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The Physiology and Pathology of Heat Stress in Australian Desert Birds The Physiology and Pathology of Heat Stress in Australian Desert Birds Shangzhe Xie BSc/BVMS, MVS (Conservation Medicine) A thesis for the Doctor of Philosophy December 2018 The University of Adelaide Faculty of Sciences School of Animal and Veterinary Sciences Roseworthy Campus 1 Table of Contents Abstract ................................................................................................................................................... 5 Declaration of originality ........................................................................................................................ 8 Acknowledgements ................................................................................................................................. 9 Chapter 1 Introduction ......................................................................................................................... 10 Chapter 2 Stress responses to heat ...................................................................................................... 69 Chapter 3 Behavioural adaptations of captive birds to high environmental temperatures .............. 102 Chapter 4 Organ histopathology and haematological changes associated with heat exposure in Australian desert birds ........................................................................................................................ 142 Chapter 5 Physiological, histopathological and biochemistry changes in birds exposed to heatstroke ............................................................................................................................................................ 170 Chapter 6 Heat shock protein expression is upregulated after acute heat exposure in three species of Australian desert birds ........................................................................................................................ 216 Chapter 7 Discussion and conclusion .................................................................................................. 251 Appendix 1 Supporting publications – Conference presentations ..................................................... 272 Appendix 2 Popular media .................................................................................................................. 280 2 Summary of Figures and Tables Chapter Label Summarized caption Figure 1 The pathophysiology of heat stroke in humans Figure 2 The relationships between nervous system, endocrine system and thermoregulation Figure 3 Peripheral inputs resulting in neuronal and endocrine 1 responses to maintain normothermia Figure 4 Induction of epigenetic adaptation processes during the critical period of early development Figure 5 The difference between a bird’s response to stimuli and stressors Figure 1 Temperature increase within the incubator Figure 2 Corticosterone (CORT) responses 2 Figure 3 Heterophil:lymphocyte (H:L) ratio responses Figure 4 Relationship between CORT and H:L changes Figure 5 Water consumption of each species Table 1 Bird species studied Table 2 Summary of time spent on stationary behaviours Table 3 Summary of time spent feeding Table 4 Summary of time spent in the sun 3 Table 5 Summary of time spent on the ground Table 6 Summary of number of wing venting events per observation period Figure 1 Percentage of time spent on stationary behaviour Figure 2 Percentage of time spent feeding Figure 3 Percentage of time spent in the sun Figure 4 Percentage of time spent on the ground 3 Chapter Label Summarized caption Table 1 Summary of histopathological findings Table 2 Summary of haematology findings Figure 1 Histological sections from the lung of a budgerigar Figure 2 Histological sections from 4 the lung of a diamond dove Figure 3 Histological sections from the liver of a diamond dove Figure 4 Histological sections from the liver of a budgerigar Figure 5 Histological sections from the kidney of a diamond dove Table 1 Descriptive statistics and reference intervals for galahs Table 2 Descriptive statistics and reference intervals for rock doves Table 3 Descriptive statistics and table of ascending values for GLDH in galahs and rock doves Table 4 Summary of galah blood 5 results Table 5 Summary of rock dove blood results Figure 1 Heart rate in galahs Figure 2 Heart rate in dock doves Figure 3 Respiration rate in galahs Figure 4 Respiration rate in rock doves Figure 5 Summary of galah blood results Figure 6 Summary of rock dove blood results Table 1 List of forward and reverse primers Table 2 Summary of differential 6 gene expression in each organ of each species Figure 1 Direction and significance of fold changes of each gene Figure 2 Difference in Ct values and standard deviation 4 Abstract Arid environments pose a unique set of challenges to organisms. These challenges include the lack of basic resources such as food and water, as well as extremes in temperatures. Birds are small flying endotherms that maintain high body temperatures close to lethal limits, which is advantageous in hot climates. However, as global temperatures increase, birds need to be able to respond to weather changes quickly and appropriately for their own well-being and survival. The inability to respond appropriately to heatwaves can be fatal to individual birds and translate into large-scale mortality events. As there were gaps in the current knowledge regarding the physiological stress responses and behavioural adaptations of Australian desert birds to high ambient temperatures, I designed and conducted separate studies to investigate these responses. I found that the corticosterone (CORT) and heterophil:lymphocyte (H:L) ratio responses of budgerigars (Melopsittacus undulatus), zebra finches (Taeniopygia guttata) and diamond doves (Geopelia cuneata) to heat exposures were different. These species differences may reflect their ability to detect and adapt to high temperatures. There was also no significant correlation found between the change in CORT and H:L ratios, which may reflect differences in the timescales of these responses. Based on the species differences in CORT response, I hypothesized that there would also be differences in the behavioural response to high ambient temperatures, as CORT has effects on the behaviour of birds. Observation of eight species of birds at the Adelaide Zoo confirmed my hypothesis. Psittaciform birds spent less time feeding and more time resting in cooler microsites during hot periods. Columbiform birds continued feeding and spent more time in the sun during hot periods rather than resting in cooler microsites. White-Browed Woodswallows, the only passerine species assessed, spent a significantly lower proportion of 5 time on stationary behaviours and higher proportion of time feeding compared to the other species. The smallest birds in the study, they also utilised wing venting more than other species of birds, possibly because it is more important for them to conserve water. These results suggest that columbiform birds may have an advantage during heatwaves as they can continue feeding through high ambient temperatures, as long as there is adequate access to food and water. When physiological and behavioural adaptations are unable to prevent birds from maintaining their body temperatures below lethal limits, pathological changes are expected. There is currently very little documentation of these pathological changes in the literature, which makes diagnosis of heat injuries in birds difficult. I examined the histopathological changes in the organs of the birds from the CORT and H:L ratio study and found that the main changes were in the lungs and liver, albeit to different degrees and frequencies in different species. There were also changes in the hearts, kidneys and gastrointestinal tracts of some birds, but these were less frequently observed. Having established there are species differences in how birds respond physiologically, behaviourally and pathologically when exposed to heat, I then sought to further characterize these responses and adaptations at a molecular level. I selected genes of interest and measured the mRNA expression of these genes in the organs of the birds from the CORT/H:L study. The results revealed that acute exposure of native Australian birds to high temperatures (45°C) would result in upregulation heat shock protein (hsp) genes, but there was no significant upregulation of other genes with protective effects against cell damage (BCL-2 and VEGFA) nor genes associated with inflammation (interleukins). There was also no downregulation of the genes involved in the coagulation pathway (fibrinogen) in these birds. The gastrointestinal tracts of all 3 bird species had the highest number of hsp genes upregulated, possibly indicating that this is the organ that requires the most protection to 6 continue its function. Diamond dove organs also had the highest number of hsp genes upregulated, possibly a reflection of their ability to protect their cells better during high temperatures. The findings from my thesis have filled in gaps in the current knowledge regarding the physiological stress and behavioural responses of Australian desert birds to high ambient temperatures. I have also found clinical and histopathological changes in birds exposed to varying degrees of heat, which can be used to help diagnosis of heat injuries in birds. These findings have also revealed that there are important differences in the ways different species of birds respond to heat and that there is no single strategy that can be applied to help all birds
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