Covariation of thermal biology and foraging mode in two Mediterranean lacertid lizards.
Foraging modes, usually classified as sit-and-wait vs. widely foraging (Pianka 1966, Huey and Pianka 1981), according to the mobility of predators, are correlated with major differences in ecological (Eckhardt 1979, Huey and Pianka 1981), physiological (Anderson and Karasov 1981, Huey et al. 1984), life history (Vitt and Congdon 1978), and morphological (Webb 1984) characters. Foraging modes of lizards fit well into this dichotomous view of foraging strategies (Pietruszka 1986, McLaughlin 1989). Widely foraging lizards have higher rates of energy expenditure and higher rates of food intake than do sit-and-wait species (Anderson and Karasov 1981); they show greater endurance but lower burst speed (Huey et al. 1984); their relative clutch mass is often lower (Vitt and Congdon 1978, Magnusson et al. 1985); and they eat more prey that are sedentary and clumped (e.g., termites) and fewer prey that are active (Huey and Pianka 1981, Magnusson et al. 1985).
Since the pioneer demonstration by Cowles and Bogert (1944) that desert lizards behaviorally regulate their body temperature ([T.sub.b]), thermoregulation has come to be seen as a major aspect of reptilian ecology (Huey and Stevenson 1979, Huey 1982), with crucial effects on locomotion and foraging performance (Bennett 1980, Avery et al. 1982). However, there is no agreement in the literature about the ways in which movement behaviors influence, and are restricted by, thermoregulatory behavior (but see Hillman 1969, Anderson and Karasov 1988). Whereas some authors have suggested that thermoregulation would require complex behaviors (e.g., postural adjustments) incompatible with continuous movements and, hence, with active foraging (Regal 1983), others have argued that active foragers would be more able to exploit the thermal patchiness of their environment (Magnusson et al. 1985), thus achieving body temperatures that would enhance locomotor performance (Bennett 1980, Hertz et al. 1983, van Berkum 1986, Van Damme et al. 1989). Such disagreement reflects a surprising lack of data, in that thermoregulatory behavior determines the efficiency of locomotor and foraging performance (Bennett 1980, Avery et al. 1982, van Berkum 1986, Van Damme et al. 1991), and movement patterns, together with available microclimates, determine the duration of exposures to different thermal conditions and, hence, the rates of heat exchange with the environment. In other words, movement patterns translate into body temperatures through species-specific heat exchange rates that are modulated behaviorally by the selection of, and time of residence in, thermally different patches (Diaz 1991, Carrascal et al. 1992). Thus, neither the behavioral mechanisms of thermoregulation (e.g., shuttling heliothermy) nor the alternative locomotion patterns suggested by the dichotomous view of predator search modes (MacArthur and Pianka 1966, Pianka 1966, Schoener 1969, McLaughlin 1989) can be properly understood without considering the effects they have on each other.
In this paper, we study two widely distributed Mediterranean lacertid lizards that differ both in their habitat selection patterns and in thermal conditions within their habitats: Psammodromus algirus and Acanthodactylus erythrurus (see Salvador 1985, Arnold 1989). Lacertids are usually viewed as active foragers, although there is some evidence of interspecific variation in movement rates (Huey and Pianka 1981, Huey et al. 1984). Subtle differences in movement behavior between species with similar foraging modes may actually provide a conservative, fine-grained test of the interaction between their thermal biology and their position along the continuum of foraging modes. This test would cast light on the behavioral and ecophysiological effects of movement intensity (i.e., foraging mode), without following the usual procedure of comparing extreme sit-and-wait and continuous searchers.
Our main objective is to analyze the integration of different behavioral and ecophysiological traits in these lacertid lizards that exploit different habitats. As an example, frequent shuttles between sun and shade, which require continuous movements, are likely to be a more feasible strategy in forest thermal mosaics than in xeric shrubsteppes with a scarcity of shade. Rather than testing whether or not the combinations of traits that we study represent adaptive syndromes (requiring a much larger scale study with more emphasis on evolutionary mechanisms), our goal is to understand how these traits interact in a comprehensive and structured way, defining patterns of covariation that represent equally efficient thermoregulatory strategies. We specifically address the following questions:
1) To what extent are behavioral thermoregulation and movement behavior (i.e., foraging mode) dependent one on each other?
2) How does the interaction between movement and basking behavior relate to interspecific differences in thermal preferences and heat exchange rates?
3) Are these associations consistent with interspecific differences in habitat selection patterns?
