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Home , Comparative physiology, Dinosaur renaissance, Ectotherm, Endotherm, Homeothermy

Evolution, 33(3), 1979, pp. 983-997

ECTOTHERMY AND THE SUCCESS OF

MICHAEL J. BENTON Department of Geology, The University, Newcastle-upon-Tyne, NE1 7RU, England, U.K.

Received February 28, 1978. Revised October 9, 1978

Dinosaurs were the dominant terrestrial AAAS symposium published as Olson and tetrapods of the Mesozoic and their eco- Thomas (1979) and references to papers logical roles and biological impact are gen- from this volume are, as a result, brief. erally compared with those of in the Cenozoic. This has led to the as- DISCUSSION OF EVIDENCE FOR sumption that dinosaurs were - ENDOTHERMY ic also (Bakker, 1971, 1979) and there Interest in the thermoregulatory physi- seems to be some evidence in support of ology of dinosaurs has revived recently this hypothesis. However, this evidence is (Bakker, 1975a; Desmond, 1975; Gould, not conclusive. Could it be that dinosaurs 1977; May, 1977; Marx, 1978; Olson and were in fact ectothermic and could their Thomas, 1979), although speculations success be explained most simply in terms have been made on this topic for at least of a normal reptilian ? 100 years. Audowa (1929) and Nopcsa In this paper I review the published evi- (1934) suggested that dinosaur dence for and against dinosaur endother- might have been related to their ectother- my and attempt an assessment in terms of my, but other later authors have suggested the thermoregulatroy physiology of living that it was connected with their endother- animals, and I discuss the success and the my (Wieland, 1942; Russell, 1965; Cloud- extinction of dinosaurs in connection with sley-Thompson, 1971; Bakker, 1972, published data on Mesozoic paleoclima- 1973). tology. It is argued that endothermy in Broili (1941) and Schuh (1951), extrap- dinosaurs would have been energetically olating from finds in and syn- costly and yet there appears to have been apsids, predicted that dinosaurs would be no need for it. Ostrom (1979) complains found with "hair," necessary insulation in that critics of dinosaur endothermy merely an endotherm. However, others have re- offer alternatives and do not disprove the lated the large size and naked of di- arguments of their opponents. This paper nosaurs to endothermy, arguing that the attempts to show why dinosaurs (with the absence of small dinosaurs is connected possible exception of some theropods) had with the problems of excessive heat loss to be ectothermic. by small uninsulated with a Before proceeding, the four basic de- high surface/volume ratio (Bakker, 1971, scriptive terms used in thermoregulatory 1972, 1973; Ricqles, 1974). These latter physiology should be defined accurately interpretations were criticized by Thul- (Cowles, 1940, 1962; McNab, 1978). A born (1973) and Feduccia (1973) who poikilothermic animal has no control over pointed out that young dinosaurs were body temperature, which follows external small and naked and could only have conditions, while a homeothermic animal avoided cooling stress problems if they has a constant body temperature. An ec- were ectothermic. totherm derives heat from external sources The evidence most recently presented (generally solar radiation directly or indi- for dinosaur endothermy includes erect rectly) and an endotherm from internal gait, paleoclimates and distribution, small sources (generally metabolic or muscular agile dinosaurs, brain size, predator-prey heat). ratios, bone histology, and the parietal- This paper was written before the pineal complex. 983

