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Keywords:

  • adaptive growth rate;
  • Rana temporaria;
  • temperature

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Growth rate, like any other trait, should be under balancing selection in natural populations, with selection adjusting mean growth rate in a population in relation to its site-specific costs and benefits. In the present study, we tested for differences in thermal growth optima between a northern and a southern region of Rana temporaria by rearing tadpoles in three different temperatures in the laboratory (10, 15 and 20 °C). Because of the rapid increase in post-melt temperature at high latitudes, spawn and tadpoles from the northern region experience significantly higher minimum, mean and maximum temperature throughout the period of pre-metamorph development. Frogs up north also enjoys a shorter breeding season and activity season overall. This suggests that growth and development should be maximized at a relatively higher temperature in the north as a result of directional selection. In accordance with this prediction we found that tadpoles from the northern region grew faster at relatively higher temperature than frogs in the south, whereas the opposite was true at relatively lower temperatures. North tadpoles also had a higher mortality and poorer physiological performance than south tadpoles at low temperatures. In summary, our results conclusively support the hypothesis that frogs in the north are adapted to relatively warmer developmental conditions than frogs in the south.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Large body size is associated with high fitness in a wide range of taxa and for a number of reasons. For example, large males may have more access to females because they are better fighters or are more attractive (Andersson, 1994), have fewer potential predators (Schwanner, 1985), or simply because they have a thermoregulatory advantage from a lower area–volume ratio (Peters, 1983). Furthermore, in many species it is beneficial to reach a large size quickly, e.g. to reduce the time spent in more predation sensitive life history stages (Roff, 1992). It thus agrees with intuition that in many organisms growth rate is under positive directional selection. In recent years, however, there is also a growing awareness in the scientific community that high growth rate may be a two-edged sword (Arendt, 1997). As metabolic enzymes have different thermal optima, growth and development can only proceed within a thermal window (e.g. Randall et al., 1997). Furthermore, high growth rate has been associated with relatively poor development of tissue structure compared with growth at lower rates, resulting in an increased risk of cancer (Eklund & Bradford, 1977; Kajiura & Rollo, 1994), reduced immunodeficiency (Bradford & Famula, 1984), coronary lesions (Saunders et al., 1992) and skeletal deformities (Riddell, 1981; Serafin, 1982; Yamasaki & Itakura, 1988). Therefore, it is likely that numerous life history traits are constrained by growth, such as reproductive investments (Charnov, 1991; Roff, 1992; Stearns, 1992), resistance to starvation (Gotthard et al., 1994) and probability of survival (Jonsson et al., 1992). Thus, mean growth rate is likely to be adjusted by balancing selection in relation to local costs and benefits (Berven & Gill, 1983; Beattie, 1987; Conover & Present, 1990; Niewiarowski & Roosenburg, 1993; Gotthard et al., 1994).

In a study of growth, the ideal model organism would be one in which its major determinants can easily be manipulated under the most sensitive life history stages, i.e. when the strength of selection is maximal. The common frog, Rana temporaria, meets these requirements under the pre-adult phase and acclimate very well to artificial conditions in the laboratory. In the current experiment we compared growth and development between tadpoles from two Swedish distribution regions, one on the south-west Swedish coast ca. 21 km NE Gothenburg (58°45′N, 12°05′E; henceforth ‘South’), and one in the alpine part of the species’ distribution (Ammarnäs, 65°55′N, 16°15′E; henceforth ‘North’).

Climate gradient in a selection regimes perspective

The two regions selected for this study are separated by approximately 1600 km from north to south. In the south, our R. temporaria sampling sites are situated at relatively large, deep, permanent bodies of water (compared with our northern locality) that are abundant in fish. This area is characterized by a spring water temperature that stays relatively cold for longer and a long spawning and activity season (Elmberg, 1990; Fig. 1). In the alpine region, the frogs use relatively shallower bodies of water (Elmberg, 1990; personal communication) with a temperature that increases sharply subsequent to snow melt, partly because frogs only spawn in ponds that are not shaded by vegetation (J. Elmberg, personal observation). The activity season in the north is on average only 4 months, whereas in the south it lasts for ca. 6.5 months (Elmberg, 1990). At the northern spawning sites, fish predators are absent or rare, probably because of the ephemeral nature of the breeding ponds.

image

Figure 1.  Mean, mean maximum and mean minimum temperatures for the relevant periods. All differences are highly significant (mean: t=12.4, P≪ 0.0001; mean max: t=11.8, P≪ 0.0001; mean min: t=8.6, P ≪ 0.0001; nnorth=510, nsouth=464).

