The influence of maternal thermal environments on reproductive traits and hatchling traits in a Lacertid lizard,Takydromus septentrionalis

The thermal environment can induce substantial variation in important life-history traits. Experimental manipulation of the thermal environment can help researchers determine the contribution of this factor to phenotypic variation in life-history traits. During the reproductive season, we kept female northern grass lizards, Takydromus septentrionalis (Lacertidae), in three temperature-controlled rooms (25, 28 and 32 °C) to measure the effect of the maternal thermal environment on reproductive traits. Maternal thermal environment remarkably affected reproductive frequency and thereby seasonal reproductive output, but had little effect on reproductive traits per clutch or hatchling traits. Females kept at 32 °C produced more clutches and thus had shorter clutch intervals than females from 28 to 25 °C. Clutch size, clutch mass, relative clutch mass, egg size and hatchling traits did not vary among the three treatments. The eggs produced by the females were incubated at 27 °C and the traits of hatchlings were measured. The result that egg (offspring) size was independent of maternal thermal environments is consistent with the prediction of the optimal egg size (offspring) theory. The eggs produced by low temperature females (28 and 25 °C) took longer time to complete their post-oviposition development than did eggs produced by high temperature females (32 °C). This suggests that the eggs from low temperatures might have been laid when the embryos were at relatively early stages. Therefore, maternal thermal environment prior to oviposition could affect post-oviposition development in T. septentrionalis.     

Relatively low upper threshold temperature in lizards from cool habitats

We used the slender forest skink (Scincella modesta) as a model animal to test for the hypothesis that the upper threshold of incubation temperature is relatively low in lizards using shaded (and thus, cool) habitats. Eight gravid females were collected in early May 2005 from a population in Hangzhou, Zhejiang (eastern China). All females laid a single clutch of 7–13 eggs between mid-May and early June. Eggs were incubated at 24, 28 and 30 (±0.2) °C. None of eggs incubated at 30 °C hatched. Eggs incubated at 24 and 28 °C differed in incubation length but not in hatching success. The incubation length at 24 and 28 °C averaged 22.3 and 20.3 days, respectively. Hatchlings from eggs incubated at 24 and 28 °C did not differ in all examined morphological traits, but hatchlings from eggs incubated at 28 °C performed apparently worse in the racetrack than did their counterparts from eggs incubated at 24 °C. The temperature of 28 °C is close to the upper thermal threshold for successful embryonic development in S. modesta. Compared to other oviparous lizards using open (and thus, warm) habitats, the upper thermal threshold and the range of optimal temperatures for embryonic development are both lower in S. modesta. Our study supports the previous conclusion that species living in thermally different habitats may differ in the upper thermal threshold and the range of optimal temperatures for embryonic development.     

Temperature-dependent rate of clutch production in a tropical lizard (Paroedura picta: Gekkonidae): Intraspecific test of the metabolic theory of ecology

Recently, a general model based on scaling of metabolic rate and reaction kinetics that predicts dependence of various biological rates on temperature and body size has been proposed as a core of the “Metabolic Theory of Ecology” (MTE). However, its thermal component has been rarely explicitly tested and its usefulness for prediction of thermal effect on key life-history traits such as reproductive rate and hence fitness is still questionable. Here, we tested its applicability to temperature-dependent rate of clutch production in a tropical gecko. The thermal effects on reproductive rates in reptiles are only poorly known and difficult to estimate, because most species lay clutches largely infrequently. Females of the Madagascar ground gecko (Paroedura picta) lay clutches in unusually short intervals, which allowed us to use this species as a model for estimation of dependence of rate of clutch production on temperature. We kept adult females at three constant temperatures (24, 27, 30 °C) and recorded their reproductive characteristics. Increasing temperature positively influences rate of clutch production, but in a manner not predicted by a simple model of reaction kinetics. The results in P. picta suggest that predictions of fitness consequences of shifts in thermal environment can be more complicated than expected under the general relationship of the MTE.     

Does the cost of incubation set limits to clutch size in common eiders Somateria mollissima?