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Erect gait. -Dinosaurs had erect stance saurs. However, this may be connected and advanced gait. Among living animals, with gait rather than . only endotherms have erect gait; and it Most living have a sprawling was suggested that this and the supposed stance, whereas the agile theropods had ability of dinosaurs to achieve fast speeds an erect stance. The erect posture which indicated endothermy (Schuh, 1951; Os- supported the great weight of brontosaurs trom, 1970, 1974; Bakker, 1971, 1972, allowed agile motion in smaller dinosaurs. 1973, 1974, 1975a; Dodson, 1974). How- The generally warm Mesozoic climates ever, this view has been widely criticized (see below) may have maintained their as a logical non sequitur (Thulborn, 1973; body temperatures high enough during the Bennett and Dalzell, 1973; Feduccia, day for activity and their carnivorous diet 1973, 1974; Bennett, 1974; Halstead, provided readily assimilable energy. After 1976). The fact that the only living ani- a cool night, body temperatures may have mals with erect gait are endotherms does been increased by basking or uptake of not mean that every animal with erect gait heat from rocks in the early morning as in is an endotherm-it should also be noted living reptiles. Ostrom (1978, 1979) sug- that many mammals and other endo- gests that the only possibly endothermic thermic animals (see below) have a dinosaurs were these small theropods, sprawling gait (Jenkins, 1971). In addi- particularly in view of their possible re- tion, Alexander (1976) calculated speeds lationship to . of only 1-3.6 ms-t from trackways of di- Brain size. -Feduccia (1973) suggested nosaur footprints, although one hadrosaur that the small lizard-like brain size of di- trackway indicates a speed of 7.5 ms- nosaurs speaks for ectothermy, but finds (Russell and Beland, 1976). Thus large of "ostrich dinosaurs" with large brains dinosaurs, at least, may have moved rel- (Russell, 1972) were interpreted as evi- atively slowly and the erect stance may be dence for endothermy (Dodson, 1974; no more than the most efficient way of Ricqles, 1974; Bakker, 1974, 1975a). supporting a heavy body (Bennett and However, the large brains of these dino- Dalzell, 1973; Feduccia, 1973; Bennett, saurs are associated with good eyesight 1974; McNab, 1978). and balance (Halstead, 1975b) and do not Paleoclimatology and distribution.- necessarily imply advanced -like Finds of dinosaurs within the Cretaceous intelligence. In any case, internal ther- Arctic Circle (Russell, 1973) have been moregulation requires a smaller mass of thought to indicate endothermy also (Bak- neural tissue than that required by ecto- ker, 1975a; Desmond, 1975), but precise therms for the behavioral control of inter- data on Mesozoic climates are not given nal temperature (Jerison, 1973) and thus (Halstead, 1975b, 1976). There is no evi- brain size may not be a reliable indicator dence of glaciation in the Mesozoic of endothermy (cf. Robinson, 1971). (Schwarzbach, 1963; Bakker, 1975b) and Predator-prey ratios. -Herbivores climates at these high latitudes need not (whether endothermic or ectothermic) can have been cold. In general, Mesozoic cli- support about 5% of their biomass of en- mates were warmer than today (Dorf, dothermic predators, and for ectothermic 1970; see below). () carnivores, this predator-prey ra- Small agile dinosaurs. -Many smaller tio is apparently nearer 30-50% (Bakker, dinosaurs (especially lightly built thero- 1972, 1975a, 1975b, 1979). Bakker pods like Compsognathus, Saurorni- (1972, 1973, 1974, 1975a, 1975b) calcu- thoides and ) were presum- lated predator--prey ratios for certain fos- ably agile and must have been able to sil populations and used the values he move rapidly (Ostrom, 1978). At first obtained as indices of ectothermy or en- sight, this is very different from many liv- dothermy. He noted a drop from 50% in ing lizards and might be thought to be the Early to 10% in the Late good evidence for endothermy in dino- Permian and concluded that this repre-

This content downloaded from 137.222.249.97 on Fri, 29 Jan 2016 22:22:16 UTC All use subject to JSTOR Terms and Conditions ECTOTHERMY AND THE SUCCESS OF DINOSAURS 985 sented the changeover from ectothermy to phocalcic salts, and they develop espe- endothermy in populations of rep- cially in rapid growth (Ricqles, 1974). The tiles. idea has arisen that these Haversian sys- Charig (1976) listed many possible tems indicate endothermy (Enlow and sources of error in applying predator-prey Brown, 1957; Currey, 1962; Ricqles, ratios to fossil communities, such as col- 1969, 1972a, 1972b, 1974, 1976; Bakker, lector bias, incompleteness of the fossil re- 1972, 1974, 1975a; Dodson, 1974). cord, relative life spans, and interactions Large mammals, most birds, advanced of other animals in food chains. I would and dinosaurs have extensive add that some "prey" (e.g., Bron- Haversian systems, and , and tosaurus) might have been unavailable for have them less developed. They predation owing to very large size, al- are not present in small mammals, pas- though they could have been scavenged serine birds, lizards, snakes or primitive after they died, but their inclusion would reptiles (Enlow, 1969; Ricqles, 1974, greatly lower the apparent predator-prey 1976). The first two in this list are the ratio. The present-day elephants effective- "most" endothermic vertebrates (i.e., they ly have no natural predators because of have the highest rates of mass-specific their large size. Of course, the ratios can ), and they might be expected only indicate whether the predator is en- to have such structures most highly de- dothermic or ectothermic: the amount of veloped (McNab, 1978). Thus, Haversian prey required would be the same whatever systems are present in most living endo- its thermoregulatory state. If ectothermic therms and some living and tyrannosaurs ate their young or other car- tend to be associated with large size (Hal- nivores, or if they were partly scavengers, stead, 1976). Bouvier (1977) lists animals the ratios could be explained readily (Tra- with secondary Haversian systems and cy, 1976). shows that their presence is not correlated In fact, it seems that ratios of large with endothermy. The correlation seems ectothermic predators to prey closely ap- instead to be with (McNab, proach those for endothermic predators, 1978). thus casting doubt on the value of this Dinosaurs were large, and yet their eggs concept as a measure of the presence of were mechanically limited in size; the endothermy in dinosaurs (Thulborn, 1973; hatchlings often being only 1-2% of the Farlow, 1979; Russell and Bieland, 1979). weight of their parents (Colbert, 1961). A Halstead (1976) suggested that ratios vary vulnerable young dinosaur may have had with the size of the animals involved, to grow fast in order to achieve its adult and not with thermoregulatory state. size and this would have involve contin- Bakker apparently used unspecified uous bone remodelling. The presence of "corrections"in some calculations of rela- Haversian systems in these forms is prob- tive numbers of faunal elements and ably explained by their large size and rap- some of his assumptions about ingestion id growth. rates are not well founded (Farlow, 1976; Parietal-pineal complex.-Living rep- Russell and Beland, 1979). His conclu- tiles may control their body temperature sions cannot be properly assessed until by behavioral means to within a very nar- these corrections, assumptions, and his row range. This control is effected in re- original data are published. sponse to information from the pineal Bone histology.-In large mammals the gland and parietal eye, and these struc- regeneration and internal remodelling of tures tend to disappear in the fossil record bone involves the development of Haver- as animals become endothermic. Certain sian systems (Enlow, 1962). Haversian fossil amphibians and early fossil reptiles bone and good vascularization are asso- (e.g., batrachosaurs, cotylosaurs, pelyco- ciated with the freeing and fixing of phos- saurs: Olson, 1976) show large parietal

