Field thermal ecology of the eastern short-horned lizard (Phrynosoma douglassi brevirostre) in southern Alberta

Field thermal ecology of the eastern short-horned lizard (Phrynosoma douglassi brevirostre) in southern Alberta

G. LAWRENCE POWELL AND ANTHONY P. RUSSELL Department of Biology, University of Calgary, 2500 University Drive N. W., Calgary, Altu., Canada T2N IN4

Received April 16, 1984

POWELL, G. L., and A. P. RUSSELL. 1985. Field thermal ecology of the eastern short-homed lizard (Phrynosoma douglassi brevirostre) in southeastern Alberta. Can. J . Zool. 63: 228 - 238.

Phrynosoma douglassi brevirostre has a median body temperature ( T h ) of 32.9"C in southeastern Alberta, with a sharply peaked and negatively skewed Th frequency. The range of the Th frequency distribution in daylight hours during the active season (activity temperature range) is wide (20.0°C). The realized thermal niche is approximately 7°C wide, centred loosely on the median Th. The populations examined are active over a wide range of ambient temperatures. With regard to substrate temperature and air temperature at 10 cm, the populations examined are intermediate between thermoconformity and thermal independence, but with regard to air temperature at 1 m they display more thermal independence. Habitat use is most varied on sunny days. Th is not significantly different between situations, indicating that shuttling is an important thermoregulatory strategy. There is a significant difference in median Th between small lizards and large lizards, but not between either of these size groups and medium-sized lizards. Small lizards utilize significantly warmer substrates than the other two size groups. Large lizards are more closely coupled to substrate temperature, and less closely coupled to air temperature, than small lizards. Medium-sized lizards have a wider realized thermal niche than the other two size groups and are intermediate in their thermal relations relative to the other two size groups.

POWELL, G. L., et A. P. RUSSELL. 1985. Field thermal ecology of the eastern short-homed lizard (Phrynosoma douglassi brevirostre) in southeastern Alberta. Can. J . Zool. 63: 228-238.

Chez Phrynosoma douglassi brevirostre, la temperature mediane du corps ( T h ) est de 32,9"C dans le Sud de ]'Alberta et la courbe de frequence de Th comporte un sommet pointu et une asymetrie negative. L'etendue de la distribution de frequence de Th durant les heures de lumiere, pendant la saison active (etendue de la temperature d'activite) est large (20,0°C). La niche thermique rkalisee est d'environ 7°C de largeur et est a peu pres contree sur la temperature Th mediane. Les populations etudiees sont actives sur une grande ktendue de temperatures ambiantes. Par rapport i la temperature du substrat et a la temperature de l'air a 10 cm, les populations sont intermediaires entre la thermoconformitk et I'indkpendance thermique, alors qu'elles manifestent une plus grande independance thermique par rapport ri la tempkraturc de I'air 1 m. Les lizards font une utilisation plus variee de I'habitat par temps ensoleille. La temperature Th ne varie pas significativement d'une situation a une autre, ce qui indique que les deplacements constituent une importante strategic thermoregulatrice. 11 y a une difference significative entre la temperature Th mediane des petits lizards et celle des lizards de grande taille, mais pas entre la temperature Th de I'une ou l'autre de ces classes de lizards et celle des Iezards de taille moyenne. Les petits Ikzards utilisent des substrats relativement plus chauds que les deux autres groupes. Les gros Iezards sont asscciks de plus prks a la temperature du substat et moins a la temperature de l'air que les petits Iezards. Les lizards de taille moyenne ont une niche thermique rkalisee plus itendue que les autres groupes et occupent une position intermediaire dans leurs relations thermiques relatives aux deux autres groupes.

[Traduit par le journal]

Introduction Cold climates exhibit strong seasonal or daily changes

in temperature, with winter temperatures generally below freezing, and reptiles that live in such climates are of interest because of their ability to exist in conditions of periodic severity.

It has been proposed that reptiles do not make evolutionary adjustments to cold climatic conditions, but merely invade or persit i n areas where ameliorating environmental conditions permit (Cloudsley-Thompson 197 I). A body of data now exists, however, that suggests that this is not so, and that evolutionary adjustments have been made by some species. The most comprehensive review of these evolutionary traits is that of Spellerberg (1976), who lists viviparity, a low critical minimum temperature (CT,,,,), low voluntary body temperature (Th), eurythermy, and possibly small body size and super- cooling tolerance as reptilian cold-climate adaptations. Cold- climate reptiles generally display low correlations between Th and air or substrate temperature (Vitt 1974; Gibson and Falls 1979), many high- and middle-latitude species exhibit metabolic compensation (Prieto and Whitford 197 l ; Aleksiuk 197 1 a , 197 1 b, 19766; Bennett and Dawson 1975; Patterson and Davies 1978; Fitzpatrick et al. 1978; Bennett 1980; Ragland et al. 198 1 ; Smith et al. 198 l) , and some species seasonally acclimate to low temperature or changing photo-

period by way of metabolic depression (Mayhew 1965; Aleksiuk 1976a; Patterson and Davies 1978).

As uncertainties surround their evolutionary origin, reptilian traits associated with cold climates will herein only be considered in the context of their immediate adaptive value. Spellerberg (1976) listed four factors which in combination will act to constrain latitudinal or altitudinal distribution of a reptilian species: ( i ) its typical thermoregulatory method; (ii) the habitat structure required for successful employment of this method; (iii) the net available radiation over the year; and (iv) its mode of reproduction.

There is little to suggest that thermoregulatory methods of cold-climate reptiles differ from those of reptiles in general. Shuttling heliotherms typically have the lowest CT,,,, values (Spellerberg 1972a) and so would be expected to predominate in cold-climate herpetofaunas. Their eurythermy is advanta- geous and other forms of thermoregulation, such as thigmo- thermy, are energetically more expensive for the maintenance of a high Th (Huey and Slatkin 1976).

