Elevational Effects on the Growth and Development of Tadpoles of Sauter s Frog Rana sauteri Boulenger in Taiwan
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1 Acta Zoologica Taiwanica 13(1): 1-10 (2002) Elevational Effects on the Growth and Development of Tadpoles of Sauter s Frog Rana sauteri Boulenger in Taiwan Su-Ju Lai 1,3, Yeong-Choy Kam 2, Fu-Hsiung Hsu 3 and Yao-Sung Lin 1* 1 Department of Zoology, National Taiwan University, Taipei, Taiwan 106, R.O.C. 2 Department of Biology, National Changhua University of Education, Changhua, Taiwan 500, R.O.C. 3 Zoology Division, Taiwan Endemic Species Research Institute, Chichi, Nantou, Taiwan 552, R.O.C. ABSTRACT The patterns of growth and development of tadpoles of Rana sauteri at Chitou (1100 m) and Mienyueh (2350 m) were investigated. At Chitou, tadpoles of different developmental stages could be found from December to March, indicating that the larval period is prolonged, and the growth and development of tadpoles are not synchronized. At Mienyueh, the majority of tadpoles ceased to develop after reaching phase 2 in August even though they did not stop growing until December. Tadpoles resumed growth and development the following spring, and underwent metamorphosis by June. It appears that tadpoles ceased to develop early enough so that they could channel a greater proportion of energy into growth to obtain a larger size to better survive the cold winter. In addition, tadpoles at Mienyueh ceased to develop early enough so that they could overwinter in phase 2, a simpler type, to reduce the risk of limb frostbite and larval mortality during the extreme cold temperatures between December and February. Our results suggest that the different patterns of larval growth and development in these two R. sauteri populations are adaptive strategies for the survival of tadpoles in the mountains of Taiwan. Key words: growth, development, metamorphosis, overwintering, subtropics, tropics, tadpoles INTRODUCTION Overwintering tadpoles are commonly observed in temperate regions (Feder and Burggren, 1992), and their growth and metamorphosis have been examined for Rana catesbeiana (Viparina and Just, 1975), R. clamitans (Berven et al., 1979), R. sylvatica (Berven and Gill, 1983), and R. aurora draytonii (Fellers et al., 2001). The occurrence of overwintering tadpoles in temperate regions has been attributed to the short growth season which limits the opportunity for successful metamorphosis (Wilbur and Collins, 1973; Roff, 1980; Werner, 1986). It has been suggested that cold temperature regimes prevent metamorphosis, due to changes in endocrine secretions and tissue sensitivity to endocrines associated with metamorphosis (Kollros, 1961; Norris and Platt, 1974; Lofts 1976). Rana sauteri is a small-sized brown frog commonly found at elevations of from 300 to 3500 m in the Central Mountain Range of Taiwan (Lue *Corresponding author: Tel: ext. 2121; Fax: ; yslin@ccms.ntu.edu.tw
2 Lai et al. et al., 1990; Chou and Lin, 1997; Lai et al., 2003). Kuramoto et al. (1984) reported that tadpoles of R. sauteri occur almost year round, but they metamorphose in March at Kwantzuling (elev. 200 m) and in April to June at Alisan (elev m). Lai et al. (2003) reported that mid- and high-elevation populations breed in the fall and spring, respectively, and tadpoles apparently overwinter and metamorphose the next spring. Taiwan is located in a subtropical region, and overwintering tadpoles have never been reported in anuran species here. In theory, the ability of tadpoles to overwinter is an important example of physiological plasticity, allowing R. sauteri to distribute over a wide elevational range in mountains of subtropical Taiwan. The purpose of this study was to examine overwintering tadpoles of R. sauteri at different elevations. Specifically, we compared the patterns of growth and development of R. sauteri tadpoles at Chitou (1100 m) and Mienyueh (2350 m). MATERIALS AND METHODS Field survey stations Two field survey stations were established: Mienyueh at a high elevation (2350 m) and Chitou at a medium elevation (1100 m). Mienyueh is situated at Alisan, Chiayi County (24 º 40 ' 19 " N, 120 º 46 ' 49 " E). We studied the growth and development of tadpoles in a creek that was about 0.5 m in width, had flowing water from May to October, but became a series of pools connected by subterranean streams from December to April. Chitou is situated in Luku, Nantou County (23 º 33 ' 08 " N, 120 º 48 ' 07 " E). We