Abstract
In organisms with complex life cycles, such as amphibians, morphological variation itself is strongly influenced by environmental factors and maternal effects. Although temperature and food level exert a strong influence on larval growth and development, little is known about the interacting effects of these factors on age and size at metamorphosis. In this study, plasticity in growth rates, larval mass, larval period, and body size at metamorphosis were experimentally examined for a high-altitude toad (Bufo minshanicus) under different combinations of temperature and food level. Larval period and mass at metamorphosis were sensitive to food level, and varied with temperature. At high food level, tadpoles reared at 29.8°C had shorter larval period lengths and larger mass at metamorphosis than those reared at 25.8 and 22.6°C, but not between 25.8 and 22.6°C. Interestingly, tadpoles at 29.8°C that were offered with a higher level of food supply achieved a larger size than those with a lower level of food supply; however, food supply did not affect body mass at the two lower temperature settings. Thus, the effects of food level were dependent on water temperature. Although there was high mortality at 29.8°C, surviving tadpoles have been much stronger to achieve faster growth and reach a larger mass at metamorphosis, which were positively correlated with juvenile survival and adult fecundity. Thus, under varied environmental conditions, we could say that there is more plasticity in development and growth of larvae in high altitude populations than in the same species or other species from low altitude populations.
Introduction
Environmental variation is very common. In amphibians, variations in the length of the larval period and growth rate represent adaptive responses to the variable environments of spawning sites (Wassersug, 1974, 1975; Wilbur, 1980). The relative opportunity for growth and mortality risks in both aquatic and terrestrial habitats influence the timing of metamorphosis and that trade-offs between growth rate and mortality risk could stabilize a complex life history (Wilbur and Collins, 1973; Werner, 1986). Variation in growth rate and timing of metamorphosis generate variation in size at metamorphosis, which is an important fitness component (Berven, 1982; Smith, 1987; Semlitsch et al., 1988; Álvarez and Nicieza, 2002; Castano et al., 2010).
Many environmental factors such as temperature or food availability may influence the size at metamorphosis (viewed by Wilbur and Collins, 1973). Low temperatures retard differentiation more than growth, thereby increasing stage-specific size (Smith-Gill and Berven, 1979; Álvarez and Nicieza, 2002). As a result, larval anurans grown at cold temperatures have prolonged developmental periods but they are also larger as metamorphs than conspecifics grown at warmer temperatures. This variation in metamorphic traits may have strong effects on later fitness as early metamorphosis and large size at metamorphosis are favored because of their positive effects on juvenile survival and adult fecundity (Wells, 2007). Temperature variation is especially relevant for populations exposed to strong time constraints, such as those living at high latitudes or altitudes, where time for larval development is limited by the short growth season and pond freezing (Smith-Gill and Berven, 1979; Merilä et al., 2004). However, previous researchers observed that the temperature variation of the reaction norms among species and phylogenetic groups was a puzzling problem, suggesting that there is interplay between phylogeny and adaptation to specific habitats (aquatic and terrestrial) (e.g., Blouin, 1992; Morand et al., 1997; Joly et al., 2005).
High food availability results in faster growth to a larger size at metamorphosis (Nathan and James, 1972; Steinwascher and Travis, 1983; Pandian and Marian, 1985; Arendt and Hoang, 2005; Peacor and Pfister, 2006). Contrarily, low resource availability due to low food level, high larval density, or both would also constrain metamorphosis, such that if conditions were poor throughout the larval period, then slowly growing tadpoles might take a long time to reach the minimum size for metamorphosis (viewed by Wilbur and Collins, 1973). Werner (1986) suggested that the evolution of size at metamorphosis results from a trade-off between performance in aquatic habitats and performance in terrestrial habitats, before and after metamorphosis, respectively. It is generally assumed that selection should favor a shortened larval period but a larger size at metamorphic climax (Wilbur, 1972, 1977; Wilbur and Collins, 1973; Smith-Gill and Gill, 1978).
