Tuatara: Volume 24, Issue 2, August 1980
Thermoregulation in Reptiles with Special Reference to the Tuatara and Its Ecophysiology
Thermoregulation in Reptiles with Special Reference to the Tuatara and Its Ecophysiology
I Problems of Thermoregulation in Reptiles
Like fish and amphibians, reptiles are ectothermic animals, which is to say that they produce very little metabolic heat and their body temperature depends essentially on that of the environment. However, in contrast to the first two groups, reptiles are all more or less thermophilic and can only accomplish their main functions — i.e. locomotion, feeding, reproduction, etc. — at relatively elevated temperatures. For example, even in species living in very cold regions, such as Lacerta vivipara and Vipera berus which in Europe live as far north as the polar circle, digestion cannot be carried out below a temperature of 16 to 18°C and spermiogenesis below 21-22°C (Joly and Saint Girons, 1975). These limiting temperatures vary for different physiological functions and from one species to another, and differences as great as 14°C have been found between, for example, the lower limiting temperature for locomotion (Cowles and Bogert, 1944; Saint Girons and Saint Girons, 1956).
The relationship between the body temperature and the intensity of a particular biological phenomenon also varies for different functions between 10° and 35°C, which represents the range of normal body temperatures experienced. Oxygen consumption, for example, increases by a factor of 2.4 for every 10°C rise in temperature, and the heart rate increases by a factor of 2.2 (Bennett and Dawson, 1976). These co-efficients or Q10's, which reflect the basic chemical reactions occurring, vary in effect according to the temperature, and generally they decrease as the temperature increases. For example (Fig. 1), the frequency of rattling in rattlsnakes changes from a Q10 of 3 between 10° and 20°C to a Q10 of 1.4 between 20° and 30°C (Martin and Bagby, 1972). For other functions, usually those which do not proceed at a great rate, the Q10 may be much greater. This is particularly the case, for example, with the rate of spermiogenesis which increases by a factor of 6.7 between 22° and 32°C (Joly and Saint Girons, 1975).
Fig. 1: The relationship between body temperature and rattling frequency of the rattlesnake, Crotalus atrox. From Martin and Bagby, 1972.
The notion of an optimal body temperature or preferred body temperature has led to numerous discussions in the herpetological literature (Brattstrom, 1965; Heatwole, 1976; Werner and Whitaker, 1978). Many workers consider that this temperature corresponds to the mean body temperature measured in nature, which is obviously an aberration because these measures will forcibly include many animals which are in the process of basking and therefore have reduced body temperatures, or animals which are for example searching for food under cold conditions. Logically, one should only record temperatures of an animal when it is given a real choice. When one studies reptiles under these conditions it is quite evident that their body temperature varies only by a matter of ±2°C and that the mean calculated under these circumstances corresponds to the real preferred body temperature. It is worth noting, however, that when diurnal reptiles are maintained in the laboratory within a thermal gradient (Fig. 2), they generally choose night body temperatures which are definitely lower than those which they prefer during the day (Regal, 1967; Spellerberg, 1974), and the difference may be as great as 15°C for species living in temperate and cold regions. This difference is less marked for species living in intertropical forests, but some change between day and night would appear to be essential since animals maintained continuously at their preferred temperature in the laboratory die within two or three months.
Fig. 2: Characteristic and continuous body temperature recording over a 24-hour period, selected by European reptiles in a thermal gradient chamber. The period of light phase is indicated for each by the vertical line. From Spellerberg, 1976.
Even though the production of metabolic heat by reptiles is very low, these animals possess other physiological means to assist their thermoregulation (Templeton, 1970, Heatwole, 1976; Tucker, 1967). Most important of these is the control exerted over the dermal vascularity. Increases in heart rate and dilation of superficial blood vessels significantly augment the rate of thermal exchanges with the environment, and conversely thermal exchange is retarded when the heart rate is reduced and the dermal blood vessels are constricted. In general, over the range of temperatures which are voluntarily tolerated by reptiles, the rate of heating is almost invariably faster than the rate of cooling.
It is clear from the above that, overall, reptiles possess a large number of means of maintaining the internal body temperature at a preferred level, so long as they have an external source of heat.
