Integrating Thermal Physiology and Ecology of

Amer. Zool.,19:357-366

(1979).

Integrating

Thermal and Ecology Physiology A Discussion of Approaches Raymond

Department

of Zoology NJ-15,

B. Huey of Washington,

University

of Ectotherms:

Seattle, Washington

98195

AND R. D. Stevenson Center for Quantitative

Science in Forestry, Fisheries and Wildlife HR-20, Seattle, Washington 98195

University

of

Washington,

synopsis. An understanding of interactions between the thermal physiology and ecology of ectotherms remains elusive, partly because information on the relative performance of whole-animal physiological systems at ecologically relevant body temperatures is limited. After discussing physiological systems that have direct links to ecology (e.g., growth, locomotor ability), we review analytical methods of describing and comparing certain as? pects of performance (including optimal temperature range, thermal performance breadth), apply these techniques in an example on the thermal sensitivity of locomotion in frogs, and evaluate potential applications.

INTRODUCTION af? (Tb) profoundly Body temperature fects the ecology of ectotherms by influand behavior. The encing both physiology effects of temperature on many physio? 1975), logical systems are known (Dawson, and the responses used by amphibians and in regulating Tb are well estab? reptiles lished and Bogert, 1944; Bratt? (Cowles strom, 1963; 1965; Heath, Lillywhite, of the interac? 1970). An understanding tions between physiological performance We thank A. F. Bennett, M. E. Feder, S. S. Hillman, A. R. Kiester, P. Licht, E. P. Smith, S. C. Stearns, C. R. Tracy, D. B. Wake, and E. E. Williams for discussions. We thank P. E. Hertz, W. W. Reynolds, S. C. Stearns, F. van Berkum, and reviewers for constructive suggestions on the manuscript. H. B. Lillywhite and O. E. Greenwald kindly provided original data. R. B. H. thanks W. W. Reynolds for the opportunity to participate in the symposium on Thermoregulation in Ectotherms. Page charges were supported by N.S.F. Grant PCM 78-05691 to W. W. Reynolds. Re? search supported by N.S.F. Grant GB 3773IX to E. E. Williams, by the Miller Institute for Basic Research in Science, the Museum of Vertebrate Zoology, the Graduate School Research Fund, and N.S.F. Grant DEB 78-12024 to R.B.H., and by the College of Forest Resources to R.D.S. 357

and ecology is, however, still elusive (Huey and Slatkin, 1976). This gap partly results from a surprising lack of information on whole-animal (e.g., physiological systems locomotion, growth, reproductive output) that have direct links to ecology and from the diffkulty of defining and estimating statistics (e.g., optimal temperature range, thermal that char? breadth) performance acterize the thermal sensitivity of these re? In this paper we enumerate some sponses. relevant physiological ecologically systems, review methods of describing their ther? mal sensitivity with an example, and dis? cuss ecological that can be atproblems tacked by similar approaches. Our interest in thermal and physiology evolved from field studies on tem? ecology in lizards. Certain perature regulation in habitats species regulated precisely only where the potential costs (time and energy) or risks (predation) of raising Tb appear low (Ruibal, 1961; DeWitt, 1967; Regal, 1967; 1976), lizards

Hertz,

1974; 1974; Lister, Huey, that the behavior of suggesting cannot be understood solely from considerations. physiological and Slatkin the (1976) formalized Huey

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and R. D. Stevenson

that behavior view thermoregulatory should between the reflect a compromise benefits and the associated costs or risks of and then derived a temperature regulation cost-benefit model with three parameters at various Tb, the frequency (the benefit of environmental distribution tempera? tures in a habitat at a given time, and the cost to aehieve Tb). This model particular for the extent of tem? predicts, example, that maximizes perature regulation energy of thermal gain or the relative advantages vs. thermal generalists specialists (eurytherms, stenotherms). In attempting to estimate the physiologi? cal benefits of Tb, these or related analyses confront serious problems. First, the avail? able data on physiological of Tb, effects which have been gathered to determine the physiological of the pre? significance ferred Tb (the Tb selected in a laboratory Licht et al., 1966), are thermal gradient; on tissue or cellular focused usually sys? tems rather than on (Dawson, 1975) which whole-animal are systems, ecologi(Bartholomew, cally more relevant 1958). statistics Second, important descriptive such as the physiologically Tb "optimal" as the best-performance defined (herein Tb; Fig. 1) or the "thermal performance breadth" as the range of defined (herein Tb over which an animal per forms well; are estimated Fig. 1) normally indirectly (e.g., inferring optimal Tb from preferred can be useful as first Tb). These estimates but have limitations approximations, and Slatkin, 1976; 1977; (Huey Reynolds, "optima/"temperature-^

