Repeatability of Individual Differences in Locomotor Performance and Body Size During Early Ontogeny of the Lizard Sceloporus Occidentalis (Baird & Girard)

The demonstration of repeatability of relative body size and of locomotor performance in growing lizards is relevant to the functional and genetic basis of these traits as well as to an understanding of how they are influenced by natural selection. Relative locomotor performance of hatchlings was strongly repeatable among body temperatures (28, 33 and 370C). We estimated the repeatabilities of individual differences in locomotor performance (speed, stamina) and body size (mass, snout-to-vent length, 'condition' index) for free-ranging lizards (Sceloporus occidentalis [Baird & Girard]) over three time intervals between near hatching and 13 months of age, during which time the lizards increased in body mass by an order of magnitude. Relative locomotor performance and body size were significantly repeatable between adjacent censuses, even across the winter hibernation period and over periods of rapid growth. However, these traits (especially body size) were usually not significantly repeatable over long time intervals, in part because of small sample sizes of recaptured animals. Even so, stamina of 2-week-old lizards predicted their stamina over a year later. These patterns generally held even when the confounding effects of body size were controlled. Studies of natural selection on performance and on body size of growing lizards should be restricted to short-term intervals. Key-words: Repeatability, thermal biology, locomotion, body size, lizard, natural selection, ontogeny, performance * Present address: Dr F.H. van Berkum, Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, USA. t Present address: Dr T. Garland, Jr, Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706, USA. Introduction Repeatability is an important statistical concept that quantifies the stability of a phenotypic trait within individuals, relative to differences in that trait among individuals (Bulmer, 1980; Falconer, 1981; Lessells & Boag, 1987). If repeated measurements of a given individual are very similar relative to the differences among individuals, then repeatability is high; if measurements within individuals are very different, then repeatability is low. Repeatability is particularly useful in assessing the gain in precision achieved by making multiple measurements of individuals, in evaluating the precision of a given type of measurement, in establishing the degree of individuality, and in determining the upper bound on heritability (Bennett, 1980, 1987; Bulmer, 1980; Falconer, 1981; Arnold & Bennett, 1984; Wells & Taigen, 1984; Herzog & Burghardt, 1988). Repeatability is also valuable in predicting the ontogenetic consistency of individuals (Tolley, Notter & Marlowe, 1983; Huey & Dunham, 1987) and in placing bounds on the appropriate time limit for studying natural selection on phenotypic traits (sensu Huey & Dunham, 1987). Thus, for many analyses of individual variation (Bennett, 1987), estimation of repeatability should be a key first step. As part of a study of natural selection on speed, stamina, and body size of the lizard Sceloporus occidentalis (Baird & Girard) in nature, we here analyse the long-term repeatability of these traits during these lizard's first year of life a substantial fraction of their ecological lifespan. We also examine the repeatability of locomotor performance measured at different body temperatures, thereby establishing if the relative performance of an individual is stable even at different body temperatures (Bennett, 1980). Locomoter performance and body size are ecologically-relevant traits (Huey & Stevenson, 1979; Arnold, 1983) that potentially influence fitness by affecting feeding success (Greenwald, 1974; Webb, 1986), escape 98 from predators (Christian & Tracy, 1981; Huey & F. H. van Hertz, 1984a; Ferguson & Fox, 1984) and social Berkum et al. dominance (Rand, 1964; Regal, 1971; Trivers, 1976). Body temperature is a key physiological variable that has a profound influence on all aspects of ectotherm physiology, including locomotion (Dawson, 1975; Bennett, 1980; Avery, Bedford & Newcombe, 1982; Huey, 1982). We address three main issues: (i) is the relative locomotor performance of an individual stable through time? For example, do individuals with high stamina at birth maintain high stamina later in life? Both speed and stamina of adult lizards are highly repeatable in the laboratory (Bennett, 1987) and in the field (Huey & Dunham, 1987). However, the repeatability of performance during early ontogeny when lizards are growing rapidly has not been examined previously. (ii) Are the relative body size and 'condition' index (mass113/snout-to-vent length) of an individual repeatable during early ontogeny? That is, do individuals that are large at hatching also remain relatively large later in life? To our knowledge, the long-term repeatability of body size in natural populations has been documented only in birds (Smith & Zach, 1979; Boag, 1983; Price & Grant, 1984; Smith, Arcese & Schluter, 1986). (iii) Is the relative locomotor