................................................................................22 1.2.1 Gill structure .......................................................................................................23 1.2.2 Gill microstructure ..............................................................................................24 1.2.3 Habits, habitats and gill structure in fish.............................................................27 1.3 Fish stress and welfare ...............................................................................................29 1.3.1 What is animal welfare?......................................................................................29 1.3.2 Can the term welfare be applied to fishes? .........................................................29 1.3.3 Measures of welfare ............................................................................................30 1.3.4 The stress response..............................................................................................31 1.4. Aquaculture and fish welfare ....................................................................................33 1.4.1 What aquaculture is.............................................................................................33 1.4.2 Aspects of aquaculture that may compromise fish welfare ................................34 1.5 The study species .......................................................................................................37 1.5.1 Arctic charr and trophic polymorphism..............................................................38 1.5.2 Brown trout and within species variability in behaviour and physiology...........39 1.5.3 Common carp and variable coping styles ...........................................................41 1.6 Aims and structure of this thesis................................................................................42 CHAPTER 2 ........................................................................................................................44 2.1 Introduction................................................................................................................45 2.1.1 Trophic polymorphism in fishes .........................................................................45 2.1.2 The biology of Arctic charr.................................................................................47 2.1.3 Trophic polymorphism in arctic charr ................................................................47 2.1.4 Gill structure and function in fish .......................................................................49 2.1.5 Fluctuating asymmetry in gill structure ..............................................................51 2.1.6 Aims of the present study....................................................................................52 2.2 Material and Methods ................................................................................................53 2.2.1 Subjects ...............................................................................................................53 2.2.2 Morphometrics....................................................................................................53 2.2.3 Measuring fluctuating asymmetry ......................................................................55 2.2.4 Measuring body condition ..................................................................................56 2.2.5 Otolith size and age data .....................................................................................56 2.3 Results........................................................................................................................57
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