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The hypothesis that growth rate and development is under balancing selection and therefore should diverge along a latitudinal, climatological axis, can be tested using the following predictions: frogs from the north will (i) be better adapted at relatively higher than lower temperatures than frogs from the south (i.e. show better conversion of food into tissue, i.e. relatively higher growth rate) as water temperatures, somewhat contrary to intuition, are higher in the north than in the south during the larval phase (Fig. 1). (ii) Selection in a laboratory environment will act more strongly (in terms of survival) at low temperatures on tadpoles from the north than from the south, and (iii) there will be corresponding differences in physiological performance at low temperatures between sites. (iv) As the tail is related to predator avoidance in tadpoles (Van Buskirk et al., 1997), the relative proportion of the total length that constitutes the tail should be higher for the southern tadpoles that experience higher fish predation.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Frog spawn from 47 females from the southern region (Angered 58°45′N, 12°05′E) and from 47 females from the northern region (Ammarnäs 65°55′N, 16°15′E) was collected on 4 April 2000 and 20 May 2000, respectively. The spawn was collected from two different breeding ponds in the south and three different ponds in the north. The ponds are separated by several kilometres and should have no or very limited gene flow; to what extent they represent unique genetic populations cannot, however, be verified without a molecular genetic analysis. In order to look for differences in growth rate between the ponds in our experiments we initially performed a nested ANOVA with latitude (N vs. S) and pond number nested within latitude as factors. The effect of pool number nested within latitude was not statistically significant (F[3,2547]=1.4, P=0.245) whereas the effect of latitude was highly significant (F=45.5, P < 0.0001; Model R2=0.02, F[4,2547]=13.6). We verified that correcting for differences among ponds did not affect the conclusions. We therefore present our results with pond effects pooled by latitude.

The spawn was kept at 4 °C for 3 days including transport at both sampling events. Sub-samples of frog spawn was preserved in 5% formalin at collection in order to look for differences between the sites in developmental stages at collection. A sample was also weighed and counted to admit estimation of the total clutch size, calculated from the mass of the entire spawn. The eggs were staged using the Gosner table (Gosner, 1960).

Climatological differences between the southern and the northern populations

Ideally, we would have wished to test for differences in water temperature between the two sampling areas throughout a prolonged period of ongoing selection. However, as this was not logistically feasible, we used air temperatures (mean temperature per 24 h) collected by the Swedish Meteorological and Hydrological Institute over a 10-year period less than 14 km from each sampling site and at the corresponding altitude.

Experimental design

A pool system was arranged with two replicate pools (152 × 122 × 25 cm, henceforth A and B) per three water temperature treatments (10, 15, 20 °C). Ninety-four 1.0 L plastic containers with wire mesh-fitted bottoms (to ensure water circulation) were hung from crossbars in all six pools. Each container received 14–16 frog eggs sampled haphazardly from the original spawn sample, i.e. ca. 90 eggs per female were separated into six samples, allocated to two replicas (one per A and B pool) in three temperature treatments. The temperatures were selected to include an overlap in developmental tolerance for both regions (Elmberg, 1990; Elmberg, personal communication).

The six pools were set up using tap water (Gothenburg, Sweden), which was aerated for a minimum of 4 days before the onset of the experiments. A water conditioner, Aqutan (Heisenberg, Germany), was used to eliminate any heavy metals, although there was no a priori reason to expect unnatural levels in the water (Olsson et al., 1987). The water was cooled to 10 °C using a custom made cooling system (Comfort teknik, Gothenburg, Sweden), and heated to the pre-selected levels using a total of nine submersible commercially available aquarium heaters. The water temperatures fluctuated no more than ±1 °C throughout the experiment and the water levels were kept constant using a custom made tap system, fine-tuned to equilibrium flow levels prior to the onset of the experiment. The photoperiod was set to 14:10 L:D using fluorescent tubes. The tadpoles received ad libitum access to fish food (SeraSan, Heinsberg, Germany) by being fed one to three times per day, depending on consumption rate in the different temperature treatments.