Burrowing forms, or thigmotherms as they are called, utilise the temperature gradients in the soil, which in general is hottest close to the surface during the day. In intertropical humid forests the environmental gradients are very small and the body temperature of these reptiles varies very little throughout the day and night, and even throughout the whole year the body temperature will not vary much between 20° to 25°C. This is very different from the case in regions where the climate is much more variable, and especially in the desert regions which lack any adequate vegetation cover. In these habitats the sand-living forms, which are the only reptiles which have really been analysed from this point of view, are able to thermoregulate with remarkable precision. The Saharan viper Cerastes, for example, by burying its body in the sand with just the head poking out, is able to maintain its body temperature between 32° and 33° throughout the whole of the day, despite the fact that there are much greater variations of the air temperature and the surface soil temperatures (Saint Girons and Saint Girons, 1956).
Terrestrial reptiles, and particularly those which live in trees, have page 64 at their disposal an environment which is much more heterogeneous from the thermal point of view, and they utilise principally solar radiation for raising body temperature and a variety of means for avoiding excessive heat. In temperate and cold regions the main problem is one of heating the body, and I should like to give as an example some results of a recent study on the European vipers which are living in a region in Brittany where summers are generally quite cool (Saint Girons, 1978).
Fig. 4: Thermoregulation of vipers on different days:
(A) during a more or less overcast day;
(B) a day with normal sunshing (two species shown);
(C) a very hot day.
—— or - - - - - Body temperature of a viper
….. Temperature of a metal thermometer in the sun, at 50 cm of height
+ + + Air temperature
• • • Temperature in a burrow
In regions with very cold winters or even cool winters and a lot of rain, reptiles are incapable of obtaining sufficient heat during that season to enable them to digest their food. Under these conditions, temperatures between 4° and 8°C become the most suitable for the page 67 animals because their metabolic rate is almost non-existent in this temperature range but locomotion still remains a possibility. These animals will effectively seek out cool conditions and not, as most people think, regions in the habitat which are the warmest possible. Thermoregulation is not completely abandoned, however, and in the case of extreme cold, reptiles may dig themselves down more deeply in the soil if they can. In regions which are cold and temperate, the lethal temperatures usually fall between —2° and —4°C. Males, which do not have to withstand the loss of energy due to vitellogenesis experienced by the females, but which must complete their spermiogenesis, as quickly as possible, will emerge frequently at the end of winter when there is the odd sunny day but they do not eat. They then lose weight much more rapidly than during the period of hibernation.
In reality then, even in cold regions adult reptiles are able to survive even if they only attain their preferred body temperature for a few hours every day and for as few as 40 days a year. But they are unable to reproduce under these conditions. In ovoviviparous species the females must at the same time make sure that embryonic development proceeds and they must also replace their energy reserves which have been depleted as a result of the process of vitellogenesis. Snakes, which do not eat during the period of gestation, are not able to breed more than one year in two. Oviparous species are somewhat better off, but eggs which are laid in the soil obviously do not have the benefits conferred on them by the thermoregulation of the female and they do not have time to develop before the arrival of winter in the coldest regions. This is why species which apparently have the same thermal needs and preferred temperatures often do not have the same distribution in terms of altitude or latitude.
Fig. 5: Diagrammatic representation of behavioural thermoregulation in Amphibolurus inermis and temperature relation for non-burrowing lizards, Diplodactylus michaelsoni and Diporiphora bilineata, during the period when A. inermis has retreated to its burrow. From Bradshaw and Main, 1968.
In intertropical humid forests, which have relatively constant and hot climates, temperature regulation poses no problems and reptiles here are able to adopt a great number of modes of existence. In principle, however, there is no essential difference from those methods which are utilised in other regions. The preferred body temperature is realised by placing the whole or part of the body in the sun and by choosing a microhabitat which is homogeneous and has a convenient temperature, either soil or on the surface of, say, a bush. The preferred body temperature of reptiles living in intertropical forests and even subtropical forests generally falls between 27° and 30°C, probably less for burrowing forms. However, one should remember that because of the very small amount of cooling which occurs at night in the tropics, the mean body temperature of the animal over a 24-hour period is in fact much higher than that of reptiles living in temperate regions. This constancy of body temperature reaches the point in some species where they appear no longer to need to bother to thermoregulate behaviourly. The minimal voluntarily-tolerated temperatures also are often quite high, and may be above 15°C.
