There is a fundamental difference between the metabolic rates ofhomeothermic or tachymetabolic (= fast rate of chemical change) animals and those of heterothermal bradymetabolic (= slow rate of chemical change) animals whose body temperatures tend to vary according to that of the environment. In today's mammals and birds the metabolic rate is about four times greater than that in extant reptiles.
The occurrence of blood shunting from superficial to deep tissues as a means of conserving heat is now well established among modern reptiles. Cowles (1958) argued that it originated from the dermal vascularity of Amphibia and must have served in the remote past as a necessary adjunct to their notable dependence on supplemental dermal respiration. Later, it became a mechanism for collecting and dispersing heat in reptiles and, finally, the essential temperature regulator of the endotherms.
There has been considerable speculation regarding the possible capacity of the dinosaurs to produce metabolic heat to some measure in excess of that of modern reptiles. Benedict (1932) showed that the rate of metabolism in reptiles decreases with increase in body size, while Schatz (1957) claimed that the dinosaurs had extremely slow rates of metabolism. Other workers, however, have maintained that the dinosaurs were not only homeothermic, but were also tachymetabolic, and their arguments have been criticised severely. There are two factors which strongly suggest that the dinosaurs may have differed physiologically from modern reptiles. First, they were the dominant terrestrial vertebrates for over 100 million years, in which respect they have been equalled only by the mammals. Second, they disappeared, apparently quite suddenly, about 65 mya, whereas crocodiles, turtles, lizards and snakes underwent no major change at that time and have even shown a modest amount of adaptive radiation subsequently. Several authors have postulated that the evolution of endothermy could have been a critical factor in the extinction of the Mesozoic archosaurs (Chap. 12).
In 1968, Bakker claimed that dinosaurs were fast, agile, energetic creatures that lived at a high physiological level reached elsewhere among land vertebrates only by the later, advanced mammals (Sect. 7.4). Three years later, he specifically proposed that they might have been homeothermic, and that the production of heat was endothermal (Bakker 1971a). Then he wrote an article in which he summarised all the arguments for endothermy or tachymeta-bolism in dinosaurs, classifying them broadly as: 'gross anatomical', 'cellular', and 'community structure'. In 1972, he introduced a fourth category of argument, based on palaeolatitudinal zonation (Bakker 1972). Bakker's arguments have been criticised by Feduccia (1973), Bennett and Dalzell (1973),Thulborn (1973, 1975), and Feduccia (1974), among others. They were defended by Ostrom (1974b),Dodson (1974),by Bakker himself (1974),and later by Wilford (1986). Defending arguments were expanded into a controversial book by Des mond (1975): Bakker's own book on the subject appeared rather later (Bakker 1987). A comprehensive and unbiased review of the dispute was given by Charig (1976) who pointed out that although he, himself, was not opposed to the concept of endothermy (which he considered to be neither proved nor disproved), he was opposed to the use of fallacious argument,with which many of the papers cited above would, he claimed, appear to have been liberally endowed!
Bakker (1971a, 1972) proposed that, since the dinosaurs had a fully erect gait -indicated by the anatomy of their joints and their fossilised footprints - their metabolic rates and levels of activity must greatly have exceeded those of modern reptiles. This interpretation was challenged by Bennett and Dalzell (1973) and Feduccia (1974) on the grounds that no logical connection between fully erect posture and endothermy has been demonstrated. Metabolic data based on studies of modern lizards fail to reveal any correlation between limb length and metabolic rate: at equal body temperature, standard metabolic rate is solely a function of body size. "Dinosaurs may well have been homeothermic, but Bakker fails to construct a convincing case. This failure rests on an inadequate analysis of the biomechanics of fossil and contemporary vertebrates and on the inability to establish a physiological connection between homeothermy, metabolism and posture" (Bennett and Dalzell 1973).
Feduccia (1973) also pointed out that Bakker (1971a) was imprecise in his terminology. "Without defining terms, Bakker (1971a, p. 637) speaks of homeothermic mammals,and concludes (Bakker 1971a,p. 656) with homeothermic dinosaurs. One assumes that he is using homeothermy synonymously with endothermy. But his terminology is confusing when he states (Bakker 1971a, p. 646) 'Endothermy and thermal homeostasis require a larger energy budget than ectothermy and heterothermy, and therefore homeothermy requires more continuous food-getting activity...' Ostrom's statement (1969, p. 369) that dinosaurs, etc., '...were homeothermic and perhaps endothermic... ' is also somewhat confusing, but one is generally led to believe that both authors consider the dinosaurs to be very close to birds and mammals in their abilities at temperature regulation" (Feduccia 1973).