MATERIAL AND METHODS
Although the phylogenetic relationships of lacertids have not been resolved, the available data (see Bauwens et al. 1995 and references therein) indicate that the related genera Psammodromus and Gallotia diverged from other clades within the family (including Acanthodactylus) very early in the history of the Lacertidae (33-35 x [10.sup.6] yr BP). Psammodromus algirus is a medium-sized lacertid lizard (adult snout-vent length up to 82 mm) that inhabits a great variety of habitats in the western Mediterranean, being commonest in broad-leaved (both deciduous and perennial) degraded forests with a well-developed undergrowth of shrubs (Arnold 1987, Diaz and Carrascal 1991). It is a ground-dwelling, shuttling heliotherm with a bimodal pattern of daily activity in the summer months (Carrascal and Diaz 1989). Its foraging mode is somewhat displaced toward the active-searching side of the continuum (McLaughlin 1989), as judged by our data on percentage of time spent moving and movement rate (see Table 3 and Results). In fact, many food items are searched for and captured in the leaf litter beneath shrubs or trees, although short foraging incursions into open areas, usually triggered by the detection of large and/or fast moving prey (Diaz and Carrascal 1993), are not infrequent.
Acanthodactylus erythrurus is also a medium-sized lacertid (adult snout-vent length up to 82 mm) that prefers open, sandy areas with sparsely distributed vegetation (Arnold 1987). It belongs to an advanced clade of Eurosaharian species from xeric climatic zones (Arnold 1989), and it is the only species within its genus that is present in western Europe. Other species of Acanthodactylus are found in North Africa and the Middle East. Its distribution range in the Iberian Peninsula is contained within that of P. algirus (Salvador 1985). However, both species show differences in microhabitat selection patterns, with Psammodromus algirus more dependent on dense vegetation cover (Mellado 1980). A. erythrurus adults show a unimodal circadian rhythm during all months in which they are active (Pollo and Perez-Mellado 1989). Both species are active at the same times of year (Barbadillo 1987), but A. erythrurus is clearly a less active forager than P. algirus, based on its considerably lower percentage of time moving and movement rate (see Table 3 and Results). Casual observations, both in the field and in captivity, and dietary data (Perez-Mellado 1992) suggest that A. erythrurus feeds mainly on ants (probably a widespread prey type in shrubsteppe habitats) and on fast-moving prey that it captures in the open after short, rapid attacks launched from ambushing sites.
Field observations of behavior were obtained in two different areas representative of the habitats typical of each species. The behavior of P. algirus was recorded in Soto de Vinuelas, Madrid, central Spain (40 [degrees] 35[minutes] N, 03 [degrees] 34[minutes] W). The study plot ([approximately equal to]10 ha) is located within a protected, large Mediterranean evergreen forest in which holm oaks (Quercus rotundifolia) are the dominant species in the tree and shrub layers. Canopy height averages 1.3 m, with a mean cover of 54.5% (estimates obtained using a scored stick held vertically at a number of random spots; details in Diaz 1993). Behavioral data for A. erythrurus were collected in a plot of [approximately equal to]25 ha at La Punta (Devesa del Saler, Valencia, southeastern Spain, 37 [degrees] 40[minutes] N, 0 [degrees] 30[minutes] E). The study plot is a well-preserved dune field sparsely covered with several species of small shrubs and grasses (Ononix natrix, Helichrysum stoechas, Halimium halimifolium, Ammophila arenaria). Vegetation cover is 40%, with a mean vegetation height of 50 cm.
Field observations of behavioral thermoregulation
Field observations were conducted on P. algirus in June-July 1990 and on A. erythrurus in June-July 1992. In both cases, samples were taken between 0700 GMT (onset of the activity period; Carrascal and Diaz 1989, Pollo and Perez-Mellado 1989) and 1200 (sun zenith). Activity of focal individuals was observed with binoculars from a distance of 3-6 m, dictating continuous behavioral observations to a portable tape recorder. When transcribing the tapes, we took time measurements with a precision of [+ or -]1 s. No sequence of [less than]5 min was included in the analyses. Only lizards not reacting to observer presence were monitored. For each observed individual, we noted time of day, sex, and an estimate of its snout-vent length. At the end of each observation period, we recorded the environmental operative temperatures ([T.sub.e]), both in full sun and in deep shade, with the aid of an electronic digital thermometer (precision of 0.1 [degree] C). Measurements were taken at the exact place where the lizards were initially observed and at the nearest available sunlit or shaded patch (for lizards in the shade or in full sun when first sighted, respectively). For this purpose, we used hollow copper cylinders, approximately the size of a lizard, that were closed at both ends, except for a small fissure allowing introduction of the thermometer's probe. The cylinders were sufficiently sealed so that no air transfer occurred through the fissure.