Obviously there exists a great number of intermediates between the three extreme cases which have been treated here. In general, in middle latitudes the reptiles have to struggle against the cold in spring and autumn, and against heat in summer, at least in continental regions where the temperature variations are extremely large.
The problems of thermoregulation are obviously quite different for reptiles which are aquatic or semi-aquatic. Species which never leave water, such as sea-snakes and marine tortoises, as well as a number of forms which live in fresh water, do not have at their disposal a very large thermal gradient (Graham, 1974). By exposing their body to the sun's rays at the surface of the water they are no doubt capable of raising the body temperature by two or three degrees Centigrade above the surrounding liquid. But this does not restrict them to living in only warm regions, and the very long gestation period of sea-snakes for example — 5-6 months instead of 2-3 is usual — demonstrates that they find themselves in a difficult thermal situation.
Semi-aquatic forms, such as crocodiles, tortoises, many snakes and page 70 a few lizards, are more or less attached to water in some way. An oviparous sea-snake, for example, which feeds in the oceans and may be occupied with hunting for many days or even weeks, will return to the land to digest its prey, at least in winter. During this period, with the aid of classical methods of behavioural thermoregulation, it will maintain its body temperature near 28°C during the whole of the day (Saint Girons, 1964). Other species will regularly bask in the sun on the land, where they often will spend the greatest part of the day (Fig. 6)). The preferred body temperature is apparently the same as that of other reptiles: 26°-30°C in intertropical regions, 30°-33°C in temperate regions (Brattstrom, 1965; Johnson, 1974). In addition to the classical methods of thermoregulation, many of these species will maintain their body temperature at the required level by leaving part of their bodies in the water. In regions which are particularly cold, reptiles make feeding excursions into the water which are as short as possible, and they return to land to re-warm themselves. Again, under the conditions physiological adaptations which accelerate heating and retard the rate of cooling obviously are extremely useful.
In many cases, identical thermal preferences will be found in species which live in very different climates and which have modes of living which are extremely different. Only reptiles which are strictly burrowers or aquatic and which, of course, have very limited possibilities for thermoregulation, are strictly localised in and restricted to hot regions. For the other species, the geographical distribution depends as much on inter-specific competition and other environmental factors such as the soil and the vegetation as it does on thermal factors. This is in contrast to the situation in other ectotherms. The case of diurnal lizards living in and regions with hot summers is very different, because their mode of existence obliges them to withstand elevated body temperatures. Here behavioural adaptations alone are insufficient and must be reinforced by appropriate biochemical adaptations. In all probability these adaptations depend essentially on the thermal sensitivity of several important key enzymes. For example, it has been shown that even though the relationship between the activity of the enzyme myosin-ATPase and the temperature may vary from one species to another, the maximum temperature for full activity of the enzyme is almost always only a few degrees Centigrade below the preferred body temperature (Licht, 1967). The problem is also complicated by the existence of iso-enzymes with different thermal characteristics, which can be mobilised according to the temperature to which the animal is exposed, as has been demonstrated in the case of lactate dehydrogenase in muscles (Aleksiuk, 1971; Hoskins and Aleksiuk, 1973). The possibilities of adaptation then, of species which are exposed to an unstable environment as is usually the case with reptiles, are thus very great, and this explains the wide distribution in both altitude and latitude of a number of species which have few competitors.
Although thermoregulation is an essential part of the existence of all reptiles, it does not cover obviously all of the biology of these animals (Cloudsley-Thompson, 1971). The independence of an aquatic environment displayed by reptiles — that is, the passage through evolution of reptiles from amphibians — is due to a series page 72 of adaptations of a completely different order, and even now the ecological niche occupied by a given species depends on a number of factors and notably the division of food resources. However, thermoregulation has played an essential role in the evolution of all the amniotic vertebrates, and probably since the Lower Carboniferous.
II Ecophysiological Problems Associated with the Tuatara
It is particularly interesting to compare this last representative of a group of reptiles which flourished in the past with the living squamates (lizards and snakes), particularly those which most resemble the Tuatara and have an analogous mode of life in cold temperate regions.