We examined the effect of natural clutch size on the cost of incubation in a population of common eiders Somateria mollissima nesting in Tromsø, northern Norway. The body condition of females at day 5 in the incubation period was not related to clutch size (3–6 eggs), but females incubating large clutches lost more mass and had a lower body condition at day 20 in the incubation period than females incubating small clutches. Females incubating large clutches had a slightly shorter incubation period and a lower egg predation rate. The results do not support the hypothesis that the female's ability to produce eggs is the only ultimate control of clutch size in eider. Instead the results suggest that there may be an interaction between the allocation of body reserves to eggs and incubation, and that females producing large clutches allocate more of their body reserves to incubation than females producing small clutches, in order to shorten the incubation period and to minimise the risk of predation on eggs.     

Measuring temporal variation in reproductive output reveals optimal resource allocation to reproduction in the northern grass lizard, Takydromus septentrionalis

We measured the reproductive output of Takydromus septentrionalis collected over 5 years between 1997 and 2005 to test the hypothesis that reproductive females should allocate an optimal fraction of accessible resources in a particular clutch and to individual eggs. Females laid 1–7 clutches per breeding season, with large females producing more, as well as larger clutches, than did small females. Clutch size, clutch mass, annual fecundity, and annual reproductive output were all positively related to female size (snout–vent length). Females switched from producing more, but smaller eggs in the first clutch to fewer, but larger eggs in the subsequent clutches. The mass-specific clutch mass was greater in the first clutch than in the subsequent clutches, but it did not differ among the subsequent clutches. Post-oviposition body mass, clutch size, and egg size showed differing degrees of annual variation, but clutch mass of either the first or the second clutch remained unchanged across the sampling years. The regression line describing the size–number trade-off was higher in the subsequent clutch than in the first clutch, but neither the line for first clutch, nor the line for the second clutch varied among years. Reproduction retarded growth more markedly in small females than in large ones. Our data show that: (1) trade-offs between size and number of eggs and between reproduction and growth (and thus, future reproduction) are evident in T. septentrionalis ; (2) females allocate an optimal fraction of accessible resources in current reproduction and to individual eggs; and (3) seasonal shifts in reproductive output and egg size are determined ultimately by natural selection.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 315–324.     

Causes and consequences of egg mass variation between and within blue tit clutches

Causes of egg-size variation between and within clutches were studied in clutches of the blue tit ( Parus caeruleus L.). We measured the mass of each egg in the laying sequence in unmanipulated clutches, in clutches of parents experimentally supplied with extra food before egg-laying, and in clutches of parents supplemented with extra food after the start of egg-laying. Hatchlings were weighed at an age of two days and their mass was found to be positively related to egg mass. No general trend of decreasing or increasing egg mass was found within the laying sequence. Females provided with extra food before egg-laying laid clutches with significantly less variation in egg mass than did control females. The reason for this was that the first-laid egg of unmanipulated females was lighter than the rest of the eggs in the clutch. This pattern disappeared in clutches of females receiving extra food. Thus, the reduction in egg mass variation among clutches of foodsupplemented females depended on an ability of these females, in contrast to control females, to lay a first egg of the same mass as the rest of the clutch. Eggs laid after the initiation of incubation were significantly heavier than equivalent eggs in those clutches where incubation started after clutch completion. The difference was small, however, and the adaptive significance of the finding is questionable. We argue that intra-clutch variation in egg mass is connected with greater fitness consequences than in inter-clutch variation. Furthermore, our results indicate that energetical constraints on the laying female are more important as a cause of the observed intra-clutch variation in egg mass than are adaptive responses to the environment.     