In a pilot study, we analyzed the variation of [T.sub.e] in the field. We sampled the temperature of 30 copper models disposed on a linear transect in the Soto de Vinuelas area. Distance between consecutive models was 6 m, a greater distance than that moved across by focal individuals whose behavior was sampled for 520 min in the field (an area rarely exceeding the surface of a 5-m radius circle). Every 60 min, from 0600 to 1100 GMT, we recorded the [T.sub.e] of models and noted if they were in full sun or deep shade. By means of a two-way ANOVA with time of day and sun exposure as factors, we partitioned the variation observed in [T.sub.e]. The percentage of variance explained by time of day was 54.6% ([F.sub.5, 121] = 60.69, P [much less than] 0.001; degrees of freedom were reduced because we used only the models fully exposed to sun or shade, eliminating the ones corresponding to sun-filtered patches, as in our field study). Differences between sun and shade accounted for 29.9% of the variance observed ([F.sub.1, 121] = 103.04, P [much less than] 0.001). The error component (random differences between sampling points) accounted for 15.1% of the variance observed. Thus, [T.sub.e] varied much more among times of day and sun-shade patches (84.9% of variance for both components together) than among temperature readings at different spots within the same time of day and sun-shade category. This empirical result demonstrates that operative temperatures within a given habitat (holm oakwood) varied quite little among microsites that were fully illuminated or fully shaded. Therefore, our unreplicated [T.sub.e] measurements associated with focal animals provided a useful indication of the thermal state of their environment.
We checked that the copper models provided reasonably close approximations of actual lizard temperatures by comparing, under the same conditions of radiant heat loads (100-W bulb at different heights), their temperature readings with the cloacal temperatures of two freshly dead lizards of each species. At equilibrium, the mean values of lizard [T.sub.b] and model [T.sub.e] were highly correlated ([R.sup.2] [greater than] 0.99 for both species), satisfying the criterion for [T.sub.e] determinations in Bakken et al. (1985). The resulting regression equations had slopes and intercepts that did not differ from one and zero, respectively. There were seven replicates for each dead lizard; P. algirus: [T.sub.b] = -1.04 + 0.99 ([T.sub.e]); A. erythrurus: [T.sub.b] = -0.71 + 1.01([T.sub.e]). Thus, this procedure allowed us to measure the approximate temperatures attained by lizards at the pertaining microsites and times (availability of [T.sub.b] data; Bakken and Gates 1975, Grant and Dunham 1988, Bakken 1992, Hertz 1992).
As behavioral variables, we selected: (1) the duration of each basking event (where basking is defined as a period of [greater than]10 s motionless in full sun); (2) the number of basking events per minute (basking rate); (3) the duration of movements and pauses, recording shuttles between sun and shade; (4) the number of movement periods per minute (movement rate); and (5) the distance covered in each movement period. We also recorded the total time employed in each behavioral sequence. Combining these original variables, we calculated the percentage of time spent basking, the average moving speed (including stops [less than]1 s), and the amount of time spent moving in the sun and in the shade.
The availability of ground surface exposed to sun in each study area was estimated from the line transects done while searching for lizards to monitor their behavior. The percentage of ground not covered by vegetation that was in full sun was estimated visually at 100-m intervals.
Rates of heat exchange
All heating and cooling rates were experimentally determined at the Estacion Biogeologica El Ventorrillo, using 15 individuals of P. algirus in July 1990 and 11 individuals of A. erythrurus in July 1992. The animals, captured at the sites where behavioral sequences were obtained, were introduced into a portable refrigerated box until their body (cloacal) temperatures ([T.sub.b]) fell to [approximately equal to]20 [degrees] C (approximately the temperature of a lizard retreated into the deep shade of its refuge; L. M. Carrascal and J. A. Diaz, personal observation). Each animal was measured (snout-vent length) and weighed before being employed in a trial. For A erythrurus (n = 11), snout-vent length was [Mathematical Expression Omitted] and body mass was 5.5 [+ or -] 0.9 g; for P. algirus (n = 15), snout-vent length was 69.4 [+ or -] 5.6 mm and body mass was 8.3 [+ or -] 1.9 g. Thus, lizards were significantly larger in our sample of P. algirus than in that of A. erythrurus (P [less than] 0.001 in both t tests).
The experimental subject was fixed with two bands of transparent masking tape, around the base of the tail and on top of the forelimbs, to a 12 x 25 cm wooden table, and was exposed to direct solar radiation. To standardize conditions of radiant heating, we oriented the body axis of lizards toward the sun, although heating rates in the similarly-sized Lacerta monticola are unrelated to the lizard's body orientation toward the sun (Martin et al. 1995). The slope of the body axis in the horizontal plane was always 0 [degrees], as P. algirus and A. erythrurus bask and forage on nearly flat ground. A Miller-Weber quick-reading mercury thermometer ([+ or -] 0.1 [degree] C) was inserted into the lizard's cloaca and continuous readings of [T.sub.b] were obtained at 20-s intervals (Avery and MacArdle 1973). Heating experiments finished when the cloacal temperature reached 36-37 [degrees]. This procedure did not allow animals to use postural adjustments during heating because we were interested in measuring physiological, not behavioral, interspecific differences. After animals were warmed, they were moved to a full-shade position for measurement of cooling rates. Body temperature readings were again registered every 20 s from the moment [T.sub.b] began to fall.
For each heating or cooling trial, we measured the operative temperature in the immediate surroundings of the experimental lizard, using a thermocouple inserted into a copper model placed on the wooden table.