Minshan’s toad is a medium-sized bufonid [adult snout-vent length (SVL) ranges from 55 to 98 mm] that lives in forests, fields, and high pastures at altitudes between 1700 and 3700 m in the northeastern Tibetan plateau (Fei and Ye, 2001). Under natural conditions, the spawning pond selection of Minshan’s toad is little affected by the presence of predators (e.g., fish) within the elevation range of this species. This species exhibits a short breeding season (5-18 days), during which it is a typical explosive breeder (Wells, 2007). The timing of larval development in the field was long (2.5-3 months) in cold water (10-25°C, mean temperature less than 17°C), thus tadpoles may be better adapted to cooler temperatures. The high population densities (50-70 tadpoles per m2) were observed in a natural population (Yu, personal observations). Tadpoles usually metamorphose in the same year, and thus are not found overwintering under water (Yu, personal observations). High altitude populations with seasonal time constraints may have the capacity to grow and differentiate rapidly to compensate for a short growing season (viewed by Wheeler et al., 2013). Thus, we could say that there is more plasticity in development and growth of high altitude populations due to environmental variation (viewed by Merilä et al., 2000). In this sense, we tested experimentally how temperature and food availability affect fitness-related metamorphic traits.
Factorial ANOVA tables for the effects of temperature and food level on metamorphic traits in a Bufo minshanicus population.
Materials and methods
Study species and rearing condition
We collected 30 eggs from each of the fresh egg masses from 65 B. minshanicus females in one population in Huangyuan County (36°40′N, 101°20′E, altitude 2546 m), Qinghai, China, on March 28-29, 2012. Hatchlings from all egg masses were kept in two 100-l plastic containers with an automatic aerator. Tadpoles had reached Gosner stage 26 (absorption of external gills and fully formed spiracle; Gosner, 1960) at the start of the experiment. There were a total of 600 tadpoles, which were randomly allocated into six experimental treatments. For each temperature, 200 individual vessels (100 for each diet treatment), each of which is 0.3 l, were randomly placed in two rectangular tanks (110 cm × 90 cm × 60 cm; L × W × H) filled with fresh water to a depth of 8 cm. Room (air) temperature was kept at 25.8°C. In the experiments where temperature was manipulated, either aquarium heaters were used to raise the water temperature to 29.8°C, or cooling units equipped with thermostats were used to reduce the temperature to 22.6°C. Two temperatures (22.6 and 25.8°C) were chosen because they fall within the range this species experiences in the field and lab (Zhang et al., 2007), while 29.8°C may approach avoidance temperature (Yu, personal observations). Tadpoles were exposed to a 12L:12D photoperiod throughout the study period and the water in the containers was changed weekly.
Experiment design
A 2 × 3 factorial design was used to examine the effects of food level and temperature on larval growth rates and postmetamorphic performance. To evaluate the effects of food level, half of the tadpoles in each temperature treatment were placed on a low food regimen (30-40 mg per tadpole per day, LFL) and half were placed on a high food regimen (60-80 mg per tadpole per day, HFL). These food levels were chosen to be consistent with previous lab experiments on this species by Zhang et al. (2007). Ration levels were increased based on tadpole mass as the larval period progressed to keep up with the normal demands of growth and development. Larvae were fed with commercial fish food (Bieyanghong, Biological Co. Ltd., Hangzhou, China, medium protein content, MPC; 30% protein, 10% lipids, 18% algae, 4% fiber, 10% ash).
Data analysis
Six hundred vessels in six experimental treatments were checked daily, until the first metamorph (defined as the emergence of the first forelimb, Gosner stage 42; Gosner, 1960) was discovered and collected. Several variables were measured: (1) age at metamorphosis (number of days from the beginning of the experiment until metamorphosis); (2) mass and SVL at metamorphosis [SVL was measured with digital calipers (to the nearest 0.01 mm) and body mass was weighed with an electric balance (to the nearest 0.001 g)]; (3) growth rate = exp{[log(final mass) – log(initial mass)]/days} – 1 (Anholt et al., 2000); and (4) the proportion of tadpoles surviving until metamorphosis.
Length of larval period, mass at metamorphosis, SVL, growth rate and survival were analyzed with a MANOVA with type III mean squares using temperature and food level treatment as factors. If the overall MANOVA results were significant, the data were analyzed with ANOVAs by using post hoc multiple comparisons (Fisher’s LSD) or Chi-square test to evaluate differences between food levels or between temperatures (SPSS 13.0, SPSS Inc., 2004, Chicago, IL, USA). All P-values given are two-tailed, with values presented as means ± standard error.
Results
The effects of rearing temperature and food level on length of larval period were significant (temperature, , ; food level, , , table 1, fig. 1). Moreover, a significant interaction between temperature and food level (, ) revealed that age at metamorphosis varied inversely with temperature at a low food level (Post Hoc all ). HFL tadpoles reared at 29.8°C had shorter larval period lengths than those reared at 25.8 and 22.6°C (all ), but not between 25.8 and 22.6°C ().