Body Temperature FIG. 1. Hypothetical performance curve of an ectotherm as a function of body temperature.

and Fitzpatrick, 1979): most imBeitinger such estimates convey no infor? portantly, disadmation on the relative physiological vantage of activity at other Tb. was A partial solution to these difficulties several (Moore, by biologists pioneered 1948; Brett, 1939; Fry and Hart, 1971). an animal's one measures per? Basically, of Tb and formance over a broad spectrum to these then fits a curve performance data. One can then estimate Tb, optimal or relative thermal breadth, performance at any Tb from these curves. performance and their applications These procedures are the subjects of this discussion. INTERPRETABLEPHYSIOLOGICAL ECOLOGICALLY SYSTEMS and physiologists Although ecologists in thermal are keenly interested biology, goals. Consider they usually have different to studies on their contrasting approaches To an ecologist, the thermal locomotion. of locomotion is critical for sensitivity an animaFs ability to capture evaluating and interact soprey, escape predators, sen? To a thermal the cially. physiologist, activity prositivity of this whole-animal ever sharper vides a baseline for focusing of thermal adaptations on the mechanisms and biochemical at the tissue, cellular, levels. Our contention here is that attempts to and ecology should integrate physiology of whole-animal usually rely on studies rather than of or cellular tissue functions In other activities 1958). (Bartholomew, is more di? words, a study on acceleration to ecological rectly related performance than is a study on the rapidity of muscle contraction (the latter is, of course, appro? Licht evaluations). priate for mechanistic for example, a classic discovered, (1967) biochemical case where data appear the "optimaP* ecologically misleading; ac? for alkaline-phosphatase temperatures tivity were above the lethal temperatures for some of the lizards he studied! From this intentionally restricted per? ac? whole-animal of spective, examples contivities that should make significant tributions to fitness include rates growth

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Physiology

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359

80H

7H

70H tn 5-i

I

6050-

4"

40-^

Pituophis melanoleucus

30-4 15

20

25

30

Body Temperature, ^C

35

15

20

25

30

35

Body Temperature, ?C

FIG. 2. A. Growth (g/wk) of Bufo boreas juveniles during third week since metamorphosis (from Lil? lywhite et al., 1973). B. Percentage of strikes by

gopher snakes (Pituophismelanoleucus)that resulted in capture of a mouse (from Greenwald, 1974). Curves for both graphs fitted by eye.

and rates, efficiencies (Fig. 2A), digestive healing from injury, surviving disease, pre? success dation (Fig. 22?) and avoidance, or velocity, maximum acceleration agility, of rate metabolic scope, egg production, and social dominance. Despite the impressive variety and quality of studies on the of temperature significance physiological levels (Dawson, at tissue or lower regulation on whole-animal 1975), information per? is scattered and rare (e.g., Moore, formance et al, 1973; 1971; Lillywhite 1939; Avery,

and of thermal (or degree specialization), the tolerance range (Fry et al, 1946), with or associated upper and lower threshold is When completeness lethal temperatures. a to curve performance fitting required, data allows specification of predicted per? formance at any Tb (Huey, 1975). measures differ in physiological These and Optimal temperatures significance. thermal breadth describe performance at which animals temperatures perform "best" or "well" respectively, and are closely related of to the physiological concept In et al, (Precht 1973). capacity adaptation the the tolerance contrast, range estimates over which any ac? range of temperatures tivity or survival is possible, and is thus re? lated to the concept of resistance adaptation

1974; 1975; Greenwald, Kluger, Huey, data; 1978, unpublished 1978; Bennett, Waldschmidt, 1978; Tracy, unpublished data). A major and immediate goal of re? search in this area must be to fill this gap. DESCRIBINGTHERMALSENSITIVITY Measures

of performance

systems show maxi? Many physiological mum response at intermediate Tb and re? at higher or lower Tb (Figs. duced response curves approxi1, 2, 3). Similar response of many systems mate the performance (Brett, 1971). To characterize the thermal sensitivity of such systems, we need at least three de? measures scriptive (Fig. 1): the "optimal" (or optimal temperature temperature the thermal breadth performance range),