Both heating and cooling rates (in degrees per minute) were determined as the slopes of the linear regressions relating [T.sub.b] to time elapsed. This was a better procedure than the use of time constants (Spotila et al. 1973) because the [T.sub.b] values of these small species perching in the sun did not attain or even approach an equilibrium temperature, at least within the lizard's tolerance range. In fact, the MS errors were extremely low for the linear regression models, and the coefficients of determination for heating and cooling trials were all [greater than]0.95.
Selected body temperatures
In September 1992, 13 individuals of each species (all adults with a snout-vent length [greater than]50 mm) were captured at the study areas and were transported to the Estacion Biogeologica El Ventorrillo (Navacerrada, Madrid; 40 [degrees] 40[minutes] N, 3 [degrees] 50[minutes] W), where they were allowed to acclimatize for 1 wk in 100 x 50 x 40 cm terraria subject to a light: dark cycle of 12:12 h. Food (crickets and mealworms) and water were supplied ad libitum. Duration of captivity was [less than]25 d and, by the end of the study, the animals were released at the areas where they had been collected.
A 150-W light bulb suspended 11 cm above one end of a terrarium created a thermal gradient with operative temperatures ranging from 18 [degrees] to 58 [degrees] C. A second 60-W bulb outside the cage illuminated the cool end of the gradient. This thermal gradient covered the range of temperatures available during the annual activity period in the study areas of both species (L. M. Carrascal and J. A. Diaz, personal observation). Food and water were provided ad libitum in the experimental terrarium during the trials.
A Miller-Weber quick-reading mercury thermometer was used to measure [T.sub.b] of active lizards after I h in the thermogradient. These temperature readings were considered to be estimates of Selected [T.sub.b] values, that is, temperatures lizards would attempt to achieve in the field, in the absence of physical and biotic restrictions (Licht et al. 1966). All measurements were taken using single animals instead of pairs or groups. We obtained two estimates per individual, always on different days, and used the mean of the two replicates for subsequent analyses.
We also used the thermogradient to record two other [T.sub.b] measurements that provide an approach to the threshold [T.sub.b] levels controlling basking behavior (Heatwole and Taylor 1987). We defined the Shade Seeking temperature as the cloacal temperature at the moment when a lizard stopped basking and began moving to cooler places. After spending some time in the shady end of the gradient, lizards began to move back to the hot end, presumably to bask again; we measured their [T.sub.b] at that time as an estimate of the Resume Basking temperature. Measurement of these temperatures began after animals were left undisturbed for [greater than or equal to]15 min. We obtained two replicates for each individual on different days, and averaged them for subsequent statistical analyses. To test whether or not two temperature readings per individual were enough data to describe interspecific differences in [T.sub.b], we performed repeated-measures ANOVAs with the body temperature data obtained in the thermogradient, estimating the effect size (variance partitioning) of the between-factor term (species) and the within[repeated]-factor term (first and second measurements per individual). The results of these analyses for Selected, Resume Basking, and Shade Seeking [T.sub.b] showed that the repeated-measures factor (within-individual variation) was not significant in any case (P [greater than] 0.3, df = 1, 24 in the three ANOVAs). Moreover, its contribution was always [less than]5% of the total variance. The percentage of variance explained by the between-species term was 4.2 times higher than the percentage explained by the between-measurements term for Selected [T.sub.b], 498 times higher for Shade Seeking [T.sub.b], and 30 times higher for Resume Basking [T.sub.b]. Therefore, the average of two readings per individual was a proper sample to test interspecific differences in [T.sub.b].
All measurements of Selected [T.sub.b] values were taken during the time of day when both species are active in the field, and we interspersed measurements of the two species to control for possible differences linked to time of day.
Analysis of behavior in a thermogradient
The same thermogradient described in the previous section was used to study the selection of basking sites differing in mean [T.sub.e] values, and the patterns of basking behavior in the two species, controlling for the effects of the thermal and physical (e.g., vegetation structure) environment. Lizards used in this procedure were the same animals employed in the study of selected [T.sub.b] values. Subjects were placed in the experimental terrarium 5 min before the behavioral observations began. This time was considered to be long enough for the animal to recover an undisturbed pattern of behavior. During the following 25 min, the same variables of thermoregulatory behavior measured in the field were precisely recorded in a quantitative way, using a computer behavioral observation program (The Observer, NOLDUS) run out in a notebook computer. We obtained two samples per individual on different days, so that overall behavioral sequences totalled 50 min/individual. Again, we interspersed trials for both species to control for differences linked to time of day.
For the behavioral sequences, we divided the terrarium into five zones differing in the amount of radiation received and, hence, in [T.sub.e] (estimates obtained from the extreme with the 150-W bulb onwards: 58 [degrees], 34.5 [degrees], 22.1 [degrees], 18 [degrees], 17.3 [degrees], and 17 [degrees] C). We defined basking events as stays of [greater than]10 s immobile in the two zones closest to the bulb end, and we measured the duration and rate of basking events in each of the two basking zones.
