AN ASSESSMENT OF THE EVAPORATIVE RELEASE OF HEAT FROM THE BUCCOPHARYNGEAL, CUTANEOUS, AND CLOACAL EPITHELIA OF BIRDS AND REPTILES by Ty C.M. Hoffman A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy ARIZONA STATE UNIVERSITY May 2007 AN ASSESSMENT OF THE EVAPORATIVE RELEASE OF HEAT FROM THE BUCCOPHARYNGEAL, CUTANEOUS, AND CLOACAL EPITHELIA OF BIRDS AND REPTILES by Ty C.M. Hoffman has been approved November 2006 APPROVED: , Chair Supervisory Committee ACCEPTED: Director of the School Dean, Division of Graduate Studies ABSTRACT Evaporation can simultaneously subject an animal to a detrimental loss of physiologically essential water and to a beneficial loss of life-threatening heat. Buccopharyngeal evaporation occurs from the mouth and pharynx, and it is only one component of an animal's total evaporation. For tetrapods other than mammals, non- buccopharyngeal evaporation (the remainder of total evaporation) occurs despite an incapacity for sweating. High rates of non-buccopharyngeal evaporation have been measured in many bird species, and rates of non-buccopharyngeal evaporation have been shown to change gradually during acclimation to changes in temperature or aridity. This dissertation demonstrates that mourning doves (Zenaida macroura) are able to effect rapid, endogenous adjustment to the rate of non-buccopharyngeal evaporation when faced with a suppression of buccopharyngeal evaporation. This implies that non- buccopharyngeal evaporation can serve as a transient mechanism for thermoregulation. However, the adjustment of non-buccopharyngeal evaporation shown in mourning doves prompts the question of how that non-buccopharyngeal evaporation is apportioned among the non-buccopharyngeal epithelia. Historically, researchers have assumed that all non-buccopharyngeal evaporation occurs from the skin (cutaneous evaporation). This research demonstrates that the cloaca can be the site of much of an animal's total evaporation and that cloacal evaporation sheds enough heat to be important for thermoregulation. Both Gila monsters (Heloderma suspectum) and Inca doves (Columbina inca) underwent a transition from negligible to significant rates of cloacal evaporation as ambient temperature increased beyond a iii critical point. Cloacal evaporation accounted for 82% of Gila monsters' total evaporation at 40°C and for 21% of Inca doves' total evaporation at 42°C. Heat dissipation by cloacal evaporation could allow these species to inhabit hotter microclimates for longer time periods, potentially increasing time allocated to foraging and reproductive behaviors. Evidence that cloacal evaporation is not a universal feature of animals possessing a cloaca is provided by results from Eurasian quail (Coturnix coturnix) and ball pythons (Python regius). Both exhibited negligible cloacal evaporation even when heat-stressed. These negative results, especially from the ball python, a tropical snake unlikely to require cloacal evaporative cooling, serve as preliminary evidence that cloacal evaporation is an adaptive mechanism for thermoregulation. iv ACKNOWLEDGEMENTS I offer my sincerest gratitude to all of the members of my doctoral committee, without whose guidance, tutelage, advice, and friendship I could not have completed the work that has led to this dissertation. My final committee includes Glenn E. Walsberg, the chair of the committee, and Dale F. DeNardo, Jon F. Harrison, and Kevin J. McGraw. Original members include William F. Fagan and Jeffrey R. Hazel. v TABLE OF CONTENTS Page List of Tables ...............................................................................................................viii List of Figures................................................................................................................ix Chapter 1 INTRODUCTION (EVAPORATIVE HEAT-LOSS AND EVAPORATIVE WATER-LOSS: THE IMPORTANCE OF RETAINING AND OF RELEASING WATER) ...........................................................................1 References................................................................................................6 2 INHIBITING BUCCOPHARYNGEAL EVAPORATION PRODUCES AN ADAPTIVE INCREASE IN NON-BUCCOPHARYNGEAL EVAPORATION IN MOURNING DOVES (Zenaida macroura) .......... 10 Summary................................................................................................ 10 Introduction............................................................................................ 11 Materials and Methods ........................................................................... 14 Results ...................................................................................................20 Discussion.............................................................................................. 