This content downloaded from 137.222.249.97 on Fri, 29 Jan 2016 22:22:16 UTC All use subject to JSTOR Terms and Conditions 986 MICHAEL J. BENTON openings, whereas dinosaurs do not. This Spotila et al. (1973) modelled an iner- might be taken as evidence of endother- tially homeothermic dinosaur maintaining my, but there is no pineal in crocodiles. its internal temperature at 30 C, but Bak- The loss of the parietal-pineal complex ker (1975b) suggested that 38 C+ would may be related to the fact that both groups be a more likely temperature because of of reptiles live in warm climates and do its "high activity." Ignoring the circular not need such a precise regulator (Roth, logic here, 38 C is the normal body tem- 1979). perature of a eutherian mammal, and many highly active reptiles and non-eu- LARGE SIZE OF DINOSAURS AND therian mammals normally operate at INERTIAL HOMEOTHERMY lower temperatures (Schmidt-Nielsen, Studies of large living reptiles (alliga- 1975). The alleged "high activity" of large tors: Colbert et al., 1946, 1947; Galapagos dinosaurs still remains highly speculative tortoise: Mackay, 1964; Komodo monitor: and indeed Spotila (1979) suggests that a McNab and Auffenberg, 1976) have shown "very active . . . lifestyle is entirely com- that rates of internal temperature change patible with the thermoregulatory status are very slow during normal subtropical as ectothermic homeotherms." diurnal temperature fluctuations. By ex- trapolation, temperatures of medium to HEAT-EXCHANGE STRUCTURES AND large dinosaurs living in similar climatic THERMOREGULATION conditions would remain constant to with- Several early reptiles displayed sail-like in 1 or 2 C inertially without internal structures which have been interpreted heat production (Colbert et al., 1946, variously as defensive, display, camou- 1947; Spotila et al., 1973; McNab and flage, or temperature-control organs. The Auffenberg, 1976; McNab, 1978; Spotila, Early Permian pelycosaurs Edaphosaurus 1979). However, Gunn (1943) speculated and Dimetrodon in particular had large that dinosaurs would have displayed diur- dorsal "sails," produced by elongation of nal cycles of body temperature fluctuation the neural spines, which are usually sup- only somewhat more out of phase with posed to be involved in temperature reg- external temperature changes than in ulation (Rodbard, 1949; Romer, 1966; Ol- smaller reptiles. Working from data on son, 1971; Bramwell and Fellgett, 1973; recent reptiles, he assumed that basal heat Halstead, 1975a). The large herbivorous production was constant for a given sur- dinosaur Ouranosaurus and the carnivore face area and that large reptiles thus pro- Spinosaurus form the Cretaceous of duced less heat per gram body weight. North Africa both had dorsal sails formed However, metabolism in reptiles is not similarly from elongated neural spines. directly proportional to body weight or These are proposed as structures to in- surface area (Bennett and Dawson, 1976), crease heat-loss during vigorous exercise and these speculations cannot be regarded in a hot environment (Halstead, 1975a). as valid. Thus dinosaurs achieved thermal Recent work on Stegosaurus (Farlow et constancy by large size (Cloudsley- al., 1976) has suggested that its apparently Thompson, 1972; Halstead, 1975a, 1975b, well-vascularized dorsal plates could have 1976). High metabolic rates may have acted as efficient forced heat convection been produced by activity metabolism and "fins" in a dry, hot environment. Cooling large size rather than thermoregulation structures are seen, for example, in pres- (Bennett and Dawson, 1976). Thus it ent-day African elephants which extend seems that dinosaurs could have been ec- their large well-vascularized ears in order tothermic inertial homeotherms; indeed, to lose excess heat (Sikes, 1971). if they had been endotherms, large dino- Small animals with large expanses of saurs would have suffered overheating membrane or expanded ribs associated (McNab and Auffenberg, 1976; McNab, with gliding or flight (e.g., , ptero- 1978). saurs, the supposed Triassic