performance of an individual hatchling consistent at different body temperatures? In other words, is an individual that is relatively fast at one body temperature (Tb) also relatively fast at other body temperatures? This appears to be the case in several previous studies, including one of adult S. occidentalis (Bennett, 1980; Huey & Hertz, 1984a; Huey & Dunham, 1987). We have examined the repeatability of performance and size in S. occidentalis, a semi-arboreal iguanid lizard that lives in a variety of habitats in western North America from Mexico to Washington state. At our study area in south-central Washington, the lizards are abundant in an open oak-pine forest, where they are active on logs, trees, and under small shrubs. They breed in the late spring, hatchlings are born in July and August and the lizards hibernate from about September (adults) or October (hatchlings) through April. Sexual maturity is not reached until the second or perhaps third year. They are 'sit-and-wait' foragers and eat a variety of arthropods. Materials and methods Hatchlings used in this study came from the Tuthill Ranch, Klickitat County, Washington (under permit from the Department of Wildlife). Some ('lab-reared', n = 296) were raised from eggs laid in the laboratory (summer 1985) and then released on 19 August 1985 (average 23 days of age, range 19 to 28 days) in groups of eight to 10 (randomized with respect to sibship) onto marked sites in a study area near where the dams were originally captured. Methods of obtaining and incubating eggs and of maintaining lab-reared hatchlings are detailed elsewhere (Tsuji et al., in preparation). Several field-reared hatchlings, collected on 22 August 1985, were used in the studies of thermal repeatability of speed (n = 23) and of stamina (n = 18). A few other field-reared hatchlings (n = 17) were collected at this time for baseline estimates of body size and of speed, and these lizards were released on 24 August 1985. Finally, other field-reared hatchlings were captured on the same study area during subsequent recaptures of the lab-reared hatchlings (see below). Before all sets of racing trials, we noted sex, snout-to-vent length (SVL), body mass, and tail status (complete tail, freshly broken, or regenerating). Subsequently, we calculated a 'condition' index, as mass113/SVL, for those individuals possessing a complete, original tail. (This index is frequently used as a measure of condition, e.g. body fatness. However, it does not differentiate between fatness and stockiness and thus the index may be better considered as a general measure of body stockiness.) These data enabled us to examine repeatability of size and condition as well as to check for allometric and sex effects on locomotor performance (see below). Measuring locomotor performance Maximal speed was determined by chasing hatchlings along a computerized, 1.2-m racetrack (Huey et al., 1981) with vertical photocell stacks at 0 1-m intervals. Body temperature was maintained at 33-340C, near the mean activity temperature of these lizards (Tsuiji, 1986). At each census, individual lizards were run four times with a one-hour rest between races and an individual's maximum speed was assessed as the single fastest speed among all 0 2-m intervals. By the August 1986 census, the lizards were nearly adult size; hence the length of the racetrack was increased to 2m (0.25m between photocells) for the final census (maximum speed determined among all 0 5-m intervals). 99 Stamina was indexed as the total time a lizard Repeatability of could maintain station while running slowly on performance the moving belt (initially at 0 225km h-1, see below) of a motorized treadmill. At each census we increased the treadmill speed slightly (0.275km h-1 in October 1985, 0-3km h-1 in May 1986, 0 3km h-1 in August 1986) to reflect probable ontogenetic shifts in stamina (Pough, 1983; Garland & Else, 1987). To minimize stress, stamina was measured only once per census or per temperature. The persons conducting the performance trials could not be the same at all censuses. (For speed, the sequence for the five censuses was FHvB, FHvB, FHvB, RBH, RBH; and for stamina, RBH, RBH, RBH, TG, RBH.) The calculated repeatabilities should thus be underestimates of the true repeatabilities. Temporal repeatability Speed and stamina (see below) of the lab-reared hatchlings were initially assessed twice prior to release (8-17 August 1985). Speed was determined first when lizards averaged 13 days old (range 12-15) and then 19 (18-21) days old, whereas stamina was measured when they averaged 16 (15-18) and 21 (20-23) days old. We recaptured and remeasured hatchlings on three occasions spread over a year (28 September7 October 1985 = 'October census'; 20-25 May 1986 = 'May census'; 23-27 August 1986 = 'August census'). During each recapture, we also caught some field-reared hatchlings and measured their size and performance. Lizards were probably hibernating for most of the time between the October and May censuses. However, because they did grow during that time (Table 1), they could not have been hibernating full time. By the last recapture hatchlings were about 13 months