23 References.............................................................................................. 40 3 CLOACAL EVAPORATIVE COOLING: A PREVIOUSLY UNDESCRIBED MEANS OF INCREASING EVAPORATION AT HIGHER TEMPERATURES IN A DESERT ECTOTHERM, THE GILA MONSTER (Heloderma suspectum) ...................................................... 45 Summary................................................................................................ 45 Introduction............................................................................................ 46 Materials and Methods ........................................................................... 50 Results ...................................................................................................60 vi Page Discussion.............................................................................................. 63 References.............................................................................................. 75 4 CLOACAL EVAPORATION: AN IMPORTANT AND PREVIOUSLY UNDESCRIBED MECHANISM FOR AVIAN THERMOREGULATION...................................................................... 79 Summary................................................................................................ 79 Introduction............................................................................................ 80 Materials and Methods ........................................................................... 84 Results ...................................................................................................94 Discussion.............................................................................................. 98 References............................................................................................ 109 5 APPORTIONMENT OF WHOLE-BODY EVAPORATION AMONG ITS BUCCOPHARYNGEAL, CUTANEOUS, AND CLOACAL COMPONENTS IN THE BALL PYTHON (Python regius)................. 115 Summary.............................................................................................. 115 Introduction.......................................................................................... 116 Materials and Methods ......................................................................... 119 Results ................................................................................................. 125 Discussion............................................................................................ 128 References............................................................................................ 138 6 CONCLUSION........................................................................................... 143 References............................................................................................ 148 vii LIST OF TABLES Page Table 3.1 RATES OF EVAPORATION FROM GILA MONSTERS............................ 69 3.2 RATES OF EVAPORATION FROM VARIOUS ARID AND SEMIARID LIZARDS .............................................................................................. 70 4.1 HYGROMETRIC AND RESPIROMETRIC MEASUREMENTS OF INCA DOVES AND EURASIAN QUAIL ..................................................... 104 4.2 KEY TO SYMBOLS USED IN CHAPTER 4............................................. 105 5.1 KEY TO SYMBOLS USED IN CHAPTER 5............................................. 134 5.2 EVAPORATION AND RESPIRATION IN BALL PYTHONS .................. 135 viii LIST OF FIGURES Page Figure 2.1 NON-BUCCOPHARYNGEAL EVAPORATION FROM MOURNING DOVES..................................................................................................34 2.2 NON-BUCCOPHARYNGEAL COMPENSATORY CAPACITY OF AND APPORTIONMENT OF NON-BUCCOPHARYNGEAL EVAPORATION FROM MOURNING DOVES....................................35 2.3 EFFECT OF AMBIENT TEMPERATURE ON SKIN TEMPERATURE OF MOURNING DOVES...................................................................... 37 2.4 EFFECT OF AMBIENT TEMPERATURE ON EVAPORATIVE CONDUCTANCE OF MOURNING DOVES........................................38 2.5 PROBABLE SKIN TEMPERATURES OF EXPERIMENTAL MOURNING DOVES..................................................................................................39 3.1 BUCCOPHARYNGEAL, CUTANEOUS, AND CLOACAL EVAPORATION FROM GILA MONSTERS....................................................................71 3.2 DIFFERENCES BETWEEN AIR TEMPERATURE AND BODY TEMPERATURE OF GILA MONSTERS ............................................. 72 3.3 EFFECT OF DEHYDRATION ON RATES OF EVAPORATION FROM GILA MONSTERS................................................................................ 73 4.1 EFFECT OF CLOACAL PATENCY AND HUMIDITY ON RATES OF EVAPORATION FROM INCA DOVES ...........................................