Thermal constraints on embryonic development as a proximate cause for elevational range limits in two Mediterranean lacertid lizards

Local adaptation and range restrictions in alpine environments are central topics in biogeographic research with important implications for predicting impacts of global climate change on organisms. Temperature is strongly coupled to elevation and greatly affects life history traits of oviparous reptiles in mountain environments. Thus, species may encounter barriers for expanding their ranges if they are unable to adapt to the changing thermal conditions encountered along elevational gradients. We sought to determine whether thermal requirements for embryonic development provide a plausible explanation for elevational range limits of two species of lacertid lizards that have complementary elevational ranges in a Mediterranean mountain range (Psammodromus algirus is found at elevations below 1600 m and Iberolacerta cyreni is found at elevations above 1600 m). We combined experimental incubation of eggs in the laboratory with modelled estimates of nest temperature in the field. In both species, increasing temperature accelerated development and produced earlier hatching dates. The species associated with warmer environments (P. algirus) experienced an excessive hatching delay under the lowest incubation temperature. Moreover, newborns from eggs incubated at low temperatures showed poor body condition and very slow rates of postnatal growth. In contrast, eggs of the strictly alpine species I. cyreni exhibited shorter incubation periods than P. algirus that allowed hatching before the end of the active season even under low incubation temperatures. This was countered by lower reproductive success at higher temperatures, due to lower hatching rates and higher incidence of abnormal phenotypes. Elevational range limits of both species coincided well with threshold temperatures for deleterious effects on embryonic development. We suggest that incubation temperature is a major ecophysiological factor determining the elevational range limits of these oviparous lizards with predictable consequences for mountain distributions under future warmer climates.     

Incubation Temperature Effects on Hatchling Performance in the Loggerhead Sea Turtle (Caretta caretta)

Incubation temperature has significant developmental effects on oviparous animals, including affecting sexual differentiation for several species. Incubation temperature also affects traits that can influence survival, a theory that is verified in this study for the Northwest Atlantic loggerhead sea turtle (Caretta caretta). We conducted controlled laboratory incubations and experiments to test for an effect of incubation temperature on performance of loggerhead hatchlings. Sixty-eight hatchlings were tested in 2011, and 31 in 2012, produced from eggs incubated at 11 different constant temperatures ranging from 27°C to 33°C. Following their emergence from the eggs, we tested righting response, crawling speed, and conducted a 24-hour long swim test. The results support previous studies on sea turtle hatchlings, with an effect of incubation temperature seen on survivorship, righting response time, crawling speed, change in crawl speed, and overall swim activity, and with hatchlings incubated at 27°C showing decreased locomotor abilities. No hatchlings survived to be tested in both years when incubated at 32°C and above. Differences in survivorship of hatchlings incubated at high temperatures are important in light of projected higher sand temperatures due to climate change, and could indicate increased mortality from incubation temperature effects.     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

孵化温度对王锦蛇胚胎代谢和幼体适合度的影响

孵化温度所驱动的爬行动物的表型变异是生理生态学研究的热点。本研究以王锦蛇(Elaphe carinata)为实验动物,检验了24℃和28℃孵化温度对王锦蛇胚胎代谢速率、孵化过程中的卵重量、孵出幼体代谢和行为的影响。研究结果显示:卵重和胚胎的呼吸代谢均与孵化时间呈正相关;28℃下胚胎代谢速率大于24℃;幼蛇孵出15 d内体重随着生长时间的延长而减小,24℃孵出幼体的代谢速率大于28℃孵出幼体,两温度下孵出幼体的呼吸代谢速率和生长时间无显著关系;28℃孵出幼体的疾游速和吐信频次均大于24℃;两孵化温度孵出幼体的选择体温无显著差异,但在消耗完体内的剩余卵黄后28℃孵出幼体有60%的个体摄食,而24℃孵出幼体无摄食个体。总体而言,王锦蛇28℃孵出幼体适合度优于24℃孵出幼体。     

Fluctuations in incubation temperature affect incubation duration but not morphology,locomotion and growth of hatchlings in the sand lizard Lacerta agilis (Lacertidae)