The primary empirical objective of this study was to examine the relationship of Th to substrate and air temperature in Phrynosorna douglassi brevirostre in Alberta. Secondly, the range and distribution of Th were examined in an attempt to ascertain the activity temperature range. It was hypothesized that these populations, living in a cold climate, would be

P ~ W E L L A N D RUSSELL 229

eurythermal and regulate T, relat~vely independently of environmental temperatures, and that relationships between insolation, microhabitat selection, and Th would exist and would be affected by relationships of insolation and microhabit selection to environmental temperature. These relationships were accordingly examined to clarify the correlation between habitat structure, insolation, and thermoregulatory method (Spellerberg 1976). Finally, it was hypothesized that there would be some subdivision of the "thermal niche" on an ontogenetic basis, as Huey and Slatkin ( 1976) proposed that lizards of different sizes would have different thermal properties. To test this, the relationships between T, , environmental temperature, and microhabitat selection within and between lizard size groups were examined. This further defines thermoregulatory method and clarifies the correlation between this method and habitat structure as it changes through the lizard's life.

Methods and materials Field methods

Data were collected at five separate study sites in southeastern Alberta in 1979. 1980, and 198 1 . Details of the climatic, physical, and biotic characteristics of the range are given in Powell (1982) and Powell and Russell ( 1984, 1985). Cloacal temperatures (CLTEMP) were taken from hand-captured lizards. Efforts were made to capture lizards with as little activity on their behalf as possible. in order to minimize both precapturc trauma and possible changes in body temperature due to evasive action by the lizards (Avery 1982). CLTEMP was recorded imniediately after capture. Phrynosomes generally dash only short distances if they move at all upon being disturbed, therefore CLTEMP

taken immediately after capture is probably not significantly different from that before capture. In the 1979 field season CLTEMP was taken with a custom-made tlexible thermistor probe attached to a Yellow Springs Instruments telethermometer. In the 1980 and 1981 field seasons, Schultheiss rapid-acting rectal thermometers were used for all captures except for young-of-the-year individuals, which were too small to acconimodate the thermometer bulb and had to be sampled with the fine-gauge thermistor and telethermonieter. The thermometers were standardized against each other in the laboratory. CLTEMP is used as a measure of Th i n this study (see below for discussion). Readings were only taken from animals during the daylight hours of the active season.

Substrate temperatures (SUBTEMP) was recorded at the time of capture with the same instrument used to take CLTEMP, by laying it tlat on the ground, shading i t from direct sunlight, and waiting for the reading to stabilize. SUBTEMP was always taken as closely as possible to the spot where the lizard was first seen and immediately after CLTEMP was taken. If the capture was made in the grass. the temperature of the grass litter at soil level was taken in lieu of soil temperature. Air temperature at I0 cm above the ground (AIRTEN) and at 1 m ( A I R O N E )

were taken by shading the instrument used to take CLTEMP and holding it at the appropriate height until the reading stabilized.

In addition to the thermal data, weight and snout-vent length (SVL)

were measured at the time of capture; information on the character of the day and situation of the lizard at time of capture was also recorded. Character of the day (WETH), defined by the degree of insolation, was classified in three ways: ( i ) sunny: direct sunlight with little or no cloud obscuring the disk of the sun; ( i i ) cloudy: clouds obscuring sun all or part of the time, little or no direct sunlight; (iii) intermittent: mixed cloud shadows and direct sunlight in rapid succession.

These WETH classifications describe the character of the day as i t was in the 2 h preceding the capture. The situation of the lizard (SITU)

is defined as the microhabitat that the lizard was fouhd in at the time of capture. if this could be determined with assurance. SITU is classified in four ways: ( i ) in open: on bare soil. rock or in thin grass. not immediately close to shelter; ( i i ) in shade: under shelter of vegetation or by rock, in full shade; (ii i) in shade mosaic: under shelter of vegetation or by rock, partially in open and partially in shade; ( iv) in

grass: in thick grass with litter layer. but not under any sort of shelter. SITU was classified primarily by exposure to sunlight, or, in the case

of "in grass." by the exposure to sunlight and air flow, because of the heliothermic nature of horned lizards (Heath 1965). By these criteria the above four categories encompass all of the situations of thermoregulatory significance in which lizards were found.

An~11s.sis Terminology follows Pough and Gans (1982), except where other-

wise noted. All data analyses for the thermal study were performed using subprogrammes of the Stcrti.stic.al pcrcakage Jhr the sot-icrl sc.ienc.es (Nie ct (11. 1975; Hull and Nie 1979). 'The lowest acceptable proba- bility was 0.05; probabilities between 0.05 and 0.01 are referred to as significant, between 0.01 and 0.001 as highly significant, and less than 0.001 as extremely significant. Normality of distribution of each of the grouped thermal variables (CLTEMP, SUBTEMP. AIRTEN, AIRONE)

was tested by the Kolmogorov-Smirnov goodness-of-fit test; skewness and kurtosis for each was also determined, as were the means, medians, modes, standard errors, standard deviations, variances, and ranges. Pearson's rank correlation coefficients for the thermal variables, and first- and second-order partial correlation coefficients among them were determined. A crosstabulation of WETH and slTu for all of the grouped cases was computed.

The grouped cases were separately subdivided by WETH, SITU, SVL, and sex, and simple statistical breakdowns of each thermal variable under each classification were performed. SVL was recoded into three size categories for classification purposes: ( i ) small (22.0-37.5 mm SVL; 0.7-4.0 g); ( i i ) medium-sized (37.6-57.5 mm SVL; 4.1 - I 1.0 g); (ii i) large (57.6-80.0 mm SVL; 1 1.1 -30.0 g). These three SVL

classifications correspond to the age-size classifications defined by Powell and Russell ( 1985).

Differences between means were tested first with an ANOVA, then with Student's t-test if the distribution of the variable with normal, or with a Mann-Whitney U-test if i t was not. The asymmetrical distribution of large samples of body temperatures render most estimations of central tendency and tests for differences between them of question- able value (Werner and Whitaker 1978; DeWitt and Freidman 1979). 'The median and surrounding 66% of the distribution is used in this study. Similar definitions appear in Werner and Whitaker (1978), DeWitt and Freidman ( 1979). and Magnuson et a/. ( 1979). Differ- ences between medians are tested by the median test. The significances of differences in the distribution of CLTEMP between lizard size groups were tested with the Kolmogorov-Smirnov two-sample test. The degree to which CLTEMP was regulated with regard to a particular environmental thermal variable (ETV) was evaluated by k, the coefficient of s in a simple linear regression of the ETV against CLTEMP

(Huey and Slatkin 1976). The significances of differences in k were tested by an ANOVA and by pair-wise t-tests for the homogeneity of the regression coefficients in two regressions (Steel and Torrie 1960). 'The significance of the difference between each k and 1 .O, the slope of the isothermal line, was also tested in this manner. A k which is significantly less than I .0 was taken as a sign that thermoregulation was actually taking place (Huey 1982; Huey and Pianka 1977).