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Podopteryx and Longisquama, Kuehneo- range of internal temperature tolerance, saurus and other gliding lizards) would but the absence of such structures in most also experience an increase in heat-loss or contemporaneous dinosaurs could suggest uptake via these structures. This would one of the following: cooler Mesozoic cli- probably be an incidental effect and "sail" mates elsewhere, other heat-loss adapta- or membrane structures have different ba- tions in other dinosaurs, a misinterpreta- sic functions and origins in large and small tion of the function of "sails" or that animals. heat-loss problems were not generally In a medium or large , a bask- acute. Thus, although "sails" were prob- ing structure would increase considerably ably basking structures involved in ther- the rate of morning heating when the an- moregulation, they do not seem to offer imal stood broadside to the sun, and day- information on thermoregulatory physiol- time cooling could be effected if the ani- ogy. It may be of importance to note that mal faced the sun with the minimum area sails have evolved in parallel in a herbi- of sail presented to it. However, this ad- vore and presumably coexisting carnivore ditional vascularized area would also in- in the cases of both Edaphosaurus and crease rates of evening cooling if there was Dimetrodon, and Ouranosaurus and Spi- a sudden drop in temperature at sunset. nosaurus. Probably vessels in the "sail" could also dilate and constrict in order to assist OF ENDOTHERMY the regulation of heat loss and gain. Early It is important to remember that the Permian pelycosaurs are generally as- difference between an endotherm and an sumed to have been ectothermic (Bakker, ectotherm need not be too great. The only 1975a, 1975b; Olson, 1976; Ricql'es, 1976), basic change necessary in the evolution of and in general only the larger genera have endothermy was an increase in the con- sails (Halstead, 1975a), but the largest pel- centration of mitochondria (Bennett and ycosaur, the 1/3-ton Cotylorhynchus (Ro- Dawson, 1976). Other changes, some or mer, 1966), a possible inertial homeo- all of which may occur over a period, are therm, had no sail. However, no small new neural circuitry, development of in- genus had a sail and this may confirm the voluntary responses like , pant- function to increase the rate of body heat- ing or sweating, regulation of peripheral ing in the morning in a large ectotherm circulation, insulating layer of , feath- (Bramwell and Fellgett, 1973). Bakker ers or (Satinoff, 1978). Heath (1968) (1971, p. 652) argued for a non-thermo- suggested that endothermy arose in mam- regulatory display function for the pely- mal-like reptiles in response to the acqui- cosaur sail, comparing it with that found sition of an erect stance which was sup- in the living lizards Basiliscus and Hy- posed to involve increased muscular drosaurus. However, only the males of tension. However, this idea is probably Basiliscus possess crests (Pope, 1957) and not tenable since body temperature in males of Hydrosaurus have larger crests mammals is maintained without muscular than females (Schmidt and Inger, 1957), contractions and all the cells, not just skel- and there is little evidence of such sexual etal muscle, are involved (Jansky, 1973). dimorphism in pelycosaurs (Romer and The membrane sodium pump, con- Price, 1940, p. 171-172). trolled by thyroxine, produces heat and The dorsal sails of the Cretaceous di- stimulation of this mechanism may have nosaurs Ouranosaurus and Spinosaurus been the step involved in the evolution of and the plates of the Jurassic Stegosaurus mammalian endothermy (Edelman and could be heat-loss convectors in an ecto- Ismail-Beigi, 1971; Stevens, 1973). thermic or endothermic model. In a hot Heinrich (1977) proposed that endo- environment, an endotherm would have thermy arose in vertebrates and in greater need of them because of its smaller order to permit high levels of activity for