In contrast to the tortoises and the crocodiles, which occupy an ecological niche very different from that of the squamates, the Tuatara holds a place rather similar to a large terrestrial lizard which is oviparous, insectivorous and nocturnal. These are the characters which one finds reasonably frequently in the lizards, particularly the iguanids and the agamids, but not in a similar climate. Effectively lizards living in temperate cold climates are always of small size and, with few exceptions, ovoviviparous and diurnal. These particulars of Sphenodon punctatus therefore pose a number of problems, especially concerning the question of thermoregulation.
All the diurnal reptiles living in cold temperate regions are able to move readily and even hunt at relatively low environmental temperatures. They are also able to take advantage of dew, which is often the only source of liquid in the environment. It evaporates rapidly in summer, and must be collected by the animals before sunrise if they are to profit from it. In addition, for some species such as Anguis fragilis, which lives principally on earthworms and slugs which are only really active at dawn and dusk or following rain, the activity of the lizard is forcibly limited to temperatures between 10° and 16°C. This does not stop the animal, however, from maintaining its body temperature constant and at a relatively high level during the day, because the males at least during spermiogenesis and the females during the period of gestation must be able to reach a body temperature of 30°C for a number of days. The few nocturnal reptiles living in cold temperate zones — mainly the New Zealand gecko genus Hoplodactylus — have a behaviour which is very analogous to this, and even if they hunt exclusively during the night, they bask during the day either by exposing themselves directly to the sun or placing themselves under a flat stone or under bark. In a recent paper, Werner and Whitaker (1978) have shown that the body temperature of H. maculatus often falls between 25 and 30°C during the middle of the day (Fig. 7).page 73
The minimum temperature voluntarily tolerated by the Tuatara (roughly 6°C) is very low and, like other nocturnal reptiles living in the same region, hunting activities are usually carried out at temperatures between 10 and 15°C, at least in spring and autumn and in the coldest regions of the animal's home range. The first observations of the Tuatara, by Bogert (1953), showed that the Tuatara sometimes exposes itself to the sun during the day, usually at the entrance to its burrow, yet for many years the highest body temperature recorded from the animals in nature was 18°C, and following the study of Wilson and Lee (1970) the preferred body temperature would appear to be between 18 and 19°C. As a result of these data one must admit that this species shows adaptations to cold which are unknown in any other reptile.
Fig. 7: Body temperatures of Hoplodactylus maculatus and concurrent air temperatures. From Werner and Whitaker, 1978.
These differences in behaviour do not depend on age or sex, or at least not at the time when our observations were made, for it is possible that at other times certain stages of the reproductive cycle — spermiogenesis, for example — involve increased thermic needs. At the moment, the only hypothesis we can formulate is that the temperatures sought by the animals differ according to the quantity of food absorbed the night before. Indeed, it is known at least in the species which swallow their large victims whole, that the preferred temperature at the beginning of the digestive process is about 2°C page 75 higher than that of animals which have not eaten (Regal, 1966; Saint Girons, 1978; Bradshaw et al, 1979). It is thus very possible that, so far as thermoregulation is concerned, the Tuatara does not really differ from other lepidosaurians living in cold temperate regions, or differs less than originally thought, but certainly more research is necessary and especially under natural conditions and with properly controlled laboratory experimentation.
Published results on the sensitivity of the Tuatara to changes in environmental temperature are also somewhat unsatisfactory. So far as metabolism is concerned (Milligan, 1924; Wilson and Lee, 1970), the oxygen consumption at 20°C and 30°C is approximately two-thirds of the mean of other reptiles of the same weight, but it falls non-the-less within the margin of variation for the whole group of species studied. An elevated rate of metabolism, of course, at a given body temperature would be the expected adaptation to cold conditions. The respiratory quotient is quite normal in the Tuatara and remains unchanged despite an increase in the consumption of oxygen in active animals, of the order of 5-6 times greater than that in animals at rest, as in the majority of reptiles.