When all siblings in a given temperature treatment had hatched (stage 23; Gosner, 1960) five individuals from each container were randomly sub-sampled for measurements. Head length, tail and total body length were measured using a stereoscope (six times enlargement), after which the mean hatching mass was calculated and submitted for statistical analysis. The tadpoles were then returned to their respective containers.

Fifteen days after the first measurement, five tadpoles were again sampled and measured as above. Swim endurance was tested on the five measured tadpoles by giving them a slight tap on the side of the head after which time until resumed rest was recorded as an index of endurance. This procedure was repeated three times for each tadpole after which the mean value was calculated and the tadpoles returned to their container.

Statistical analysis and potential confounding variables

Trait growth rate was calculated as second measurement – first measurement. The same general results were obtained using ratios of measurements. Because water adhesion to the tadpole introduced such a major confounding variable on mass at hatching, and drying the skin is detrimental to an amphibian’s survival, a sample of tadpole hatchlings from different families were killed and weighed after completely soaking up excess water with a paper towel. The mean mass of these tadpoles was used as the mass at hatching for all tadpoles. This of course overlooked inter-individual differences in mass at hatching, but this variation appeared small compared with the large differences in growth and mass at the second reading (see below).

A potential confounding factor of between-site differences in offspring traits is any difference between sites in maternal traits, such as body size or body condition (e.g. Roff, 1992). As the eggs in this study were collected immediately subsequent to spawning, we were unable to score maternal characteristics. However, to compensate for this, we looked for differences in clutch size between the two sites, as clutch size is strongly related to maternal body size (Anurans in general: Davies & Halliday, 1977; Kaplan & Salthe, 1979; R. temporaria: Elmberg, 1991; Ryser, 1996). There was no difference between north and south in mean clutch size (1735 ± 89 SE vs. 1935 ± 98 SE, north and south, respectively; t-test, t90=1.5, P=0.14, nnorth=45, nsouth=47), and we therefore concluded it appropriate to test for differences in growth characteristics between the main regions without controlling for clutch size in the analysis.

Eggs from the northern site had developed on average 2.5 stages more at collection than eggs from the southern site (average Gosner stage at collection was 8.5 ± 0.5 SE in the south and 11.0 ± 1.7 SE in the north; t-test, t91=9.96, P=0.0001, nsouth=47, nnorth=46). At the relevant temperatures, this represents ca. 0–3 days (personal observation of development at 10–20 °C). This difference in developmental stage at spawn collection resulted in significantly shorter time to hatching in the north than in the south spawn in all three temperatures, with a hatching time differing by 1.6 days on average in 10 °C, 2.4 in the 15 °C and 0.9 days in the 20 °C treatment. Because of this slight difference, we refrained from using pre-hatching data on developmental rate in our analysis. Thus, all results presented in this paper are based on a comparison of growth and development of hatched tadpoles.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Climatological differences between north and south

The data clearly demonstrates that the northern region experience significantly higher minimum, mean and maximum air temperature throughout the period of pre-metamorph development (Fig. 1). This is a conservative estimate of the difference in water temperatures between ponds in the north vs. south as frogs in the north breed in shallow pools without shade and with faster increasing day length towards the summer than in the south. Furthermore, the increase in temperature during the laying and subsequent developmental period is significantly faster in the north than in the south. This was evident from a significant heterogeneity of slopes test with temperature as the dependent variable, and the interaction between latitude and week of the year during the spring rise in temperature as the predictor variable (standardized to the same numerical values for both latitudes, as breeding takes place ca. 7 weeks later in the north; slope south=0.92 ± 0.17 SE, P=0.0001, slope north=0.98 ± 0.18 SE, P=0.0001; week × latitude, F[1, 12]=31.5, P=0.0001). More importantly, during the period of egg development and larval growth (ca. 22 March and 7 weeks onwards, and 22 May and 7 weeks onwards, respectively, for south and north; Cedhagen & Nilson, 1981), the mean air temperature in the north is 9.6 °C (±0.16 SE, n=464), whereas in the south it is only 6.6 °C (±0.18 SE, n=510; Fig. 1; t972=12.4, P < 0.0001). The corresponding differences in mean maximum temperature is 14.7 °C (±0.21 SE) and 11.0 °C (±0.23 SE), respectively (Fig. 1; t972=11.8, P < 0.0001), and mean minimum temperature 4.4 °C (±0.17 SE) and 2.3 (±0.18 SE; Fig. 1; t972=8.6, P < 0.0001). Thus, during the period of early ontogeny, the frogs in the northern population are developing at higher temperatures on average.