Li, H., Zhou, Z.‐S., Ding, G.‐H. and Ji, X. 2011. Fluctuations in incubation temperature affect incubation duration but not morphology, locomotion and growth of hatchlings in the sand lizard Lacerta agilis (Lacertidae). —Acta Zoologica (Stockholm) 00 : 1–8. Studies looking for potential effects of temperature and temperature fluctuations on phenotypic traits of reptile hatchlings have shown species variation, but have not always allowed a distinction between effects of fluctuation per se and temperature extremes themselves. To examine whether incubation temperature fluctuation has a key role in influencing the phenotype of offspring, we incubated eggs of the sand lizard Lacerta agilis at one of the four temperature regimes (27, 27 ± 2, 27 ± 4 and 27 ± 6 °C). We found that: (1) hatchlings incubated under the four temperature regimes did not differ from each other in any of the morphological and physiological traits examined; (2) interactions that included temperature treatment did not affect any trait examined; (3) the mean incubation length was longer in the 27 ± 6 °C treatment than in the other three treatments; and (4) female hatchlings were shorter in head length and width but longer in snout‐vent length as well as abdomen length than males derived from the same‐sized egg. Our data show that both the type and the magnitude of temperature variation can affect incubation length. We found no evidence for phenotypic divergence in responses to temperature fluctuations during incubation and therefore suggest that temperature variation does not affect the phenotype of hatchlings in L. agilis.     

The role of climate in constraining the elevational range of the Water Pipit Anthus spinoletta in an alpine environment

The study of determinants of species’ ranges along elevational gradients may shed light on the ecological factors that constrain their distribution and fundamental niche. We analysed the influence of the climate, habitat at different spatial scales and topography on Water Pipit Anthus spinoletta density in mountain landscapes across a wide elevational gradient. Variables associated with spring and annual temperature values were the main determinants of Water Pipit density, especially at the lower distributional limit (700–1200 m asl), where the species avoided warmer areas. At high‐elevation sites (1600–2300 m asl), the main constraint to the species’ distribution was habitat structure and composition, with steep rocky areas being avoided. Highest densities were found in open but locally heterogeneous habitat at intermediate to high elevations, and the habitat variables that played a major role at the landscape scale were medium‐tall shrublands and woodlands, but with contrasting effects depending on elevation. These results suggest that different sets of variables may constrain density, and effects may differ at the upper and lower elevational limits, with climate being more important at lower elevations and local habitat more important at higher elevations. Ongoing global warming is likely to cause an upward shift in range boundaries of alpine species, but local habitat features could constrain the upward expansion, resulting in range contractions accompanying range shift.     

Incubation temperature affects hatching success,embryonic expenditure of energy and hatchling phenotypes of a prolonged egg-retaining snake,Deinagkistrodon acutus (Viperidae)

We used eggs of Deinagkistrodon acutus to study the effects of incubation temperature on hatching success, embryonic expenditure of energy and hatchling phenotypes. One egg from each of the 15 fertile clutches was dissected for determination of egg composition, and a total of 164 eggs were incubated at five constant temperatures. Embryonic mortality increased dramatically at 30 °C, and none of eggs incubated at 32 °C hatched. Within the range from 24 to 30 °C, temperature affected incubation length and most hatchling traits examined. The mean incubation length at 24, 26, 28 and 30 °C was 36.4, 28.7, 21.8 and 15.7 days, respectively. Embryos developing at higher temperatures (28 and 30 °C) consumed more energy but produced less developed (and hence smaller) hatchlings, which characteristically had larger residual yolks but smaller carcasses. A principal component analysis resolved two components (with eigenvalues ⩾1) from ten size (initial egg mass)-free hatchling variables, accounting for 79.3% of variation in the original data. The first component (43.8% variance explained) had high positive loading for size-free values of dry mass, lipid mass, energy contents and ash mass of hatchlings, and the second component (35.5% variance explained) had high positive loading for size-free values of SVL, carcass dry mass and fatbody dry mass. Hatchlings from different incubation temperatures did not differ in scores on the first axis of the principal component analysis, whereas hatchlings from higher incubation temperatures (28 and 30 °C) had significantly lower scores on the second axis than did those from lower incubation temperatures (24 and 26 °C). As the second axis mainly represents traits relating to the developmental condition at hatching, the analysis therefore provided further evidence that eggs incubated at higher temperatures produced less developed hatchlings. Taken together, our data show that the optimal temperatures for embryonic development are relatively low in D. acutus largely due to its use of relatively cool habitats.     