This content downloaded from 137.222.249.97 on Fri, 29 Jan 2016 22:22:16 UTC All use subject to JSTOR Terms and Conditions 988 MICHAEL J. BENTON extended periods. High temperature set MESOZOIC PALEOCLIMATOLOGY points (40 C or more) may have evolved from an inability to dissipate rapidly all The climate represented by the Late of the heat produced as a result of high Permian reptile beds appears to have been activity rates. Constant high body tem- largely equable with some swampy and peratures involved changes in biochemis- arid conditions (Cox, 1967; Olson and try resulting in more rapid substrate turn- Vaughan, 1970; Robinson, 1971; Bakker, over by enzymes. 1975b). Recovery from the Late Carbon- Endothermy is not an all or nothing iferous glaciation of southern Gondawana- thing. "Primitive" living mammals (mono- land may have produced generally cool tremes, didelphid marsupials, , conditions in some areas (King, 1961). Solenodon, certain hedgehogs) regulate Arid areas appear to have become more their body temperatures at relatively low extensive during the Triassic (King, 1961; levels (27-33 C) which are far below nor- Cox, 1967; Dunbar and Waage, 1969; mal levels in placentals (37-38 C) (Bak- Robinson, 1971) and the Upper Triassic ker, 1971; Crompton et al., 1978). Many Red Bed environment of certain early or- so-called "cold-blooded" animals are, in nithischian dinosaurs was hot and season- fact, endotherms which generate heat by ally arid (Thulborn, 1978). muscular activity (Indian python: Hutch- When dinosaurs were most widespread, inson et al., 1966; lizards: Bartholomew in the Jurassic and Cretaceous, climates and Tucker, 1964; Leatherback : were generally hot or warm and equable Frair et al., 1972; : Carey, 1973; Car- (Colbert, 1953, 1964; King, 1961; ey and Teal, 1969b; Mako and Porbeagle Schwarzbach, 1961, 1963; Vakhrameev, : Carey, 1973; Carey and Teal, 1964; Berlin et al., 1966; Bowen, 1966; 1969a; many large flying insects [moths, Axelrod and Bailey, 1968; Volkheimer, butterflies, bees, beetles, locusts, dragon- 1969, 1972; Dunbar and Waage, 1969; flies]: Heinrich, 1974). Different forms of Montford, 1970; Barnard, 1973; Spotila et endothermy have arisen independently al., 1973; Ricqles, 1974; Hallam, 1975). several times. There is no clear dividing Temperatures were more uniform globally line between ectotherms and endotherms (Lowenstam, 1964; Dunbar and Waage, either today or presumably also in the 1969; Hallam, 1975; Dott and Batten, past, and thus attempts to reclassify ver- 1976; Donn and Shaw, 1977) and latitu- tebrates on the basis of endothermy alone dinal temperature gradients were less (Bakker and Galton, 1974; Bakker, 1975a) steep than today (Bowen, 1966; Donn and hardly seem justified (cf. Charig, 1976). Shaw, 1977). There is no evidence of gla- Present evidence seems to suggest that ciation in the Mesozoic (Schwarzbach, dinosaurs were ectothermic, the larger 1963; Bakker, 1975b) and tropical or tem- ones being inertial homeotherms. Mam- perate floras have been found in the Ju- mal-like reptiles (therapsids) were domi- rassic of the Arctic (Vasilevskaya, 1973) nant on land in the Late Permian and they and Antarctic (Barghoorn, 1953). How- were replaced gradually in most medium- ever, there were apparently some temper- large terrestrial niches by archosaurs ature fluctuations during and at the end throughout the increasingly arid Triassic. of the Cretaceous (Lowenstam and Ep- An attempt is made here to explain the stein, 1959; Lowenstam, 1964; Smiley, replacement of mammal-like reptiles by 1966; Krassilov, 1973, 1975; Vakhrameev, dinosaurs in terms of the advantage of ec- 1975; Van Valen and Sloan, 1977; Mc- tothermy in an arid environment. Thus, Lean, 1978). Seasonal conditions have we must first consider Mesozoic paleocli- been recorded from the Jurassic (Bowen, matology and then compare the relative 1966; Dawson, 1970) and Cretaceous efficiency of ectotherms and endotherms (Dodson, 1971). Dorf (1970, p. 345) sum- in arid conditions. marizes Mesozoic climates, as interpreted

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TABLE 1. Characters of typical ectotherm (reptile) and endotherm (mammal).