1973). (Precht etal, These measures in ecological differ as well. Thermal performance significance breadth is relevant to the important of niche width (Roughecological concept or lethal tem? Threshold 1972). garden, set absolute limits on where or peratures when animals can survive and (Porter Gates, 1969; Heatwole, 1970; Spellerberg, lizards are rarely 1972a, 1973). However, in active at near-threshold Tb, except (DeWitt, 1967). For example, emergencies the difference between the maximum Tb ever recorded for active individuals and the (Critical upper Tb at loss of coordination

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360

and R. D. Stevenson Tb was altered optimal by the sub? that field reflect a realization Tb's sequent and ecol? between compromise physiology their

Ranaclamitans

1966; DeWitt, ogy (Soule, 1963; Licht^a/., 1967; Regal, 1967; Huey, 1974). Workers the "preferred" then often substituted Tb thermal of lizards in laboratory gradients (Licht et al, 1966). With some exceptions, do promany tissue and cellular functions ceed fastest near the preferred Tb (Daw? son,

?C Bodytemperature, FIG. 3. Distance jumped by Rana clamitans as a function of Tb (from Huey, 1975; see Appendix I). The fitted curve is a product exponential (see Ap? pendix II). Thermal for 33 species of Maximum) = 1.0?- 19.4?C lizards is 6.0?0.58?C, range from Heatwole, (calculated 1970) and the difference between the minimum Tb ever recorded for active lizards and the lower Tb at loss of coordination Thermal (=Critical 4 for of is even lizards Minimum) species = 10.2? (12.8?1.21?C, larger range 15.3?C: calculated from Spellerberg, Because activity Tb are thus very I972a,b). different from threshold Tb, the cessation of activity before reaching near-threshold is probably not a result of temperatures such temperatures. We believe avoiding that this cessation is instead related to the in physiological decline general perform? ance at non-optimal Tb (Fig. 1). [Extremely like Dip? ectotherms high-temperature sosaurus dorsalis may, however, be excepThus tolerance limits tions.] seemingly have less relevance to temperature regula? tion per se or to the day-to-day activities of ectotherms than do optimal temperatures or thermal breadths (Bar? performance 1958; Warren, 1971; tholomew, Huey, 1978: but 1975; Feder, 1978; Humphreys, see Spellerberg, 1973).

Traditional measures

methods

of estimating

descriptive

The a priori assumption of early workers and Bogert, (e.g., Cowles 1944) that the mean Tb of field-active lizards represents

Nevertheless, Tb 1975). preferred altered hormonal or be time, by may context state, and behavioral physiological 1977), (Huey and Slatkin, 1976; Reynolds, that the preferred Tb is some? suggesting what labile and may also reflect a com? and ecology. between promise physiology More importantly, as noted above, pre? ferred no information about Tb conveys the actual disadvantages to an animal of active at other Tb. However, being any when direct measures of physiological per? formance are unavailable or impractical, the most meanTb is probably preferred measure of thermal behavior ingful 1977) and may also provide (Reynolds, into the nature of be? important insight havioral integration. In contrast, tolerance range can be di? measured the differ? rectly by calculating ence between the Critical Thermal Maxi? mum and Minimum 1939; Kour (Moore, and Hutchinson, 1970; Spellerberg, 1972a, Snyder and Weathers, 1975). Fewer measures of performance breadth as imhave been suggested, plied herein partly because breadth is inperformance from tolerance frequently distinguished and because the renewed at? range partly tention to the theoretical of significance niche width is recent 1967; (Janzen, Brattstrom, 1968; Levins, 1969; Kour and Hutchison, 1970; Ruibal and Philibosian, and Slatkin, 1970; 1976; Lister, Huey 1976; Hertz, 1977; Huey, 1978; Feder, measures 1978). Most field or laboratory are imprecise or rely on untested assump? tions (Huey and Slatkin, 1976, p. 370). The use of tolerance to estimate range per? formance breadth not only confounds the and ecological important physiological distinctions between these measures but may also be unreliable. For (above),