Hatching and viability of rotifer diapausing eggs collected from pond sediments

1. Planktonic rotifers inhabiting variable environments produce diapausing eggs that accumulate in the sediment of lakes and ponds, forming egg banks that may withstand adverse periods. A common assumption in zooplankton diapausing egg bank studies is to count as viable all eggs in the sediment that look healthy. This assumption should be challenged by asking how effectively ‘healthy‐looking’ eggs represent viable eggs. 2. In this study, viability of more than 1100 ‘healthy‐looking’ diapausing eggs belonging to the Brachionus plicatilis species complex was assessed in a laboratory hatching experiment. Eggs were collected at different depths from sediment cores obtained from 15 ponds located in coastal and inland areas of Eastern Spain. 3. Only approximately one half of the ‘healthy‐looking’ diapausing eggs hatched after incubation in experimental conditions. Almost all the hatchlings (99.4%) survived to maturity. The proportion of ‘healthy‐looking’ diapausing eggs that hatched varied among areas and among ponds within area, and substantially declined with sediment depth. Most of the hatchlings (88%) were obtained from the uppermost 2 cm of sediment. ‘Healthy‐looking’ eggs from upper sediment layers hatched after significantly shorter incubation times than eggs recovered from deeper layers. 4. Both decreased hatching success and increased incubation time for hatching with sediment depth suggest that older ‘healthy‐looking’ eggs are less responsive to hatching stimuli and could become unviable. However, the strong correlation found between the number of ‘healthy‐looking’ eggs and the number of hatchlings indicates that the abundance of ‘healthy‐looking’ eggs is a good index of egg bank viability.     

Islands in the sky or squeezed at the top? Ecological causes of elevational range limits in montane salamanders

Many animal and plant taxa reach their highest endemism and species richness in montane regions. The study of elevational range limits is central to understanding this widespread pattern and to predicting the responses of montane species to climate change. Yet, because large‐scale manipulations of the distributions of most species are difficult, the causes of species’ elevational range limits (e.g. competitive interactions, physiological specialization) are poorly understood. Here, we harness the power of new mechanistic approaches to dissect the factors that underlie the elevational replacement of two salamander species in the Appalachian Highlands. Our results challenge the long‐held idea that competitive interactions drive the lower elevational range limits of montane species and that physiological stress prevents low‐elevation species from expanding to high elevations. We show that physiological constraints drive the lower elevational range limit of the montane‐endemic species, Plethodon jordani. Conversely, we find that competition with P. jordani prevents the low‐elevation species, P. teyahalee, from expanding its range to include higher‐elevation habitats. These results are broadly consistent with the biogeography and behavior of other montane species, suggesting that similar mechanisms underlie patterns of elevational zonation across a variety of taxa and montane regions. To the extent that our findings are taxonomically and geographically widespread, these results challenge the idea that competitive release at species’ lower elevational range limits is driving the downslope range shifts exhibit by some montane taxa. Instead, our results raise the sobering possibility that even small changes in climate might cause erosion of the ranges of many high‐elevation species.     

孵化温度对赤链蛇胚胎代谢和幼体行为的影响

研究了赤链蛇(Dinodon rufozonatum)在孵化过程中卵的生长、孵化期、胚胎代谢和孵出幼体行为表现的热依赖性。结果显示:孵化温度对孵化期、卵增重、孵化过程中消耗的总能量和孵出幼体的运动表现有显著影响,但不影响胚胎代谢率、孵化成功率和幼体吐信频次。孵化期随着孵化温度的升高而缩短,孵化过程中,24℃终末卵重和胚胎代谢率显著大于30℃,而27℃与其他两个温度没有差异;27℃孵出幼体游速较24℃快,30℃孵出幼体与其他两个温度孵出幼体的游速无显著差异。上述结果显示:24—30℃是赤链蛇适合的孵化温度范围,与赤链蛇所处的生境温度相近。     

Plant population differentiation and climate change: responses of grassland species along an elevational gradient

Mountain ecosystems are particularly susceptible to climate change. Characterizing intraspecific variation of alpine plants along elevational gradients is crucial for estimating their vulnerability to predicted changes. Environmental conditions vary with elevation, which might influence plastic responses and affect selection pressures that lead to local adaptation. Thus, local adaptation and phenotypic plasticity among low and high elevation plant populations in response to climate, soil and other factors associated with elevational gradients might underlie different responses of these populations to climate warming. Using a transplant experiment along an elevational gradient, we investigated reproductive phenology, growth and reproduction of the nutrient‐poor grassland species Ranunculus bulbosus, Trifolium montanum and Briza media. Seeds were collected from low and high elevation source populations across the Swiss Alps and grown in nine common gardens at three different elevations with two different soil depths. Despite genetic differentiation in some traits, the results revealed no indication of local adaptation to the elevation of population origin. Reproductive phenology was advanced at lower elevation in low and high elevation populations of all three species. Growth and reproduction of T. montanum and B. media were hardly affected by garden elevation and soil depth. In R. bulbosus, however, growth decreased and reproductive investment increased at higher elevation. Furthermore, soil depth influenced growth and reproduction of low elevation R. bulbosus populations. We found no evidence for local adaptation to elevation of origin and hardly any differences in the responses of low and high elevation populations. However, the consistent advanced reproductive phenology observed in all three species shows that they have the potential to plastically respond to environmental variation. We conclude that populations might not be forced to migrate to higher elevations as a consequence of climate warming, as plasticity will buffer the detrimental effects of climate change in the three investigated nutrient‐poor grassland species.     

