of the European Cetacean Society, Inverness, Scotland (in press). GALLIVAN, G. J. 1992. What are the metabolic rates of cetaceans? Physiol. Zool. 65:.
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Technical Comment
Measurement of Basal Metabolic Rates: Dor.'t Lose Sight of Reality in the Quest for Comparability J. R. Speakman R. M. McDevitt K. R. Cole Department of Zoology, University of Aberdeen, Aberdeen, Scotland, U.K. AB9 2TN
Accepted 7/6/93
Gallivan (1992) raises some interesting questions concerning the measure ment of basal metabolic rates (BMRs), following the recent debate (Kasting et al. 1989; Innes and Lavigne 1991) about whether the metabolic rates of cetaceans are elevated above the expectation from the Kleiber (1961) equa tion. Gallivan (1992) reaches the conclusion that all previous attempts to measure BMRs of cetacea are worthless because they do not conform to the original criteria set by Kleiber for measurement of basal metabolism. Con sequently, the question of the level of cetacean metabolic rates remains unanswered. More surprisingly, Gallivan (1992) suggests that the reason previous studies have failed to measure BMR is because scientists have not "taken the trouble" to read the original details of the definition of conditions under which BMR should be measured. In this short comment we wish to make two major points. First, for the avoidance of any doubt, the criteria set by Kleiber for the definition of con ditions under which BMR should be measured are only "mature animals in the post-absorptive state and measured in the range of metabolically indif ferent environmental temperature at rest, or at least without abnormal ac tivity" (Kleiber 1961, p. 204: criteria for inclusion of 26 studies in derivation of interspecific regression of BMR on mass). Kleiber himself recognized that measurement of a truly basal metabolic rate could probably be achieved only in humans (Kleiber 1961). The conditions were introduced because the term "basal metabolism" was already in widespread use, so it was better to attempt to impose conditions on the term to ensure as much comparability as possible, rather than attempt to introduce a new term for animal measures
Physiologicalloology 66(6):1045-1049. 1993. © 1993 by The University of Chicago. All rights reserved. 0031=935X/93/6606-9365$02.00
1046 J. R. Speakman, R. M. McDevitt, and K. R. Cole of "basal metabolic rate." This is nevertheless an arbitrary set of conditions that are not exhaustive. The sampling protocol used in the respirometry setup, for example, can have a considerable effect on the resultant BMR measurement (Hayes, Speakman, and Racey 1992). Such uncontrolled factors as the total duration of measurement and the selection of some variable arbitrary duration over which the lowest rate is measured (e.g., the lowest 5 min, or 10 min, etc.) may introduce up to 10% variation in the estimated metabolism. Gallivan (1992) also points out the effects of total time spent in the chamber on the resultant measurement. Body temperature has a profound effect on metabolic rate. Animals that regulate their body at lower normothermic temperatures generally have lower BMRs than those which regulate their temperatures at higher levels (see, e.g., the comparison of passerine to nonpasserine birds: Lasiewiski and Dawson 1967). Many animals are capable of varying their body tern perature over relatively wide limits, yet the Kleiber criteria do not make any rigid requirements about the body temperature. Aschoff and Pohl (1971) distinguished clear differences in the basal metabolism of animals according to whether their metabolism was measured during the phase of the circadian cycle when the animal is normally active or during the phase when it is normally quiescent. Measurements made in the quiescent phase are signif icantly lower. These differences in part reflect the circadian cycling in body temperature. Nevertheless, there is no restriction in the Kleiber criteria concerning the phase of the circadian cycle. Perhaps the most significant factor for wild animals, which is ignored in the Kleiber criteria, is the problem of elevation of the measurements due to handling and capture stress. Individual species seem to vary in their tolerance of handling. Short-tailed field voles (Microtus agrestis) had no posthandling elevation of metabolism, whereas wood mice (Apodemus syl vatic us) had their metabolism elevated by up to 65% for 2 h after handling (Hayes et al. 1992). There is clearly much variation in measures of BMR that stems from vari ation in these uncontrolled factors. The variation that is introduced because of these uncontrolled factors may outweigh the variation that stems from minor violations of the defined conditions. It is rather simplistic, then, to insist that all measures must conform absolutely to the Kleiber criteria (as Gallivan r1 QC)2] does). Minor deviations from the established criteria, which, if Gallivan's strict adherence is employed, would invalidate a BMR measure, may have far less effect than variations in the unestablished criteria, which would not invalidate a measure.