studied the growth and development of tadpoles in a creek that was about 10 m wide, and had perennially flowing water. Survey intervals and procedure We conducted a survey once a month from May 1995 to June 1996 at the two locations. For each survey, tadpoles in the water were collected randomly at three to five areas along the bank with a hand net. They were pooled, and then 15 to 30 individuals were randomly selected, placed in a petri dish, and photographed with a ruler beneath them to facilitate measuring their total lengths and body lengths. Total length was measured from the anterior end of the body to the posterior tip of the tail, and body length was from the anterior end of the body to the posterior end of the cloacal opening. We determined the developmental phases of tadpoles according to the development stages defined by Gosner (1960). For convenience, we categorized tadpoles into four developmental groups: tadpoles at Gosner stages 23~25 were defined as phase 1; tadpoles at Gosner stages 26~32 with limb buds developed but too small to be visible from the dorsum were defined as phase 2; tadpoles at Gosner stage 33~41 with limb buds long enough to be observed from the dorsum were defined as phase 3; and tadpoles at Gosner stage 42 with a triangular head and protruding forelimbs were defined as phase 4. Tadpoles at stages (metamorphic climax) were collected and brought back to the laboratory. When the tails had been completely absorbed, we measured the body length and body weight of the froglet. Meteorological data The mean monthly temperatures from May 1995 to June 1996 at Mienyueh and Chitou were obtained, respectively, from the Alisan Meteorological Station (2300 m in elevation) of the Central Weather Bureau of Taiwan and the Chitou Meteorological Station (1200 m) of the Experimental Forest Station of National Taiwan University. Statistical analysis We performed all statistical analysis of data
3 Growth and Development of Sauter s Tadpole using the StatView program (SAS Institute, 1998). The means of total length between adjacent months, froglet sizes between populations, and the ratio of body length to total length of tadpoles between populations were compared using Student s t-test. Froglet sizes between months at Chitou were compared using ANOVA and Fisher s LSD test (Sokal and Rohlf, 1981). We did not compare the means of total length of phase 3 and 4 tadpoles at Mienyueh or of phase 4 tadpoles at Chitou between adjacent months due to the small sample sizes. RESULTS Developmental phases Temperatures during the larval period ranged C from July 1995 to May 1996 at Mienyueh and C from October 1995 to March 1996 at Chitou (Table 1). At Mienyueh, tadpoles were found in 11 months. All tadpoles (100%) were in phase 1 in July and had developed to phase 2 by August (Fig. 1). Tadpoles ceased development and remained in phase 2 from September to the following March. However in November and December, a few individuals in phase 3 (3.7% to 13.3%) were sampled. In April and May, some tadpoles rapidly developed from phase 2 to phases 3 and 4. In June, no tadpole was observed in the creek. At Chitou, tadpoles were found for 6 months from October 1995 to March All tadpoles were in phase 1 in October (Fig. 1). In the following months of December to March, phase 2, 3, and 4 tadpoles were present; however, no tadpoles were observed in April. Growth At Mienyueh, tadpoles increased in total length from July to August (Table 2). They remained in phase 2 but significantly increased in total length from September to November. They reached their maximum size in November. In the following months from December to May, the total length of phase 2 tadpoles fluctuated but remained largely unchanged. For phase 3 and 4 tadpoles, the average body sizes did not significant differ among months (Table 2). At Chitou, tadpoles increased in total length from October to November (Table 3). In the following months from November to March, phase 2, 3, and 4 tadpoles were present. Phase 2 tadpoles significantly increased in size from November to December, and tadpoles increased in size with the progression of phases (Fig. 2). The mean monthly total length within a phase fluctuated but remained largely unchanged. In addition, tadpoles at Mienyueh experienced a negative monthly growth rate for a much longer time (December to April) than those at Chitou (January to February). There were also significant differences in total length between tadpoles at Chitou and those