Results Simple intcruc-tions of C'LTEMP und onvironment

Thermal data on 456 captures were gathered in 1979, 1980, and 1981. CLTEMP could not be taken on all captures, particularly those of young-of-the year individuals, since they were too small to accomn~odate the Schultheiss thermometer. In these cases the ETV measurements were still taken. The main statistical features of the four pooled thermal variables are given in Table I. CLTEMP has the highest mean of the four, and the narrowest range. The distribution is not normal, but is sharply peaked and negatively skewed (Fig. I A). This distribution is markedly different from those of the environmental thermal variables (SUBTEMP, AIRTEN, and AIRONE). SUBTEMP has

C A N . J . ZOOL.. V O L (1.3. I085

TABLE I. Descriptive statistics of thermal variables, with Kolmogorov-Smirnov two-sample test statistics for non-normality

Standard Thermal Mean deviation Median Minimum Maximum Range variable ("C) ("C) ("C) ("C) ("c) ("C) 1 1 Non-normality

CLTEMP 32.09 3.64 32.96 18.50 38.50 20.00 4 1 1 .Z' = 2.937""": SUBTEMP 29.70 5.51 29.49 16.00 45.80 29.80 458 % = 0.889NS AIRTEN 23.76 4.40 23.49 1 4.00 35.00 2 1 .OO 258 Z = 1 .034NS AIRONE 23.54 4.72 23.03 12.00 35.00 23.50 458 2 = 1.376"

Nurt:: All cases pooled. c'L2TkMP 11 is smaller than those ol' sr1I3 l 1:MI' and A I K o N I . owins to the small \i/c 01' some li~ards. which prevented measurement ol'tcrnperaturcs: A I K T ~ N 11 is small because i t was taken in I980 and I08 I o n l y : ( ' I . II .~II ' . cloacal temperature: SLJH'T'1:MP. substrate temperature: h l K r I : N , a i r tempcraturc at 10 cm: A I K O N I : , air tempcraturc at I m; NS. not \ignil'icant.

-l'Significant, 0.05 2 1 ) 5 0.01. :l::Txtrernely significant, p < 0.001.

TABLE 2. (A) Spearman rank correlation coefficient matrix for the

four thermal variables

SLIBTEMP A I RTEN A I R O N E

CLTEMP 0.68 12""" 0.5557""" 0.3857""" SUBTEMP - 0.805 1 ""* 0.6749""" AIRTEN - 0.9246"""

( B ) First order partial correlation coefficients of environmental thermal variables with CLTEMP

SUBTEMP A I R'TEN A I R O N E

SUBTEMP - 0.4956""" 0.6303""" AIRTEN 0.04 1 I NS 0.5657""" AIRONE -0.1203" -0.3997""" -

Norb.: NS. not signil'icant; :':. significant (0.05 2 p 2 0.01): -'..'.'I:. extremely significant ( p < 0.001 ).

the widest range of the ETVS and the highest mean (Table I ). The distribution is normal, though slightly flattened and negatively skewed (Fig. IS). The mean and peak of SUBTEMP are to the left of those of CLTEMP (Fig. I A). AIKTEN has a narrower range and mean than SUBTEMP (Table I ) . The distribution is normal, but more tightly clumped than that of SUBTEMP. dis- playing more flattening and skewness to the right (Fig. IC). A I K O N E has an extremely significantly different mean from AIRTENS ( I ) < 0.001; Wilcoxon signed-rank test), but a some- what greater range (Table I ) . Its distribution is significantly non-normal, slightly negatively skewed but less tlattened than that of A I K T E N (Fig. I D).

The Spearman rank correlation coefficient matrix for the four thermal variables (Table 2) shows that CLTEMP has a correlation of high significance with each of the ETVS. The magnitude of the correlation coefficient decreases between sUBTLMP

and AIRTEN, and again between AIKTEN and AIKONE. SUBTEMP is strongly correlated with AIKTEN and less strongly with AIRONE; both correlations are highly significant. AIRONE and AIRTEN

have a large correlation coefficient of high significance. Table 2 displays the first-order partial correlation matrix for

all of the ETVS and CLTEMP. Controlling for the effects of SUBTEMP drastically reduces the values of the correlation coefficients of AIKTEN and AIKONE. Elimination of the effects of AIKTEN produces an extremely significant correlation coefficient for SUBTEMP and an extremely significant negative correlation coefficient for AIKONE. Controlling for the effect of A I R O N E results in extremely significant first-order partials for

TABLE 3. Second order partial correlation coefficients of environmental thermal variables with CLTEMP

SUBTEMP S Ll BTEM P AIRTEN

and and and AIRTEN A I R O N E A I K O N E

SUBTEMP - - 0.4424""" AIRTEN - 0.3044""" -

A I R O N E -0.3229""" - -

."'pExtrcmcly signil'icant ( 11 < 0.00 I )

SUBTEMP and AIK'I 'EN, both of which have similar values to their respective corresponding zero-order coefficients in Table 2. This first-order correlation coefficient matrix indicates that the ETV which has the greatest effect on the correlations of the other ETVS with cL7rt;.MP is SLIBTEMP.

The table of second-order correlation coefficients of the ETVS with CI~TEMP (Table 3) shows that SUBTEMP has the largest coefficient when the effects of AIKTEN and AIKONE are controlled for. A I K O N E has an extremely significant negative correlation with CI-TEMP when AIKTEN and SUHTEMP are controlled for. All of the second-order partial correlation coefficients have smaller absolute values than their corresponding Pearson's r values, and so none of them explains a great deal of the variation in CLTEMP.

The first-order partial correlations between the ETVS are almost all stronger than the correlations between any one of the ETVS and CLTEMP (Table 2). which implies that the ETVS all respond in a similar fashion to a commonly experienced thermal regime. rather than representing factors which separately and additively affect CLIT'EMP. The relationship of each to CLTEMP must be considered separately.

