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Allometric Studies in Mammalian Metabolism

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Allometric Studies in Mammalian Metabolism YOF o n ALLOMETRIC STUDIES IN MAMMALIAN METABOLISM C.R. WHITE 2004 Table of Gontents Abstract 1 Acknowledgements 3 Publications Arising 4 lntroduction 5 1 Mammalian basal metabolic rate is proportional to body mass'/3 7 Abstract 7 INTRODUCTION 7 METHODS I RESULTS 12 DISCUSSION 14 2. Does BMR contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological and 16 life-history variables Abstract 16 INTRODUCTION 16 METHODS 17 Allometry of mammalian BMR 17 Variation in mammalian BMR 19 and other physiological, ecological and Correlations between BMR 19 life-history variables RESULTS 20 Allometry of mammalian BMR 20 mammalian taxa and Variation in mammalian BMR between 22 zoogeographic regions Correlates to BMR 27 DISCUSSION 28 Allometry of mammalian BMR 28 Variation in BMR between mammalian taxa 30 Correlates to BMR 31 Acknowledgements 35 3. Interindividual metabolic rate and cost of transport variation in an Australian murid rodent, the spinifex hopping mouse 36 Notomys alexis Abstract 36 INTRODUCTION 36 METHODS 38 Study Species 38 Body temperature 39 39 Resting.:- ito, ExêlClSê Vs2 40 Maximum running speed 42 Repeatability 43 RESULTS 44 Thermoregulation and metabolism M Locomotion 44 t ntrai n divi d u al re pe atabi I ity a n d i nte ri n divi d u al va ri ation 46 DISCUSSION 47 Thermoregulation and metabolism 47 Does calculation from pooled data alter BMR allometry? 48 Locomotion 53 Energetic cosfs and benefits of hopping and burrowing specialisation 54 t ntraindividual repeatability and interindividual vari ation 58 BMR correlates 58 I ntraspecifi c correl ated v ari ati o n 60 Acknowledgements 62 4. The influence of foraging mode and arid adaptation on the basal metabolic rates of burrowing mammals 63 Abstract 63 INTRODUCTION 63 METHODS 65 Atlometric relationships between BMR and body mass 65 Phylogenetic analysis of covariance 65 Comparison of groups with heterogenous regression s/opes 67 RESULTS 68 DISCUSSION 70 conventionator phylogenetically informed? on the choice of method 70 of burrowing or Reduced BMR of fossorial mammals: Cost 72 thermalsfress2 Adjustment of BMR as an adaptation to arid environments 71 Acknowledgements 73 111 5. The allometry of burrow geometry 74 Abstract 74 INTRODUCTION 74 METHODS 75 RESULTS 76 B u rrow cross-secfi o n al a re a 76 Nest chamber volume 77 DISCUSSION 79 B u rrow cross-secfl o n a I a re a 79 Nest chamber volume 81 exponent 6. Requirements for estimation of the 'true' allometric 82 relating mammalian basal metabolic rate and body mass Abstract 82 INTRODUCTION 82 METHODS 83 Generation of BMR and body mass values for añificial species 83 Analysis protocol 84 RESULTS 86 DISCUSSION 86 7. Phylogenetically informed regression methods do not systematically bias determination of the scaling exponent relating 89 mammalian basal metabolic rate and body mass Abstract 89 INTRODUCTION 89 METHODS 91 BMR and body mass generation for'artificial species' 91 Comparison of conventional and PI regression: A¡lificial data 91 Comparison of conventional and Pl regression: Published data 92 RESULTS and DISCUSSION 93 1V regression slopes: g. Allometric analysis beyond heterogeneous 97 Use of the Johnson-Neyman technique in comparative biology Abstract 97 INTRODUCTION 97 Data Simulation 100 Simulated data set 1: different slopes, same intercept 100 Simulated data set 2: different slopes, overlap at edge of x-range 101 simulated data set 3: different slopes, overlap in middle of x-range 102 Real data: BMR of arid-adapted, burrowing mammals 102 Real Data: Heart masses of mammals and birds 103 DISCUSSION 104 Acknowledgements 105 Calculation of the region of non-significance 106 Literature Cited 108 Appendices (I¡) basal metabolic Appendix A. Body mass (M), body temperature and 145 rate (BMR) of mammals relationship relating Appendix B. Determination of Qro from an exponential 159 metabolic rate and body temperature construction for Appendix C. A model for calculation of the cost of burrow 160 semi-fossorial mammals Appendix D. Body masses, basal metabolic rates (BMR)' habitat (arid/mesic) and foraging mode (fossorial/semi-fossorial) of burrowing 167 mammals burrowing Appendix E. Description of phylogenetic derivations for 171 mammals Appendix F. Body masses (M, g), burrow cross-sectional areas (46, cm2), (Vn, mammals, semi- and nest chamber volumes cm') of fossorial 173 fossorial mammals, birds, reptiles and other invertebrates and veÉebrates Appendix G. Source code for LIREG-SD 176 Abstract Terrestrial mammals span a size range of -6 orders of magnitude from 2 g shrews to 4000 kg elephants. The consequences of these size differences are well known: the 4000 kg elephant lives longer than the 2 g shrew, for