Mortality and its effect on density and growth rate

Apart from maternal effects, a potential confounder in all studies of growth phenomena is food stress and competition for resources (density dependence). It is well known that competition between tadpoles results in a reduction in mean size at metamorphosis and increased variation in growth between individuals (Wilbur & Collins, 1973; Wilbur, 1977). We tried to control for food competition by allowing tadpoles ad libitum access to food at all times. However, as outlined above, in the present study tadpoles were expected to do more or less well at different temperatures depending on temperature-induced selection and local adaptation. Mortality may therefore also vary between populations and temperature treatments and density may come to vary accordingly. Indeed, mortality was higher at low temperatures for the northern population (Kruskal–Wallis non-parametric analysis of variance, χ21=4.3, P=0.038), with an average loss of 2.9 (north) vs. 2.0 (south) tadpoles through the experiment. In the 15 and 20 °C treatments, the non-significant corresponding differences for north and south mortality were 2.1 vs. 2.4, and 3.0 vs. 2.7 on average (P=0.26 and P=0.33, respectively). However, there was no correlation between density, indexed by the number of tadpoles at the second reading, and growth in mass in the south or the north at the two lowest temperatures (–0.13 < r < 0.20; 0.20 < P < 0.80; n=45, and n=47 in 10 °C, S and N, respectively, and n=45 and n=46, respectively, in 15 °C). At 20 °C, however, there was a negative correlation between mean growth rate and density at both latitudes, with a correlation coefficient for north tadpoles of –0.38 (P=0.009, n=45), and a corresponding negative correlation for the south tadpoles (r=–0.42, P=0.006, n=46). Thus, there was no difference in mortality between latitudes in this treatment, but there were effects of density on growth rate at both latitudes. Furthermore, the density effect differed between latitudes as revealed by a heterogeneity of slopes test (effects on growth of the interaction term between latitude and density; slope N=–5.7 ± 2.74, slope S=–13.1 ± 2.47, F[1,88]=56.2, P=0.0001).

The experiment was set up to cover a temperature range wide enough to admit predictions of shifts in relative growth optima between the north and the south. South tadpoles were predicted to grow better at relatively low temperatures, and north ones at relatively high temperatures, with mid temperatures aimed to be close to a switch point where the difference in mean growth rate between latitudes was expected to be less pronounced and its sign unpredictable. This pattern was largely confirmed (Fig. 2). At 10 °C, south tadpoles grew at more than twice the rate of north tadpoles (Fig. 2; t-test, t90=12.1, P < 0.0001). However, at 15 °C, north tadpoles grew more than 30% faster than south tadpoles and a similar result was confirmed also at 20 °C (Fig. 2; 15 °C: t81=5.0, P < 0.0001; 20 °C: t89=9.8, P < 0.0001). Because growth rate in 20 °C was influenced by density, we controlled for this effect by comparing residuals between north and south tadpoles from a growth-density regression equation. Subsequent to this compensation for the confounding effect of density on mean growth rate, the difference in growth between north and south tadpoles in 20 °C was highly significant (residual scores, north=44.4, south=–43.5, t89=8.1, P < 0.0001, nnorth=46, nsouth=47).

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Figure 2.  Mean growth rate in body mass. The differences between populations are significant for each temperature (10 °C: t=12.1, ≪ 0.0001, d.f.=90; t=5.0, P ≪ 0.0001, d.f.=81; 20 °C: t=9.8, P ≪ 0.0001, d.f.=89).