We used analyses of covariance (ANCOVA) to compare field observations of behavior between both species, taking the operative temperature in full sun as the covariate. This statistical procedure was used to remove the effect of differences in thermal environment ([T.sub.e]) between the two study areas. However, other important ecological features (number of predators, distance to the nearest refuge, food availability, et cetera) may differ between habitats to an unknown extent. Thus, we assumed that the main habitat differences that influence the behaviors studied are correlated with the thermal environment. Rates of heat exchange were also compared using ANCOVAs, with operative temperature as the covariate. To assess interspecific differences in selected temperatures, we employed t tests. For behavioral observations in the thermogradient, we used Mann-Whitney U tests. All statistical analyses were carried out using SPSS for Windows 5.0 (Norusis 1992).
Field observations of behavior
Operative temperatures were higher in the study area of A. erythrurus than in that of P. algirus, both in full sun (A. erythrurus: 41.9 [+ or -] 1.04 [degrees] C, [Mathematical Expression Omitted], n = 29; P. algirus: 39.0 [+ or -] 0.72 [degree], n = 43; t = 2.40, P = 0.019) and in full shade locations (A. erythrurus: 32.6 [+ or -] 1.21 [degrees], n = 29; P. algirus: 25.3 [+ or -] 0.66 [degree], n = 43; t = 5.71, P [less than] 0.001).
Percentage of time spent basking and basking rate (number of basks per minute) were negatively related to [T.sub.e], although average bask duration was not. The pattern of covariation between these behavioral variables and [T.sub.e] was similar for both species (test for homogeneity of regression slopes: P [greater than] 0.1). Basking behavior in the field did not differ significantly between the two species after we corrected for the effects of differences in thermal environment between study areas (see observed and adjusted values in Table 1 and results of ANCOVAs in Table 2). Thus, percentage of time spent basking, bask duration, and number of basks per unit time were similar in both species.
With respect to locomotion (Tables 3 and 4), [T.sub.e] was inversely related to the percentage of time spent moving, the movement rate (number of moves per minute), the average duration of individual moves, and the percentage of total time moving that was spent in full sun. Average speed did not covary with operative temperature in the pooled sample of the two species, although there was a significant interaction between species and covariate. A reanalysis of the relationship between speed and [T.sub.e], using simple correlations within each species, showed that average speed was positively correlated [TABULAR DATA FOR TABLE 1 OMITTED] related with [T.sub.e] in A. erythrurus (r = 0.67, n = 14, P = 0.008) but not in P. algirus (r = -0.21, n = 41, P = 0.194).
TABLE 2. ANCOVA with variables describing thermoregulatory behavior of A. erythrurus and P. algirus in the field. Interspecific differences are tested in the Treatment (species) rows. The sign of covariation with [T.sub.e] is shown in brackets, except for bask duration, which is not correlated with temperature.
df F P
% time spent basking
Covariate ([T.sub.e] [-]) 1, 69 70.41 [less than]0.001 Treatment (species) 1, 69 1.32 0.254 Interaction 1, 68 0.72 0.400
Basking rate (no./min)
Covariate ([T.sub.e] [-]) 1, 69 31.81 [less than]0.001 Treatment (species) 1, 69 2.82 0.098 Interaction 1, 68 2.83 0.097
Bask duration (s)
Covariate ([T.sub.e]) 1, 58 2.32 0.134 Treatment (species) 1, 58 2.68 0.107 Interaction 1, 57 0.32 0.572
P. algirus and A. erythrurus differed significantly in all behavioral traits associated with locomotor performance (see observed and adjusted values in Table 3 and results of ANCOVAs in Table 4). Percentage of time spent moving and duration of individual moves were higher in P. algirus, whereas A. erythrurus spent a higher proportion of its total locomotion time moving in full sun (see treatment effects in Table 3). For these variables, the pattern of covariation with [T.sub.e] was similar in both species (see nonsignificant interaction terms in Table 4). For the movement rate, the effects of the interaction between species and [T.sub.e] were significant (Table 4). The movement rate decreased significantly with operative temperature in A. erythrurus, but it remained constant throughout the observed range of operative temperatures in P. algirus [ILLUSTRATION FOR FIGURE 1 OMITTED]. The variance of moving rates was significantly higher in A. erythrurus ([s.sup.2] = 3.33) than in P. algirus [TABULAR DATA FOR TABLE 3 OMITTED] ([s.sup.2] = 0.46; [F.sub.12, 12] = 7.309; P = 0.002).