In the plot of CLTEMP against SUBTEMP (Fig. 2), scatter is to both sides of the isothermal line, tending to increase below it as SUBTEMP increases. The regression is extremely significant and the line is significantly less steep than the isothermal line, lying above i t . The scatter in the plot of CLTEMP against AIKTEN

(Fig. 3) is more diffuse than that in Fig. 2. although the regression is extremely significant. Most of the points lie above the isothermal line. tending towards it as AIKTEN increases, and the regression line is significantly less steep than the isothermal line. Broad scatter is evident in the plot of CLTEMP against AIKONE (Fig. 4). most of the points lying above the isothermal line. Scatter decreases as AIRONE increases, and the points trend closer to the isothermal line. The regression is extremely significant. and the regression line is significantly less steep than the isothermal line. The regression of CLTEMP on SUBTEMP has the largest r' and the smallest standard error (Fig. 2), while the

POWELL A N D RUSSELL

CLTEMP

n=411

I I I I I I I I

20

. :.a

I . . . . . .

Regress ion b z 0 . 4 6 3

standard error of b = 0 . 0 2 3

a z 1 8 . 3 4 6

B. SUBTEMP

FIG. 2. Plot of CLTEMP against SUBTEMP with regression line, isothermal line (CLTEMP = SUBTEMP), and relevant regression statistics. All cases pooled.

> 0 z

- 1 sd III+l sd mean

w 143

Regress ion

b z 0 . 4 7 2

standard error

Of b ~ 0 . 0 3 5 a = 2 0 . 8 7 1 F = 1 0 6 . 9 7 7 (1.222) * * *

n = 2 2 4

FIG. 3. Plot of CLTEMP against AIRTEN with regression line, isothermal line (CLTEMP = AIRTEN) , and relevant regression statistics. All cases pooled.

all the pooled captures is given in Table 4. The majority of captures (73.4%) were made on clear sunny days, and most captures (79.0%) were made in the open. Only on sunny, clear days were lizards found in all four SITU classifications, and this is the only WETH classification in which lizards were found in shade mosaics. On cloudy days the majority of captures (77.6%) were made in the open. The proportion of captures made in the open is highest (87.0%) on days of intermittent sun. All of the rest of the captures made in this WETH classification were made in the grass. The X' value for this contingency table is significant.

-1 s d l v l + l sd mean

FIG. I. Frequency distributions of (A) CLTEMP, (B) SUBTEMP, (C) AIRTEN and (D) A I R O N E . All cases pooled. Median and 533% of distribution ( i n A) or mean and -+ I standard deviation ( 1 sd) (in B, C, and D) indicated.

regression of CLTEMP on AIRONE has the smallest r' and the largest standard error (Fig. 4). The k values computed from the pooled cases of A I R I E N and SUBTEMP are similar in magnitude and not significantly different from one another, but both are significantly different from the k value computed from the pooled cases of AIRONE (Table 7D).

A breakdown of the relationship between SITU and WETH of

CLTEMP has the highest median under sunny conditions, the lowest median under cloudy conditions, and a median lying between these two extremes under conditions of intermittent sun. The medians of CLTEMP under all three WETH classifica-

232 CAN. J . ZOOL. VOL. 63. 19x5

Regression

b z 0 . 3 1 5 standard error o f b = 0 . 0 3 5

a = 2 4 . 8 8 2

~ 1 , 4 0 8 ) = 8 1 . 3 5 3 * * *

n = 4 1 0

FIG. 4. Plot of CLTEMP against AIRONE, with regression line, isothermal line (CLTEMP = AIRONE), and relevant regression statistics. All cases pooled.

TABLE 4. Contingency table showing relationship between SITU (situation in which lizard was captured) and WETH (character of the day. defined by insolation). Percent of captures of each WETH classification

in each SITU classification are given

SlTU Row

In In In shade In totals WETH open shade mosaic grass (5%)

Sunny 78.0 6.3 8.4 7.3 73.4 Cloudy 77.6 6.9 0.0 15.5 14.8 Intermittent sun 87.0 0.0 0.0 13.0 11.8

Column totals (%) 79.0 5.6 6.1 9.2

X 7 = 16.4368* (df = 6)

tions are mutually significantly different. There are no significant differences between any of the medians of CLTEMP under the four different SITU classifications.

Mean SUBTEMP is only significantly different between captures made in the open and captures made in shade mosaics, this last SITU classification having the highest mean and smallest standard deviation for this variable. There is a significant difference i n AIRTEN between captures made in the open and captures made in shade mosaics, and an extremely significant difference between mean AIR'rEN values of captures made in the grass and those made in shade mosaics. Shade mosaic capture data exhibit the largest mean and the smallest standard deviation for AIRTEN. AIRONE is not significantly different between captures made in the open and captures made in the grass or between instances of captures made in the shade and those made in shade mosaics. All other AIRONE means for possible pairings of SITU classifications are at least significantly different. The mean AIRONES for captures made in full shade or in shade mosaics are larger than those for those made in the open or in the grass.

The mean of each ETV is highest on sunny days, lowest on cloudy days, and intermediate on intermittently sunny days. SUBTEMP is at least significantly different between all three

-33% t7I+33% median

B. Medium-sized

- 3 3 % r n + 3 3 % median

CLTEMP("C1 -33% 171+33%

med~an FIG. 5. CLTEMP distributions of the three lizard size groups, with

medians and ?33% of the distributions indicated.

WETH classifications. There is a highly significant difference in mean AIRTEN between sunny days and cloudy days, but no difference between each of these and the mean AIRTEN on inter-

POWELL A N D RUSSELL

TABLE 5. Descriptive statistics, with test statistics and probabilities for differences in means, for the thermal variables. broken down by sex

Thermal Mean Standard Standard Test statistic and variable Sex ("C) deviation error I I significance

CLTEMP Female 32.05 3.75 0.23 265 U l , = 18447.5NS Male 32.13 3.48 0.29 143

SUBTEMP Female 29.26 5.3 1 0.32 285 t,, = 2.05* Male 30.36 5.65 0.44 167

AIRTEN Female 23.71 4.61 0.35 173 to = 0.30NS Male 23.87 3.95 0.43 8 5

AIRONE Female 23.23 4.72 0.28 286 U , , = 21 357.5NS Male 24.06 4.7 1 0.37 166

NOTE: NS, not significant; '*. significant (0 .05 2 1) 2 0.01 )

mittently sunny days. Mean A I R O N E is highly significantly dif- are no significant differences in the k values of SUBTEMP,

ferent between sunny days and cloudy days, and significantly AIRTEN, and AIRONE between lizards size groups. different between sunny days and intermittently sunny days. There is no difference in mean A I R O N E between cloudy days and Discussion intermittently sunny days.