The major premise of the arguments of Ostrom (1969) and Bakker (1971a) relied upon the fact that there are no living terrestrial vertebrates with erect posture that are ectothermic. From this, both authors concluded that all erect terrestrial vertebrates must be endothermic but, as Feduccia (1973) replied, the converse does not hold.
Erect posture, vertebral excavations, along with a myriad of other more specific adaptations were probably all part of a complex structural system to support the tremendous weight of these giants. Furthermore, Heath (1968) who also postulated that the dinosaurs might have been endothermal, noted too that higher vertebrates and insects probably developed thermoregulation as a response to rapid fluctuations of temperature in terrestrial environments.
To such criticisms Ostrom (1974b) replied: "Of course an endotherm maybe adapted for a sprawling existence with non-erect posture. Endothermy does not impose upright carriage, but ectothermy may be a major constraint that makes erect posture and locomotion impossible." Whereas Dodson (1974) wrote: "It is commonly accepted that the rigors of the climate selected for endothermy among therapsids; it is equally probable that the same selective agents affected a similar state among advanced thecodonts. The fossil record strongly supports the interpretation that dinosaurs attained physiological refinement first, as expressed in erect posture and bipedality, and that mammals avoided competition and extinction by maintaining small body size and inconspicuous habits through the Mesozoic. The remainder of the Era is not to be thought of as a benign hot-house. We owe the preservation of North American Jurassic and Cretaceous dinosaurs to orogenies that produced widespread tectonic deltas, and it may be assumed that these orogenies affected climate as did their counterparts in the Triassic."
While the quality of dinosaur muscle (in which most thermogenic activity must have taken place) cannot be assessed, one subtle aspect of their anatomy which strengthens the comparison with birds and mammals is the finding, now well established, that the histology of dinosaur bone is characterised by the extensive development of dense secondary Haversian canal systems (see refs. in Dodson 1974; de Ricqles 1974). In contrast, the bones of living ecto-therms are relatively poorly organised, having few Haversian canals and very little reorganisation of spongy tissues. Moreover, in strongly seasonal climates, where drought or winter cold forces ectotherms to become dormant, growth rings appear in the outer layers of compact bone, much like the rings in the wood of trees in similar environments. Such growth rings are hardly ever seen in the bones of tachymetabolic birds and mammals, nor do they appear in those of dinosaurs. Comparative studies of the histology of reptilian bones make possible a functional interpretation of their structure (Fig. 73). This suggests that several orders of fossil reptiles, including therapsids, dinosaurs, and pterosaurs, were tachymetabolic (de Ricqles 1974, 1976, 1980). According to Bouvier (1977), however, comparative histological data show that secondary Haversian bone is found among both ectotherms and endotherms. Not all endotherms possess extensive Haversian systems nor do all ectotherms lack them. Moreover, the function of these may partly be to increase the mechanical strength of bone. Consequently, Haversian bone should not be utilised as an indicator of thermoregulatory strategy as Bakker has attempted to do. On the other hand, if de Ricqles (1976,1980) was correct, his data do strongly support the suggestion that not only dinosaurs but also therapsids (as well as ptero-
■ Fig. 73. An attempt to visualise gross functional relationships between bone histology, morphology and thermal physiology among terrestrial tetrapod vertebrates. Typical primitive ectothermic pattern is shown on the left, typical advanced endothermic pattern on the right. Many groups of tetrapods may of course show various intermediate conditions, for one or several factors involved, and hence should be placed at or near the middle. (Cloudsley-Thompson 1978 after de Ricqles 1974)
saurs) were endotherms with tachymetabolic thermoregulation (see list of papers by de Ricqles in Thomas and Olson 1980; Reid 1984,1997).