Integrating

Thermal

of the known tolerance ranges example, in fact cordo not and reptiles amphibians relate directly with intuitive predictions by breadths. of performance herpetologists that we have inforMost herpetologists that believe frogs have wider mally queried than do lizards. Yet breadths performance of lizards (X = tolerance ranges sample from N = 29; calculated 36.7?.52?C, broader actually 1972a)_are Spellerberg, N = than those of frogs (X = 30.1?.91?C, from Brattstrom, 5; calculated 1963). tolerance between a correlation Moreover, is seembreadth range and performance a a limited extent: to only ingly possible that would correlation imply precise curves are performance physiological ocsimilar ?an improbable geometrically until a in biology! currence Therefore, demon? is correlation actually strong a to maintain strated, it seems appropriate between tolerance distinction range and breadth. performance measures of describOf the traditional thermal performance, only tolerance ing and estimated. can be directly range easily are less suitaEstimates of other measures and ble for detailed analyses of physiology ecology. Direct measures of descriptive statistics and thermal per? temperatures widths can be estimated by the performance of an animal measuring over a spectrum of Tb and fitting a curve to this procedure, we the data. To exemplify data (Fig. 3, from use some preliminary 1975) on the acute effect of Tb on Huey, distance jumped I) by a green (Appendix frog (Rana clamitans) and fit these data to a Optimal formance

product-exponential (Appendix equation data should be fitted II). [When possible, In the absence to a theoretical curve. of such a curve, as is the case here, standard should be fol? curve-fitting procedures lowed.] Thermal tolerance range. Curve fitting is not required; the differ? merely compute and ence between the lower upper threshold Tb. For Rana clamitans (Fig. 3), this range is 30.0?C. this By calculating in several for individuals range popula-

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one can compare the relative tions, breadth of ranges among populations. Methods for estimating whether one range is hotter than another will be suggested below in the discussion on comparing op? timal temperature ranges. Optimal temperature vs. optimal temperature range. While many of us casually refer to "the optimal temperature" of an animal, we should probably refer instead to its optimal temperature range (see Heath, 1965). The of many physiological continuity systems a zone of temperatures strongly implies within which does not performance The width of 1). change substantially (Fig. this temperature-insensitive zone has profound implications for ecological and be? havioral analyses (Huey and Slatkin, 1976) and even for selection of an appropriate statistical method for comparing optima. We should therefore initially determine an individual whether has an optimal tem? perature or an optimal temperature range. the mean and First, we might determine variance of the animal's at performance each of several test temperatures (Fig. 3). Then we might determine the number of test temperatures in the maximal per? formance identi? range that are statistically cal. A consistent of insignificant pattern differences among three or more intervals a broad implies optimal temperature Statistical range. identity of only two tem? which could indicate either that peratures, an optimal range exists or that the optimal is intermediate between the temperature two test temperatures, is ambiguous. For Rana clamitans (Fig. 3), jumps at 15?C and 20?C do not differ significantly. The tem? intervals (5?C) in this study were perature large, so these data are somewhat ambigu? ous. Nonetheless, the general jumping a broad optimal pattern suggests temper? ature range. When an optimal exists, temperature one can estimate the optimal Tb by 1) the single best performance Tb selecting the mid(e.g., by ANOVA); 2) selecting the two best performance point between Tb; or 3) fitting a curve to the data and of the solving for the optimal Tb. Solution 3, II) product-exponential (Fig. Appendix of 16.8?C, whereas the yields an estimate

362

R. B. Huey

and R. D. Stevenson

estimate is 17.5?C. the object of curve fitting is for a data for indi? of populations, comparison viduals must be examined separately. while de? data for individuals, Lumping load considera? the experimental creasing drawbacks. First, bly, has two serious dif? individual unless data are normalized, in? in magnitude of performance ferences at each test tempera? crease the variance if optimal ture. Second, Tb is genetically or is affected polymorphic by age, season, time of day, or acclimation (see Reynolds, that individuals 1977), one might conclude have broad temperature ranges optimal is merely hetwhen instead the population for optimal Tb (Roughgarden, erogeneous midpoint When