at Mienyueh at each developmental phase (Fig. 2). Metamorphosis At Mienyueh, most tadpoles remained at phase 2 and metamorphosed in May. At Chitou, tadpoles continued to metamorphose from November to March. Sizes of froglets were significantly smaller at Mienyueh than at Chitou (length: t = 8.58, p < 0.01; weight: t = 8.68, p < 0.01) (Table 4). At Chitou, the sizes at metamorphosis were larger in February, but smaller in March compared to those in February (ANOVA, F 4, 137 = , p < 0.01). DISCUSSION Patterns of growth and development of Rana sauteri tadpoles at Mienyueh and Chitou differed. Rana sauteri is an explosive breeder with a short breeding time (Kuramoto et al., 1984; Lai et al., 2003). In Chitou, adult frogs aggregated in lotic habitats and bred over about a month in October. Tadpoles of different developmental stages could
4 Lai et al. Table 1. Monthly average temperatures obtained from the Alishan meteorological station for the Mienyueh survey station and the Chitou meteorological station for the Chitou survey station for the period from May 1995 to June 1996 Year Month Mienyueh ( C) Chitou ( C) 1995 May June July Aug Sept Oct Nov Dec Jan Feb Mar Apr May June be found in the stream from October to March, whereas tadpoles at lower elevations have a much shorter larval period (Lai et al., 2003). This finding suggests that the larval period is prolonged, and that the growth and development of tadpoles are not synchronized. Prolongation of the larval period is probably due to the temperature-dependent growth of tadpoles (Feder and Burggren, 1992; Lai et al., 2003). In addition, tadpoles in January and February experienced negative growth rates, suggesting that food is limited during the winter period. We assumed that tadpoles which succeeded in obtaining food grew normally and reached metamorphosis in a short time, but those that only obtained food occasionally, or not at all, grew slowly, and consequently took longer to reach metamorphosis. As a result, a mixture of tadpoles of various sizes and developmental stages was sighted during the larval period. At Mienyueh, R. sauteri aggregated and bred in July. The majority of tadpoles stopped developing after they reached phase 2 in August, which differed from the development of tadpoles at Chitou. The cessation of development of tadpoles at low temperatures, as occurred in Mienyueh, may be a result of reduced sensitivity of hormone receptors to thyroid hormones (T 3 and T 4 ) (Frieden et al., 1965; Norris and Platt, 1974; Lofts, 1976; Duellman and Trueb, 1986). Even though the development of Mienyueh tadpoles was retarded, they continued growing until December. Smith-Gill and Berven (1979) reported that low temperatures retard larval development more than growth. Tadpoles at Mienyueh experienced negative monthly growth rates for a much longer time (December to April) than did those at Chitou, also suggesting that food limitation and/or unfavorable thermal environments imposed severe stress on the tadpoles. In spring, rising temperatures caused tadpoles to grow and develop rapidly in April, and they had undergone metamorphosis by May. Tadpoles in temperate regions metamorphose at a smaller size before winter when metamorphosis becomes disadvantageous, and the remaining tadpoles overwinter and metamorphose the following spring (Wilbur and Collins, 1973; Roff, 1980; Werner, 1986; Alford and Harris, 1988). Because inhibition of low temperatures on development is greater than that on growth, the developmental stage-specific growth of tadpoles at low temperatures is greater than that at high temperatures. Therefore, the sizes of tadpoles which metamorphosed after overwintering are larger than those which metamorphosed before winter (Viparina and Just, 1975; Smith-Gill and Berven, 1979). However, this differs from what we found for Mienyueh tadpoles. Mienyueh tadpoles were indeed larger than Chitou tadpoles at all developmental stages, but the size at metamorphosis at Mienyueh was smaller. Smith-Gill and Berven (1979) showed that tadpoles of R. pipiens raised at 13 C were larger than those at 23 C at a given developmental stage. However,
5 Growth and Development of Sauter s Tadpole 100 Mienyueh Tadpole composition (%) July Aug Chitou Sept Oct Nov Dec 1996 Jan Feb Mar Apr May Oct Nov Dec 1996 Jan Feb Mar Month Figure 1. Monthly percentage compositions of tadpoles at different developmental stages at Meinyueh from July 1995 to May 1996 and at Chitou from October 1995 to March 1996.