安徽滁州雌性丽斑麻蜥繁殖特征

在安徽滁州地区丽斑麻蜥(Eremias argus)年产两窝卵。窝卵数及窝卵重与雌体体长呈正相关,相对窝卵重与雌体体长无关,卵重与窝卵数无关。窝卵数、窝卵重及卵重在窝序间无明显的差异。卵长径与卵短径呈正相关,卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数增加繁殖输出。     

中国石龙子雌体繁殖特征和卵孵化的地理变异

浙江丽水和广东韶关中国石龙子均年产单窝卵,窝卵数,窝卵重和卵重均与雌体SVL呈正相关,雌体头部形态,繁殖特征,产卵起始时间和孵孵化的热依赖性等有显著的地理变异;韶关石龙子产卵起始时间为5月中旬,比丽水经子约早两周,韶关石龙子窝卵数较大,卵较小,窝卵重与丽水石龙子无显著差异。韶关石龙子特定SVL的窝卵数比丽水石龙子多2．8枚卵,中国经子卵数量和大小之间有种群间权衡,无种数内权衡,同一种群内卵数量与卵大小无关,孵化温度影响石龙子孵出幼体的一些特征,24℃孵出细幼体比32℃孵出幼体大,躯干发育好,剩余卵黄少,韶关24℃孵出幼体的体重,躯干干重小于丽水幼体,韶关32℃孵出幼体的SVL小于丽水幼体,剩余卵黄大于丽水幼体,表明适宜卵孵化温度范围有地理变异。丽水石龙子卵对极端高温和低温的耐受性较强,适宜卵孵化温度范围较宽。     

The variance of incubation temperatures does not affect the phenotype of hatchlings in a colubrid snake, Xenochrophis piscator

It has been documented in some reptiles that fluctuating incubation temperatures influence hatchling traits differently than constant temperatures even when the means are the same between treatments; yet whether the observed effects result from the thermal variance, temperature extremes or both is largely unknown. We incubated eggs of the checkered keelback snake Xenochrophis piscator under one fluctuating (Ft) and three constant (24, 27 and 30 °C) temperatures to examine whether the variance of incubation temperatures plays an important role in influencing the phenotype of hatchlings. The thermal conditions under which eggs were incubated affected a number of hatchling traits (wet mass, SVL, tail length, carcass dry mass, fatbody dry mass and residual yolk dry mass) but not hatching success and the sex ratio of hatchlings. Body sizes were larger in hatchlings from incubation temperatures of 24 and 27 °C compared with the other two treatments. Hatchlings from the four treatments could be divided into two groups: one included hatchlings from the 24 and 27 °C treatments, and the other included hatchlings from the 30 °C and Ft treatments. In the Ft treatment, the thermal variance was not a significant predictor of all examined hatchling traits, and incubation length was not correlated with the thermal variance when holding the thermal mean constant. The results of this study show that the mean rather than the variance of incubation temperatures affects the phenotype of hatchlings.     

Seasonal shifts in clutch size and egg size in the side-blotched lizard,Uta stansburiana Baird and Girard

Summary There is evidence that the side-blotched lizard, Uta stansburiana, and some other organisms of temperate latitudes produce fewer and larger eggs as the reproductive season progresses. There are at least two models that could explain this phenomenon.Proponents of the parental investment model claim that females are selected to increase egg size, at the cost of clutch size, late in the season in order to produce larger and competitively superior hatchlings at a time when food for hatchlings is in low supply and when juvenile density is high. In this model the selective agent is relative scarcity of food available to hatchlings late in the reproductive season, and the adaptive response is production of larger offspring.The alternative explanation (bet-hedging model) proposed in this paper is based on the view that the amount of food available to females for the production of late-season clutches is unpredictable, and that selection has favored conservatively small clutches in the late season to insure that each egg is at least minimally provisioned. Smaller clutches, which occur most frequently late in the season, are more likely to consist of larger eggs, compared to larger clutches, for two reasons. Firstly, unlike birds, oviparous lizards cannot alter parental investment after their eggs are deposited, and therefore, in cases of fractional optimal clutch size, the next lower integral clutch size is selected with the remaining reproductive energy allocated to increased egg size. With other factors constant, eggs of smaller clutches will increase more in size than eggs of larger clutches when excess energy is divided among the eggs of a clutch. Secondly, unanticipated energy that may become available for reproduction during energy-rich years will similarly increase egg size a greater amount if divided among fewer eggs.     