So far as I am aware, there are no data on the temperature requirements of the Tuatara during the period of digestion. This is not surprising, however, as there have been few studies of this problem in lizards in general, and one knows only that the lizards which are the least sensitive to cold lose weight once they are maintained at temperatures below 20°C. At this temperature, digestion is still possible, because the animals continue to eat and do not die from alimentary intoxication, but digestion is too slow to compensate for the losses of energy even though they are extremely small.
In most species which live in cold zones, vitellogenesis occurs in spring, and under conditions which show that this physiological function does not require an elevated temperature so long as females have the necessary energetic reserves. This is not the case, however, for spermatogenesis. The time taken for embryonic development is also directly proportional to the temperature, but we have few precise results on this subject, unfortunately. In cold regions the period of incubation or gestation generally lasts about three months, but during very cold or wet summers the young often cannot reach the point of birth before the arrival of winter, and the result very often is a great mortality of young. So far as I am aware, there are no data on the temperature sensitivity of different physiological functions in the Tuatara, and we know only that the embryonic development occupies a particularly long period.
For reproduction to be assured, one needs something more than just the satisfactory conclusions of these various physiological processes. The cycles of the male and the female must be synchronised, and the young must find favourable ecological conditions when they emerge from the egg. In cold temperate zones, the active season page 76 is too short or too cold for spermatogenesis, mating and embryonic development all to follow one another successively. As a consequence, either spermatogenesis occurs the preceding summer and the spermatozoids are stored during winter in the defferential canals of the males (and also in the genital tracts of the females when there is autumn mating), or spermatocytogenesis occurs at the end of summer, in which case the gametes overwinter as young spermatids and spermiogenesis is terminated at the beginning of spring. In all cases, breeding occurs before the finish of spring and births before the end of summer. In the coldest regions, either at high altitudes or high latitudes, all species are ovoviviparous because by this strategy the embryos are able to profit from the active thermoregulation of the mother. Eggs buried in the soil would not be able to hatch before winter.
The sexual cycle of the Tuatara is poorly understood and would appear to be somewhat peculiar. A number of rather haphazard observations, many of which would appear to be somewhat contradictory, suggest that spermatogenesis occurs in spring and mating at the beginning of summer, but the eggs are not laid until the following spring (i.e. October to December in New Zealand). Incubation therefore lasts for 15 months, indicating that when the eggs finally hatch in summer, a period of two years has elapsed after mating, which is somewhat extraordinary. The problem of embryonic development in cold zones has been resolved in the Tuatara not by ovoviviparity, as is the case in other lepidosaurians, but by the possibility of an extremely slow development which is no doubt completely arrested during winter. I should like to emphasise, however, that the chronology of the sexual cycle of the Tuatara needs to be confirmed, and such a scheme of reproduction would appear to be extremely aberrant. It would be particularly interesting to know what is the duration of spermatogenesis, and whether deferred fertilisation exists. The oviducts of the female do not contain seminal receptacles which are morphologically differentiated, but one knows that in other reptiles the spermatozoids are able to survive for a number of months in diverticula in the vaginal tract. One should note also that the uterine glands, which are particularly abundant and large in the Tuatara, resemble quite closely those of the tortoises and those of lizards as welt, and this suggests that a more detailed study of the egg-shells would be of some interest.
Amongst reptiles, the Tuatara is the only one where the male does not have a copulatory organ, which suggests immediately that a study of mating behaviour in this animal would be of some interest. In addition, one finds on the ventro-lateral surfaces of the cloaca two large sebaceous glands which are more developed in the male than in the female and which are not found in other reptiles. Their function is of course at this stage unknown, and would be of interest to study.page 77
There are many other morphological peculiarities of the Tuatara, but one is worth underlining because it is bound to be of eventual significance in the understanding of the pituitary gland of this animal. This peculiarity resides in the mode of contact between the neurosecretory fibres coming from the supra-optic and the para-ventricular nuclei in the hypothalamus and the primary capillaries of the hypophyseal portal blood system. In birds these capillaries terminate simply on the roof of the diencephalon, whereas in other tetrapod vertebrates the capillaries break up in the limiting glial membrane which they do not really traverse. In the Tuatara, on the other hand, groups of neurosecretory fibres go in front of the capillaries and locally traverse the limiting glial membrane at the level of the pars tuberalis, thus realising the third type of hypothalamic-hypophyseal contact which is theoretically possible (Gabe and Saint Girons, 1964). We know nothing unfortunately of the functional significance of this different form of neuro-hypophyseal contact.