Influences of temperature and food level on age at metamorphosis of Bufo minshanicus (Gosner stage 42; open columns, 29.8°C; black columns, 25.8°C; gray columns, 22.6°C).
Citation: Amphibia-Reptilia 37, 1 (2016) ; 10.1163/15685381-00003028
Influences of temperature and food level on body length, mass, growth rate and survival of Bufo minshanicus at forelimb emergence (open columns, 29.8°C; black columns, 25.8°C; gray columns, 22.6°C).
Citation: Amphibia-Reptilia 37, 1 (2016) ; 10.1163/15685381-00003028
Mass at metamorphosis was affected by temperature (, ; table 1) and food level (, ). There was a significant interaction between food level and temperature (, ). The tadpoles reared at 29.8°C had the largest mass (all ), while those reared at 25.8°C had the smallest (all ). HFL tadpoles were heavier than LFL tadpoles (fig. 2). However, the effect of food quantity differed according to temperature. Indeed, diet differences did not affect body mass at 22.6 () and 25.8°C (). However, at 29.8°C, tadpoles feeding on a high food level had a larger body mass than those raised on a low food quantity ().
Rearing temperature and food level had a significant effect on SVL at metamorphosis (all , table 1), and the interaction between rearing temperature and food level was significant (). At 29.8°C, HFL tadpoles had a larger SVL than LFL tadpoles (), but not at 25.8 () or 22.6°C ().
The effects of rearing temperature and food level on mortality at metamorphosis were significant (all , table 1, fig. 2). The interaction between temperature and food level was not significant (, ). Mortality at high food level was independent of rearing temperature (Chi-square test: , df = 2, ), but at low food level, tadpoles at 29.8°C suffered from significantly reduced survival as compared to 25.8 and 22.6°C (, df = 2, ).
Growth rate was positively influenced by both temperature and food level (all , table 1, fig. 2). A significant interaction between temperature and food level (, ) revealed that growth rates of HFL tadpoles were significantly higher than LFL tadpoles across the three experimental temperatures (all ). At 29.8°C, tadpoles had a greater growth rate than those raised at low food level (all ), but not at 25.8 and 22.6°C ().
Discussion
Many environmental factors including temperature, food availability, pond desiccation, and predation risk may influence growth and development in larval anurans (viewed by Laurila et al., 2001). In most cases, the effect of enhanced growth conditions is faster development (viewed by Álvarez and Nicieza, 2002). Our results show clearly that both food level and temperature influenced the length of larval period of Minshan’s toad tadpoles. Larvae grown at high temperatures or high food level have shorter developmental periods than those in any other treatment. In other words, high food level and high temperature caused the fastest development of Minshan’s toad tadpoles. Of particular interest was the interaction between temperature and food level. The response of tadpoles reared at a high food level to shortened larval period depended on temperature. HFL Tadpoles reared at 29.8°C had shorter larval periods than those reared at 25.8 and 22.6°C. Similarly, some studies have found that tadpole development rates are slower and time to metamorphosis is prolonged in colder environments (54 out of 61, table 2), while two species showed that development rate was more rapid at low temperatures (Licht, 1975; Wheeler et al., 2013). Additionally, five species were not affected by water temperature (Miyamae and Masafumi, 1979; Buchholz and Hayes, 2002; Alcobendas et al., 2004).