Gold 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 cmbryogenesis 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 phcnotypcs, 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.     

孵化水热环境对渔异色蛇孵化卵和孵出幼体的影响

渔异色蛇卵孵化时能从环境中吸收水分导致质量增加,卵质量的增加与初始卵质量和孵化基质湿度有关。较大幅度的孵化基质湿度变化对孵化期、孵化成功率、胚胎动用孵内物质和能量、孵出幼体的性比、大小和质量无显著影响。孵化期随温度升高而缩短,并显示极强的窝间差异。温度对孵出幼体的性别无影响,但显著影响孵化成功率、胚胎对卵内物质和能量的动用、幼体的大小和质量、躯干和剩余卵黄的质量。孵出幼体总长的两性差异不显著,但雌体体长大于雄体而尾长小于雄体。３２℃不适于孵化渔异色蛇卵,该温度下孵出的幼体躯干发育不良,剩余孵黄较多,尾部均呈畸形,孵化过程中能量转化率较低。２４℃和２６℃中孵出的幼体躯干发育良好,孵化过程中能量转化率较高,各项被测定的幼体特征指标均极相似。     

The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard

Abstract Why is the sex of many reptiles determined by the temperatures that these animals experience during embryogenesis, rather than by their genes? The Charnov‐Bull model suggests that temperature‐dependent sex determination (TSD) can enhance maternal fitness relative to genotypic sex determination (GSD) if offspring traits affect fitness differently for sons versus daughters and nest temperatures either determine or predict those offspring traits. Although potential pathways for such effects have attracted much speculation, empirical tests largely have been precluded by logistical constraints (i.e., long life spans and late maturation of most TSD reptiles). We experimentally tested four differential fitness models within the Charnov‐Bull framework, using a short‐lived, early‐maturing Australian lizard (Amphibolurus muricatus) with TSD. Eggs from wild‐caught females were incubated at a range of thermal regimes, and the resultant hatchlings raised in large outdoor enclosures. We applied an aromatase inhibitor to half the eggs to override thermal effects on sex determination, thus decoupling sex and incubation temperature. Based on relationships between incubation temperatures, hatching dates, morphology, growth, and survival of hatchlings in their first season, we were able to reject three of the four differential fitness models. First, matching offspring sex to egg size was not plausible because the relationship between egg (offspring) size and fitness was similar in the two sexes. Second, sex differences in optimal incubation temperatures were not evident, because (1) although incubation temperature influenced offspring phenotypes and growth, it did so in similar ways in sons versus daughters, and (2) the relationship between phenotypic traits and fitness was similar in the two sexes, at least during preadult life. We were unable to reject a fourth model, in which TSD enhances offspring fitness by generating seasonal shifts in offspring sex ratio: that is, TSD allows overproduction of daughters (the sex likely to benefit most from early hatching) early in the nesting season. In keeping with this model, hatching early in the season massively enhanced body size at the beginning of the first winter, albeit with a significant decline in probability of survival. Thus, the timing of hatching is likely to influence reproductive success in this short‐lived, early maturing species; and this effect may well differ between the sexes.     

Do temperature fluctuations during incubation always play an important role in shaping the phenotype of hatchling reptiles?

Fluctuating temperatures (FTs) influence hatchling phenotypes differently from constant temperatures (CTs) in some reptiles, but not in others. This inconsistency raises a question of whether thermal fluctuations during incubation always play an important role in shaping the phenotype of hatchlings. To answer this question, we incubated eggs of Naja atra under one CT (28 °C, CT), two temperature-shift [cold first (CF) and hot first (HF) in which eggs were first incubated at 24 or 32 °C and then at the other, each for 20 days, and finally at 28 °C until hatching], and one FT thermal regimes. Female hatchlings were larger in snout–vent length but smaller in tail length, head size than male hatchlings from the same-sized egg; female hatchlings had more ventral scales than did male hatchlings. The FT and HF treatments resulted in shorter incubation lengths. Tail length was greatest in the CT treatment and smallest in the FT treatment, with the CF and HF treatments in between; head width was greater in the CT treatment than in the other three treatments. Other examined hatchling traits did not differ among treatments. The observed morphological modifications cannot be attributed to the effect of thermal fluctuations but to the effect of temperatures close to the upper and lower viable limits for the species. Our results therefore support the hypothesis that hatchling phenotype is not altered by thermal fluctuation in species with no phenotypic response to incubation temperature within some thresholds.     

