Robin M. Andrews

Metabolism of Squamate Reptiles: Allometric and Ecological Relationships

We used multiple regression analysis to evaluate the relationship between metabolic rate and three independent variables-mass, temperature, and standard or resting state-for squamate reptiles. For comparisons among adults of different species, mass raised to the .80 power explains 88% of the variation in metabolic rate. (The .80 mass exponent is significantly greater than the .75 predicted by theoretical considerations.) A further 8% of the variation in metabolic rate is explained by body temperature and whether the lizard is in a standard or resting metabolic state. Residuals were used to determine whether metabolic rates varied as a function of phylogenetic relationship or ecological grouping. Familial associations explained 16% of the variation in metabolic rate for varanids, lacertids, iguanids, colubrids, scincids, xantusiids, gekkonids, and boids. More variation (45%) was explained when lizards were partitioned into four ecological categories: day-active predators, hervibores, reclusive predators, and fossorial predators. A single equation relating metabolic rate to mass is thus inappropriate to estimate the metabolism of squamates. For intraspecific comparisons, the mass exponents of the relationship between metabolic rate and mass are significantly lower than .80 for 25 of 28 data sets. Estimating the metabolic rates of juvenile squamates from equations based on comparisons among species is thus invalid. Moreover, there is significant variability among mass exponents among the 14 species that met the statistical requirements for analysis of covariance, and a common mass exponent cannot be assumed for intraspecific comparisons.

EFFECT OF INCUBATION TEMPERATURE ON MORPHOLOGY, GROWTH, AND SURVIVAL OF JUVENILE SCELOPORUS UNDULATUS

Incubation temperature affects a wide range of phenotypic traits of hatchling rep- tiles. The main objective of this research was to determine if such phenotypic traits persist long enough in the field to have an effect on fitness. Eggs of Sceloporus undulatus lizards were incubated at six temperature regimes, five constant and one fluctuating, with means ranging from 23-33 C. Hatchlings were measured and their subsequent morphology, growth, and survival were monitored for 7-9 months, one to two months before individuals reached adult size. Phenotypic traits of lizards that hatched at the field site were used for comparative purposes. Morphological traits persisted for 7-9 mo. In contrast, growth rates did not differ among incubation temperature treatments after individuals were released in the field. Overall, 29 (27%) of 107 individuals that were released survived to the spring following hatching, and individuals from eggs incubated at the lowest tem- perature had higher survival than individuals from all other groups. The phenotypes of lizards incubated at intermediate temperatures tended to be most similar to those of field hatched lizards. We rejected two predictions about phenotypic responses to incubation temperature. The first pre- diction was that extreme incubation temperatures would be associated with the most deviant phe- notypes. Observed phenotypic responses to temperature were either linear or, only one extreme temperature produced a deviant phenotype. The second prediction was that hatchlings incubated at warm temperatures and that hatched early in the season would have higher survival in general and higher overwinter survival in particular than hatchlings incubated at cool temperatures and that hatched later in the season. The reverse was true; observed survival was greatest for hatchlings from the coolest incubation treatment that hatched last.

Cold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus

Evolutionary origins of viviparity among the squamate reptiles are strongly associated with cold climates, and cold environmental temperatures are thought to be an important selective force behind the transition from egg-laying to live-bearing. In particular, the low nest temperatures associated with cold climate habitats are thought to be detrimental to the developing embryos or hatchlings of oviparous squamates, providing a selective advantage for the retention of developing eggs in utero, where the mother can provide warmer incubation temperatures for her eggs (by actively thermoregulating) than they would experience in a nest. However, it is not entirely clear what detrimental effects cold incubation temperatures may have on eggs and hatchlings, and what role these effects may play in favouring the evolution of viviparity. Previous workers have suggested that viviparity may be favoured in cold climates because cold incubation temperatures slow embryogenesis and delay hatching of the eggs, or because cold nest temperatures are lethal to developing eggs and reduce hatching success. However, incubation temperature has also been shown to have other, potentially long-term, effects on hatchling phenotypes, suggesting that cold climates may favour viviparity because cold incubation temperatures produce offspring of poor quality or low fitness. We experimentally incubated eggs of the oviparous phrynosomatid lizard, Sceloporus virgatus, at temperatures simulating nests in a warm (low elevation) habitat, as is typical for this species, and nests in a colder (high elevation) habitat, to determine the effects of cold incubation temperatures on embryonic development and hatchling phenotypes. Incubation at cold nest temperatures slowed embryonic development and reduced hatching success, but also affected many aspects of the hatchlings’ phenotypes. Overall, the directions of these plastic responses indicated that cold-incubated hatchlings did indeed exhibit poorer quality phenotypes; they were smaller at hatching (in body length) and at 20 days of age (in length and mass), grew more slowly (in length and mass), had lower survival rates, and showed greater fluctuating asymmetry than their conspecifics that were incubated at warmer temperatures. Our findings suggest that cold nest temperatures are detrimental to S. virgatus, by delaying hatching of their eggs, reducing their hatching success, and by producing poorer quality offspring. These negative effects would likely provide a selective advantage for any mechanism through which these lizards could maintain warmer incubation temperatures in cold climates, including the evolution of prolonged egg retention and viviparity.

Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity

Viviparity in squamate reptiles is presumed to evolve in cold climates by selection for increasingly longer periods of egg retention. Longer periods of egg retention may require modifications to other reproductive features associated with the evolution of viviparity, including a reduction in eggshell thickness and clutch size. Field studies on the thermal and reproductive biology of high (HE) and low (LE) elevation populations of the oviparous lizard, Sceloporus scalaris, support these expectations. Both day and night-time temperatures at the HE site were considerably cooler than at the LE site, and the activity period was 2 h shorter at the HE than at the LE site. The median body temperature of active HE females was 2°C lower than that of LE females. HE females initiated reproduction earlier in the spring than LE females, apparently in order to compensate for relatively low temperatures during gestation. HE females retained eggs for about 20 days longer than LE females, which was reflected by differences in the degree of embryonic development at the time of oviposition (stages 35.5–37.0 versus stages 31.0–33.5, respectively). These results support the hypotheses that evolution of viviparity is a gradual process, and is favored in cold climates. Females in the HE population exhibited other traits consistent with presumed intermediate stages in the evolution of viviparity; mean eggshell thickness of HE eggs (19.3 μm) was significantly thinner than that of LE eggs (26.6 μm) and the size-adjusted clutch sizes of HE females (9.4) were smaller than those of LE females (11.2).

Effects of Reproductive Condition, Season, and Site on Selected Temperatures of a Viviparous Gecko

The relationship between thermal and reproductive biology is complex and poorly understood. We measured selected body temperatures (Tsel) for the viviparous gecko Hoplodactylus maculatus. Tsel was compared among pregnant females, nonpregnant females, and males from two sites: a cool site with biennially reproducing geckos and a warm site with annually reproducing geckos. Tsel was measured at five times of day during three seasons and compared with microhabitat temperature (Ttop) and field body temperature (Tb). Tsel varied with time of day in all comparisons, and the effect of reproductive condition on Tsel differed between sites and seasons. At both sites, when Tsel differed between reproductive conditions, pregnant females had higher Tsel than nonpregnant females and males. Stage of pregnancy affected the degree of elevation of Tsel. Measurements of microhabitat temperature and field Tb showed that, even in the warmest season, geckos rarely had the opportunity to achieve Tsel at the cool site but were able to do so at the warm site. The elevation of Tsel with pregnancy is extreme in this species (up to 8°C), which suggests that an increase in Tb is critical to successful reproduction. Interactions between the effects of time of day, season, and reproductive condition on Tsel must be considered in the assessment of thermoregulation in reptiles.

Evolution of Viviparity: Constraints on Egg Retention

Extended egg retention is an important component of the cold climate model for the evolution of viviparity in squamate reptiles. The presumptive selective benefits of extended egg retention are that (1) eggs retained in utero are subject to a warmer thermal environment than those laid in nests, and (2) embryonic development in utero is faster than embryonic development in nests as a result of these temperature differences. We tested these assumptions with observations on the montane lizard, Sceloporus virgatus. We measured the diel temperature cycles of gravid females and of nest sites in the field and contrasted the embryonic development of eggs laid at the normal time and eggs retained for an additional 13 d, 20 d, and 30 d in laboratory experiments. The mean temperatures of gravid females and of nest sites were very similar at 25.4° and 25.2°C, respectively. Thus, egg retention did not alter the thermal environment of developing embryos of S. virgatus. Moreover, embryonic development was retarded by egg retention; embryos from retained eggs were smaller and less differentiated than control eggs. Egg retention also lengthened the incubation period from 57 d for eggs laid at the normal time to 65 d, 66 d, and 71 d for eggs retained 13 d, 20 d, and 30 d, respectively. Thus, egg retention reduces the time available for hatchlings to grow prior to winter and delays sexual maturation.

