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Digestive Physiology …………………………………………………………… The seasonal energetics of three species of Australian tropical frogs (Anura: Hylidae). Lorrae Jean McArthur B. Sc. (Hons) (Monash) Faculty of Education, Health and Science Charles Darwin University A thesis submitted to satisfy the requirements for the award of the degree of Doctor of Philosophy (Science) March 2007 Declaration "I hereby declare that the work herein, now submitted as a thesis for the degree of Doctor of Philosophy by Professional Doctorate of the Charles Darwin University, is the result of my own investigations, and all references to ideas and work of other researchers have been specifically acknowledged. I herby certify that the work embodied in this thesis has not already been accepted in substance for any degree, and is not being currently submitted in candidature for any other degree." Signed: Date: ii This dissertation is dedicated in memory of Daniel Frederick McArthur (1927-2004) iii Acknowledgments The Commonwealth Government kindly provided me with an Australian Postgraduate Award scholarship, and tuition was gratefully received from Charles Darwin University (CDU). The Australian Federation of University Women for South Australia (2003) and the Northern Territory (2002) also graciously provided scholarships. Internal funding to conduct research was provided by the Charles Darwin University, under the Undergraduate Training Research Opportunity Program of the Faculty of Education, Health and Science, and in part from Keith Christian’s Australian Research Council grant. External funding to conduct research was gratefully received from the Australian Society of Herpetologists (2004), Peter Rankin Trust Fund (2003), Centre for Tropical Wetland Management of CDU (2003 and 2002), Australian Geographic (2002) and Linnean Society of New South Wales (2002). All applicable institutional Animal Care guidelines were complied with and all required permits were obtained. All methods were approved by the Charles Darwin University Animal Ethics Committee (project reference number A01020). I gratefully acknowledge the services of the Parks and Wildlife Services of Northern Territory for allowing me to collect and conduct research on frogs (permit reference numbers 13390 and 17225). Technical assistance was extraordinary and greatly appreciated. Gavin Bedford assisted in calorimetry methods; Mark Meekan of the Australian Institute of Marine Science (AIMS) allowed the use of the image analysis program Optimas; Ellie Hayward and Yusuke Fukuda both assisted in frog tissue preparation and analyses; varied assistance was provided by the Technical Services staff of the School of Science; Keith McGuiness reminded me of basic math skills; and the interaction among the many wonderful staff, students and researchers that I have had the pleasure of meeting and working with during my time at CDU. Wendy Telfer, Chris Tracy, Timothy Schultz and Gavin Bedford kindly provided editorial comments, and Sebastian Iglesias and Colin Trainor reviewed final drafts. Work associates Jeanne Young, Chris Tracy and Steven Reynolds, and the many enthusiastic field volunteers, Sally Kent, Jenny Brazier, James Smith, iv Jenny Kapp, Nicola Buddle, Scott Wyatt, Peter Clifton, David Rose, Kate Goodrich, Robert Bednarik, Murray Burke, Anna Chard, Chris Haynes, Birgit Hallenstein, Sommer Jenkins, Yeni Mulyani, Penny Wurm, Wendy Telfer, Valerie Boll, Geoffrey Carr, Petra Mross, Fiona Morrow, and Graham Chamber are greatly appreciated for the many late hours that they spent catching frogs in all weather conditions. Special acknowledgements go to my supervisor, Keith Christian, for research direction, technical support and unwavering assistance during the writing phase of my research. Michael Guinea unknowingly mentored and encouraged me alongside my sisters, Sonya McKenzie and Danielle McLachlan. Furthermore, I am grateful to Birgit Hallenstein, Wendy Telfer, Jennifer Koenig, Sebastian Iglesias and Brett Murphy who supplied me with unbounding enthusiasm and encouragement over the course of this endeavour, and to Ron Firth, Chris Brady, Yeni Mulyani, Gillian McCloskey, and Colin Trainor for unique in-office amusement and provisions. v Table of Contents Abstract ………………………………………..…………….…..………….………1 Chapter 1. General introduction and background …………………….…………..…..… 2 1.1 Physiological constraints of Australian frogs ………….…………….………….……….. 3 1.1.1 The Australian climate: the need for adaptation? ………………………....…........ 3 1.1.1.1 Frogs adapted to temperate climate ……...……..…………...……….… 5 1.1.1.2 Frogs adapted to desert climate …………………………....……….….. 5 1.1.1.3 Frogs adapted to tropical climate ………….….………….....………….. 6 1.2 Wet-dry tropics ….………………...………………………...……………....…………… 7 1.2.1 Climate of the wet-dry tropics ……………………………….