Energy Flow and Predator: Prey Ratios
Another indication of thermogenesis is afforded by the ratio of predatory animals to their prey. Thus, by extrapolating from the food consumption of birds and mammals, it is possible to obtain crude estimates of the theoretical ingestion rate of 'tachymetabolic dinosaurs' and similar extrapolation from the ingestion rates of reptiles and amphibians provides theoretical estimates of the ingestion rate of 'bradymetabolic dinosaurs'. By deriving an empirical equation relating the ratio of predatory forms to prey, it should be possible to determine whether the predators were ectothermic or endothermic. This ratio is constant, regardless of the body size of the animals in the system, in consequence of the effects of scaling in predator:prey energy flow; but it differs very considerably according to whether the predator is bradymetabolic or tachy-metabolic. Bakker (1975) expressed this argument as follows: "The energy budget of an endothermic population is an order of magnitude larger than that of an ectothermic population of the same size and adult weight, but the pro-ductivity...is about the same... A given prey population, either ectotherms or endotherms, can support an order of magnitude greater biomass of ecto-thermic predators than of endothermic predators, because of the endotherms' higher energy needs. A herd of zebras produces about a quarter or a third of its weight in carcasses per year, but a population of mice may yield up to six times its weight because of its rapid turnover, reflected in short life span and high metabolism per unit weight. Now, the energy budget per unit of predator standing crop also decreases with increasing weight: lions require more than ten times their own weight in meat per year, whereas shrews need 100 times their weight. These two bioenergetic scaling factors cancel each other, so that if the adult size of the predator is roughly the same as that of the prey (and in land vertebrates it usually is), the maximum ratio of predator standing crop to prey standing crop in a steady-state community is a constant independent of the adult body size in the predator-prey system."
Some fossil deposits yield hundreds or thousands of individuals representing a single community. Their live weight or biomass can be calculated from reconstruction of complete skeletons, and the total predator:prey ratios are then easily worked out. Such an analysis of energy flow strongly indicates that the energy budgets of the dinosaurs were like those of large mammals, not elephant-sized lizards (Bakker 1972).
Bakker (1972) based some of his calculations on the estimate that a Komodo dragon (Varanus komodoensis) takes large prey about once a month, together with the assumption that the weight of the prey is roughly half that of the lizard. From this he deduced that the Komodo dragon consumes its own weight in prey every 60 days. There is evidence, however, as Thulborn (1973) pointed out, that the animal can kill prey two or three times as heavy as itself, and may ingest its own weight in prey every 10-15 days, whereas the tiger consumes its own body weight in food approximately every 24 days.
Another objection that may be brought against Bakker's argument is that palaeontologists, when collecting fossils, invariably go for the rarer predators rather than for herbivores - which are far less interesting. The bias results in an apparent exaggeration in the biomass of predators. This, however, would slant the ratio in the direction of bradymetabolism, while the enormous size of the herbivores would be bound to distort the ratio even if the vagaries of fossilisation are ignored (Cloudsley-Thompson 1978). Other objections raised by Charig (1976) included the fact that no allowance can be made for differing life spans, that some prey species were more palatable than others, robust skeletons are more likely to be preserved than fragile ones, and species that lived in the lowlands would have been more likely to be preserved than upland species.
Bakker (1972) suggested that the dinosaurs were built for sustained locomotion at moderate speeds and inferred from this that they were endothermic, but Thulborn (1973) considered that they were not built for sustained speed, but rather attained their maximum speed in short bursts. The cheetah can attain a maximum speed of 97 km h-1 for about 15-20 s, but soon slows down if not successful in catching its prey. Lizards, although cold-blooded, are also capable of fast running for short periods and a similar mechanism could have permitted sophisticated cheetah-like predation in communities of ectother-mic dinosaurs.
In order to test Bakker's (1972) hypothesis, Farlow (1976) investigated the trophic dynamics of a community of large Upper Cretaceous dinosaurs in the Oldman Formation - sediments that were deposited along the margin of a great inland sea that once covered much of the western interior of North America. The environment of deposition appears to have been tracts of fluvial marshes that separated islands of higher, drier ground. The climate was warm-temperate, and Farlow suggested that the upland plant communities were probably park-like in aspect. The large dinosaurs of this community comprised animals that were between a hippopotamus and a large African elephant in adult weight. Calculations suggest that the annual secondary production of tachymetabolic herbivorous dinosaurs would have been insufficient to meet the food requirements of a bradymetabolic carnivorous dinosaur population as large as is preserved in the Oldman Formation. However, ectothermic dinosaurs would have been easily able to make energetic ends meet. Unfortunately the situation is complicated by the possibility that carnivores are over-represented in collections from Oldman. Because of this, Farlow (1976) was unable to decide between ectothermy or endothermy, and the question still remains undecided. Bakker's idea, though sound in theory, should not be applied in practice (Charig 1976)!