Possible sor4rcses o f error Breakdown by size and sex

There are no significant differences between the means of the four thermal variables of the two sexes, with the exception of SUBTEMP (Table 5).

The median CLTEMP of small lizards is significantly lower than the median CLTEMP of large lizards, but neither is significantly different from the median CLTEMP of medium-sized lizards (Table 6A). The mean SUBTEMP associated with the capture of small lizards is significantly higher than those associated with medium-sized and large lizards, which are not significantly different from each other (Table 6C). There are no significant differences between lizard size groups in mean associated AIRTEN (Table 6D) or in mean associated AIRONE (Table 6E). Small lizards (Fig. 5A) have a more sharply peaked CLTEMP distribution than medium-sized (Fig. 5B) or large lizards (Fig. 5C). The ranges of the three distributions are similar, but medium-sized lizards have a wider 33% of the range to the left of the median (Fig. 5B). There is no significant difference in median CLTEMP between male and female medium-sized lizards. There is a significant difference in CLTEMP distribution between large lizards and small lizards, but no such significant difference in CLTEMP distribution between either of these size groups and medium-sized lizards (Fig. 6B).

The association of SVL with SITU is extremely significant. Larger lizards tend to be found in the open less often, but in the shade and grass more often. A larger proportion of small lizards than of medium-sized lizards is found in shade mosaics, but most of the shade mosaic captures are of large lizards. As lizard size class increases, the distribution of captures over the SITU

classifications becomes more equable, but the open is still the predominant SITU classification in which captures were made.

There is an extremely significant difference between the k values of AIRONE and SUBTEMP of large lizards, but otherwise there are no significant differences in k within this group (Table 7C). The k of AIRONE is significantly smaller than the k values of SUBTEMP and AIRONE in medium-sized lizards,;but there is no significant difference between the k values of AIRTEN and SUBTEMP in this size group (Table 7B). There are no significant differences between any of the k values of small lizards (Table 7A). All of the k values of each size group are significantly different from their respective isothermal lines ( t > to ,,,). There

It is impossible to determine how much effect capture stresses had on CLTEMP, or even to state with assurance that the effect was a constant factor in all captures. On hot days lizards were generally more difficult to capture and subdue than on cooler days. Activity could raise the CLTEMP of a lizard captured on a hot day, but the likelihood and extent of this bias are difficult to assess (Avery 1982).

Phrynosomes are able to maintain well-marked differences in temperature between the head and the rest of the body, the difference decreasing with increasing Th (Heath 1 9 6 4 ~ ) . Tem- perature regulation in reptiles is strongly dependent on brain temperature (Heath 1 9 6 4 ~ ; Hammel et al. 1967; Cloudsley- Thompson 1968, 197 1 , 1972; Mayhew 1968). Regulation of Th may be relaxed in comparison with regulation of cephalic temperature, and in such circumstance the lizard would appear to be more eurythermal than it is in fact, from the point of view of its temperature control centre. No pertinent experimental data on P. d . brrvirostre from Alberta, or elsewhere, are available. This phenomenon is only of importance at the lower end of the Th range (Heath 1964u), and in any case the distribution of field-gat hered CLTEMPS indicates the breadth of the activity temperature range. It is emphasized, however, that while the lizard is assumed to be regulating Th similarly over the whole body and that this temperature is equivalent to CLTEMP, in fact body and head thermoregulation may be different to some extent.

It can be argued that the difference in SITU distributions of the SVL classifications are to some extent artefactual. Small lizards are expected to be more difficult to find in any situation but the open, whereas large lizards would be more noticeable, still or flushed, in the grass or under cover. This objection may have some validity, but an effort was made in the field to flush lizards from available shelter, whether their presence was evident or not. Similarly, the representatives of the thermal data can be questioned on the ground that they do not sufficiently represent lizards under shelter, or on cloudy days. However, the data collected in this study are interpreted as the Th and ETVS

of active lizards during daylight hours in the active season. Data were collected as the availability of active lizards per- mitted, under all weather conditions in the active season, and this is taken to represent true activity.

234 CAN. J . ZOOL. V O L . 63. 19x5

TABLE 6. Descriptive statistics, with test statistics for differences in central tendency, for the four thermal variables of each lizard size group (comparisions of CLTEMP distributions between lizard size

groups included)

SVL Thermal SVL SVL

group variable("C) group 2 group 3

(A) CLTEMP medians, with X' statistics for pairwise differences in median and multiple median test X' statistic

I Median = 32.10 2.486NS 8.876"" 2 Median = 32.96 - 1.347NS 3 Median = 33.04 - -

Multiple median test: X' = 8.919*

(B) Kolmogorov-Smirnov two-sample test Z statistics for pairwise differences in CLTEMP distribution

I 1 .286NS 1.492* 2 - 0.683NS

(C) SUBTEMP means with t statistics for pairwise differences in mean and ANOVA F statistic

1 Mean = 30.89 2. lo* 2.35* SD = 5.74 SE = 0.57 n = 103

2 Mean = 29.45 - 0.37NS SD = 3.36 SE = 0.39 n = 188

3 Mean = 29.24 - -

SD = 5.46 SE = 0.42 n = 167

ANOVA: F = 3.648*

(D) AIRTEN means with t statistics for pairwise differences in mean and ANOVA F statistic

I Mean = 24.69 1.391VS 1.73NS SD = 4.42 SE = 0.61 n = 53

2 Mean = 23.67 - 0.44NS SD = 4.12 SE = 0.42 n = 96

3 Mean = 23.39 - -

SD = 5.50 SE = 0.44 n = 109

ANOVA: F = 1.986NS

(E) AIRONE means with Mann-Whitney U statistics for pairwise differences in mean and Kruskal-Wallis ANOVA X' statistic

I Mean = 24.07 9267.0NS 7694.ONS SD = 4.75 SE = 0.47 n = 103

2 Mean = 23.65 - 14536.ONS SD = 4.34 SE = 0.32 n = 187

3 Mean = 23.09 - -

SD = 5.08 SE = 0.39 n = 168

Kruskal-Wallis one-way ANOVA: X 2 = 1.474NS

NOTE: SVL classifications: group I , 22.0-37.5 mm (small): group 2. 37.6-57.5 mni (medium-si~ed); group 3, 576-80.0 mm (large). NS. not significant. 'I:. significant (0.05 r p r 0.01): :";", highly signil'icant (0.01 r p 2 0.001).