Incubation temperature and phenotypic traits of Sceloporus undulatus: implications for the northern limits of distribution

Cold environmental temperature is detrimental to reproduction by oviparous squamate reptiles by prolonging incubation period, negatively affecting embryonic developmental processes, and by killing embryos in eggs directly. Because low soil temperature may prevent successful development of embryos in eggs in nests, the geographic distributions of oviparous species may be influenced by the thermal requirements of embryos. In the present study, we tested the hypothesis that low incubation temperature determines the northern distributional limit of the oviparous lizard Sceloporus undulatus. To compare the effects of incubation temperature on incubation length, egg and hatchling survival, and hatchling phenotypic traits, we incubated eggs of S. undulatus under temperature treatments that simulated the thermal environment that eggs would experience if located in nests within their geographic range at 37°N and north of the species’ present geographic range at latitudes of 44 and 42°N. After hatching, snout–vent length (SVL), mass, tail length, body condition (SVL relative to mass), locomotor performance, and growth rate were measured for each hatchling. Hatchlings were released at a field site to evaluate growth and survival under natural conditions. Incubation at temperatures simulating those of nests at 44°N prolonged incubation and resulted in hatchlings with shorter SVL relative to mass, shorter tails, shorter hind limb span, slower growth, and lower survival than hatchlings from eggs incubated at temperatures simulating those of nests at 37 and 42°N. We also evaluated the association between environmental temperature and the northern distribution of S. undulatus. We predicted that the northernmost distributional limit of S. undulatus would be associated with locations that provide the minimum heat sum (∼495 degree-days) required to complete embryonic development. Based on air and soil temperatures, the predicted northern latitudinal limit of S. undulatus would lie at ∼40.5–41.5°N. Our predicted value closely corresponds to the observed latitudinal limit in the eastern United States of ∼40°N. Our results suggest that soil temperatures at northern latitudes are not warm enough for a sufficient length of time to permit successful incubation of S. undulatus embryos. These results are consistent with the hypothesis that incubation temperature is an important factor limiting the geographic distributions of oviparous reptile species at high latitudes and elevations.     

产卵于温暖且热稳定巢内的蜥蜴具有相对较高但较窄范围的孵化温度

作者用蜡皮蜥(Leiolepis reevesii)为模型动物,检验产卵于温暖且热稳定巢内的蜥蜴应有相对较高但较窄的孵化温度的假设。卵在三个恒定温度(27、30和33℃)、一个波动温度处理下孵化。温度的平均值而非方差影响孵化期,27、30和33℃的平均孵化期分别为101.1、69.6和55.3d。幼体性别不受孵化温度影响。不同处理孵出的幼体仅有稍许形态差异,但运动表现差异显著。27℃孵出幼体在跑道上的表现比其它处理孵出幼体差。卵能在27℃和33℃下孵化,但这两个孵化温度并不适宜。蜡皮蜥适宜的孵化温度范围可能处于最频繁的巢温变化范围(28℃-32℃)内。与其它在低温生境或温暖生境但产卵于浅巢的有鳞类爬行动物相比较,蜡皮蜥有相对较高但较窄适宜的卵孵化温度。因此,作者的数据支持上述假设。     

Influence of incubation temperature on hatching success,energy expenditure for embryonic development,and size and morphology of hatchlings in the oriental garden lizard,Calotes versicolor (Agamidae)