……………..……. 7 1.2.2 Frogs of the wet-dry tropics – Family Hylidae ……………...…………………… 8 1.2.2.1 Cyclorana australis ……………………………………..……………… 9 1.2.2.2 Litoria caerulea ……………….……………………….………………. 9 1.2.2.3 Litoria dahlii ……………………….……………………….…………. 9 1.2.3 Some habitat assemblages of frogs in the wet-dry tropics ……...……………….. 10 1.2.3.1 Lowland wetland (Howard River) ……………………………..……. 10 1.2.3.2 Lowland wetlands (Knuckey Lagoons) ……...……….…….………… 11 1.2.3.3 Lowland woodland (Mickett Creek) …...…….…………….…………. 11 1.2.3.4 Dry coastal vine forest (East Point) …....………………………….….. 12 1.3 Scope and aims of the dissertation ……………...……...………..……….…………….. 13 1.3.1 Frog ecology ……………………………………..……………….……………... 14 1.3.2 Digestive physiology ……………………………………………………………. 14 1.3.3 Gastrointestinal flexibility ………………………..………………………..……. 15 1.3.4 Respiratory physiology …………………………..………………………...……. 16 1.3.5 Energy flow ……………………………………...………………………………. 17 1.4 Bibliography …………………………………………...……..………………………… 19 Chapter 2. Seasonal ecology ………………...…………………….……………….. 24 2.1 Abstract …………………………………………………...……..………...………….... 25 2.2 Introduction ………………………………………………………………….………..... 26 2.3 Materials and Methods ……………………………………..………………………...… 28 2.3.1 Experimental protocol ………………………………….……………………..… 28 2.3.2 Visual encounter surveys of seasonal frog activity………..…………………….. 28 2.3.3 Measurements of frog body temperature when active using field sampling…… 29 2.3.3.1 Measurements of microclimate during field sampling………..…….. 30 2.3.4 Measurements of frog body temperature when not active using radio telemetry .. 30 2.3.4.1 Measurements of microclimate during radio telemetry ……………….. 31 2.3.4.2 Surgical procedures ………………………………………….…...…… 31 2.3.5 Statistical analyses ………………...……………………………….………...….. 33 2.4 Results …………………………….……………………………..………………….….. 34 2.4.1 Seasonal frog activity and climatic variables ………….…………………...…… 34 2.4.2 Relationship between frog activity and climatic variables ….……….....………. 35 2.4.3 General spatial use of microhabitat when active ………………….………..…… 35 2.4.4 Refuge sites of frogs when not active ………………...…………………..….…. 37 vi 2.4.5 The average night and day seasonal Tb of frogs and associated microclimate ….. 38 2.4.6 Correlations between frog Tb and microclimate …………………..………….…. 39 2.5 Discussion ………………………………………………………………………….…... 41 2.6 Bibliography ……………………………………………………………………….…... 46 Chapter 3. Digestive Physiology ………………………...….……………...………. 50 3.1 Abstract ……………………………………………………………………..….………. 51 3.2 Introduction …………………………………………………………….……...……….. 52 3.3 Materials and Methods …………………….……………………………….………..…. 54 3.3.1 Experimental protocol ………….…………………………………………..…… 54 3.3.2 Calorimetry ………………………………………………...……………………. 56 3.3.3 Statistical analyses ………………………………………………….…………… 57 3.4 Results ………………………………………………………………………………..… 58 3.4.1 Temperature effect on PT …………………………………………………..…… 58 3.4.2 Seasonal effect on PT ……………………………………………..……...……… 58 3.4.3 Temperature effect on DE …………………………………………………..…… 59 3.4.4 Seasonal effect on DE ………………………………………….…...…………… 60 3.4.5 Field fecal analysis …………………………………………...…..……………… 60 3.5 Discussion …………………………………………………………...…………………. 64 3.6 Bibliography ………………………………………………………..……………..……. 67 Chapter 4. Gastrointestinal Flexibility ……………..……………….…………..…. 70 4.1 Abstract ……………………………………………………………………………...…. 71 4.2 Introduction ……………………………………………………………………....…….. 72 4.3 Materials and Methods …………………………………………………………....……. 75 4.3.1 Experimental protocol ………………………………………………...………… 75 4.3.2 Morphology …………………………………………………………………..…. 75 4.3.3 Histology …………………………………………………………………...……. 76 4.3.4 Statistical analyses ……………………………………………...…..…………… 78 4.4 Results ……………………………………………………………………………..…… 79 4.4.1 Morphology …………………………………………………...………………… 79 4.4.2 Histology ……………..…………………………………………..……………… 80 4.4.3 Correlations between intestinal mass and histology ………………….….……… 81 4.5 Discussion ………………………………………………………………...……………. 84 4.6 Bibliography ………………………………………………………...…….……………. 88 Chapter 5. Seasonal Respiratory Physiology ………………...……...……..………. 90 5.1 Abstract ………………………………….…………….…………..………...…………. 91 5.2 Introduction ………………………………..………………………………………..….. 92 5.3 Materials and Methods …………………..…………………………………………..…. 95 5.3.1 Experimental protocol …………………………….………………………..…… 95 5.3.2 Experimental treatments …………………………………………...……………. 96 5.3.3 Statistical analyses ……………………..………...……………………………… 98 5.4 Results ………………………………………………………………………………… 100 5.4.1 Aestivation ………………………..………………………………….………… 100 5.4.2 Recovery ………………………..……………………………………………… 102 5.4.3 Wet and dry season, fed versus unfed …………………………………….…… 103 vii 5.4.4 Fully hydrated versus 70% hydrated …………………………………………... 104 5.5 Discussion ………………………..………………………………..….………………. 106 5.6 Bibliography …………………………..………………………………………………. 109 Chapter 6.
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