TABLE 7. k values of each lizard group, and all pooled cases, with t statistics for within-group differences between k values for different

environmental thermal variables

SUBTEMP

AIRTEN

AIRONE

SUBTEMP

AIRTEN

AIRONE

SUBTEMP

AIRTEN

AIRONE

SUBTEMP

AIRTEN

AIRONE

(A) Small lizards 0.39437 0.726 (df= 80)NS 0.032 (df= 1 19)NS (n=61) 0.48574 - 0.616(df=8 1 )NS (n = 23) 0.39719 - -

(n=62)

(B) Medium-sized lizards 0.49149 1.089 (df=273)NS I .986(df=361)* (n= 183) 0.58306 - 2.280 (df = 280)* (n=94) 0.35717 - -

(n= 1 82)

(C) Large lizards 0.49535 0.952 (df=268)NS 3.522 tdf=327)*** (n = 165) 0.42835 - 1.788 (df=269)NS (n= 107) 0.274 19 - -

(n= 166)

(Dl Pooled cases 0.46477 0.390 (df=629)NS 3.859 (df=8 15)*** (n = 409) 0.48396 - 2.950 (df=630)* (n = 224) 0.30738 - -

(n=410)

NOTE: NS. not significant; ". signil'icant (0.05 r p r 0.01 ); :'::';:': . extremely significant ( p < O . ( M ) I ) .

Ch~lrac.teri.stic.s I$ the T,, distribution The kurtosis and strong negative skewness of the grouped

CLTEMP frequency histogram (Fig. 1A) is typical of Th distributions of vertebrate ectotherms (Spellerberg 1976; Werner and Whitaker 1978; DeWitt and Friedman 1979). The rates of most enzyme-mediated physiological processes can be described as exponential functions of temperature (DeWitt and Friedman 1979). If an ectotherm is regulating a physiological process whose rate is a positive exponential function of temperature, a normal distribution of the rate (to be expected in an actively thermoregulating ectotherm) would result in a negatively skewed Th distribution (Spellerberg 1976; Dew itt and Friedman 1979). However, the Th distribution of the field- caught lizards represents a complex balancing of the ecological and energetic costs of thermoregulation with the imperatives of physiology (Soule 1963; Huey and Slatkin 1976). Without experimental data on the selected Th distributions of P . d . brevirostre, the effects of these costs on the Th frequency histogram cannot be evaluated. Part of the leftwards tail of Fig. IA undoubtedly represents the CLTEMPS of lizards captured on cool days, or when the sun was low in the sky (Werner and Whitaker 1978). Increased activity and tighter thermoregulation at higher ETVS is implied by the strong peakedness of the CLTEMP distribution (Fig. lA), especially as the vertical range of scatter in the plots of CLTEMP against each of the ETVS (Figs. 2, 3, 4)

POWELL AN11 KUSSLLL 235

decreases as the value of the ETV increases. The range of the pooled CLTEMPS (Table I ) can be taken as

the activity temperature range, the Th range of active animals caught in the daylight hours, during the active season. The median plus the surrounding 66% of this distribution corre- sponds roughly to the thermal niche in Magnuson c.t ell. (1979), although it must be considered as the realized niche rather than the fundamental niche since it is defined froni field data rather than thermal gradient data. Thus a certain amount of conformity to the thermal exigencies of the environnient must be expected (Soule 1963; Huey 1974~1, 1974b; Huey and Slatkin 1976). The activity temperature range is 20°C wide, but the realized thermal niche is only approximately 7°C in breadth. There are few physiological data available on P . douglassi to set the realized thermal niche and activity temperature range in context. Phrynosomcr clouglcl.s.si from montane New Mexico has an absolute perniissible Th range of 40.75"C (CT ,,,,,, = 2.75"C, CT, ,<,, = 43.5"C; Prieto and Whitford 197 I ) , but whether this can be applied directly to the Alberta populations is moot. The New Mexico populations are found in a montane forest habitat (Smith 1946; Prieto and Whitford 197 1 ; Montanucci 198 1 ), whereas the Alberta populations inhabit mixed grass prairie at a lower altitude. In addition. there is evidence that the low CT,,,,, and accompanying relatively less depressed oxygen consumption at lower temperatures in the New Mexico P . ck,uglcr.s.si (compared with sym- patric P . c*ornutum) is correlated with an enzymatic and (or) respiratory pigment adaptation (Prieto and Whitford I97 1 ), resulting in temperature compensation over part of the T, range. Given these caveats, the CLTEMP distribution of the Alberta sample fits well within the absolute permissible T, range established by Prieto and Whitford ( 197 1 ) . 'The upper limit of the CLTEMP distribution (38.5"C). the median (32.96"C). and the realized thermal niche of the Alberta populations all lie within the upper half of this absolute permissible T, range. Reptiles typically regulate T, within the upper part of their activity temperature ranges (Cloudsley-Thompson 197 1 ).

I t is difficult to state with any certainty the extent to which the Alberta populations of P . d. br~viro.str~ can be considered eurythermal. Like all members of the genus P/lrynosorncl, it is a shuttling heliotherm (Heath 1965), and this thermoregulatory strategy is correlated with low CT,,,,, (Spellerberg I972cl). Cold-climate reptile species tend to have wide voluntary T, ranges (Spellerberg 1976). Eurythermy is also favoured in thermally variable climates (Soule 1963) and when the energetic costs of thermoregulation are high (Huey 1 9 7 4 ~ , 1974h, 1982; Huey and Slatkin 1976), as is the case in a thermally variable climate. However, the habitat of the Alberta populations is structurally simple, and opportunities for basking are abundant. Thermoregulation in periods of clear weather would not be energetically expensive, and the main potential cost, that of predation from exposure in the open. would be obviated to some extent by the species' crypsis and spininess (Pianka and Parker 1975). The climatic variability in this part of the species' range would constitute the major selective force favouring eurythermy, particularly as yearly activity starts before the average date of the last spring frost (Powell 1982).