TABLE 4. ANCOVA with variables describing locomotor performance in the field of A. erythrurus and P. algirus. Interspecific differences are tested in the Treatment (species) rows. The sign of covariation with [T.sub.e] is shown in brackets, except for speed, which is not correlated with temperature.
df F P
% time spent moving
Covariate ([T.sub.e] [-]) 1, 69 6.92 0.010 Treatment (species) 1, 69 8.32 0.005 Interaction 1, 68 1.16 0.286
Movement rate (no./min)
Covariate ([T.sub.e] [-]) 1, 69 4.55 0.037 Treatment (species) 1, 69 4.42 0.039 Interaction 1, 68 7.10 0.010
Move duration (s)
Covariate ([T.sub.e] [-]) 1, 59 6.19 0.016 Treatment (species) 1, 59 4.59 0.036 Interaction 1, 58 0.21 0.650
Covariate ([T.sub.e]) 1, 49 0.65 0.425 Treatment (species) 1, 49 7.87 0.007 Interaction 1, 48 10.24 0.002
% moving time in full sun
Covariate ([T.sub.e]) 1, 59 0.30 0.588 Treatment (species) 1, 59 129.73 [less than]0.001 Interaction 1, 58 0.51 0.479
In A. erythrurus, locomotion took place in full sun (Table 3) in a significantly larger proportion than expected by chance (t test against the null hypothesis that the mean proportion of locomotion time spent in full sun equals the 44.5% availability of ground surface exposed to sun: t = 118.6, P [much less than] 0.001). P. algirus, however, crossed sunny areas while moving (Table 3) in a proportion almost coincident with the availability of ground surface exposed to sun (35.6%; t = 0.079, P = 0.937).
Selected body temperatures and thermoregulatory set points
Selected [T.sub.b] was significantly higher in A. erythrurus than in P. algirus (P = 0.033; Table 5). Similarly, mean Shade Seeking temperature was also higher in A. erythrurus (P [less than] 0.001; Table 5). Resume Basking temperature, however, did not differ significantly between the two species (P = 0.097; Table 5).
[TABULAR DATA FOR TABLE 5 OMITTED]
Heating and cooling rates
Table 6 summarizes the heating and cooling rates of P. algirus and A. erythrurus, adjusted for body mass and [T.sub.e]. The rate of heat gain increased significantly with [T.sub.e] ([F.sub.1,41] = 326.39, P [less than] 0.001; covariate effect in the corresponding ANCOVA) and decreased with body mass ([F.sub.1,41] = 4.86, P = 0.033) in the pooled sample of the two species. Although the heating rate was significantly higher in P. algirus ([F.sub.1,41] = 11.50, P = 0.002), the regression slope of heating rate vs. [T.sub.e] differed significantly between species (interaction term: [F.sub.1.41] = 11.82, P = 0.001). Regression slope was lower in A. erythrurus (standardized regression coefficients: 0.109 for A. erythrurus and 0.161 for P. algirus). Thus, heating rates increased more rapidly with [T.sub.e] in P. algirus than in A. erythrurus.
The cooling rate was significantly higher in A. erythrurus ([F.sub.1,40] = 13.67, P = 0.001), and it decreased with [T.sub.e] (measured in the shade; [F.sub.1,40] = 7.52, P = 0.009) but not with body mass ([F.sub.1,40] = 0.14, P = 0.714) in the pooled sample of both species. Regression slopes of cooling rates vs. [T.sub.e] did not differ significantly between the two species (interaction term: [F.sub.1,40] = 0.06, P = 0.810).
These results demonstrate the existence of physiological differences in the heat exchange mechanisms of these two species. A. erythrurus warmed more slowly and cooled faster than P. algirus.
Behavior in a thermogradient
Observations of field thermoregulatory behavior were complemented with data collected under controlled and perfectly comparable laboratory conditions to detect subtle interspecific differences in (1) the selection of thermal properties of basking sites, and (2) the trade-off between bask duration and basking rate. Although the percentage of time spent basking did not differ significantly, the two species showed different ways of attaining a given basking time. Mean duration of basking periods was higher in A. erythrurus than in P. algirus, whereas the number of basks per unit time was higher in P. algirus (Table 7). These results modulate the nonsignificant pattern obtained using field data. Within the two zones of the thermogradient available for basking, the percentage of time spent basking in the warmest zone ([T.sub.e] = 58 [degrees] C) was higher in P. algirus, whereas A. erythrurus basked mainly in the [TABULAR DATA FOR TABLE 6 OMITTED] not-so-warm patch ([T.sub.e] = 34.5 [degrees]). P. algirus spent a higher proportion of time in the deep shade areas (the three zones farthest from the light bulb; Table 7).
Thus, behavioral thermoregulation strategies differed between the species. P. algirus basked more often and for shorter periods, but at warmer patches than did A. erythrurus. Alternatively, cooler patches (i.e., areas in deep shade) were visited more often by P. algirus in between-basking activity bouts.
Our results suggest that the observed differences between P. algirus and A. erythrurus reflect a functional interaction between thermoregulatory and movement (foraging) behavior. We will first evaluate such differences and then argue how they combine into strategies that are consistent with the habitat preferences and probable evolutionary history (Arnold 1987, 1989) of these species.