example, but the shtew's heart beats faster than the elephant's, and 1 g of shrew uses considerably more energy per unit time than I g of elephant. This thesis examines the effect of body mass (I1) on a range of physiological variablcs and the nature ofthe residual variation about these relationships (i.e. variation not accounted for by body mass) both within and between species. L The relationship between mammalian basal metabolic rate (Bl\{R.) and body mass (I1) has been the subject ofregular investigation fo (b, where BMR : a M\remains a point of co geometric (b:213) and quarter-power þ : 314) scaling continue to be made and rebutted in the literature. Here a new analysis of the allometry of mammalian BMR that accounts for variation associated with body temperature, digestive state and phylogeny finds no support for a metabolic scaling exponent of 314. Data encompassing five orders of magnitude variation tn M and featuring 619 species from 19 mammalian orders show that BlvIRn Mzt3. 2. BMR is a useful measurement only if if the strictly defined conditions required for its measurement are adhered to. If variation associated with body temperatue and digestive state is removed, the BMRs of eutherians and marsupials do not differ and no significant allometric exponent heterogeneity remains between orders. Of the 19 orders considered here, only Chiroptera and Dasyuromorphia have significantþ different BMRs after eliminating body mass effects. The usefulness of BMR as a general measurement is supported by the observation that, after the removal of body masb effects, the residuals of BMR are significantly correlated with the residuals for a variety of physiological and ecological variables, including maximum metabolic rate, field metabolic rate, resting heart rate, litter size, andpopulation density. 3. Mammalian BMR is one of the most widely measured physiological metrics, with the nature and causes of the interspecific relationship between M and BMR continuing to be investigated and debated. However, analysis of interspecific databoth neglects considerable intraspecific variation and averages out the variation on which natural selection acts. This chapter assesses intraspecific variation in a range ofphysiological variables including BMR in the murid rodent, Notomys alexis. Most variables were significantly repeatable, suggesting that individual measurements were reliable. Mean values were similar to values predicted by allometry, but variation between individuals was considerable and in many cases approached 50% of that observed between species. A number of variables were significantly correlated, and the implications of these correlations are discussed. 4. The low BMR of fossorial mammals has been suggested either to compensate for the enotmous energetic demands of subterranean foraging ("cost of burrowing hypothesis") or to prevent overheating in closed burrow systems ("thermal stress hypothesis"). These hypotheses are examined by comparing fossorial (subterranean foraging) and semi- fossorial (surface foraging) burrowing mammals. In support of the thermal stress hypothesis, the BMRs of mesic fossorial and semi-fossorial mammals can not be reliably distinguished, nor can the BMRs of large (> 77 Ð arid fossorial and semi-fossorial mammals. However, in support of the cost of burrowing hypothesis, small (< 77 g) artd fossorial species have significantly lower BMRs than semi-fossorial species of similar size. The greatly reduced BMR of small arid fossorial species may compensate for the enormous energetic demands of subterranean foraging in an environment where resources are sparse and widely distributed. 5. The allometric relationship between body mass and burrow cross-sectional arca for burrowing animals holds across greater than six orders of magnitude variation in body mass. Only birds that construct relatively large burrows, and vermiform animals that construct relatively naÍow burows, are separated from the remaining burrowing species. No difference is found between the cross-sectional area of burrows constructed by fossorial and semi-fossorial mammals, although solitary fossorial mammals do construct significantþ larger nest chambers than semi-fossorial and colonial fossorial mammals. These large nest chambers probably provide a better thermally insulated microenvironment and offsei the thermoregulatory problems faced by these animals, which are characterised by low, labile body temperatures and poor thermoregulatory ability' 6. IIow many species covering what range of body masses are required to arrive at a reasonable estimate of the relationship between BMR and M? To answer this question, 4600 artificial species are generated based on the variation in BMR and Mobserved in extant mammals. Randomly selected subsets of the artificial species are examined
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