1972). Thermal performance thermal performance

breadth. To estimate select an breadth, level (e.g., 80% of arbitrary performance maximum and then solve performance) the curve to determine the range of Tb is over which that performance standard or exceeded For 1975). equalled (Huey, the estimate from the productexample, curve is for Rana clamitans exponential 21.7?C (Fig. 3). The choice of performance of course; and the esti? level is arbitrary, mate for thermal breadth performance will vary between the estimates for toler? ance range and the optimal temperature on the selected per? range, depending formance level. [Because performance in degrees breadth is measured Celsius, one can compare breadths of performance animals forms of very different having vs. locomotion (e.g., jumping by frogs sprinting by lizards).] placement of tolerance ranges Comparing and optimal temperature ranges. When an op? timal temperature range exists (or when tolerance the above comparing ranges), which compare methods, optimal temper? would be biologically atures, misleading. In this case, we rephrase to the problem the optimal determine whether tempera? A is higher than ture range of population B. The simplest method that of population is to compare (e.g., 17.5?C for midpoints Rana clamitans) for individuals among A more general populations. technique that has greater content information can

the op? After determining also be derived. 15?C to timal temperature (e.g., range 20?C, Fig. 3) for each individual, compare "lower bound" temperatures average Next, set (15?C, Fig. 3) among populations. of criteria for differential placement For that example, range A specify ranges. is higher than range B only if the lower bound and the upper bound of A are both than those of B. [Alsignificantly higher one could that A is ternatively, specify if B is than at least one bound higher in A.] Although this significantly higher is more complex "bound" method than a is information more "midpoint" approach, A Thus we determine not that gained. only is higher than B "on average," but also the basis for this average difference. More? would alert us to over, the bound approach situations where the range of B is entirely within the range of A. contained INTEGRATINGTHERMALPHYSIOLOGYAND ECOLOGY The above methods can be used to the sensitivity of physiological quantify to Tb, a prerequisite for inperformance thermal and tegrating physiology ecology. of optimal Tb alone may suffice Knowledge for many analyses, but curve fitting per? mits further It can be analytical power. for example, to know that Rana useful, clamitans should jump about twice as far at Tb = 16.8?C than it should at Tb = 5.0?C or 31.5?C. Some basic applications of optimal Tb are particularly Measures to analyses of geographic dis? appropriate tributions of animals 1973; (Spellerberg, Huey and Slatkin, 1976; see also Clark and Kroll, 1974), of times of activity and of habitats 1964; Corn, 1971; Huey (Rand, and Webster, and Pianka, 1976; Huey and of competitive interactions 1977), 1959; Ruibal, 1961; Rand, 1964; (Inger, and 1976; Webster, Lister, 1976; Huey Schoener, 1977). Optimal Tb could be used to estimate patterns of geographic variation and even to measure rates (Moore, 1949) of evolution of phenotypic characters (see

Integrating

Thermal

Physiology

and Brown 1949; Feldmeth, Bogert, 1971). Thermal breadth is releperformance of habitat occupancy vant to discussions and competition (Ruibal and Philibosian, and Webster, 1974; 1970; Huey, Huey and Lister, 1976; Slatkin, 1976; Huey 1976; Hertz, 1977) as well as of the preciin various sion of temperature regulation and behavioral contexts (De? ecological and Slatkin, 1967; 1976; Witt, Huey selection Moreover, 1976). Greenberg, for thermal performance breadth pressure and fluctuatconstant may differ between (Levins, 1969; Kour and ing environments Hutchison, 1970; Huey and Slatkin, 1976), of thermal and knowledge performance breadths is necessary for certain zoogeog1967; Feder, (Janzen, raphic analyses 1978; Huey, 1978). As we have argued, tolerance range and associated threshold or critical tempera? tures have restricted ecological significance 1971; Feder, 1978; Humphreys, (Warren, to analyses of 1978). They relate primarily "thermal (Heatwole, safety margins" to adaptations to extreme condi? 1970), tions, and to understanding why animals avoid extreme temperatures. Extensions An immediate of this methodextension the dimensionology involves increasing inter? demonstrated ality. May (1975) actions between and salinity temperature on embryonic of the fish development Bairdiella C. R. Tracy icistia. (personal is similarly examining the communication) effects of Tb and hydration state on jumping ability of a frog. A second extension involves the dimen? sion of time. in a Acclimation results shift (presumably time-dependent adap? curve (Fry and tive) in the performance an animal at con? Hart, 1948). [Holding a stant, moderately high Tb may produce in perform? time-dependent impairment ance: thus not all shifts are adaptive and Ferrance, (Hutchison 1970).] The ex? tent and rate of acclimation, which can easwith the above methods, ily be quantified also gives a longer term estimate of niche