6 Lai et al. Table 2.Total length and monthly growth rate of tadpoles of Rana sauteri at different developmental phases at Mienyueh Year Month Phase 1 (mm) Phase 2 (mm) Phase 3 (mm) Phase 4 (mm) Monthly growth rate b (mm/month) 1995 July ± 0.46 (15) a Aug ± 1.50 (15)* Sept ± 2.95 (15)** 2.39 Oct ± 2.72 (15)** 3.79 Nov ± 3.84 (14)** (1) 6.34 Dec ± 2.22 (12) ± 4.66 (3) Jan ± 4.23 (15) Feb ± 3.81 (30) Mar ± 3.67 (30)** Apr ± 3.13 (27)** ± 0.04 (2) (1) May ± 4.72 (14) ± 2.43 (12) ± 1.88 (4) 7.13 *Significantly different at the 5% level (t-test, p < 0.05) compared to the length in the following month. ** Significantly different at the 1% level (t-test, p < 0.01) compared to the length in the following month. a Values are the mean ± SD. Sample sizes are in parentheses. b Monthly growth rate = mean of total length of this month mean of total length of the previous month. when approaching metamorphosis (Gosner stage 40-42), tadpoles at 13 C had reduced their body size (by ca. 3 ml) by a greater amount than those at 23 C (by ca. 1 ml). This may be the case for Mienyueh tadpoles in this study, in that tadpoles at Mienyueh experience extreme cold temperatures during winter, which may result in smaller sizes at metamorphosis. In addition, the ratio of body length to total length of tadpoles at Mienyueh was 36.88%, which was smaller than that of at Chitou (38.11 %; t = 5.28, p < 0.01). This may partially explain why larger tadpoles at Mienyueh yielded smaller metamorphs when compared to Chitou tadpoles. And, if the sample size were to be increased in further studies, this tendency in metamorphosis would possibly be explained more clearly. In conclusion, we contend that the different patterns of larval growth and development in these two R. sauteri populations are adaptive strategies for the survival of tadpoles in the mountains of Taiwan. Lai et al. (2003) suggested that low temperatures in winter at high elevations and high temperatures in summer at low elevations are the primary environmental factors that define the breeding success of this species. Selection of a suitable temperature regime to maximize growth and survival of tadpoles at different elevations is an adaptive mechanism for formation of elevational clines. The majority of tadpoles at Mienyueh did not develop even though ambient temperatures in summer are rather mild. Tadpoles ceased to develop early enough so that they could channel a greater proportion of energy into growth to achieve a larger size for a better survival rate throughout the cold winter. In addition, tadpoles in Mienyueh ceased to develop early enough so that they could overwinter at phase 2, a simpler type, to decrease mortality at low temperatures. Tadpoles at phases 3 and 4 developed to more-advanced stages with the appearance of hind limbs and even forelimbs
7 Growth and Development of Sauter s Tadpole Table 3.Total length and monthly growth rate of tadpoles of Rana sauteri at different developmental phases at Chitou (sample sizes in parentheses) Year Month Phase 1 (mm) Phase 2 (mm) Phase 3 (mm) Phase 4 (mm) Monthly growth rate b (mm/month) 1995 Oct 8.42 ± 0.39 (30) a Nov ± 4.30 (24)** ± 3.89 (5) (1) Dec ± 2.89 (15) ± 1.53 (14) (1) Jan ± 2.35 (16)** ± 2.41 (13) (1) Feb ± 2.91 (19)** ± 2.50 ( 9) ± 0.21 (2) Mar ± 1.96 (14) ± 1.60 (13) ± 1.56 (3) 4.05 *Significantly different at the 5% level (t-test, p < 0.05) compared to the length in the following month. ** Significantly different at the 1% level (t-test, p < 0.01) compared to the length in the following month. a Values are the mean ± SD. Sample sizes are in parentheses. b Monthly growth rate = mean of total length of this month mean of total length of the previous month. Mean total length (mm) Mienyueh Chitou Developmental phase Figure 2. Mean total length of tadpoles in relation to developmental phases.