Our analysis of the [T.sub.b] values measured in a thermogradient revealed that A. erythrurus preferred higher temperatures than did P. algirus, since both Selected [T.sub.b] and Shade Seeking [T.sub.b] were higher in the former species. A relatively higher Selected [T.sub.b] in A. erythrurus was also found by Bauwens et al. (1995), using samples from other populations of these species. Moreover, field [T.sub.b] values are higher in A. erythrurus than in P. algirus (Pollo and Perez-Mellado 1989), and information on the thermal sensitivity of sprint speed in these two species shows that both the optimal temperature for sprinting and the critical thermal maximum are higher in A. erythrurus than in P. algirus (Bauwens et al. 1995). Thus, A. erythrurus runs fastest at higher temperatures and tolerates higher temperatures than does P. algirus. These differences are consistent with the [TABULAR DATA FOR TABLE 7 OMITTED] kind of areas in which both genera presumably have evolved: hot, xeric steppes for Acanthodactylus, and Mediterranean open forests with lower [T.sub.e] values for Psammodromus (Arnold 1973, 1983, 1989, Salvador 1982, Perez-Mellado 1992).
Nevertheless, Resume Basking [T.sub.b] was statistically indistinguishable between the two species. This could be due to the fact that small variations in [T.sub.b] have less pronounced effects on organismal performance at low than at high [T.sub.b], since performance curves are asymmetrically skewed toward low [T.sub.b] (Huey and Stevenson 1979, Huey 1982, Huey and Kingsolver 1989). According to the data in Bauwens et al. (1995), the Resume Basking [T.sub.b] values of both species were within the temperature range allowing lizards to run at [greater than or equal to]80% of their maximal sprint capacity. Specifically, they fell within the broad, flat zone of the thermal sensitivity curve below the thermal optimum for sprinting. Shade Seeking [T.sub.b] values were also within the 80% thermal performance breadths of both species. However, the Shade Seeking [T.sub.b] of P. algirus was somewhat higher than its optimal temperature for sprinting (34.3 [degrees] C), whereas that of A. erythrurus was almost coincident with its thermal optimum for sprinting (38.0 [degrees]). It is, therefore, not surprising that both species differed in their Shade Seeking [T.sub.b] values (upper set points of temperature regulation).
Heating and cooling rates were also different in the two species. A. erythrurus warmed more slowly and cooled faster than P. algirus. A proximate cause for the relatively lower heating rate in A. erythrurus could be its higher reflectance due to a paler coloration (Norris 1967, Porter 1967, Pearson 1977). The darker coloration of P. algirus, conversely, could favor a more rapid absorption of solar radiation in its forest, sun-shade patchy habitat, and facilitate a rapid elevation of [T.sub.b] after longer stays in the shade. Reflectance curves for both species would be needed to test these ideas in an appropriate biophysical model.
The low heating rate of A. erythrurus and its relatively low increase with increasing [T.sub.e] levels, could be seen as physiological traits favoring thermoregulation in hot, xeric habitats with low vegetation cover. A shuttling heliotherm chasing prey in open, sunny areas would need a relatively low heating rate to prolong the time spent within its preferred thermal range without being forced to shuttle continuously between sun and shade. This would allow lizards to ambush prey while motionless in the sun. On the other hand, the fast cooling rate of A. erythrurus would allow a rapid readjustment of [T.sub.b] if it surpassed the preferred thermal range, which might occur accidentally in hot, sparsely vegetated environments. The selection of basking site thermal properties also seemed consistent with inter-specific differences in heat exchange rates. Thus, in a laboratory thermogradient, P. algirus basked more often in the warmest end, which was avoided by A. erythrurus. These results show a pattern of basking site selection that is consistent with high-temperature avoidance in hot environments (Bradshaw 1986).
Our data suggest a complex set of interactions among preferred [T.sub.b] levels, rates of heat gain and heat loss, and selection of basking sites that has led to different behavioral and physiological solutions for regulating [T.sub.b] in contrasting thermal environments. The two patterns found in these two species are: (1) a lower preferred [T.sub.b], a lower tolerance of maximum [T.sub.b] values, a faster heating rate, a slower cooling rate, and a selection of basking sites with higher temperatures in the forest-dwelling species (P. algirus); and (2) the opposite for all these variables in the species inhabiting warm Mediterranean areas with low vegetation cover (A. erythrurus).
Movement rate (moves per minute) and percentage time moving, which are usually viewed as indices of foraging intensity in lizards (Huey and Pianka 1981, McLaughlin 1989), differed significantly between A. erythrurus and P. algirus. Locomotor capacities shown by these two species are also consistent with previous results on the physiological correlates of foraging modes. Thus, Huey et al. (1984) found that sit-and-wait lacertids from the Kalahari usually had relatively high sprint speeds. Accordingly, maximal sprint speed is higher in A. erythrurus than in P. algirus (Bauwens et al. 1995). Our choice of species seems appropriate for a conservative test of the covariation of thermo-regulation and movement intensity, as interspecific differences in movement behavior were significant but relatively small.
