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RESPIRATION AND ENERGY UTII.ISAT¡ON IN THE EGGS OF THE AUSTRA!.IAN FRESHWATER CROCODILE, CROCODYLUS JOHNSTAM KREFFT, 1873 PETER JOHN WHITEHEAD B.Sc. Adelaide Department of Zoology University of Adelaide A thesis submitted to the University of Adelaide in partial fulfilment of the requirements for the degree of Master of Science. APRIL 1987 F.ì*¡,-fu:f ro/+,t, i co NT ENTSi Page SUMMARY .t DECLARATION vi ACKNOWLEDGEMENTS vil 1. GENERAL INTRODUCTION AND METHODS 1 1.1. INTRODUCTION 1 1.1.1 Biology ol Crocodylus iohnstoni 1 1.1.2. Reproduction in crocodilians ...... 2 1.1.3. Physiology of eggs .3 1.1.4. Energetics of development .5 1.1.5. Outline of studies .7 1.2. MATERIALS AND METHODS 1.2.1. Collection of eggs 10 1.2.2. Egg characteristics 10 1.2.3. Egg incubation 12 1.2.4. Gas sampling and analyses .14 1.2.5. Statistics .. 14 1.2.6. Symbols, abbreviations and terminology 14 1.2.7. Permits ... 15 2. METABOLIC RATE OF EGGS AND HATCHLINGS 16 2.1. INTRODUCTION ..1 6 2.2. METHODS 20 2.2.1. Oxygen consumPtion 20 2.2.2. Gas tensions in respirometers ......... ---..........22 2.2.3. Oxygen tension and rate of consumption ............----.....22 2.2.4. Carbon dioxide production 23 2.2.5. Oxygen consumPtion of hatchlings 23 2.3. RESULTS 25 2.3.1. Oxyg en consumption of eggs 25 2.3.1.1. Rate (Voz) 25 2.3.1.2. Maximum rate of oxygen consumption ,30 2.3.1.3. Pre-hatching rate of oxygen consumption .31 2.3.1.4. Total oxygen consumption .31 2.3.2. Carbon dioxide excretion, and resPiratory exchange ratio 34 2.3.3. Gas tensions and oxygen consumption 36 2.3.4. Oxygen consumption of pipped eggs 37 2.3.4.1. Rate of oxygen consumption ............ 37 2.3.4.2. Total oxygen consumption .38 2.3.5. Oxygen consumption of hatchlings 38 2.3.5.1. Rate 38 2.3.5.2. Total oxygen consumption 39 2.3.5.3. Effect of temperature on metabolic rate 39 2.4. DISCUSSION 41 2.4.1. Patterns of embryonic metabolic rate ..........41 2.4.1.1. Maturation 43 2.4.1.2. Delayed emergence and hatching synchrony .......43 2.4.2. Egg or hatchling mass, and oxygen consumption ......48 2.4.3. Resp¡ratory exchange ratio (RE) . 51 2.4.4. Temperature effects on embryonic metabolic rate .....54 2.4.5. lnitiation of pulmonary respiration 55 2.4.6. Oxygen consumption of hatchlings . 56 2.4.7. Temperature and hatchling metabolic rate ................-.57 2.5. SUMMARY 58 3. EMBRYONIC GROWTH 60 3.1. INTRODUCTION 60 3.1.1. Growth models 60 3.1.1.1. Exponential .......... 60 3.1.1.2. Sigmoid growth Patterns 61 3.1.2. Gror¡¡th patterns in embryonic reptiles .63 3.1.3. lncubation temperature and embryonic growth 63 3.1.4. Outline of studies 64 3.2. METHODS ..65 3.2.1. Wet mass of embryos and egg contents ,65 3.2.2. Drying of embryos and egg contents .6ô 3.2.3. Data analysis 66 3.3. RESULTS .67 3.3.1. Pattern of grovrtth: Wet mass .67 3.3.1.1. Embryonic yolk-free mass ....... .67 3.3.1.2. Extra-embryonic membranes 67 3.3.1.3. Relationship of egg mass to embryo mass .. 70 3.3.1.4. Yolk-free hatchling mass 71 3.3.2. Pattern of growth: Dry mass .71 3.3.2.1. Embryonic yolk-free mass ..71 3.3.2.2. Egg mass and dry embryo mass .13 3.3.2.3. Extra-embryonic membranes 73 3.3.2.4. Hatchling dry mass 75 3.3.3. Water content of embryos 75 3.4. DISCUSSION 3.4.1. Pattern of growth 77 3.4.1.1. Gas exchange limitations 77 3.4.1.2. Accumulation of excretory products .. 79 3.4.2. lncubation temperatures and growth rates 81 3.4.3. Reptilian and avian growth rates .85 3.5. SUMMARY .89 4. GROWTH, MA¡NTEhIANCE AND METABOLIC RATE 90 4.1. INTRODUCTION 90 4.1 .1 . Energy for growth ,.90 4.1 .2. Energy for maintenance ..91 4.1.3. Separation of growth and maintenance energy ..