8 Lai et al. Table 4.Size at metamorphosis for Mienyueh and Chitou populations of Rana sauteri (a) Mienyueh Year 1996 Month May Total length (mm) ± 0.63a Weight (mg) 0.11 ± 0.02 Sample size 26 a Values are the mean ± SD (b) Chitou Year Month Nov Dec Jan Feb Mar Total length (mm) ± 0.26a ± ± ± ± 0.15 Weight (mg) 0.19 ± ± ± ± ± 0.01 Sample size a Values are the mean ± SD. in the latter. The growth of limbs can increase the surface area/volume ratio which raises the risk of limb frostbite during extreme cold temperatures between December and February. In contrast, tadpoles at Chitou showed no sign of developmental cessation probably because winter temperatures are relatively mild, and tadpoles are able to grow, develop, and achieve metamorphosis without interruption. At this point, we do not know whether the developmental cessation in Mienyueh tadpoles is temperature-induced or genetically fixed; further studies are needed to reveal the possible mechanisms underlying this phenomenon. ACKNOWLEDGEMENTS We heartily appreciate Dr. Kuang-yang Lue of National Taiwan Normal Univ., Dr. Ping-Chun Hou of National Cheng Kung Univ., and Dr. Hui- Chen Lin of Tunghai Univ. who assisted in data inventory. Thanks also go to the staff at the Experimental Forest of National Taiwan Univ. and the Taiwan Forestry Bureau for administrative assistance. This study was partially supported by the National Science Council of Taiwan (NSC B and NSC B ). REFERENCES Alford, R. A. and R. N. Harris (1988) Effect of l a r v a l gr o w t h h i s t o r y on a n u r a n metamorphosis. Am. Nat. 131: Berven, K.A. and D. E. Gill (1983) Interpreting geographic variation in life-history traits. Am. Zool. 23: Berven, K. A, D. E. Gill and S. J. Smith-Gill (1979) Countergradient selection in the green frog, Rana clamitans. Evolution 33: Chou, W. H. and I. Y. Lin (1997) Geographical variations of Rana sauteri (Anura: Ranidae) in Taiwan. Zool. Stud. 36: Duellman W. E. and L. Trueb (1986) Biology of
9 Growth and Development of Sauter s Tadpole amphibians. McGraw-Hill, New York. Feder, M. E. and W. W. Burggren (1992) Environmental physiology of the amphibian. University of Chicago Press, Chicago and London. Fellers, G. M., A. E. Launer, G. Rathbun and S. Bobzien (2001) Overwintering tadpoles in the California red-legged frog (Rana aurora draytonii). Herpetol. Rev. 32: Frieden, E., A. Wahlborg and E. Howard (1965). Temperature control of the response of tadpoles to triiodothyronine. Nature 205: Gosner, K. L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: Kollros, J. J. (1961) Mechanisms of amphibian metamorphosis: hormone. Am. Zool. 1: Kuramoto, M., C. S. Wang and H. T. Yu (1984) Breeding, larval morphology and experimental hybridization of Taiwanese brown frogs, Rana longicrus and R. sauteri. J. Herpetol. 18: Lai, S. J., Y. C. Kam and Y. S. Lin (2003) Altitudinal variation in reproductive and life history Traits of Sauter s frog Rana sauteri Boulenger, 1909 in Taiwan. Zool. Stud. 54: (in press). Lofts, B Physiology of the amphibian. Vol. 3. Academic Press, New York. Lue, K. Y., C. Y. Lin and K. S. Jung (1990) Wildlife data bank of Taiwan. (1) Amphibians (II). Ecological Research of the Council of Agriculture No. 8, Taipei. (in Chinese). Norris, D. O. and J. E. Platt (1974) T 3 - and T 4 - induced rates of metamorphosis in immature and sexually mature larvae of Ambystoma tigrinum (Amphibia: Caudata). J. Exp. Zool. 189: Roff, D. A. (1980) Optimizing development time in a seasonal environment: the ups and downs of clinal variation. Oecologia (Berlin) 45: SAS Institute (1998) StatView/Using StatView user s guide. SAS Institute, Gray, NC. Smith-Gill, S. J. and K. A. Berven (1979) Predicting amphibian metamorphosis. Am. Nat. 113: Sokal, R.R. and F. J. Rohlf (1981) Biometry: the principles and practice of statistics in biological research. Freeman, San Francisco. Viparina, S. and J. J. Just (1975) The life period, growth and differentiation of Rana catesbeiana larvae occurring in nature. Copeia 1975: Werner, E. E. (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am. Nat. 128: Wilbur, H. M. and J. P. Collins (1973) Ecological aspects of amphibian metamorphosis. Science 182:
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