Ectotherm Endotherm

Internal regulation of body temperature no yes low high Food supply required small large Range of preferred body temperatures wide narrow Water loss reduced may be high (uricotelic) (ureotelic) from paleobotanical evidence, as follows: and the development of a secondary palate "Evidence suggests that the Triassic, Ju- correlated with the evolution of endother- rassic and Early Cretaceous climates were my in cynodonts and bauriamorphs and more uniform and warmer than at present evidence from bone structure supports this with minor reversals toward cooler and (Ricqles, 1974). Thus endothermy preced- drier conditions." Bakker (1975b) suggest- ed the by 25 million ed that Jurassic and Cretaceous climates years. However, Crompton et al. (1978) may not have been so warm as has been believe that endothermy (they call it ho- assumed, but the evidence indicates only meothermy) arose only later, in small noc- limited cool periods. turnal Mesozoic mammals, and that Paleoclimatic data are derived from mammal-like reptiles were still ectother- studies of sedimentology, paleobotany mic. (whole plants and pollen and spores), in- Present-day arid regions may experi- vertebrate (e.g., coral reefs) ence diurnal cycles of temperature with and oxygen isotope ratios and other geo- cold nights, and seasonal cycles of aridity, physical methods (Bowen, 1966). Dino- with wet seasons. However, the survival saurs have been used as evidence for of an animal depends on how well it can warm Mesozoic climates (e.g., Colbert, survive the worst conditions. Animals 1953, 1964; Schwarzbach, 1963; Volkhei- may either tolerate or avoid the heat and mer, 1969, 1972), but this is best avoided aridity of a . for the present study (Ostrom, 1970). Endotherms (birds and mammals) cope with desert life chiefly by avoiding the THERMOREGULATORYPHYSIOLOGY IN worst conditions. Birds require water and ARIDREGIONS seek shade or pant in order to lose heat The apparent gradually increasing arid- (Dawson and Hudson, 1970). Large desert ity of the Triassic would favor animals mammals (camels, antelope, etc.) have which did not rely on an abundant food evolved many special adaptations such as supply and which could tolerate high tem- the ability to store heat during the day and peratures and conserve water. These are lose it overnight, shade-seeking, reflective the characters typical of an ectotherm and insulating pelage and seasonal migra- (Table 1). Ancestral archosaurs (thecodon- tions to avoid arid conditions. However, tians) were probably ectotherms, whereas most desert mammals weigh less than 250 late therapsids were probably partially en- g, and many weigh less than 50 g (Bar- dothermic (i.e., regulating their internal tholomew and Dawson, 1968). These temperatures at a lower level than euthe- small mammals largely avoid desert con- rians, say 30 C, and still relying on be- ditions by being nocturnal and/or burrow- havioral responses for part of the control ing. [Brink, 1956; Hopson, 1973; Bakker, Sustained endothermy requires constant 1975a; Olson 1976]). McNab (1978) pos- high levels of food which may not be tulates that the reduction in size of mam- available in either very hot arid regions or mal-like reptiles at the end of the Permian seasons (metabolic rates of endotherms are

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5-7 times those of ectotherms of the same conditions of those times (Bakker, 1975b) weight [Bennett and Dawson, 1976] and would not apply to archosaurs in the hot, 80-90% of the oxidative energy of an en- seasonally arid Late Triassic. Conditions dotherm is used to maintain its body tem- were such that early dinosaurs may have perature [Bartholomew, 1968]). Also, in had to aestivate to survive over the dry hot arid environments, the water needed season (Thulborn, 1978). However, en- to dissipate heat may be in short supply dothermy would have been of value to (Bligh, 1972, 1976). small insulated animals that had a large These problems may be reduced, in surface/volume ratio and were either noc- part, by being ectothermic. Reptiles are turnal (e.g., early mammals), or required "apparently well adapted for life in arid large amounts of energy for flight (e.g., regions" (Cloudsley-Thompson and Chad- birds, pterosaurs) (Bakker, 1971; Ostrom, wick, 1964, p. 160). In present-day desert 1974; Desmond, 1975). Bakker (1975b, p. regions the most abundant vertebrates are 392) argues that endothermy is superior to lizards (Mayhew, 1968; Templeton, 1972). ectothermy in wet, tropical condtions. He Lethal body temperatures for lizards are suggests that a particularly cold night around 49-50 C and for snakes, 43-44 C might lower the body temperature of a (Mayhew, 1968), while normal tolerated reptile by 10 C or so and it would be un- body temperature ranges can approach 20 able to recover. However, if estimates of C (e.g., Dipsosaurus dorsalis, the desert rates of diurnal cooling and heating in di- iguana, tolerates 29-47 C [Templeton, nosaurs (Colbert et al., 1946, 1947; Spotila 1970]), whereas most birds and mammals et al., 1973; Halstead, 1975a; McNab and tolerate a range of only about 2 C and the Auffenberg, 1976) are correct, a fall of 10 camel can only tolerate 34-40 C (Schmidt- C in a large dinosaur would require ex- Nielsen et al., 1957). Desert reptiles lose cessively cold conditions for a consider- less water than endotherms of the same able period of time. Also, this argument weight (Chew and Dammonn, 1961; only applies to wet tropical conditions Schmidt-Nielsen and Dawson, 1964; which were restricted in extent in the Late Cloudsley-Thompson, 1971). Triassic when dinosaurs were establishing It is interesting to note that the only themselves. large desert animals at present are mam- mals. But, of course, most large animals REPLACEMENT OF THERAPSIDS BY in any terrestrial environment today are ARCHOSAURS mammals, presumably because of their Late Permian and Early Triassic the- rapid adaptive radiation at the beginning codontians may be divided into two of the Tertiary and the specialized groups on the basis of presumed lifestyle. of the surviving reptile groups which were First, there were the medium-large fresh- apparently not preadapted to compete water predators (Proterosuchidae and successfully and evolve into large herbi- Erythrosuchidae)which occupied the "croc- vores or carnivores on land. Most large odile niche" (Reig, 1970; Charig and Sues, reptiles today are carnivores (Crocodylia, 1976). Water tends to buffer ambient tem- Komodo monitor, snakes) and herbivory perature fluctuations and hence endother- is less common (Porter, 1972). In the Early my is unnecessary for animals living in Triassic, when mammals were absent, relatively warm water. The second the- medium-large herbivorous reptiles were codontian group (Euparkeriidae) were abundant and, with increasing aridity medium-sized predators of arid uplands throughout that period, it seems reason- and lowlands (Ewer, 1965). able to assume that the successful ones These two groups comprise the first (archosaurs) were still ectothermic. Any (admittedly not very abundant) wave of advantages that endothermy may have radiation, the replacement of had for the Late Permian and Early Trias- mammal-like reptiles in many carnivorous sic therapsids in the wetter, more equable niches. Both groups appear to owe this