------...92 4.2. METHODS 94 4.3. RESULTS .95 4.3.1. Scaling of metabolic rate with embryonic mass 95 4.3.2. Multiple regression model 98 4.3.3. Metabolic rate and growth .100 4.3.4. Metabolic rate, growth, and temperature .101 4.4. DISCUSSION 104 4.4.1. Energetic cost of rìorì:êmbrtonic growth ........104 4.4.2. Scaling of metabolic rate with embryo mass ,........105 4.4.3. Multiple regression model .........107 4.4.4. Gror¡rth and metabolic rates in embryos of the same mass ...1 1 0 4.5. SUMMARY 112 5. NON.EMBRYONIC EGG CONTENTS 113 5.1. INTRODUCTION 113 5.2. METHODS 115 5.2.1. Separation of egg components ...................115 5.2.2.Weighing of egg components ....117 5.2.3. Drying of egg components ..117 5.2.4. Fluid losses during separation 118 5.2.5. Calculation of relative water and solid content ...........118 5.2.6. Statistical Analyses 118 5.2.7. Terminology 119 5.3. RESULTS 120 5.3.1. Egg contents - changes during incubation 120 5.3.1.1. Yolk 120 5.3.1.2. Albumen 121 5.3. 1 .3" Extra-embryonic fluids 123 5.3.1.4. Egg-shell 124 5.3.2. The water budget 126 5.3.3. Exchanges of solids between egg components 135 5.3.3.1. Wet mass 135 5.3.3.2. Dry mass 37 5.4. DISCUSSION 5.4.1. Water 146 5.4.1.1. Total water suPPlY 146 5.4.1.2. Water and hatchling size 149 5.4.1.3. Factors affecting water loss .,150 5.4.1.4. Water balance at hatching .155 5.4.1.5. Water loss at hatching ..........158 5.4.2. Solids 159 5.4.2.1. Solid content of fresh eggs 159 5.4.2.2. Depletion of Yolk solids 161 5.4.2.3. Albumen and other solids 162 5.4.2.5. Net changes in yolk solids 166 5.4.3. Conversion ratios 168 5.5. SUMMARY 171 6. THE EMBRYONIC ENERGY BUDGET 173 6.1. INTRODUCTION 173 6.2. METHODS .176 6.2.1. Calorimetry .............1 76 6.2.2. Ash content .............1 79 6.2.3. Calculation of energy densities .............1 79 6.3 RESULTS 180 6.3.1. Energy densities and ash content 180 6.3.1.1. Embryos .1 80 6.3.1.2. Extra-embryonic membranes ..... 185 186 6.3.1.4. Albumen ...191 6.3.1.5. Extra-embryonic fluids 192 6.3.1.6. Egg residues 194 6.3.2. Comparison of fresh and hatched egg 194 6.3.3. The energy budget 195 6.3.3.1. The fresh egg ......... 195 6.3.3.2. Energy re-distribution during incubation 196 6.3.3.3. Energy consumption during incubation 199 6.4 DISCUSSION .202 6.4.1. Energy densities 202 6.4.1.1. The fresh egg 202 6.4.1.2. Chemical composition and energy content ..-....."204 6.4.1.3. Oxygen consumption and energy production ......205 6.4.1.4. Changes in energy density 207 6.4.2. Variation in ash content 211 6.4.3. Cost of growth .212 6.4.3.1. lndices of energetic efficiency ........... ....212 6.4.3.2.Tota1 production efficiency in C. iohnstoni eggs .213 6.4.3.3. Changes in etficiency during incubation ..............214 6.4.3.4. Conversion ratios (solids) .214 6.4.3.5. Comparison of avian and reptilian efficiencies ...214 6.4.3.6. lncubation time and the cost of growth ..................216 6.4.4.The growth/maintenance dichotomy 225 6.5. SUMMARY .226 7. GAS CONDUCTANCE OF EGG.SHELLS 228 7.1 . INTRODUCTION 228 7.2. METHODS 232 7.2.1 . Eggs sampled 7.2.2. Extraction of gas samPles ..232 7.2.3. Analysis of gas samPles 233 7.2.4. Gaseous conditions of incubation ..233 7.2.5. Calculation of gas conductance ...234 7.3. RESULTS .236 7.3.1. Air spaces ...236 7.3.2. Gas tensions in air sPaces 237 7.3.2.1. Oxygen (Pod 237 7.3.2.2. Carbon dioxide (Pcoz) 239 7.3.2.3. Relationship between Poz and Pçg2 241 7.3.3 Egg-shell gas conductance 244 7.3.3.1. Oxygen conductance (G92) ...... 244 7.3.3.2. Carbon dioxide conductance (G coz) 246 7.3.3.3. Ratio of G692 to G92 246 7.3.4. Sub-shel! spaces 248 7.3.5. Sub-chorioallantois space 248 7.4 DISCUSS¡ON .249 7.4.1. Air spaces .249 7.4.4.1. Formation of sPaces 249 7.4.4.2. Functional significance of air spaces ...250 7.4.2. Sub-shell gas tensions ...251 7.4.3. Gas conductance 252 7.4.3.1. Changes during lncubation ...252 7.4.3.2.lmportance of water in the egg-shell 252 7.4.3.3. Components of ditfusion resistance 254 7.4.4. Egg-shell permeability 7.4.5. lnter-specific comparisons of conductance .256 7.4.6. Changes in the mineral layer 259 7.4.7 . Physiological implications .260 7.4.7.1. Oxygen availability .260 7.4.7.2. Carbon dioxide excretion 261 7.4.8. Application of avian models to reptiles .263 7.5. SUMMARY 264 8. GASEOUS ENVIRONMENT OF NESTS ..265 8.1.
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