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The Significance of Stressors on Black Bream in the Gippsland Lakes

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The Significance of Stressors on Black Bream in the Gippsland Lakes I The Significance of Stressors on Black Bream in the Gippsland Lakes A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Trevor William Ronalds B.App.Sc.(App.Chem.) M.Aq. Grad.Dip.Fish.Tech. Grad.Dip.Ed. School of Applied Sciences College of Science Engineering and Health RMIT University January 2015 Declaration I certify that except where due acknowledgement has been made, the work is that of the author alone; the work has not been submitted previously, in whole or in part, to qualify for any other academic award; the content of the thesis is the result of work which has been carried out since the official commencement date of the approved research program; any editorial work, paid or unpaid, carried out by a third party is acknowledged; and, ethics procedures and guidelines have been followed. Trevor William Ronalds January 2015 Acknowledgements Thanks are due to my initial supervisor, Associate Professor Brian Leonard for his constructive advice and criticism of research proposals and thesis drafts. Thanks also to RMIT University for offering the Gippsland Lakes Ecosystem Research Scholarship that enabled a start to be made to this study, also for making available aquaculture tanks at Lakes Entrance in East Gippsland. I am grateful to successive Heads/Deans of the School, Professor Peter Coloe and Professor Andrew Smith for making available facilities during the preparation of the thesis. A special thanks to my supervisor, Professor Ann Lawrie, without whose support this study and thesis would never have been completed. .My thanks are due also to Roy Smith, Ron Mitchelson, Rob Morecroft, and in particular, Barry McKenzie and Kevin Newman, without whose support there would not have been any fish for this study. I am indebted to: • Rob Brown and Mitchelsons Fisheries Pty Ltd. without whose support in ongoing donations of feed to maintain fish in tanks this study would not have been possible. Also to Sandy Boswel who volunteered many days to operate a video camera • Robert Brown (School of Medical Science) for passing on his expertise in histological techniques and supervising the preparation of the slides for Chapter 4 • Lauren Brown (Department of Environment and Primary Industries, Victoria) for allowing me to use black bream otolith samples previously collected by DEPI iii • Phil Francis and Peter Rummel (RMIT Microscopy and Microanalysis Centre) for help with using the ESEM to analyse otoliths for elemental composition for Chapter 5 • The Gippsland Lakes Angling Club (in particular, Paul Stray) and John Harrison for help in obtaining black bream for Chapters 4, 5 and 6. I would like especially to thank my family for their unquestioning support to allow me time to complete this thesis. iv In Memory of Mum and Dad v Summary The Gippsland Lakes and Lake Tyers are two adjacent estuarine systems approximately 15 km apart and located at about 38 ºS in south-eastern Australia. The Gippsland Lakes is an estuary of 366 km 2 permanently open to the sea and supported by a much-modified catchment of 20,600 km 2. Lake Tyers is a small riverine estuary intermittently open to the sea of approximately 25 km 2 and fed by a mostly undeveloped catchment of 470 km 2. Black bream (Acanthopagrus butcheri ) occupy both estuaries and normally prefer to remain in their native estuary. Black bream from Lake Tyers have a greater growth rate and a “superior condition” than those in the Gippsland Lakes. Analyses are presented of a study of black bream sourced from the Gippsland Lakes and Lake Tyers. The primary aims of the project were to investigate the potential of black bream as a valuable ecological indicator for chronic stress by: (1) developing an acute stress behavioural response test as an indicator of underlying chronic stress , (2) evaluating the potential of this behavioural test, various condition indices and changes in interrenal cells in the kidney to compare chronic stress in black bream from the two estuaries, and (3) investigating differences in elemental composition of otoliths and in genetic polymorphism between the estuaries as causes of differences in chronic stress.. In Chapter 2, a stimulus-startle behavioural test was developed to identify acute stress response to 30 s air exposures such as experienced by fish during catch-and-release practices for undersized fish. Undersized fish from Lake Tyers were collected from a seine net during commercial fishing and acclimated in 2000 L tanks for 3 weeks. The response time to seek cover under a hide in custom-made channel apparatus was measured following a stimulus- response at 0, 6 and 12 hours after air exposure compared with that of fish not so exposed as vi controls. The cumulative impacts of one, two and three identical air exposures 3 h apart were compared. Fish were then retained in holding tanks for 3 months for observation and mortality compared. The response time in the stimulus-response