One of the analytical tools of palaeobioenergetics is latitudinal zonation. Palaeomagnetic data makes it possible to reconstruct, to within about 5° latitude, the ancient positions of the continents before they drifted to their present positions. According to Bakker (1975), large reptiles found fossilised in sediments laid down under cold, or seasonally cold, conditions, could not have endured those conditions unless they were endothermic. Although he applied this argument only to mammal-like reptiles, it presumably carries the corollary implication that endothermy evolved as an adaptation to low temperatures in dinosaurs also. In fact, the argument cannot be applied to dinosaurs, as Charig (1976) pointed out, and Bakker's conclusions regarding palaeoclimates were contrary to those of many other workers in the field. If the dinosaurs died of cold, as Bakker (1975) also suggested, this might be taken to imply that they were ectothermic, since it has been argued that endothermy evolved in response to the colder periods of a seasonal climate (Dodson 1974).
Relying primarily on the work of John Ostrom, Robert Bakker, and Armand de Ricqles on dinosaur ecology, energetics, posture, gait and bone histology, Desmond (1975) presented an extreme view of the case that the dinosaurs were active terrestrial creatures with mammal-like physiology. In his book, he linked endothermy with high intelligence and this, in turn, with complex behaviour. He also asserted that if an adult reptile remains near the young, its limited intelligence cannot overcome the temptation to eat them. However, as R.J. Wassersug pointed out in a review of Desmond's book, "Adult crocodiles co-operate in feeding activities. Parents help their hatchlings escape the egg and nest; a mother collects hatchlings and transports them to the water in her mouth. Complex behaviour of the type posited for dinosaurs evidently does not require endothermy in the archosaurs." Moreover, Desmond (1975) exaggerated the view of de Ricqles (1974), who wrote, "If the origins of perfect 'warm-bloodedness' (endo-and homeothermy) are looked for among the primitive representatives of lineages of warm-blooded modern vertebrates, one cannot ask for a sudden appearance among them of all the associated features that one can find among living, modern warm-blooded animals." In de Ricqles' opinion, the larger dinosaurs had a peculiar physiology by any standard, one that can hardly be regarded as typically reptilian, but better understood as something of its own.
Many authors have argued that the dinosaurs were endothermic (Bakker 1968, 1971a, 1972,1974,1987; Desmond 1975; Dodson 1976; Heath 1968; Ostrom 1969, 1974b; de Ricqles 1974,1976), while others have disputed their arguments, and claimed that the dinosaurs were ectothermic (Bennett and Dalzell 1973; Feduccia 1973; Thulborn 1973,1975; Bennett 1974). Certainly, they could not have been very speedy (Alexander 1985, 1989, 1997a,b; Thulborn 1973) but bulk alone, as we have seen, may be quite sufficient to retard the dissipation of environmentally acquired heat (Colbert et al. 1946; Spolita et al. 1973). Seymour (1976) argued that the sustained high blood pressure inferred from the large vertical distance between the heart and the head in some dinosaurs (Sect. 7.3) supports, but does not prove, the proposition that dinosaurs were endothermic. The case for tachymetabolism cannot be regarded as proven, even though the dinosaurs must, almost certainly, have been homeothermic. Bennett and Dawson (1976) concluded that, if the dinosaurs did possess an elevated metabolism, it may have evolved in response to factors involved in activity rather than in thermoregulation.
Some years later, Bennett and Ruben (1986) reviewed the considerable amount of evidence for endothermy in therapsids. This included the nasal turbinal complex (the nasal cavities approached the condition found in modern mammals), the large number of traits shared by therapsids and mono-tremes, and the histology of their bones. These authors concluded that at least the more advanced of the mammal-like reptiles were tachymetabolic, the adaptive advantage of which had been discussed by Kemp (1982; Sect. 7.5.6).
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