Our data suggest that the thermal consequences of inhabiting a certain type of habitat can be counterbalanced by behavioral and physiological means that, in turn, affect movement (and, hence, foraging) behavior. Shuttling heliothermy involves movements between sun and shade (Cowles and Bogert 1944), but these movements, and interspersed periods of stationary basking, can vary both in frequency and duration (Spellerberg 1972, Diaz 1991, Carrascal et al. 1992). At the same time, a heliothermic forager should select where and how long to stay in different thermal patches while searching for food, in order to maintain its [T.sub.b] within its optimal performance range (Huey and Stevenson 1979, Avery et al. 1982, Huey 1982, Van Damme et al. 1991).
In the laboratory thermogradient, P. algirus (the more mobile species) basked more often, but for shorter periods and at warmer patches, than did A. erythrurus. For P. algirus, which moves [approximately equal to] 20% of its activity time, and may experience relatively low [T.sub.e] in the deep shade of forest habitats, accurate thermoregulation would require an efficient selection of basking sites for rapid warming. This would compensate for relatively long periods of searching in the shade. Our results are consistent with these suggestions, both in the lab thermogradient (where P. algirus selected the warmest end for basking and spent longer times in the cool end) and in the field (where its time spent moving was randomly distributed with respect to sun and shade). This strategy would be enhanced by the physiological traits noted, and it would be favored in thermally heterogeneous environments such as the broad-leaved forests preferred by P. algirus (Diaz and Carrascal 1991). Moreover, heating and cooling rates in P. algirus become equal after the early period of morning warm-up, and this coincidence gives rise to a higher frequency of shorter basking periods (Diaz 1991). Thus, sustained locomotion may be required to maintain [T.sub.b] levels within the preferred thermal range, even if movements are random with respect to sun and shade (Carrascal and Diaz 1989) and are simultaneously used for food searching.
On the other hand, scarcity of protective cover, escape abilities of fast-moving prey, and/or high predation risk in xeric shrubsteppes would promote the evolution of high maximum speeds, high physiologically optimal temperatures for sprinting, and high preferred temperatures (Bauwens et al. 1995). This would explain the higher Shade Seeking and Selected [T.sub.b] values shown by A. erythrurus, which is the fastest of the 13 lacertid species examined by Bauwens et al. (1995). Selection of not-too-hot basking sites and relatively low heating rates would help A. erythrurus to counteract environmental heat loads and to retard exceeding its preferred [T.sub.b] levels. The negative correlation between movement rate and operative temperature found in A. erythrurus [ILLUSTRATION FOR FIGURE 1 OMITTED] suggests that, in this species, extreme sit-and-wait behavior may function as a heat avoidance strategy. In fact, the variance of moving rates was significantly higher in A. erythrurus than in P. algirus. This asymmetrical distribution of variation in the amount of searching movements, with higher flexibility in the less active forager, is consistent with the results reported by Pietruszka (1986; but see Huey and Pianka 1981).
In summary, results of this study provide empirical evidence that thermoregulation and foraging mode should not be regarded as isolated tasks but as interacting behaviors, strongly dependent one on each other and giving rise to patterns of association that are coherent on functional grounds. However, we do not intend to test whether or not the traits studied are integrated in adaptive syndromes, because of the inherent limitations of comparing only two species from different habitats (see Garland and Adolph 1994). An obvious alternative to the adaptive-syndrome hypothesis could be, for instance, that all differences in thermal biology reflect ancestry in different habitats, and are evolutionarily independent of foraging mode. Our approach lacks the historical perspective that is needed to discriminate between these hypotheses. The generality of the patterns described in this paper could be tested in future studies that should compare additional species of this or unrelated lizard clades. A multispecies, explicitly phylogenetic approach (Huey 1987, Harvey and Purvis 1991, Garland et al. 1992) would lead to the detection of rates and directions of evolutionary change in both thermal biology and foraging mode, thus allowing discrimination between (co)adaptive and independent-evolution hypotheses (Huey 1987). Such an approach should complete the synthesis attempted here of two areas of lizard ecology that have traditionally been treated as separate, but that clearly are related.
We thank Dirk Bauwens, Ray Huey, David C. Smith, and two anonymous reviewers for constructive comments on previous drafts or for enlightening discussion. Nino gave us valuable laboratory assistance. Final preparation of the manuscript benefited from a stay of J. A. Diaz at the Institute of Nature Conservation (Hasselt, Belgium) that was funded by the Universidad Complutense of Madrid. This study was partially granted by DGYCIT project PB92-0044-C02-01, and is a contribution to the DGYCIT project PB92-0238. This paper is a contribution to the "El Ventorrillo" Field Station of the Museo Nacional de Ciencias Naturales (CSIC).
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|Author:||Belliure, Josabel; Carrascal, Luis M.; Diaz, Jose A.|
|Date:||Jun 1, 1996|
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