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Physiological performance

In order to look for thermal effects on physiological performance during development, we compared swim endurance between north and south tadpoles at two temperature treatments (for logistic reasons this could not be performed in all three treatments). In agreement with the growth data, south tadpoles had significantly better endurance at 10 °C than north tadpoles (Fig. 3, t90=4.8, nnorth=45, nsouth=47, P < 0.0001). At 15 °C, however, this difference had disappeared (Fig. 3, t81=0.71, nnorth=45, nsouth=38, P=0.48). In conclusion and in support of the growth data, north tadpoles performed more poorly at low developmental temperatures.

image

Figure 3.  Mean swim endurance. South tadpoles performed significantly better at 10 °C, whereas there was no significant difference in 15 °C (10 °C: t=4.8, P < 0.0001, d.f.=90; 15 °C: t=0.71, P=0.48, d.f.=81).

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Antipredation and body shape

Because of the difference in risk of predation in the southern vs. the northern regions, we predicted tail length to be relatively longer in south tadpoles. At hatching, this turned out to be the case at both 10 and 20 °C, whereas there was no difference in relative tail length at 15 °C (Table 1; 10 °C, t90=14.4, P < 0.0001, nnorth=45, nsouth=47; 15 °C, t81=0.1, P=0.91, nnorth=45, nsouth=38; 20 °C, t89=4.0, P= 0.0001, nnorth=45, nsouth=46). Subsequent to the growth period of 15 days, south tadpoles had significantly longer relative tails in 10 and 15 °C, whereas the opposite was true at 20 °C (Table 1; 10 °C, t90=4.9, P < 0.0001, nnorth=45, nsouth=47; 15 °C, t81=9.21, P < 0.0001, nnorth=45, nsouth=38; 20 °C, t89=4.0, P=0.0001, nnorth=45, nsouth=46). These results indicate that both latitude and temperature seem to influence relative tail length, but with latitude having different effects depending on the temperature.

Table 1.   Relative tail length Thumbnail image of

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The interpretation of the results in the present work relies on the fact that physiological processes in general, and developmental ones in particular, are temperature-dependent, best proceed at a population specific optimum, and that the organism is progressively constrained from optimal development with increasing deviation from this temperature. Because all metabolic enzyme systems show temperature-sensitivity with optima in species-characteristic windows (Randall et al., 1997), selection for higher developmental thermal tolerance elevates the minimum temperature at which normal development can proceed. Good evidence for a rapid response to stabilizing selection for temperature optimization comes from work on E. coli (Bennett et al., 1990, 1992; Riehle et al., 2001). Furthermore, as ectotherms lack innate capacity to regulate their own body temperature they are under strong selection to thermoregulate behaviorally, and the preferred body temperature achieved by such active thermoregulation covaries with that of the environment (for example being higher in desert lizards than in species from temperate regions) (Arak, 1996). However, for frog spawn metabolic, thermal optimization should be particularly strong because of its limited scope for active thermoregulation.

The present study was designed to evaluate evolutionary divergence between two different regions with different climatic history along a north–south frog distribution. Although we believe that the sites from which we have sampled are representative of these regions, we emphasize that our study is only meant to visualize differences between two areas that we know differ in temperature regimes, not primarily explain thermal adaptation along a latitudinal cline. Similar differences to what we have revealed could most likely also be found between populations differing in high vs. low altitude, and coastal vs. inland climate.

In the northern population, previous work has demonstrated that the frogs utilize fish-free ponds that reach higher temperatures than those experienced in the southern population, and are exposed to an increase in temperature that is relatively much more steep in early spring (Elmberg, 1991; personal communication; Fig. 1). Thus, from these findings it can be predicted that frogs from the north should be locally adapted to development at relatively higher temperatures. All results in the present work support this proposition.

Although low, pre-metamorph mortality was significantly higher for the north tadpoles at the lowest temperature, whereas the differences in mortality in the higher temperatures were not significant. This may indicate that selection has pushed thermal optima towards higher temperatures in the north resulting in less tolerance to low temperatures, at least under prolonged exposure. Why then do the south tadpoles not have a corresponding higher mortality in the warmer treatment? One reason could perhaps be that north tadpoles are more sensitive to water quality (Meriläet al., 2000) and, hence, the relatively higher food turnover associated with high growth rate in the warmest treatment could perhaps influence mortality rates and mask differences in temperature-induced mortality between the populations. We doubt this interpretation, however, because of our high filter capacity and efficient water conditioner.