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width (see Levins, 1969; Hertz, 1977) than the acute estimates discussed here. A more concerns specific application of in differences Tb analyses preferred and Weintraub among samples. Mayhew seasonal in (1971) demonstrated changes Tb of Sceloporus orcutti. This shift preferred can be interpreted as evidence of seasonal acclimatization of optimal body tempera? ture. Alternatively, the physio? perhaps is unaffected logical optimum by season, but instead only the preferred Tb, which is a behavior 1977), is changing. (Reynolds, Given a constant, physiologically "optimal" Tb, a lower preferred Tb during winter can be adaptive costs associated by reducing with attempting to maintain a high Tb (see 1976). A direct com? Huey and Slatkin, of optimal or Tb for growth parison locomotion for lizards at different seasons discriminate inference might by strong (Piatt, 1964) between these competing (but non-exclusive)

hypotheses.

CONCLUDINGREMARKS-UNSOLVEDPROBLEMS The above discussion assumes implicitly that different physiological systems of an ectotherm have similarly shaped and positioned curves. This is unperformance an (Dawson, doubtedly oversimplification If optimal 1975). temperatures vary among physiological systems (or with age, sex, or time), then no single Tb simultaall systems. One poten? neously optimizes tial approach to solving this complex would be to order physiological problem to the animal: systems by their importance thus (if optimal Tb for locomotion is higher than that for growth) an animal might select a high Tb only when the ability to run quickly is of more immediate (or long term) than is the ability to grow importance quickly. [Why selection might have resulted in multiple optima rather than converging seems a fun? systems to a single optimum damental Not all systems are used question. Tb of a simultaneously: perhaps optimal is related to its temporal system activity pattern (see Brett, 1971).] A second is that physiological problem and ecological do performance probably not scale directly. Greenwald's (1974)

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and R. D. Stevenson

snakes data on gopher (Pituophis unique melanoleucus) provide a suggestive example. Relative velocity of strikes at mice were cor? of strikes that were related with percentage in successful (r = .80), but major changes with minor percent success were associated in relative strike velocity (slope = changes from data, courtesy of O. E. 1.81, calculated in Thus a 50% improvement Greenwald). (strike velocity) performance physiological does not necessarily imply a 50% increase in suc? (predation performance ecological tissue or from cess). Extrapolation to biochemical perform? ecological systems ance must also be very sensitive to this scalreason This is an additional ing problem: unsuitable for are such systems why ecological Because

analyses. an im? metabolism represents drain of energy, and constant portant the outcosts may also influence metabolic between come of interactions physiology and further and complicate ecology sometimes Very likely, animals analyses. for certain select Tb that are suboptimal but that maximize systems physiological rate 1971; Warren, 1971) or (Brett, growth losses or risk of metabolic that minimize (Regal, 1967; Huey and Slatkin, predation and Wolf, 1978; Hum1976; Hainsworth phreys, 1978). The existence of these and other sig? that atnificant complications suggests and ecology tempts to integrate physiology are at a nascent stage of development. this is a stage that appears to Nevertheless, fu? rapid gains in the immediate promise ture.

the test. Ten sets of repeating at 5?C, and then at measured were jumps 10? and 30?C fol? between 5?C intervals At a Tb of above the protocol. lowing 33.5?C, the frog was again unable to jump To test for fatigue effects when prodded. or possible acclimation during the experi? to 20?C and the frog was cooled ment, another series of jumps recorded (b in Fig. for the two 3). Mean distance jumped series at 20?C did not differ significantly in distance at that the decrease suggesting unrelated to fatigue was Tb 3) high (Fig. did not occur. and that acclimation before

APPENDIXII Various curves were fit to the frog jumpI). The besting data (Fig. 3, Appendix of was the 2 exponen? curve product fitting and Thornton tial equations Lessem, (see that uses the 1978, for a similar model product of 2 logistic equations): P = SC(1

- eKu (Tb - e"Ki (Tb " tu>) Ti}) (1

SC is the scale P is performance, = 87.50 cm), value (estimated parameter lower (left) the for initial is the -Kq slope side of the curve (.44?C_1), Tb is body tem? tem? T} is the lower threshold perature, (3.45?C), Ku is the initial slope for perature the upper (right) side (.34?C_1), and Tu is threshold the temperature upper was The product (33.50?C). exponential estimated regres? using the SPSS nonlinear sion (Marquardt's method) subprogram.