This content downloaded from 137.222.249.97 on Fri, 29 Jan 2016 22:22:16 UTC All use subject to JSTOR Terms and Conditions ECTOTHERMY AND THE SUCCESS OF DINOSAURS 991 success to the improvement of gait and ance of a wider range of temperatures jaw action (Romer, 1966) and to ectother- than endotherms) would have been ad- my. vantageous in arid Late Triassic environ- During the Middle and Late Triassic, ments. The development of large body herbivorous therapsids also were replaced size, and thus inertial homeothermy, in progressively by thecodontians and early the less arid Jurassic and Cretaceous as- dinosaurs. With increasing aridity, the sured the continued success of dinosaurs areas of lush lowland vegetation were re- (Colbert et al., 1946, 1947; Spotila et al., duced, and those animals that could sur- 1973). It cannot be assumed that endo- vive at higher temperatures on less plant thermy is always selectively more advan- food and lower water availability would tageous than ectothermy. be favored. Again, ectotherms had the ad- vantage, and the second wave of archo- saur radiation also may be attributed to DINOSAUR EXTINCTION their ectothermy. These, and other im- Dinosaur extinction has been explained portant ecological replacements of the in terms of a temperature drop at the end Mesozoic are discussed in Benton (1979). of the Cretaceous associated with ecto- thermy (Audowa, 1929; Nopcsa, 1934), a DINOSAUR SUCCESS temperature rise at the end of the Creta- The success and extinction of the di- ceous and endothermy (Wieland, 1942), a nosaurs presents a paradox. Archosaurs temperature drop and endothermy (Rus- replaced therapsids in nearly all major ter- sell, 1965, 1966, 1967; Cloudsley-Thomp- restrial niches causing the virtual extinc- son, 1971; Bakker, 1972, 1975a), a tem- tion of the latter. The tiny descendants of perature drop and inertial homeothermy the therapsids, the early mammals, con- (Axelrod and Bailey, 1968; Halstead, tinued throughout the Mesozoic as a rel- 1975a), or a temperature rise and endo- atively insignificant group of small insec- thermy or ectothermy (McLean, 1978), tivores but replaced the dinosaurs in among many other hypotheses. nearly all their niches at the end of the Certain isotopic, micropaleontological Mesozoic. Note that the replacement of and paleobotanical evidence seems to in- therapsids by dinosaurs apparently oc- dicate a temperature drop at the end of curred by gradual processes of competi- the Cretaceous (Lowenstam and Epstein, tion, whereas the adaptive radiation of 1959; Lowenstam, 1964; Russell, 1965, Tertiary mammals occurred only after the 1966; Hall and Norton, 1967; Worsley, sudden extinction of dinosaurs. The suc- 1971; Krassilov, 1975; Percival and Fi- cess of dinosaurs has been ascribed to scher, 1977; Van Valen and Sloan, 1977), many factors, such as -eating among but McLean (1978) gives evidence of a diapsids (Watson, 1957), advanced gait temperature drop followed by a rise at this (Bakker, 1968; Thulborn, 1975), endo- time. Russell (1965, 1966) suggested that thermy (Cox, 1967; Bakker, 1971, 1972, floras became more temperate in nature at 1973, 1975a, 1979), ectothermy and iner- the end of the Cretaceous and that this tial homeothermy (Colbert et al., 1947), was associated with greater climatic sea- and uricotelism (Robinson, 1971). sonality. Axelrod and Bailey (1968) also Robinson (1971), assuming that both postulated that reduced equability in the archosaurs and synapsids were ectother- Late Cretaceous (indicated by floral mic, suggested that the former were dis- changes) could have given diurnal tem- tinguished by uricotelism alone (note that perature fluctuations that were too great Reig, 1970, p. 265, suggested that both for the inertially homeothermic dinosaurs mammals and archosaurs excreted urea to tolerate. rather than uric acid). However, if mam- If the climate became cooler, the body mal-like reptiles were endothermic, dino- temperatures of dinosaurs would fall saur ectothermy (including uricotelism, gradually as night-time cooling came to but also the need for less food and toler- exceed day-time heat absorption. When

