Inertial homeothermy, the maintenance of a relatively constant body temperature that occurs simply because of large size, is often applied to large dinosaurs. Moreover, biophysical modelling and actual measurements show that large crocodiles can behaviourally achieve body temperatures above 30°C. Therefore it is possible that some dinosaurs could achieve high and stable body temperatures without the high energy cost of typical endotherms. However it is not known whether an ectothermic dinosaur could produce the equivalent amount of muscular power as an endothermic one. To address this question, this study analyses maximal power output from measured aerobic and anaerobic metabolism in burst exercising estuarine crocodiles, Crocodylus porosus, weighing up to 200 kg. These results are compared with similar data from endothermic mammals. A 1 kg crocodile at 30°C produces about 16 watts from aerobic and anaerobic energy sources during the first 10% of exhaustive activity, which is 57% of that expected for a similarly sized mammal. A 200 kg crocodile produces about 400 watts, or only 14% of that for a mammal. Phosphocreatine is a minor energy source, used only in the first seconds of exercise and of similar concentrations in reptiles and mammals. Ectothermic crocodiles lack not only the absolute power for exercise, but also the endurance, that are evident in endothermic mammals. Despite the ability to achieve high and fairly constant body temperatures, therefore, large, ectothermic, crocodile-like dinosaurs would have been competitively inferior to endothermic, mammal-like dinosaurs with high aerobic power. Endothermy in dinosaurs is likely to explain their dominance over mammals in terrestrial ecosystems throughout the Mesozoic.

Introduction

The phylogeny of the archosaurs began in the Late Permian and diversified into two main lineages in the Middle Triassic, the Crurotarsi (crocodilians and their relatives) and the Ornithodira (dinosaurs, pterosaurs, birds and their relatives) [1]. Most palaeontologists now believe that birds evolved from dinosaurs in the Jurassic. So today we have crocodilians and birds as the surviving archosaurs, and these are sometimes considered to be an “extant phylogenetic bracket” that can be used to infer much about the status of dinosaurs. For example, Dodson [2] noted the obvious (“no-brainer”) conclusion that dinosaurs must have had 4-chambered hearts, because both crocodilians and birds do. Both birds and alligators have unidirectional flow in their lungs [3]. Crocodilians and birds also share many other anatomical features, including proteins, somatic muscles and bones, reproductive organs, sensory organs and behaviours such as maternal care and a vocal signalling repertoire [4], which set them apart from others in Clade Reptilia. It seems reasonable to accept that dinosaurs shared these features.

However, crocodilians and birds differ widely in their metabolic status: crocodilians are good ectotherms, behaviourally thermoregulate and have low metabolic rates, while birds are good endotherms, physiologically thermoregulate and have high metabolic rates. Extant phylogenetic bracketing is equivocal in this case, so there has been much debate about the metabolic status of dinosaurs. This paper cannot possibly include the literature relevant to the debate, but rather focuses on the implications associated with the proposal that ectothermic crocodilians represent a good model for dinosaurs, because large ones can behaviourally achieve high body temperatures and homeothermy at a low energy cost.

First it is necessary to define terms that this paper uses, because there is some confusion in the literature. Endothermy is the state in which metabolic rate is high enough and variable enough to permit physiological thermoregulation, resulting in body temperatures usually between about 32–40°C. Ectothermy is the state in which metabolic rate is low, so that thermoregulation (if at all) is largely behavioural manipulation of heat input from the environment, principally the sun. Homeothermy is the maintenance of a stable body temperature, at any level and without any essential connection with metabolic rate or endothermy. Animals can be homeotherms if they are capable of physiological thermoregulation, or are in a thermally stable environment, or are large enough to buffer environmental temperature changes (“inertial homeothermy” or “gigantothermy” as coined by Paladino et al. [5]). Gigantothermy is real, because it is based in physics. It has been predicted by mathematical models [5–12] and demonstrated experimentally in large crocodiles [10,13]. The argument that homeothermy can be attained at low energy cost in large dinosaur through gigantothermy is compelling. These ideas appear in high-impact literature [14–19]. The implication is that, if an ectotherm can achieve a high body temperature, then it does not need to be an endotherm.

Estuarine crocodiles (Crocodylus porosus) have been specifically used as models for large, ectothermic dinosaurs [10,11]. Body temperatures of large (up to 1 tonne) crocodiles can average above 30°C in tropical Queensland. Based on this, Seebacher et al. [10] estimated that a 10 tonne dinosaur could have a stable body temperature above 31°C without endothermy in a similar climate, even in winter. They proposed that natural selection for high metabolic rates of endothermy would be diminished if high body temperature could be attained without the energy cost typical of endotherms. It is clear that one advantage of a high and stable body temperature is coordination of biochemical and physiological activities at optimum levels, an explanation often used in relation to endotherms. Seebacher et al. also recognised that warm, ectothermic reptiles nevertheless do not show the same capacity for sustained activity levels characteristic of endotherms, but the difference in performance would be smaller if they were warmer. This is undoubtedly true, but it would be interesting to know how much smaller it would be.

Moreover, it would be more interesting to determine the total power output, including both aerobic and anaerobic sources, to assess how ectothermic, crocodile-like dinosaurs would compare to endothermic, mammal-like dinosaurs. Aerobic metabolic scope is the energy production by the respiratory metabolic pathways, as measured by the difference between resting and maximum rates of O 2 consumption. Anaerobic metabolic scope is the maximum rate of useful energy production by anaerobic glycolysis, as measured by the rate of lactate production. Both measurements can be converted to ATP production and then into power, measured as a rate in units of Watts (Joules per second). Anaerobic scope, which is a rate, should not be confused with anaerobic capacity, which is the total amount of energy produced anaerobically by the time of total exhaustion [20].