Phr?;nosomu douglu.s.si occupies a wide variety of high- altitude habitats over a broad latitudinal range (Smith 1946; Reeve 1952; Montanucci 198 1 ), and it apparently lacks some high-temperature thermoregulatory responses typical of its congeners from warmer areas (Milne and Milne 1950; Heath 1965). By the criteria listed above, it is predicted to be more

eurythernial and tolerant of cool temperatures than its congeners. and has been shown to be so in comparison to P . cSorrlutlrrn in New Mexico (Prieto and Whitford 197 1 ) and, less certainly, to P . pltrtyrhir1o.s (Dunias 1964; Pianka and Parker 1975). However, the eurytherniality of the Alberta populations of P . el. hre~~irostrc cannot be usefully defined from the data presented here.

Relcltior~.ship.s \rit/~ c~rl~~iror~rn~nfcd thc-.rrncrl ~~clriclb1c.s The independence of CLTEMP with regard to each of the ETVS

is not established. When dealing with the field Th of a heliotherm it is difficult to determine the extent to which the animal is thermoregulating against particular components of its ther- nial environment, or even if it actually is thermoregulating (Heath 1964h), as it is possible that Th and environmental temperatures are simply responding siniilarly to a common source of heat. The existence of metabolic compensation in P . clo~rglc~.s.si (Prieto and Whitford 197 I ) complicates this, since metabolic rate may be partially or wholly independent of a Th which is apparently tracking an ETV (Bennett 1980). Apparent environmental effects of C L ~ T E M P will be discussed without the inference of causality, unless otherwise noted. Although soil and air temperature are intimately related (Geiger 1965; Rosenberg I974), the relationship of each to CLTEMP will be considered separately.

SUBTEMP

As well as having the strongest zero-order, first-order partial, and second-order partial correlation coefficients with CL.TEM P, SUB- EM P greatly decreases the first-order partial correlation coefficients tbr AIKTEN and AIRONE when its effects are controlled for (Table 2). C L T ~ M P is regulated more precisely with regard to SUBTEMP as SUHI'EMP increases (Fig. 2), and the k value of this relationship places the phrynosome about midway between thernioconformity and perfect thermoregulation with regard to the substrate (Huey and Slatkin 1976). Heat transfer froni the substrate by conduction will be important in the morning (Heath I964cr) and possibly ininiediately before sundown. This influence will be controlled by posturing during the active day (Heath 1965), but even a posturing lizard will be sub-ject to the reradiative and convective effects of the substrate (Porter and Gates 1969; Muth 1977; Gates 1980), the extent of which will depend on the substrate's albedo (Geiger 1965).

AIRTEN

Reradiation from the substrate affects the temperature of the air immediately above it (Geiger 1965; Rosenberg 1974), as does the movement and temperature of the air above this region. AIKTEN and SUBTEMP taken together roughly describe the phrynosome's immediate thermal environment and are closely entrained, as is shown by the first-order partial correlation coefficient of A I K T E N with CLTEMP when the effects of SUBTEMP are controlled (Table 2). Phrynosomes generally maintain a T, above AIKTEN (Fig. 3), and the k value for this relationship is not significantly greater than that of SUBTEMP

(Table 7D). midway between thermoconformity and perfect thermoregl- lat ti on (Huey and Slatkin 1976). Convective exchange with the surrounding air will be important to a relatively small lizard, such as P . el. hrcviro.strc. (Porter and Gates 1969; Cloudsley-Thompson I97 I; Heatwold 1976; Muth 1977; Porter and James 1979; James and Porter 1979; Gates 1980). Thermoconformity with the air is only regularly found in trop- ical arboreal closed-canopy forest lizards (Huey 1974~1, 1974 b; Huey and Slatkin 1976; Avery 1982) or those inhibiting open areas where shade is scarce (Huey 1982).

236 CAN. J . ZOOL. V O L . 63. 1985

AIRONE

The k for AIRONE is lower than and significantly different from those of SLIBTEMP and AIRTEN (Table 7D). This implies that phrynosomes regulate T, more independently of A I R O N E

than they do of the other two ETVS, a feature common among reptiles at high latitudes (Vitt 1974) and high altitudes (Pearson and Bradford 1976). AIRONE would principally affect phrynosome T, through its turbulent exchange with AIRTEN.

While phrynosome Ths display some relationship to the ETVS, each of them taken separately does not explain a great deal of the variation in T,, (Table 2). This has been noted in the garter snake Thamnophis .sirtcriis at high latitudes (Gibson and Falls 1979) and in high-latitude reptiles in general (Vitt 1974). Phrynosome activity is closely correlated with substrate temperature in the sun (Heath 1965). The relationships of the ETVS

to CLTEMP may be due as much to variations in insolation correlated with variations in environmental temperature as they are to direct effects of the ETVS, as the species' heliothermy evidently frees it to some degree from thermoconformity .

CLTEMP is less strongly coupled to A I R O N E than to AIRTEN and SUBTEMP (Table 7D). Phrynosomes in Alberta are more closely coupled to the radiative portion of the thermal environment, the substrate and the air immediately above it, then to the convective portion, the air higher above the ground.

Habitut use Most captures were made in the open (Table 4), an expected

consequence of the relaxed thermoregualtion associated with myrmecophagy in this genus (Pianka and Parker 1975). The lack of significant differences in CLTEMP between the various SITU classifications is evidence that shuttling is the major ther- moregulator~ method. The most varied habitat use is on sunny days, the only days on which shade mosaics were used. Shade mosaic captures have the highest associated mean ETVS, which may indicate that the SITU classificat.ion was used as an alternate to shuttling when a constancy of insolation provides enough heat to establish a thermal gradient between the shaded and unshaded portions of the phrynosome's body.