Another unexpected characteristic of the Tuatara is its nocturnal habit in a cold temperate region, and associated with this the animal's sense organs which play an important role in the circadian rhythm of the animal, and ensure that it is able to find food and carry out thermoregulation. In certain cases the structure of sensory organs imposes a precise mode of existence. For example, iguanid lizards, which have very poorly-developed chemical senses and vision which is exclusively diurnal, are only able to capture mobile prey and then only during daylight hours. This evolution reaches its apogee in the chameleons, which are totally disoriented and helpless in complete darkness. Many other lizards which have a poor chemical sense, hunt solely mobile prey using their vision, and in these cases their circadian rhythm depends essentially on the type of vision they possess; nocturnal or diurnal. Some species with nocturnal vision, such as many of the geckos, possess possibilities of diurnal adaptation which are much more developed. Finally, amongst the many squamates which largely utilise their chemical sense for detection and capture of prey, are numerous species which are either diurnal or nocturnal depending upon the circumstances and, most notably, the necessity for temperature regulation. A small number of species maintain a strictly circadian rhythm and are unable to change for reasons which are purely behavioural.
The eye of the Tuatara, which is reasonably large, in general has a structure which is lizard-like (Underwood, 1970); the visual elements of the retina are very like cones, but modified secondarily for nocturnal vision, like those of the geckonids. The olfactory epithelium covers approximately half of the vestibule, but the ratio of olfactory cells to supporting cells is only about 1.4, which indicates that the capacity for smell is not well-developed in this animal. By comparison one may note that this ratio is 5.9 in Hoplodactylus maculatus, the only other nocturnal reptile living in these cold page 78 temperate regions (Gabe and Saint Girons, 1976). The organ of Jacobson, which plays such an important role in most squamates, is very poorly developed and the structure is very primitive in the Tuatara. The ratio of the sensory cells to supporting cells here is only 0.4 (4.7 in Hoplodactylus) and, although probably functional, this organ could certainly play a very minor role in the detection of chemical substances. The ear lacks an external orifice and a tympanic cavity, and although the tympanic membrane is also degenerate, the internal ear is of a normal lacertilian type. It is obvious that the Tuatara must have a fairly mediocre sense of hearing although not completely absent (Baird, 1970). From this quick examination of the animal's sensory apparatus, it is apparent that the Tuatara must hunt its mobile prey principally or exclusively by sight, like nocturnal geckos, and such a diet is perfectly normal for a reptile of this size living in such a habitat.
The nocturnal mode of life of the Tuatara is thus doubly surprising: one the one hand, because it corresponds to an extremely rare behaviour in cold temperate regions, one which it does share with Hoplodactylus maculatus; and on the other hand, because it is the only nocturnal reptile in the world which has poorly-developed chemical senses. As there is absolutely no indication of a regression of these sense organs, one can only suppose that it corresponds to a fundamental characteristic of the Sphenodontidae, or of the rhynchocephalians, which was not able to be modified during the secondary adaptation of the group to a nocturnal mode of existence. Such a sequence of events is difficult to explain. One may imagine that the ancestors of the Tuatara, having small thermal requirements, became nocturnal during a warm climate, and have maintained this mode of life when they were forced to exist in colder climates to which they have become adapted by others means. This is not really a very satisfactory hypothesis, however, because all the results show that the circadian rhythm, even if it is innate, may evolve rapidly when circumstances require it, and certainly much more rapidly than any sensory epithelium.
I should like to thank Dr. S. D. Bradshaw for translating, from French, the original lectures on which this article is based.
The Editor wishes to thank the following for permission to use figures that accompany this article:
Fig. 1: with permission from Copeia. Copyright American Society of Ichthyologists and Herpetologists.
Fig. 2: with permission from Biology of the Reptilia: A. d'A. Bellairs, C. Gans, E. Williams. Copyright Linnean Society of London.
Fig. 5: with permission from Journal of Zoology, London. Copyright The Zoological Society of London.
Fig. 7: with permission from New Zealand Journal of Zoology. Copyright New Zealand Department of Scientific and Industrial Research.
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