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Commentary: Observation on disease-associated preferred body temperatures in reptiles

Applied Animal Behaviour Science, 28 (1991) 375-380

Clifford Warwick

ABSTRACT
Reptiles have been reported to voluntarily maintain higher optimum body temperatures when disease is present. This behavioural strategy raises the metabolic rate, and presumably also the effectiveness of the immune system. Based largely upon this concept, keepers of reptiles often raise environmental temperatures to assist the recovery process. Case studies of disease in reptiles held privately and in other collections over a 12-year period implied that while behaviourally thermoregulated, and imposed, warmer temperatures appeared often to assist recovery, in other eases imposed warmer temperatures accelerated the disease, resulting in rapid deterioration or fatalities. A common feature observed among captive reptiles in early stages of disease was that higher preferred body temperatures were behaviourally sought, while in more advanced and serious cases, lower preferred body temperatures (leading in certain cases to torpor) were behaviourally sought. This communication examines some aspects of the ætiology of disease-associated preferred body temperatures, and suggests that behavioural thermoregulation of body temperature during disease is far more complex than was previously assumed. It is hypothesized that while a warmer temperature may offer an immunological stimulant as previously thought, and as such is often totally appropriate, stress from the disease itself (potentially complicated and increased by environmentally induced stress or distress) may act as an immunological suppressant, and thus recovery requires a "biological shut-down", as achieved during cooler temperatures. Lower and minimum body temperatures, however, are not suggested here as forming routine recovery enhancement or treatment, rather that observed behaviours during disease, and apparent enhanced recovery, suggest that lower preferred body temperatures may be integral to healing under certain conditions, and in this regard encouragement might be appropriate. The process appears difficult to define and may incorporate strategies of dual, multiple, or alternating sequential behavioural thermoregulation or imposed body temperature variation in the healing process. The potential for, in particular, captive animal treatment is also discussed.

Introduction
Reptilian biology is governed largely by their ectothermic nature, and because these animals must often actively seek warmer or cooler areas to regulate their body temperatures, ethology is fundamental to this overall strategy. Wide, and often extreme, thermal variation is common in reptiles and of substantial importance to a variety of aspects of their natural history, including ethology, physiology, metabolism, biochemistry digestion, embryonic development, growth, and reproduction. Minor changes in temperatures can have profound effects on, for example, crocodilians (Alligator mississippiensis) in terms of hatchling size and pigmentation, post-hatching growth rates, and thermoregulation by juveniles (Deeming and Ferguson, 1989). In addition, it is now well documented that temperature-dependent sex determination occurs at critical thermal temperatures, for example in crocodilians (Crocodylus palustris): eggs incubated at 28.0-31.0 C result in all females whereas at 32.5 C only males are produced, although temperatures of 31.5, 32.0, and 33.0 C produce both sexes in varying proportions (Lang et al., 1989), Therefore, changes of only 1.0 C can have important consequences for offspring sex ratios. Temperature-dependent sex determination has been reported in chelonians and lizards (e.g. Yntema, 1976; Bull, 1983, 1987; Standora and Spotila. 1985; Webb et al., 1986). It is to be expected then, that environmental interaction, related body temperatures, and temperature-sensitive periods are a complex area and demand serious attention and careful evaluation.

Reptiles commonly become victims of pathologies and injuries in captivity. Disease-associated preferred body temperatures (DAPBTs) have, however, received little examination. In captivity, reptiles with bacterial infections have been reported to seek higher than usual environmental, and thus body, temperatures (Cooper and Jackson, 1981). Behaviourally achieved or imposed warmer temperatures are thought to increase immunological and general healing efficiency (Davis, 1981). As a consequence, it is common practice to impose constant optimum or higher temperatures for the species to assist in the treatment of disease.

In nature, this is primarily dependent upon the sun and therefore basking activities are the governing element. In captivity, heat sources vary somewhat but by utilizing heat lamps or maintaining close proximity or distance from other radiant sources, these animals are able to achieve particular preferred body temperatures (PBTs) (e.g. Hazegawa, 1989; Gaywood and Spellerberg, 1989; Borkin et al., 1989). Biochemical imbalance also is reported to affect thermoregulatory behaviour. (Smits et al., 1986). While environmental warmth may induce activity and cold retard activity, stress, distress, and the overall ethological and psychological disposition of individual reptiles may influence temperature preference (Warwick, 1990).

The aims of this communication are to describe briefly several behaviours which probably are directly associated with temperature preference during disease, and to hypothesize the importance of temperature preferences in reptiles in such cases. In addition, it is intended to generally promote the potential value of the subject because further research and understanding could result in more efficient recovery enhancement or treatment of disease in captive reptiles.

Findings And Discussion
During ethological studies of captive reptiles, conducted over a 12-year period (Warwick, 1990), numerous animals were placed under personal and independent veterinary observation and treatment for disease. Additional examinations of other cases of diseased reptiles also were conducted. In almost all cases, observation and treatment was conducted for systemic bacterial infections. Freshwater chelonians were the most common examples and this may be attributable to their habitual status in water, which is potentially a high bacteria-carrying medium.

Observations of diseased captive reptiles, and occasionally wild specimens, revealed that many individuals actively seek cool areas, and even areas that are sufficiently cold to induce torpor, rather than warmer areas as previously was believed to be the most appropriate. Relocating individuals to warmer areas regularly resulted in their voluntary return to lower environmental temperatures. Consequently, a dilemma had been presented as to whether accepted procedures of maintaining raised temperatures should be followed, or whether the behavioural tendencies of the animals should be totally permitted, or even encouraged.