old. Between the October and May censuses, about one-third of our study area was cleared for cattle pasture. This contributed to the low recapture rates in 1986. Thermal repeatability Speed (n = 23 individuals) and then stamina (n = 20) were measured at a randomized sequence of body temperatures (33, 28 and 370C). The two extreme temperatures bound almost all Tb records of active adult lizards at this site, and 33 0C approximates their mean activity temperature (Tsuji, 1986). Calculating repeatability Repeatability is traditionally estimated using the intra-class correlation coefficient (Falconer, 1981; Lessells & Boag, 1987). However, this coefficient is inappropriate for growing animals as it is very sensitive to changes in the average values of traits (Bulmer, 1980; Falconer, 1981; C. Janson, personal communication). Accordingly, we estimate temporal repeatability using the inter-class correlation coefficient (Pearson's r). (When repeatability is measured over a single time interval, Pearson's r is virtually identical to the traditional intra-class correlation coefficient calculated using covariance-corrected values [Curnow, 1961].) Thus we measure whether relative not absolute performance and size are temporally stable. Because the measurements did not always appear to be bivariate normal, we report significance levels based on a non-parametric test, Kendall's tau (C. Janson, personal communication). We first calculated repeatabilities of two performance measures (sprint speed, stamina) and of three size measures (mass, SVL, condition index). Because body size influences locomotor performance in this species (Tsuji et al., in preparation), significant 'whole-animal' repeatabilities of locomotor performance might be measuring primarily the repeatability of body size. Accordingly, we also calculated size-corrected repeatabilities based on residuals of regressions of In (performance) versus In (SVL) (Huey & Hertz, 1984a). For the lab-reared lizards, we used the two sets of measurements made in the laboratory before field release, to compute an initial 'in lab' repeatability. Then, to calculate repeatabilities between laboratory and field, we selected the higher of two laboratory performance measurements and the final size measurement as the laboratory base line. Because a broken tail may influence locomotor performance (E.N. Arnold, 1987), we calculated whole-animal repeatabilities twice (once only for lizards with complete tails and once for all lizards). However, we excluded lizards with broken tails from repeatabilities involving the body size measurements or size-corrected performances. We computed separate repeatabilities for males, females, lab-reared, and field-reared lizards. However, these repeatabilities were always homogeneous (Sokal & Rohlf, 1981, pp. 588-589) and were similar in magnitude to the pooled repeatabilities (i.e. all animals combined), so we report only pooled repeatabilities. 100 Results F. H. van Berkum et al. Patterns of temporal change Between the initial (age about 2 weeks, early August 1985) and final censuses (age about 13 months, August 1986), the lizards doubled in length and increased in body mass by an order of magnitude (Table 1). Most of this growth occurred between the last two censuses (May to August 1986). Males and females were not significantly different insize until the last census, when males were slightly longer and heavier on average than females (Table 1). During their first summer, field-reared hatchlings averaged slightly longer and heavier than lab-reared hatchlings (Table 1). Whether this reflects older age or better rearing conditions of field-reared hatchling cannot be determined. In any case, differences in size disappeared by the end of the winter hibernation. Average speed increased by about 50% during the study. Males and females had similar speeds in all but the last census, when males were slightly faster than females. This difference in speed holds even when the effects of body size are removed (ANCOVA, SVL as covariate, P < 0.001). Laband field-reared lizards had similar speeds in most censuses (Table 1). Because treadmill-speed was adjusted as the lizards aged (see materials and methods), the average increase in stamina during the first year of life cannot be determined. However, males and females had similar stamina throughout the study, and field-reared lizards had slightly higher stamina than lab-reared lizards (ANCOVA, SVL as covariate, P < 0 05) until the final census. Repeatability of performance and of size For the two initial laboratory trials (see materials and methods), both speed (r = 0 45, P < 0 001, n = 298) and stamina (r = 0-65, P < 0 001, n = 295) were significantly repeatable. These values, taken only a few days apart, may be interpreted as measures of how accurately we can quantify individual differences at a single time near Table 1. Locomotor performance and body size of S. occidentalis at several censuses. Units X(?95% CI, sample size in parenthesis) are for SVL = snout-to-vent length (mm), mass (g), speed (m sow) and stamina (s). Only lizards that were recaptured at least once and that had complete tails are included.