It is possible that prey activity in the various microhabitats differs under differing insolation conditions, and that phyrno- somes track this rather than utilize different situations for ther- moregulator~ reasons under the various insolation regimes. This hypothesis cannot be tested from the available data (Powell and Russell 1984).

The significant differences in CLTEMP and in SUBTEMP

between all WETH classifications is additional evidence for the previously discussed coupling of phrynosome T,, to the radiative portion of the thermal environment, both phrynosome and substrate responding similarly to insolation.

Diferenc-es by size and sex The Alberta populations of P. el. brevirostrs display pro-

nounced sexual size dimorphism, adult males being significantly smaller than adult females (Powell and Russell 1985). The significant difference in mean associated SUBTEMP between the sexes (Table 5) is not significant as a sexual difference but as a difference between size groups (Table 6B). It is likely that the higher associated mean SuB'rEMP of the smaller males results from their greater dependence upon the convective com- ponent of the thermal environment (Muth 1977).

The difference in median CLTEMP and realized thermal niche between the size groups are evident from Fig. 5. Small lizards maintain a lower T,, than the other two size groups, while exploiting significantly hotter substrates, and display a CLTEMP

distribution significantly different from that of larger lizards. There is little information concerning differences i n T, between ontogenetic size groups in this genus. Baharav ( 1975) found no difference between juvenile and adult P. solare. Guyer (1978) found none between the three size classes (corresponding to the three used in this study) of P. el. douglas.si in southern Idaho, and noted bimodal daily activity in small lizards. This he attrib- uted to the lower thermal inertia of small lizards which requires them to seek shelter during the hotter part of the day. Size- associated differences in thermal inertia provide a probable explanation for the differences in T, and SUBTEMP between size groups. The smaller the lizard, the lower the convective thermal equilibrium it will have (Cowles and Bogert 1944; Norris 1967; Porter and Gates 1969; Cloudsley-Thompson 197 1 ; Spellerberg 1972 b, 1 9 7 2 ~ ; Muth 1977; Porter and James 1979; James and Porter 1979; Gates 1980). Muth ( 1977) states that small lizards are more tightly coupled to the convective portion of the thermal environment and will have Ths more dependent on air temperature, whereas large lizards are more tightly coupled to the radiative portion and will have T,,s more reflec- tive of substrate temperature. This should apply even over the size range of phrynosomes in Alberta.

The overall pattern of response changes between size groups. Small lizards do not show any significant difference i n thermoregulatory degree between any of the ETVS (Table 7A), indicating a closer coupling to the convective portion of the thermal environment. The low SUHTEMP k of small lizards suggests that their CLTEMP is relatively more independent of substrate temperature than the other two size groups (Tables 7B, 7C). Large lizards are more independent of A I K O N E than of AIRTEN and SUBTEMP (Table 7C), suggesting a tighter coupling to the radiative portion of the thermal environment than small lizards. Medium-sized lizards thermoregulate differentially against AIRTEN and AIRONE (Table 7B), which is not the case with large lizards (Table 7C), suggesting that the air near the ground has a stronger convective effect on medium-sized lizards than on large ones. As a phrynosome grows, its relationship with its thermal environment changes gradually. This is shown by the lack of significant difference in median CLTEMP

and CLTEMP distribution (Tables 6A, 6B) between medium- sized lizards and either of the other two size groups. The size classifications used in this study compartmentalize this change so that the significant difference between the two ends of the size range are evident.

One possible consideration in evaluating the CL'TEMP frequency histogram of large lizards is that they are all females of reproductive age (Powell and Russell 1984, 1985) and may thermoregulate more precisely when gravid. 'This is thought to be a maior selective advantage of viviparity in cold-climate reptiles (weekes 1935; ~reer-1966: ~ ~ e l l e r b e r g 1976; Tinkle and Gibbons 1977; Packard c)t ul. 1977). Gregory and Mclntosh ( 1980) noted that gravid female Thclmnophis sirtuiis maintained higher body temperatures than nongravid females and males, but Gibson and Falls (1979), while noting that females of this species are more precise thermoregulators, found no difference between body temperatures of gravid and nongravid females.

The size-based differences in thermal ecology are accom- panied by differences in microhabitat exploitation. Most small lizards are found in the open, where convective cooling would keep T,, lower than it would be in a larger lizard under similar conditions. Little time will be spent in the open, because small lizards' low thermal inertia will promote rapid cooling and

POWELL A N D RUSSELL 237

because they are more independent of substrate temperature. Large lizards make much less use of the open than small lizards. Their greater thermal inertia allows them greater independence from the immediate effects of ambient temperature and permits them to exploit other situations which may be thermally less than optimal. In addition. being more closely coupled to substrate temperature than small lizards places larger lizards in more danger of overheating in the open. neces- sitating more frequent trips to shelter. Medium-sized lizards are intermediate in microhabitat utilization between large lizards and small lizards, as would be expected, since they seem to have the thermal disadvantage of both other groups.

It is possible that the difference in microhabitat exploitation between small lizards and the other two size groups also reflects a difference in diet. This possibility cannot be tested, however, since no dietary data were accumulated for small lizards (Powell and Russell 1984).

Acknowledgements We would like to thank Leonard and Mary Jane Piotrowski,

Will and Rose McKinley, Phil Flaig, Dick and Janet Rose, and the Laidlaw family for permission to work and camp on their lands. Dr. E. Swierstra of the Dominion Agricultural Station in Lethbridge is thanked for permission to use the Onefour school- house as field headquarters. We are obliged to Mr. Larry Linton for his help with the computer and to Dr. Robin Leech for his help and encouragement in the field. For constructive criticism of this project in its various stages, we are indebted to Drs. Ray Huey, Ian Spellerberg. Paul Anderson, Nancy Henderson, and Herb Rosenberg. We are grateful to Drs. Ron Davies, Gordon Pritchard, and Bob Weyant for reading and commenting upon an earlier draft of this manuscript. The corn- ments of two anonymous reviewers were also helpful in this regard. Financial support was partially from the Department of Biology, University of Calgary, and partially from Natural Sciences and Engineering Research Council grant A-9745 to A. P. Russell. Ronica Pacholok typed the manuscript.

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Documents

Field thermal ecology of the eastern short-horned lizard (Phrynosoma douglassi brevirostre) in southern Alberta