Although in many cases during these studies behaviourally maintained or imposed constant and high body temperatures appeared consistent with improvements or recovery from disease, other examples, particularly those animals that voluntarily had avoided warmer temperatures, deteriorated rapidly when warmed and in numerous cases fatally so. The lower temperature preferences were exhibited almost exclusively by animals in relatively advanced disease conditions. It seems reasonable that increases in temperature and metabolism resulted in rapid increases in bacterial infection and subsequent general deterioration of the animals at an accelerating, and intolerable rate. Therefore, in these cases the result was that bacteria won the battle with the immune system.

Injured and diseased freshwater turtles (Deirochelys reticularia) and snakes (Natrix natrix) in natural settings would occasionally hibernate or aestivate at unusual temperatures and times and emerge in good health. In nature, therefore, lower metabolic rates can accompany recovery. In the wild, of course, cold periods ensure that behaviourally increased body temperatures are not possible at certain times and it seems reasonable to assume that significant resistance to disease, and general healing should continue to operate under such conditions. While low temperatures may then be acceptable in principle as enhancing healing, because reptilian biology naturally incorporates considerable variation in body temperatures, it could be said that precise body temperatures are not of particular importance. However, it could also be argued that such natural variation suggests that multiple niches and a variety of optimums also are implied, certainly studies on reproduction suggest this.

Low body temperatures possibly act as a "biological shutdown" or withdrawal from the pressures of disease or the environment. Although presumably at lower temperatures the immune system is relatively depressed, bacterial activity and other disease factors also are reduced significantly while some immunological activity is retained. Therefore, the resilience of the host reduces the condition to a tolerable level of infection. Biological shut-downs also may simply incorporate an element of rest for the animals which, perhaps temporarily but nevertheless significantly, reduces or eliminates overall trauma. Combined with the reduced general disease-related trauma, rest, and consequently a potentially less "stressed" immune system, could prove to be the primary reasons for recovery.

It is, therefore, interesting to hypothesize that, instead of the higher body temperatures being singly important in thermoregulatory healing, the system is at least a dual one. In this hypothesis, during the early stages of disease, higher metabolic rates offer increased immunology, partly because the physical discomfort, and thus stress, from the disease is insufficiently high to compromise the immune system. These examples appear to include the majority of cases of probable thermoregulatory healing, because animals tend to seek natural healing as soon as possible. In more advanced stages of disease where trauma is higher, stress from numerous sources probably compromises the immune system and thus the only practical survival option is a cold temperature, and the biological shutdown strategy. Essential differences between early and late stages of disease-associated preferred body temperatures (DAPBTs) may occur within critical limits. It is interesting to speculate that the probable precise definition of DAPBTs may mean that the system is only operable by the individual animal.

Disease-associated preferred body temperatures appear then to be of similar ætiology to disposition-related environmental temperature preference (DRETP), where reptiles may seek temperature variation to match their "mood" (Warwick, 1990). In DAPBTs cases, however, temperature preference is pathologically/physiologically related, rather than being primarily the result of ethological problems (although biologically these can be closely combined). Careful judgement must, therefore, be applied in evaluations of observed PBTs to avoid confusion with primarily ethological problems. DRETP and DAPBTs are probably integral under certain conditions. It is indeed conceivable that the ethological causes of DRETP, and associated stress and distress, could result in compromised immunology, disease and thus DAPBTs. In such cases prognosis is potentially poor because the animal may effectively have withdrawn from the artificial environment owing to this being concept- and design-deficient, and thus insufficiently or inappropriately stimulating for normal behavioural or psychological activity. Therefore, thermoregulatory behaviour - potentially essential to healing - may not arise.

Caution must be emphasized, however, in the imposition of hypothermia without proper behavioural indications for its appropriateness. Randomly hibernating animals may harbour diseases, that under certain circumstances could prove to be serious or fatal. In addition, other medical factors must be brought into account, for example, if certain antibiotics are to be used then these may require optimum, and constant operating temperatures which complicate behavioural or imposed hypothermia. Therefore, depending upon specific cases, antibiotics perhaps should not be employed.

Conclusions
Because ectothermic control is behavioural, ethology remains the fundamental biological principle for achieving, and monitoring thermoregulation and therefore it is of prime importance to maintain the ethological perspective. Preliminary findings suggest that it may be highly beneficial to provide wide temperature ranges in captivity (within the species' natural limits), so that PBTs may be achieved. Disease-associated preferred body temperatures probably vary with taxonomic group, species, and between individuals for a variety of reasons, for example, animal size, nutritional state, ethological/psychological "profile", and immunological condition. These observations suggest that behavioural thermoregulation of body temperature during disease is far more complex than previously assumed. The process appears to be difficult to define and may incorporate dual, multiple, or alternating sequential strategies of behavioural thermoregulation or imposed body temperature variation in the healing process.

Numerous fundamental questions need to be answered, for example, do DAPBTs vary according to the disease? Are repeated behavioural, and thus thermal, sequences necessary? There appears to be enormous potential, and opportunities, for detailed studies and the possible creation of formulae for calculating precise temperatures endemic to healing in the natural environment, enhanced treatment, or value as a remedy on its own. Controlled methods in captivity, however, probably are dependent upon many diverse factors, which may make precise definition of thermal niches extremely complicated and subjective.

References

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Warwick, C., 1990. Reptilian ethology in captivity: observations of some problems and an evaluation of their ætiology. AppI. Anim. Behav. Sci., 26: 1-13.

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Acknowledgments
I am grateful to John E. Cooper, Royal College of Surgeons of England for providing background material, and Professor Andrew Fraser, Memorial University of Newfoundland for encouragement to submit for publication.