How avian incubation behaviour influences egg surface temperatures: relationships with egg position,development and clutch size

While understanding heat exchange between incubating adults and their eggs is central to the study of avian incubation energetics, current theory based on thermal measurements from dummy eggs reveals little about the mechanisms of this heat exchange or behavioural implications for the incubating bird. For example, we know little about how birds distribute their eggs based on temperature differences among egg positions within the nest cup. We studied the great tit Parus major, a species with a large clutch size, to investigate surface cooling rates of individual eggs within the nest cup across a range of ambient temperatures in a field situation. Using state‐of‐the‐art portable infrared imaging and digital photography we tested for associations between egg surface temperature (and rate of cooling) and a combination of egg specific (mass, shape, laying order, position within clutch) and incubation specific (clutch size, ambient temperature, day of incubation) variables. Egg surface temperature and cooling rates were related to the position of the eggs within the nest cup, with outer eggs being initially colder and cooling quicker than central eggs. Between foraging bouts, females moved outer eggs significantly more than centrally positioned eggs. Our results demonstrate that females are capable of responding to individual egg temperature by moving eggs around the nest cup, and that the energy cost to the female may increase as incubation proceeds. In addition, our results showing that smaller clutches experience lower initial incubation temperatures and cool quicker than larger clutches warrant further attention for optimal clutch size theory and studies of energetic constraints during incubation. Finally, researchers using dummy eggs to record egg temperature have ignored important elements of contact‐incubation, namely the complexity of how eggs cool and how females respond to these changes.     

Variation and trade-off in reproductive output of the Andean frog<Emphasis Type="Italic"> Hyla labialis</Emphasis>

I analysed variation in number and size of eggs in association with variation in body size of Hyla labialis females from three altitudinally widely separated populations in the Colombian Andes. Females at 3,500 m were significantly larger and heavier than those at 2,700 m, which in turn were larger and heavier than those at 2,000 m. After accounting for interpopulational differences in body size, clutch size (i.e. number of eggs) and egg size differed significantly between populations, but clutch mass did not. At 3,500 m, large relative clutch mass tended to be associated with larger eggs, whereas at lower altitudes it was associated with relatively larger clutch size. Within each population, females showed a significant trade-off between clutch size and egg size, even though relative clutch mass varied substantially and a clutch rarely used up the carrying capacity of their body cavity. At 3,500 m, comparisons between the early and late breeding season within a year suggested that climate fluctuations may play a role in reproductive-output variation within a population. Laboratory-kept females in a high somatic condition after spawning laid larger clutches in the next breeding event, but the trade-off persisted despite ad libitum food supply. Comparisons between field and laboratory suggest that limits to reproductive output were due to physiological, but not morphological restrictions. Therefore, the trade-off is better explained by energy limitation for egg growth depending on clutch size, than by the body cavity limitation hypothesis.     

Phenotypic variation in hatchling Chinese ratsnakes (Zaocys dhumnades) from eggs incubated at constant temperatures

We incubated eggs of the Chinese ratsnake Zaocys dhumnades at four constant temperatures (24, 27, 30 and 30 °C) to examine the effects of incubation temperature on hatching success and hatchling phenotypes. Incubation length increased nonlinearly as temperature decreased, with the mean incubation length being 76.7 d at 24 °C, 57.4 d at 27 °C, 47.3 d at 30 °C, and 44.1 d at 33 °C. Hatching successes were lower at the two extreme temperatures (69% at 24 °C, and 44% at 33 °C) than at the other two moderate temperatures (96% at 27 °C, and 93% at 30 °C). Incubation temperature affected nearly all hatchling traits examined in this study. Incubation of Z. dhumnades eggs at 33 °C resulted in production of smaller hatchlings that characteristically had less-developed carcasses but contained more unutilized yolks. Hatchlings from eggs incubated at 27 and 30 °C did not differ in any examined traits. Taking the rate of embryonic development, hatching success and hatchling phenotypes into account, we conclude that the temperature range optimal for incubation of Z. dhumnades eggs is narrower than the range of 24−33 °C but should be wider than the range of 27−30 °C.     