We incubated eggs of Calotes versicolor at four constant temperatures ranging from 24 degrees C to 33 degrees C to assess the effects of incubation temperature on hatching success, embryonic use of energy, and hatchling phenotypes that are likely to affect fitness. All viable eggs increased in mass throughout incubation due to absorption of water, and mass gain during incubation was dependent on initial egg mass and incubation temperature. The average duration of incubation at 24 degrees C, 27 degrees C, 30 degrees C, and 33 degrees C was 82.1 days, 60.5 days, 51.4 days, and 50.3 days, respectively. Incubation temperature affected hatching success, energy expenditure for embryonic development, and several hatchling traits examined, but it did not affect the sex ratio of hatchlings. Hatching success was lowest (3.4%) at 33 degrees C, but a higher incidence of deformed embryos was recorded from eggs incubated at this temperature compared to eggs incubated at lower temperatures. Most of the deformed embryos died at the last stage of incubation. Energy expenditure for embryonic development was, however, higher in eggs incubated at 33 degrees C than those similarly incubated at lower temperatures. A prolonged exposure of eggs of C. versicolor at 33 degrees C appears to have an adverse and presumably lethal effect on embryonic development. Hatching success at 24 degrees C was also low (43.3%), but hatchlings incubated at 24 degrees C did not differ in any of the examined traits from those incubated at two intermediate temperatures (27 degrees C and 30 degrees C). Hatchlings incubated at 33 degrees C were smaller (snout-vent length, SVL) than those incubated at lower incubation temperatures and had larger mass residuals (from the regression on SVL) as well as shorter head length, hindlimb length, tympanum diameter, and eye diameter relative to SVL. Hatchlings from 33 degrees C had significantly lower scores on the first axis of a principal component analysis representing mainly SVL-free head size (length and width) and fore- and hindlimb lengths, but they had significantly higher scores on the second axis mainly representing SVL-free wet body mass. Variation in the level of fluctuating asymmetry in eye diameter associated with incubation temperatures was quite high, and it was clearly consistent with the prediction that environmental stress associated with the highest incubation temperatures might produce the highest level of asymmetry. Newly emerged hatchlings exhibited sexual dimorphism in head width, with male hatchlings having larger head width than females.     

Determinants of embryonic stage at oviposition in the lizard Urosaurus ornatus

Relatively few squamate reptiles oviposit eggs with embryos at developmental stages greater than stage 30. To investigate potential proximate and ultimate bases of this phenomenon, we experimentally induced females of the lizard Urosaurus ornatus to retain their eggs past the normal time of oviposition (NTO). This procedure allowed us to determine whether the length of egg retention is fixed or facultative and to evaluate the effects of retention on embryos, hatchlings, and females. Females were able to retain eggs facultatively for at least 29 d past the NTO. However, retention resulted in arrested development of embryos; arrest occurred at stages 30-30.5, which is only slightly more advanced than that at the NTO (stage 29.5). Embryogenesis was reinitiated when eggs were removed from females and placed in incubation media. Hatching success of these eggs was high (87%), and incubation time was not affected by the number of days that development had been arrested. However, the snout-vent length and water content of hatchlings were negatively related to the length of retention, and they ran slower than hatchlings from control eggs obtained at the NTO. Retention of eggs past the NTO had no detectable effect on the body condition or running speeds of females. Developmental arrest and the adverse effects of retention on hatchling phenotype, if widespread among squamates, would account for the limited range of embryo stages at oviposition and act as major constraints on the evolution of viviparity.     

Sunny side up: lethally high, not low, nest temperatures may prevent oviparous reptiles from reproducing at high elevations

Oviparous (egg-laying) lizards and snakes generally inhabit warmer climates than do related viviparous (live-bearing) taxa. This pattern is widely attributed to the failure of oviparous reproduction in cold climates, but the thermal regimes of potential nest-sites above and below the elevational cut-off for oviparous reproduction have never been quantified. We studied oviparous ( Bassiana duperreyi ) and viviparous ( Eulamprus heatwolei ) scincid lizards at such a site in the Brindabella Range of south-eastern Australia. Miniature data-loggers monitored temperatures of nest-sites and lizards in midsummer, partway through the incubation period of eggs in natural nests. Our results contradict the simplistic notion that mean nest temperatures determine this elevational limit for oviparity. Instead, potential nest-sites with average temperatures suitable for embryogenesis in Bassiana are available well above the threshold elevation. However, thermal minima decrease consistently with elevation and thus the maximum temperature needed for any given mean incubation temperature increases rapidly with elevation. Potential nest-sites above the elevational threshold can only attain mean temperatures high enough to sustain embryogenesis by having lethally high thermal maxima. Such nest-sites are available close to the soil surface, but cannot support development. In contrast, behavioural thermoregulation allows viviparous lizards to maintain high mean body temperatures concurrently with relatively low maximum temperatures, regardless of elevation. Paradoxically, oviparous reptiles may be restricted to low elevations not because nests that provide appropriate mean incubation temperatures are unavailable further up the mountain, but because eggs laid in such shallow nests would overheat.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 325–334.