where

APPENDIXi

REFERENCES

To determine the thermal dependence of distance jumped by a 45 g, adult male Rana clamitans (acclimated for 2 weeks at about 7?C), Huey (1975) cooled the frog until it was unable to jump when prodded The frog was transferred to a (3.5?C). water bath (5?C). After 30 min, the frog was placed on the floor and induced to jump by lightly tapping its urostyle (the av? The frog erage of 3 jumps was recorded). was returned to the water bath for 5 min

Avery, R. A. 1971. Estimates of food consumption by the lizard Lacerta vivipara Jacquin. J. Anim. Ecol. 40:351-365. Bartholomew, G. A. 1958. The role of physiology in the distribution of terrestrial vertebrates. In C. L. Hubbs (ed.), Zoogeography, pp. 81-95. Publ. 51, AAAS, Washington, D.C. Beitinger, T. L. and L. C. Fitzpatrick. 1979. Physio? logical and ecological correlates of preferred tem? perature in fish. Amer. Zool.: 19:000-000. Bennett, A. F. 1978. Activity metabolism ofthe lower vertebrates. Ann. Rev. Physiol. 400:447-469. Bogert, C. M. 1949. Thermoregulation in reptiles, a

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factor in evolution. Evolution 3:195-211. Brattstrom, B. H. 1963. A preliminary review of the thermal requirements of amphibians. Ecology 44:238-255t Brattstrom, B. H. 1968. Thermal acclimation in anu? ran amphibians as a function of latitude and al? titude. Comp. Biochem. Physiol. 24:93-111. Brett, J. R. 1971. Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchusnerka). Amer. Zool. 11:99113. Brown, J. H. and C. R. Feldmeth. 1971. Evolution in constant and fluctuating environments: Thermal tolerances of desert pupfish (Cyprinodon).Evolution 25:390-398. Clark, D. R., Jr. and J. C. Kroll. 1974. Thermal ecol? ogy of anoline lizards: Temperate versus tropical strategies. Southwest. Nat. 19:9-19. Corn, M. J. 1971. Upper thermal limits and thermal preferenda for three sympatric species of Anolis. J. Herpetol. 5:17-21. Cowles, R. B. and C. M. Bogert. 1944. A preliminary study of the thermal requirements of desert rep? tiles. Bull. Am. Mus. Nat. Hist. 83:261-296. Dawson, W. R. 1975. On the physiological signifi? cance of the preferred body temperatures of rep? tiles. In D.M. Gates and R. B. Schmerl (eds.), Perspectives of biophysicalecology, Ecological studies, Vol. 12, pp. 433-473. Springer-Verlag, N.Y. DeWitt, C. B. 1967. Precision of thermoregulation and its relation to environmental factors in the des? ert iguana, Dipsosaurus dorsalis. Physiol. Zool. 40: 49-66. Feder, M. L. 1978. Environmental variability and thermal acclimation in neotropical and temperate zone salamanders. Physiol. Zool. 51:7-16. Fry, F. E. J. and J. S. Hart. 1948. Cruising speed of goldfish in relation to water temperature. J. Fish. Res. Bd. Can. 7:169-175. Fry, F. E. J., J. S. Hart, and K. F. Walker. 1946. Lethal temperature relations for a sample of young speckled trout, Salvelinus fontinalis. Univ. Toronto Stud. Biol. Ser. 54. Ontario Fish. Res. Lab. Publ. 66:9-35. Greenberg, N. 1976. Thermoregulatory aspects of behavior in the blue spiny lizard Sceloporus cyanogenys(Sauria, Iguanidae). Behaviour 59:1-21. Greenwald, O. E. 1974. Thermal dependence of striking and prey capture by gopher snakes. Copeia 1974:141-148. Hainsworth, F. F. and L. L. Wolf. 1978. The economics of temperature regulation and torpor in non-mammalian organisms. J. Thermal Biol. 3:87. (Abstr.) Heath, J. E. 1965. Temperature regulation and diur? nal activity in horned lizards. Univ. Calif. Publ. Zool. 64:97-136. Heatwole, H. 1970. Thermal ecology of the desert dragon, Amphibolurus inermis. Ecol. Monogr. 40:425-457. Hertz, P. E. 1974. Thermal passivity of a tropical forest lizard, Anolispolylepis.]. Herpetol. 8:323-327. Hertz, P. E. 1977. Altitudinal variation in thermoreg? ulatory strategies, physiological ecology, and mor-

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