Although some species have revealed a trade-off between size and age at metamorphosis in response to temperature treatments (Travis, 1980; Berven and Gill, 1983; viewed by Kaplan, 1985; Pfennig et al., 1991; Blouin, 1992; Semlitsch, 1993; Morand et al., 1997; Alcobendas et al., 2004), some evidence suggests that metamorph body size is inversely or not correlated with the length of larval period (Miyamae and Matsui, 1979; Travis, 1981, 1983; Beck and Congdon, 2000; Loman, 2002; Lesbarrères et al., 2007; Reading, 2010; Kupferberg et al., 2011). Therefore, there remains controversy regarding the possible correlation between these two traits (Gibbons and McCarthy, 1986; Miaud et al., 1999; Merilä et al., 2000; Sommer and Pearman, 2003). In this study, our data suggest that growth and developmental rates of B. minshanicus are influenced by both temperature and food level (Laugen et al., 2005; Castano et al., 2010). In addition to earlier metamorphosis, an interesting finding was that tadpoles reared at high temperature had larger mass at metamorphosis than those reared at any other temperature treatment, which is unusual for ectotherms (Atkinson, 1994, 1996). In amphibian larvae, most species exhibit ectothermic characteristics (43 out of 64, table 2), a few species exhibit converse ectothermic characteristics (11 out of 64), and other species are not varied when temperature is increased. Perhaps an important finding of the previous study was that the larvae with higher growth rates tended also to have a larger body size at any point in time including metamorphic climax, which led to early metamorphosis (Berven, 1982; viewed by Woodward et al., 1988; Riha and Berven, 1991; Loman, 2002). Consequently, we suggest that temperature can affect mass at metamorphosis in four ways. First, temperature influences the extent to which food level can affect growth and development, which in turn influence size at metamorphosis (Álvarez and Nicieza, 2002). In our study, high food level had a positive effect on mass at metamorphosis at 29.8°C, but its influence became negligible 25.8 and 22.6°C. Therefore, the interacting effects of food level and temperature on size at metamorphosis basically reflect the influence of these factors on growth and developmental rates. Second, tadpoles reared at warm temperatures have high metabolic rates, thus they grow faster at higher temperatures and higher food availability (e.g. Lindgren and Laurila, 2009), whereas growth rates were more constrained at lower temperature and lower food levels. Reading (2010) suggested this might be due to an increase in body ‘reserves,’ possibly lipids and/or muscle mass, when tadpoles were exposed to warm, rather than cold. Similarly, Angilletta and Dunham (2003) found that the growth efficiency was either positively related or insensitive to environmental temperature in the majority of cases. Third, body size at metamorphosis may be more constrained by the ratio of body surface area to volume at low temperature than at high temperature because the lungs are not functional when the toadlet achieves metamorphosis in several Bufonids, which causes gas exchanges to be limited to just through the skin during some days after metamorphosis (Schmidt-Neilsen, 1984). Finally, the low survival (<50% in all treatments) indicated that these tadpoles may be reared under certain stressful conditions. In this study, tadpoles reared at 29.8°C may have approached the upper limit for Minshan’s toad tadpoles and some tadpoles were probably not adapted to such high temperature, which might result in higher mortality. Although 22.6 and 25.8°C belong within the range of preferred temperatures (Zhang et al., 2007), survival rates at the two lower temperature settings were similar to that of high temperature. Newman (1998) suggested that tadpoles may respond adaptively to some range of environmental changes that occur gradually, but not to those that occur suddenly, or that are extreme in magnitude. However, surviving tadpoles have been much stronger who have a higher growth rate to reach a larger mass and have a greater opportunity to escape stressful water conditions, and then transition to a terrestrial life stage. In this sense, one could say that there is more plasticity in development and growth of high altitude populations under an uncertain environmental condition.
Effect of temperature on size at metamorphosis and length of larval period in anuran amphibians. D, decreased size at metamorphosis or length of larval period when temperature is increased; I, increased size at metamorphosis or length of larval period when temperature is increased; NS, no change in size at metamorphosis or length of larval period when temperature is increased; tl, total length; bl, body length; bc, body condition; m, mass; ml, body volume.
The food level has an important effect on size at metamorphosis (Leips and Travis, 1994). Several experimental studies have demonstrated that high food availability can produce an effect of accelerated growth rates (Nathan and James, 1972; Steinwascher and Travis, 1983; Pandian and Marian, 1985). In this context, high efficiency foraging would allow tadpoles to maximize size at metamorphosis. In our study, at 29.8°C, tadpoles raised on a high food level had a larger mass at metamorphosis than those raised on a low food level, but not at 25.8 and 22.6°C. The underlying mechanism for these results probably lies in the effect of temperature on metabolism and growth rates. Tadpoles with a high food availability are able to grow faster at high temperature because the larger amount of food available will permit both the elevated metabolic rate associated with high temperatures (Lindgren and Laurila, 2009) and a greater growth rate, whereas growth rate may be more constrained at low temperature. Therefore, we suggest that Minshan’s toad tadpoles reach a larger mass at metamorphosis at high food level and high temperature, which results from faster growth in early development.
Acknowledgements
We are very grateful to J. Du, Y.L. He and T. Zhao for assistance with fieldwork. Work was approved by the Wildlife Protection Law of China. The study was funded by Joint Funds for Fostering Talents of NSFC and the People’s Government of Henan Province (Grant no. U1204306).
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Footnotes
Associate Editor: Benedikt Schmidt.