This content downloaded from 137.222.249.97 on Fri, 29 Jan 2016 22:22:16 UTC All use subject to JSTOR Terms and Conditions 992 MICHAEL J. BENTON body temperatures reached a dangerously mammals produced by the cumulative ef- low level, the animals would have become fects of decreasing temperatures and torpid and died since they lacked dermal changing vegetation. insulation and the ability to hibernate, SUMMARY being generally too large to find suitable sites (Cys, 1967). However, The evidence for dinosaur endothermy this might not apply to smaller dinosaurs is partly inconclusive, partly spurious (Russell, 1967). Russell (1965, 1966) and and, of course, its interpretation is totally Bakker (1972, 1975a) argued similarly, speculative. Extrapolations from studies but assumed that dinosaurs were endo- of thermoregulatory physiology of living thermic (note that Russell used the term reptiles suggest that ectothermic dinosaurs "homoiothermy," but he applied it to mam- could have achieved homeothermy iner- mals and birds and almost certainly meant tially simply by being large. Endothermy endothermy). The effects of colder cli- is a costly attribute and it is argued that mates would probably be greater on a it would have been distinctly disadvan- large naked ectotherm than on an endo- tageous, as well as unnecessary, in dino- therm. Present-day naked endotherms saurs (with the possible exception of small such as elephants can survive for fairly theropods). long periods in extreme cold (Sikes, 1971), Mesozoic climates were generally while cetaceans may live continuously in warmer than at present and largely arid water at or near freezing point. The latter during the Late Triassic. It is suggested have thick layers and heat con- that ectothermy could have proved ad- duction through the blubber is very slow vantageous to archosaurs in the Late (Vaughan, 1972) so that body core tem- Triassic and may have contributed to the peratures may be maintained at a high success of their replacement of the possi- level. Thus, large naked endotherms at bly endothermic mammal-like reptiles. present can survive extreme cold and Constant body temperatures without the there is no reason to suppose that dino- necessity of consuming large quantities of saurs could not have done the same if they food as in endotherms may have assured had been endothermic. However, if they the continued success and diversification were ectothermic, as I suggest, colder sea- of dinosaurs in the warm Jurassic and sonal climates could have contributed to Cretaceous. their extinction. A possible temperature drop towards The reptiles which survived into the the end of the Cretaceous, together with Tertiary were either small (lizards, snakes, increasing seasonality of climates and the land turtles) or aquatic (marine turtles, introduction of temperate floras, in con- crocodilians). Small reptiles could main- junction with the large size, naked skin tain body temperatures by behavioral and inertial homeothermy of dinosaurs, means, or hibernate during particularly may have contributed to their extinction. cold seasons and, for aquatic reptiles, ACKNOWLEDGMENTS temperature fluctuations would be par- tially buffered by the water and they could I sincerely thank Dr. David S. Brown, hibernate by burrowing in the mud (Cys, Dr. D. J. Batten, Dr. E. C. Olson, Dr. J. 1967). H. Ostrom, and Mr. John A. H. Benzie It should, however, be noted that di- for valuable comments on the manuscript. nosaur extinction was probably the result Dr. R. D. K. Thomas very kindly sent me of a combination of causes, including cli- prepublication copies of abstracts of the matic change, vegetation change and oth- papers from the AAAS symposium held in ers (Halstead, 1969). Van Valen and Sloan early 1978. (1977), in a detailed study of local dino- LITERATURE CITED saur extinction, suggest that it was a grad- ALEXANDER, R. McN. 1976. Estimates of speeds ual process of ecological replacement by of dinosaurs. Nature 261:129-130.

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Alberta, interpreted from the distribution of ar- JOHNSTON, P. A. 1979. Growth rings in dinosaur ticulated vertebrate remains. Can. J. Earth Sci. teeth. Nature 278:635-636. 15:1012-1024. KREMP, G. 0. W. 1977. The position and climatic * 1979. Ectothermy in dinosaurs: paleoeco- changes of Pangaea and five south-east Asian logical evidence from Dinosaur Provincial Park, plates during Permian and Triassic times. Paleo- Alberta. Can. J. Earth Sci. 16:250-255. data-Banks 7:1-2 1. BUDYKO, M. I. 1978. Thermal regime of dinosaurs REID, R. E. H. 1978. Discrepancies in claims for (in Russian). Zh. Obs. Biol. 39:179-188. endothermy in therapsids and dinosaurs. Nature 276:757-758.

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