Energy costs of subduing and swallowing prey for a lizard

We measured the oxygen consumption (aerobic energy cost) and lactic acid production (anaerobic energy cost) of scincid lizards, Chalcides ocellatus, eating domestic crickets. Aerobic metabolism accounted for 90% or more of the total energy cost of subduing and swallowing prey. The time required to subdue and swallow a cricket was linearly correlated with oxygen consumption. Oxygen consumption increased as a power function of cricket mass, but the maximum size of crickets swallowed by the lizards was set by morphological rather than by energetic constraints. The energy cost of subduing and swallowing was 0.2—0.4% of the utilizable energy of the cricket eaten. Net energy gain per unit time spent subduing and swallowing prey (e/t) declined monotonically with increasing cricket mass. Because the energy cost of eating is trivial, the shape of the e/t curve is determined by the function relating prey mass to the time required for subduing and swallowing; the energy value of prey was proportional to prey mass, whereas the time required for subduing and swallowing increased faster than prey mass. The energy value of anthropods is so high, relative to the costs for a lizard of pursuring, subduing, and swallowing, that these costs can be ignored for most ecological purposes.

NEST-SITE SELECTION IN RELATION TO TEMPERATURE AND MOISTURE BY THE LIZARD SCELOPORUS UNDULATUS

Development and survival of reptilian embryos are affected by the temperature and moisture within the nest. Moreover, thermal and hydric conditions during incubation also affect phenotypes of hatchlings. Thus, females should select nest sites that enhance hatching success and produce hatchlings with phenotypes fit for the local environment. The objective of this study was to determine the substrate temperature and moisture conditions selected by eastern fence lizards (Sceloporus undulatus) for nesting. In the laboratory, gravid females were housed in a large enclosure that provided suitable nesting substrate. Gradients of temperature and moisture within the substrate were established to provide a wide range of conditions from which females could choose. Fifteen (65%) females selected nest conditions within the moisture and temperature range that results in successful embryonic development. Two females (9%) nested in extremely dry conditions, and six females (26%) oviposited on the substrate surface. Females that nested in the field selected nest sites with similar conditions as females that nested in the laboratory. In general, we provide support for the idea that females choose nest sites with thermal and hydric conditions that are associated with positive hatching success.

Low Oxygen: A Constraint on the Evolution of Viviparity in Reptiles

The evolution of reptilian viviparity (live bearing) from oviparity (egg laying) is thought to require transitional stages of increasingly longer periods of embryonic development in utero, that is, longer periods of egg retention by the gravid female. Studies on sceloporine lizards demonstrate that embryonic responses to egg retention that is extended beyond the time of normal oviposition range from developmental arrest to normal development. The present study was designed to test the hypothesis that O2 availability is the proximate factor that determines the rate and degree of development that reptilian embryos undergo in utero. Eggs of Sceloporus undulatus were incubated under conditions of low (LOX), normal (NOX), and high (HOX) oxygen both early and late in development. The LOX treatment consistently had a negative effect on development in terms of embryonic differentiation and growth, length of incubation, egg mortality, and hatchling size. Moreover, the LOX treatment had a stronger negative effect later in development than earlier in development. The results support the hypothesis that limited oxygen availability in utero acts as a developmental constraint. They further indicate that selection for extended egg retention, per se, will not lead to viviparity unless each incremental increase in the duration of egg retention is coupled with selection for traits (e.g., vascularity of oviduct and chorioallantois, hemoglobin oxygen affinity, etc.) that enhance O2 availability to embryos. Such selection would be the most efficacious in cold climates where the effects of hypoxia would be the least likely to limit embryonic development.

Population Stability of a Tropical Lizard

Populations of the lizard Anolis limifrons were censused for 19 yr at the Lutz site on Barro Colorado Island (BCI) and for 4 yr at 20 additional sites in central Panama. Census data provided estimates of population density at the end of the wet season (December) and indices of per-capita food intake and annual recruitment. Year-to-year changes in density of as much as 5- to 8-fold were observed at Lutz over 19 yr and of 2- to 3-fold were observed over 4 yr at other sites. Changes in population density at 11 BCI sites were synchronous over 1983-1986, while population density fluctuated independently at non-BCI sites. Populations of A. limifrons exhibited significantly greater generation-to- generation variability than populations of West Indian Anolis and of lizards in temperate- zone habitats (mostly arid lands in North America). An index of per-capita food intake was negatively related to density both for temporal comparisons at Lutz and for spatial comparisons among sites. The relative number of young individuals at the end of the wet season was negatively related to population density and positively related to an estimate of food intake. Partial correlations indicated that the positive association between the relative number of young individuals in the population and food intake was independent of the negative association between food intake and population density. Recruitment was thus depressed when density was high and enhanced when food was relatively abundant. Despite the potential for density-dependent regulation, Anolis limifrons populations are highly unstable, presumably because of random perturbations of the environment. Rainfall is implicated causally although population density was only weakly associated with rain- fall-density at BCI was positively associated with rainfall during the dry season and negatively associated with rainfall during the wet season and with total annual rainfall. Population attributes that contribute to instability are rapid population turnover and a middle-level trophic position in a complex food web.