Technical Comment 1047
The second point we wish to make is that the arbitrary criteria defined by Kleiber were established for a very small subset of the vast diversity of the animal kingdom. This subset consists mostly of livestock and laboratory animals. For many animals the criteria that work sufficiently in the subset selected by Kleiber are actually detrimental to measurement of a BMR. In some animals the criteria are mutually impossible to achieve. For example, for small mammals the requirement that the animal be postabsorptive is difficult if not impossible to attain while still maintaining the other criteria intact. Many small shrews become continuously hyperactive when they are deprived offood (Hanski 1985). Hence, it is impossible to meet the criteria of being both postabsorptive and at rest. Before small shrews become post absorptive they enter a state of profound rest in which they have zero me tabolism and from which they never recover! Other small animals react to food deprivation in a different but no less confounding way, by relaxing their body temperatures and entering torpor to conserve energy. Their torpid rates of metabolism are severely depressed relative to those of animals that are at normothermic body temperatures. Removing the food for many animals has often, therefore, much wider im plications than the intention of eliminating the increase in metabolism due to the specific dynamic action of food. In the case of measurements of BMRfor Cetacea, Gallivan (1992) suggests that elimination of activity is the key to making good measurements. He cites his own work on Amazonian manatees (Trichechus inunguis) as evi dence of how this control of activity is feasible in a similar aquatic periodic breather. However, manatees and Cetacea are radically different in their habitual levels of activity. One could hardly wish for an animal that better meets the criterion of being at rest than a manatee or find one less likely to be continuously active than a cetacean. Cetaceans can be trained to "sta tion" where they maintain their position in the water, but even then they are not completely inactive. Some measurements of cetacean metabolic rates have been made in this condition. It is unrealistic to condemn and reject all the measures of cetacean metabolic rates because they do not conform absolutely to the criterion of being completely at rest (which in any case is not defined by Kleiber as an absolute criterion: see the extract from The Fire ofLife quoted above [Kleiber 1961, p. 204]). This is not to say that all measures of BMR for Cetacea have been perfect. Capture stress has undoubtedly been a factor in some studies that has ele vated the metabolic rates (see, e.g., Irving, Scholander, and Grinnell 1941; Ridgeway and Patton 1971), and Gallivan (1992) raises some other pertinent problems concerning estimates of the metabolism of periodic breathers. Another problem not considered previously is the fact that odontocete ce
1048 J. R. Speakman, R. M. McDevitt, and K. R. Cole taceans echolocate. The energy cost of echolocation in an insectivorous bat (Pipistrellus pipistrellus) has been shown to be very high (7 -12 X BMR) (Speakman, Anderson, and Racey 1989). Not accounting for the costs of echolocation when measuring BMR might seriously elevate the reported costs, and differences between studies could then reflect the different pro portions of time spent by study animals echolocating. We recently made a preliminary study of energy costs of resting (stationing by the pool side) in a single atlantic bottle-nosed dolphin (Tursiops truncatusi while simul taneously recording its echolocation behaviour. We estimated that the cost of echolocation is about 1.8 X BMR and that removing the effect of echo location results in an estimate of BMR that is almost identical to the Kleiber expectation (6% higher) (Cole and Speakman 1993). The Kleiber criteria, not surprisingly, do not make any prescriptions about whether the animal should be echolocating or not, yet for some cetaceans this can clearly have a substantial impact on the measurements made. The message one should take away is that it is unrealistic, and illogical, to insist on an absolutely rigid conformity to the Kleiber criteria as a method for obtaining comparability between all measures of BMR. Moreover, it is highly unlikely that the lack of conformity to the criteria stems from sci entists' not taking the trouble to look them up. Most, if not all, scientists measuring metabolic rates know the Kleiber criteria well and attempt to meet them. In the real world, however, when attempting to measure BMR it is necessary to trade off the strict adherence to the arbitrary rules with the constraints of reality for the species under study. Sometimes, getting close is as close as we are ever going to get.
Literature Cited ASCHOFF,]., and H. POHL. 1971. Rhythmic variation in energy metabolism. Fed. Proc. 29:1541-1552. COLE, K. R., and J. R. SPEAKMAN. 1993. Measurement of the resting metabolic rate of the atlantic bottlenosed dolphin, Tursiops truncatus. In P. G. H. EVANS, eel. Eu ropean research on cetaceans 7: Proceedings of the Seventh Annual Conference of the European Cetacean Society, Inverness, Scotland (in press). GALLIVAN, G. J. 1992. What are the metabolic rates of cetaceans? Physiol. Zool. 65: 1285-1287. HANSKI,1. 1985. What does a shrew do in an energy crisis? Pages 247-252 in R. H. Smith and R. M. Sibley, eds. Behavioural ecology: symposia of the British Ecological Society. Oxford, Blackwell Scientific. HAYES J. P., J. R. SPEAKMAN, and P. A. RACEY. 1992. Sampling bias in respirometry. Physiol. Zool. 65:604-619.
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INNES, S., and D. M. LWIG:--;E. 1991 Do cetaceans really have elevated metabolic rates? Physiol. Zool. 6cf: 1130 -113-:1. IRVING, L., P. F. SCHOLANDER, and S. W. GRINNELL. 1941 The respiration of the porpoise Tursiops truncatus. J. Cell. Compo Physio!. 17:145-168. KASTING, N. W.. S. A. L. ADDERLEY, T. SAFFORD, and K. G. HEWLETT. 1989. Thermo regulation in beluga (Delpbinapterus leucas) and killer (Orcillus orca) whales. Physiol. Zoo!' 62:687- 701 KLEIBER, M. 1961. The fire of life: an introduction to animal energetics. Wiley, New York. LASIEWISKI, R. C., and W. R. DAWSON. 1967. A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13-23. RIDGEWAY, S. H., and G. S. PATTON. 1971. Dolphin thyroid: some anatomical and physiological findings. Z. Vergleichende Physiologie 71:129-141. SPEAKMAN,J. R., M. E. ANDERSON, and P. A. RACEY. 1989. The energy cost of echolocation in pipistrelle bats (Plpistrellus pipistrellus). J. Compo Physiol. 165B:679 - 685.