For growth rate, the predicted pattern was also confirmed at high temperatures. South tadpoles gained in mass almost twice as fast in the cold treatment, whereas north tadpoles grew significantly faster in the two warmer treatments. These results support the notion that metabolic enzymes have thermal optima and therefore an individual cannot be equally well adapted to growth at both high and low temperatures. It therefore seems likely that selection has pushed growth optima towards higher temperatures in the northern population with the consequence of impaired growth rate at lower temperatures. The thermal switch point between the populations seems to be just below 15 °C (Fig. 2).

Because north tadpoles experience a shorter activity season, and are therefore more stressed for time for development, they should be under stronger selection for high growth rate and respond more to an increase in temperature. However, although the shorter activity season may contribute to selection for high relative growth rates in the north, this reasoning cannot explain the higher growth rate for south at 10 °C. The most parsimonious explanation to the higher growth rate at 10 °C for south tadpoles seems to be the thermal trade off hypothesis we outlined initially, i.e. with evolved differences in optimal thermal scope between north and south populations.

Density showed no effect on growth rate at 10 and 15 °C, whereas there was a significant effect in the warmest treatment. This is expected because the tadpoles became relatively larger at 20 °C, resulting in high densities compared with natural populations. Although it seems like density had higher impact on growth rate for the southern population, this difference is small compared with the large difference in growth rate.

Physiological performance, measured as swimming endurance, was also better for the southern population in the coldest treatment, but with no difference at 15 °C (unfortunately no data could be obtained at 20 °C) (Fig. 3). Although open to alternative explanations that we have no data to elaborate on (e.g. divergence in antipredation tactics between regions), the notion that the northern population is poorly adapted to low temperatures is further supported. Relative tail length was significantly higher for the southern population at 10 °C, both at hatching and after a growth period of 15 days (Table 1), and could perhaps influence the swimming performance results. However, we doubt this hypothesis. Previous studies have shown that tadpoles developing in a predator rich environment grow relatively longer and deeper tails and have a higher survival in these environments (Van Buskirk et al., 1997). However, a longer tail does not seem to contribute significantly to swimming ability (Van Buskirk & McCollum, 2000). It has therefore been suggested that a relatively longer and deeper tail might facilitate predator escape in other ways but swimming, e.g. by allowing a tadpole to lose much of the fin without affecting subsequent swimming performance (Van Buskirk & McCollum, 2000), by drawing the predator’s attention from the more vulnerable body part (Van Buskirk & McCollum, 2000), or by letting the fin act like a ‘protective wrapping’ around the important core muscle of the tail (Doherty et al., 1998). However, the actual mechanism with which the tadpole uses its tail to escape predation does not influence the interpretation of our main result, namely that south tadpoles may have longer tails in response to selection from fish predation. The pattern is not coherent, however, and a potentially complicating factor in the interpretation of these results is the temperature-sensitive trait expression during development demonstrated in other ectotherms (Shine & Harlow, 1993, 1996; Shine et al., 1995). For example, relative tail length in lizards (that do not avoid predators by swimming) tend to covary with temperature (in a non-consistent way between taxa; Shine & Harlow, 1996). It can therefore be argued that allometric relationships between traits may be altered by temperature with no apparent selective benefit to the organism. However, when the temperature-sensitivity of these allometric relationships changes between populations in a way that agrees with differences in functional biology (such as longer tail in the temperature at which the tadpole normally has to evade predators), then this may lend some support to the hypothesis that it is an adaptation to the local environment. Another reason why this result should be viewed with caution is that the reasoning is completely based on fish as predators. Other organisms (e.g. invertebrates and birds) may undoubtedly also exert significant selection.

In summary, the present work demonstrates that tadpoles in the northern and southern part of the distribution range of R. temporaria show marked differences in temperature-dependent survival, growth, development, and an estimate of physiological performance, suggesting evolutionary geographic divergence and local adaptation to different climatic conditions.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

We thank Johan Elmberg, who provided important information about the northern R. temporaria population.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References
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