test ranged from <1 min to >30 min. The response time and mortality were proportional to the number of air exposures. Fish that died first displayed a dark colour, then became higher in the water column and finally died floating on the surface. The dark colouration was only apparent when fish were in the water. This indicated that the stimulus-response test predicted mortality and could be a useful short-time test for acute stress. In Chapter 3, the stimulus-response test was used to compare the impact of chronic stress on the reaction times of black bream from the Gippsland Lakes and Lake Tyers. Undersized fish were collected as before and acclimated for up to a year in tanks. A further chronic stress was imposed on some fish: one month of cage confinement at either 14 or 32 kg m -3, unlike controls. Caged and control fish were subjected to the stimulus-response test after one air- exposure and their health assessment index (HAI), condition factor (K) and organosomatic indices for spleen (SSI), liver (HSI) and gonads (GSI) calculated. Gippsland Lakes fish had a significantly lesser proportion of fish with a response time of <1 min the stimulus-response test, a greater proportion of fish with enlarged spleens and a greater fork length, weights of whole and gutted fish, spleen, liver and gonads weights than Lake Tyers fish, but no significant difference in HAI, K, SSI, HSI or GSI or sex ratio. There was only one marginally significant criterion between caged and control fish: SSI. The differences in response time and SSI indicated that Gippsland Lakes fish might suffer a greater level of chronic stress than Lake Tyers fish, but inadequate replication made conclusions tentative. In Chapter 4, interrenal hypertrophy and hyperplasia in the head kidney (as a previously used measure of chronic stress in fish) were compared between wild-caught black bream from the vii Gippsland Lakes and Lake Tyers. The head kidney was fixed, processing and embedded in paraffin wax before being sectioned and examined microscopically. Hyperplasia but not cell or nuclear hypertrophy was found in fish from the Gippsland Lakes relative to those from Lake Tyers. Gippsland Lakes fish had a lesser condition factor than in Lake Tyers fish and green bile colour, suggesting lack of recent feeding, unlike the yellow bile colour of Lake Tyers fish. Taken together, this suggests greater chronic stress in Gippsland Lakes fish. This could be because of differences in environmental factors or genetically determined differences in black bream in responses to perceived stress. In Chapter 5, the elemental composition of otoliths was compared between black bream from the Gippsland Lakes and Lake Tyers using EDXS (electron-dispersive X-ray spectroscopy) in an ESEM (environmental scanning electron microscope). Multivariate analysis of atom% for all elements and their ratios, however, clustered otoliths from both estuaries together, with a few outliers. Of the ten main elements found, there were no significant differences in atom% C, N, O, Na, P, S, K and Ca or their ratios, e.g. S:Ca. For Cl and Sr and the Cl:Ca and Sr:Ca, however, atom% was greater in otoliths from Gippsland Lakes fish than in those from Lake Tyers, as might be expected from Gippsland Lakes being permanently open to the ocean and having a more developed catchment, as Sr is a recognised marker for pollution. Thus differences in environmental factors could have contributed to differences in chronic stress. In Chapter 5, the genetic composition of black bream was compared between the Gippsland Lakes and Lake Tyers using both microsatellite and mitochondrial primers used previously for Acanthopagrus species. DNA was extracted from muscle or fin clippings and amplified by PCR (polymerase chain reaction). ISSR (inter-simple sequence repeats) with six pairs of primers for microsatellites resulted in Gippsland Lakes and Lake Tyers fish being grouped separately by multivariate analysis, suggesting genetic differences. PCR-RFLP (PCR- viii restriction fragment length polymorphism) of the mitochondrial D-loop with the endonuclease Dde I grouped 9/47 samples from Gippsland Lakes fish and 4/47 samples from Lake Tyers, suggesting that only they were maternally A. butcheri , while the others were maternally yellowfin bream ( A. australis ) or hybrids. Thus differences in genetics could have contributed to differences in chronic stress. This study has had the following major outcomes: 1. the development of a short-term stimulus-response response test that predicted longer- term mortality 2. evidence for catch-and-release fishing rendering undersized black bream more likely to die and more susceptible to predation 3. evidence for greater chronic stress in Gippsland Lakes black bream than in Lake Tyers black bream that could be due to differences in both environment and genetics. Thus it has contributed to the knowledge and understanding of black bream in the Gippsland Lakes and Lake Tyers estuaries and has provided evidence for the suitability of black bream as a valuable ecological indicator in estuaries.
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