Impact of superparasitism time intervals on progeny survival and fitness of an egg parasitoid

1.Superparasitism influences the fitness of female parasitoids and their progeny, and increasing time interval between oviposition bouts generally reduces survival probabilities of the second clutch. However, the timing of superparasitism may, under certain conditions, favour the second clutch. 2. This study investigated the effects of superparasitism time intervals on survival and fitness of both clutches, allowing the egg parasitoid Trichogramma euproctidis to parasitise previously parasitised Ephestia kuehniella host eggs at different time intervals. 3. In short intervals (0–1 h), a significant advantage was found for the second clutch over the first clutch (93.1% survival). In contrast, the second clutch was outcompeted by the first clutch in 17–19 h and 27–29 h intervals. Females deposited their eggs into larvae (intraspecific hyperparasitism) in a 39–41 h interval with a probability of survival of 57.1%. Females mostly refused to hyperparasitise pupae (～80% rejection at 124–126 h), and when they did, their progeny never survived. 4. Hyperparasitism significantly increased parasitoid mortality in both clutches from less than 20% (superparasitism only) to over 35%. 5. Except on newly laid eggs (0–1 h), superparasiting females were frequently observed attempting to stab immatures of all stages (from 36.4% to 89.4% of all ovipositions depending on treatment), but infanticide only appeared to succeed on larvae (39–41 h). 6. When the second clutch survived, emerging parasitoids were smaller than control individuals, probably due to resource depletion. 7. These results suggest that T. euproctidis females can detect that a host has been previously parasitised but they cannot perceive superparasitism time intervals.     

Negative effects of elevated testosterone on female fecundity in zebra finches

Although factors influencing androgen deposition in the avian egg and its effects on nestling fitness are recently receiving considerable attention, little is known about the potential costs of high testosterone levels in the females. Our study aimed at determining the effect of injections of testosterone (T) in female zebra finches (Taeniopygia guttata), on clutch size, egg mass, yolk mass, and yolk androgen content. Females were given a single bolus injection of T in a range of doses after laying the first egg. Results show that administration of T negatively affected clutch size; the strength of this effect increased with increasing doses of T. Females injected with the highest testosterone dose showed suppressed oviposition of the third and the fourth eggs. Interestingly, testosterone administration made females produce eggs with relatively large yolks, suggesting that T may mediate the trade-off between number and size of eggs. Testosterone injection resulted in elevated levels of androgen in the eggs, in contrast to control clutches, which showed a decreasing pattern of androgen concentration along the laying sequence. We conclude that high androgen investment in eggs may be limited by physiological requirements of the ovulatory process.     

Egg-size variation in the bluethroat (Luscinia s. svecica): constraints and adaptation

We examined inter- and intra-clutch egg-size variation in the bluethroat (Luscinia s. svecica), an open-nesting passerine breeding in the sub-alpine region in southern Norway. By removing first clutches shortly after egg-laying, we induced laying of a repeat clutch. Females significantly reduced the number of eggs from the first to the second nesting attempt, but increased mean egg size. Females in good condition laid significantly larger eggs than those in poor condition. Consistent with predictions of the brood survival hypothesis, assuming an adaptive investment in last eggs to ensure survival of all eggs in the clutch, we found that the size of the last eggs in first clutches was generally larger than the mean egg size of the clutch, and that the relative size of the last egg increased with clutch size. However, a large last egg reflected a general increase in egg size throughout the laying sequence rather than a specific investment in the last egg only. Egg size was not significantly influenced by sex or paternity (within-pair versus extra-pair) of the embryo. In repeat clutches the last egg was not consistently larger than the mean for the clutch. We conclude that female bluethroats face resource limitations during egg formation early in the season, and that the patterns of increase in egg size with laying order for first clutches, and from first to repeat clutches, can largely be explained by proximate constraints on egg formation.     

