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University of Southampton Research Repository University of Southampton Research Repository Copyright © and Moral Rights for this thesis and, where applicable, any accompanying data 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 and the accompanying data cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content of the thesis and accompanying research data (where applicable) must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holder/s. When referring to this thesis and any accompanying data, full bibliographic details must be given, e.g. Thesis: Author (Year of Submission) "Full thesis title", University of Southampton, name of the University Faculty or School or Department, PhD Thesis, pagination. Data: Author (Year) Title. URI [dataset] UNIVERSITY OF SOUTHAMPTON FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science The effects of daily cyclic hypoxia on the ecophysiology of the Atlantic ditch shrimp, Palaemon varians By Luca Peruzza Thesis for the degree of Doctor of Philosophy Submitted November 2017 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science Thesis for the degree of Doctor of Philosophy THE EFFECTS OF DAILY CYCLIC HYPOXIA ON THE ECOPHYSIOLOGY OF THE ATLANTIC DITCH SHRIMP, PALAEMON VARIANS Luca Peruzza Oxygen partial pressure (pO2) is not always constant in aquatic environments and can vary on different time scales, from hours to weeks. In many coastal environments, such as estuaries, lagoons or marshes, pO2 levels can vary on a daily base, resulting in daily cyclic hypoxia. By monitoring temperature and pO2 in the Lymington salt marshes (UK), I was able to quantify diel and seasonal pO2 variability in this coastal habitat: diel oscillations in pO2 were measured in winter, spring and summer, and the greatest pO2 oscillations were recorded in summer, when pO2 could fluctuate from ~42 kPa to ~ 1 kPa every 12 hours, causing diel cyclic hypoxia. Even if cyclic hypoxia is common in numerous coastal areas around the world and affects many species, this phenomenon is less studied in comparison to acute or chronic hypoxia. The aim of this thesis was to characterize the short-term effects and the long-term consequences of daily cyclic hypoxia on the physiology of an important decapod crustacean, Palaemon varians. This species was found in the Lymington salt marshes (UK) and, in the laboratory, was subjected to a cyclic hypoxic regime that mimicked conditions measured in the field during summer. In the laboratory, a short 8-hour exposure to hypoxia (pO2 < critical oxygen pressure, pcrit) induced behavioural and metabolic changes and suppressed feeding and ammoniacal excretion. Long-term exposure to diel cyclic hypoxia induced changes in the transcriptome of the animals, prompted an acceleration of the moult cycle (validated at transcriptional and phenotypic level) and eventually resulted in morphological changes to the gills, which increased lamellar surface area. Further, long-term exposure to cyclic hypoxia impaired animal’s growth (in terms of body weight and length), reduced ammoniacal excretion and negatively influenced reproduction by reducing egg yolk content. Interestingly, long-term acclimation to cyclic hypoxia increased thermal tolerance and copper tolerance in comparison to control animals, probably as a consequence of the morphological changes to the gills induced by cyclic hypoxia. Overall, results underline that a short hypoxic exposure repeated daily was able to induce in P. varians alterations at multiple levels of biological organisation. In particular, the observed long-term consequences (i.e. growth reduction, reduced ammoniacal excretion and impaired reproduction) might have important ecological implications for the species and for its ecosystem. Table of Contents Table of Contents .................................................................................................................. i Table of Tables ..................................................................................................................... v Table of Figures .................................................................................................................. vii Academic Thesis: Declaration Of Authorship ............................................................... xiii Acknowledgements ............................................................................................................ xv Chapter 1 Introduction ...................................................................................................... 1 1.1 Physics of gas – fundamental principles: ................................................................. 1 1.2 Hypoxia in aquatic environments: ........................................................................... 3 1.3 What are the current limitations in defining hypoxia at ecosystem level? .............. 5 1.4 How is hypoxia identified at individual level? ........................................................ 7 1.5 Physiological adaptations to low pO2: ................................................................... 11 1.6 Chronic hypoxia: ................................................................................................... 14 1.6.1 Consequences of chronic hypoxia on whole organism’s physiology: ............. 15 1.7 Daily cyclic hypoxia in shallow water and coastal habitats: ................................. 17 1.8 Study organism: ..................................................................................................... 21 1.8.1 Habitat and ecology: ........................................................................................ 22 1.8.2 Palaemon varians’ physiological adaptations to decreasing pO2: .................. 24 1.9 Thesis aims and objectives: ................................................................................... 25 Chapter 2 Diel fluctuations in temperature and pO2 within the Lymington salt marshes (UK) and effects of a short-term hypoxic exposure on Palaemon varians in the laboratory ............................................................................... 27 Summary: ........................................................................................................................ 27 2.1 Introduction: .......................................................................................................... 28 2.2 Specific chapter hypothesis: .................................................................................. 29 2.3 Material and Methods: ........................................................................................... 30 2.3.1 Environmental variability: ............................................................................... 30 2.3.2 Laboratory determination of Palaemon varians’ pcrit: ..................................... 32 2.3.3 Design and creation of the experimental system: ............................................ 33 2.3.4 Short-term (8-hour) hypoxic exposure: ........................................................... 35 2.4 Results: .................................................................................................................. 36 i 2.4.1 Environmental variability: ............................................................................... 36 2.4.2 Laboratory determination of Palaemon varians’ pcrit and short-term (8-hour) hypoxic exposure: .................................................................................... 40 2.5 Discussion: ............................................................................................................. 44 2.5.1 Environmental variability: ............................................................................... 44 2.5.2 Laboratory determination of Palaemon varians’ pcrit and short-term (8-hour) hypoxic exposure: .................................................................................... 48 2.6 Conclusions: .......................................................................................................... 53 Chapter 3 Cyclic hypoxia accelerates the moult cycle in the Atlantic ditch shrimp Palaemon varians and induces changes in gill morphology ....................... 55 Summary: ........................................................................................................................ 55 3.1 Introduction: .......................................................................................................... 56 3.2 Specific chapter hypothesis: .................................................................................. 57 3.3 Materials and Methods: ......................................................................................... 58 3.3.1 Sampling site, animal collection and maintenance .......................................... 58 3.3.2 General experimental design ........................................................................... 58 3.3.3 Transcriptome response to hypoxia ................................................................. 59 3.3.4 Changes in inter-moult duration ...................................................................... 61 3.3.5 Gene expression of cuticular genes during moult cycle .................................. 61 3.3.6 Changes to phenotype in Palaemon varians: gill modification in response to
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