Incubation capacity contributes to constraints on maximal clutch size in Brent Geese Branta bernicla nigricans

Lack ( 1967 ) proposed that clutch size in species with precocial young was determined by nutrients available to females at the time of egg formation; since then others have suggested that regulation of clutch size in these species may be more complex. We tested whether incubation limitation contributes to ultimate constraints on maximal clutch size in Black Brent Geese (Black Brant) Branta bernicla nigricans. Specifically, we investigated the relationship between clutch size and duration of the nesting period (i.e. days between nest initiation and the first pipped egg) and the number of goslings leaving the nest. We used experimental clutch manipulations to assess these questions because they allowed us to create clutches that were larger than the typical maximum of five eggs in this species. We found that the per‐capita probability of egg success (i.e. the probability an egg hatched and the gosling left the nest) declined from 0.81 for two‐egg clutches to 0.50 for seven‐egg clutches. As a result of declining egg success, clutches containing more than five eggs produced, at best, only marginally more offspring. Manipulating clutch size at the beginning of incubation had no effect on the duration of the nesting period, but the nesting period increased with the number of eggs a female laid naturally prior to manipulation, from 25.4 days (95% CI 25.1–25.7) for three‐egg clutches to 27.7 days (95% CI 27.3–28.1) for six‐egg clutches. This delay in hatching may result in reduced gosling growth rates due to declining forage quality during the brood rearing period. Our results suggest that the strong right truncation of Brent clutches, which results in few clutches greater than five, is partially explained by the declining incubation capacity of females as clutch size increases and a delay in hatching with each additional egg laid. As a result, females laying clutches with more than five eggs would typically gain little fitness benefit above that associated with a five‐egg clutch.     

Does follicle excision always result in enlargement of offspring size in lizards?

An experimental reduction of offspring number has been reported to result in enlargement of offspring size in lizards. We applied the “follicle excision” technique to a lacertid lizard (Takydromus septentrionalis) to examine whether this effect is generalisable to lizards. Of the 82 females that produced 3 successive clutches in the laboratory, 23 females underwent follicle excision after they oviposited the first clutch. Follicle excision reduced clutch size, but did not alter egg size. This result indicates that egg size is not altered during vitellogenesis in T. septentrionalis. Females undergoing follicle excision produced a third clutch (a second post-surgical clutch) as normally as did control females. Females switched from producing more but smaller eggs early in the breeding season to fewer but larger eggs later in the season. Our results indicate that female T. septentrionalis maximize reproductive success by diverting an optimal, rather than a higher, fraction of the available energy to individual offspring. This optimized allocation of the available energy to offspring production explains why follicle excision does not result in enlargement of egg size in this species. Our study provides evidence that an experimental reduction of offspring number does not always result in enlargement of offspring size in lizards.     

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 m) was significantly thinner than that of LE eggs (26.6 m) and the size-adjusted clutch sizes of HE females (9.4) were smaller than those of LE females (11.2).     

Reproductive performance of a lacertid lizard at the core and the periphery of the species' range

The range boundaries of organisms are frequently interpreted in terms of a decline in the extent to which the life histories of outer populations are able to adapt to local environmental conditions. To test this hypothesis, we compared the reproductive characteristics of two Iberian populations of the lizard Psammodromus algirus (Linnaeus, 1758). One of them (Lerma) is close to the northern edge of the species' range, whereas the other one (El Pardo) occupies a typical core habitat 200 km further south. Gravid females were captured in the field and transported to the lab for egg laying. Second clutches were less frequent at Lerma (where clutch size and clutch mass were larger for first than for second clutches) than at El Pardo. The total mass of both clutches combined was similar at both sites. Thus, the higher frequency of second clutches at El Pardo appeared to balance the between-sites difference in energy allocation to the first clutch. Females from Lerma laid more but smaller eggs than those from El Pardo. When incubated at the same temperature, eggs from Lerma hatched sooner even when controlling for between-sites differences in mean egg size. These differences are interpreted in the light of the advantages of early hatching and high fecundity in the northern population, as opposed to large offspring size in the core population. We conclude that the life-history traits studied show enough variation, presumably of an adaptive nature, to cope with environmental challenges at the edge of the species' range.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 87–96.