¤ 2009 Zoological Society of Japan
ZOOLOGICAL SCIENCE 26: 476–482 (2009)
Effects of Salinity on the Survival, Growth, Development, and Metamorphosis of Fejervarya limnocharis Tadpoles Living in Brackish Water Chi-Shiun Wu and Yeong-Choy Kam* Department of Life Science, Tunghai University, Taichung 407, Taiwan
We studied salinity tolerance and the effects of salinity on growth, development, and metamorphosis in Fejervarya limnocharis tadpoles living in brackish water. Specifically, we examined whether tadpoles exhibit adaptive plasticity in development when exposed to different salinities. Tadpoles collected on Green and Orchid Islands off Southeastern Taiwan were assigned to salinities of 0, 3, 5, 7, 9, 11, and 13 parts per thousand (ppt). The daily survival, weekly growth, and development of tadpoles were recorded until metamorphosis. More than 50% of tadpoles survived in 9 ppt for over a month, and a few individuals survived in 11 ppt for 20 days, suggesting that F. limnocharis tadpoles tolerate salinity better than the tadpoles of most species studied to date. Tadpoles at 9 ppt had lower survivorship, and retarded growth and development (from Gosner stage 26 to 35) compared to the other treatments. Tadpoles metamorphosed early at a smaller size as salinity increased, suggesting the existence of adaptive developmental plasticity in F. limnocharis in response to osmotic stress. Phenotypic plasticity in the age and size at metamorphosis in response to salinity may provide a means for tadpoles to adapt to the unpredictable salinity variation in coastal rock pools. Key words: Fejervarya limnocharis, salinity, brackish water, growth, development, metamorphosis, phenotypic plasticity, tadpole INTRODUCTION Many anurans breed in temporary pools, which are characterized by temporal and spatial unpredictability in water availability (Alford, 1999). Before metamorphosis, anuran larvae are exposed to several kinds of physical stress (Duellman and Trueb, 1994; Alford, 1999). Various environmental factors, including pond drying, food availability, temperature, and predators, are known to influence both the time to and size at metamorphosis of anuran larvae by affecting growth and developmental rates (Alford, 1999; Bruce, 2005; Rose, 2005). Amphibian larvae exhibit high plasticity in metamorphic traits as a consequence of adapting to environmental heterogeneity and unpredictability (Newman, 1992; Rudolf and Rödel, 2007). Metamorphosing early allows larvae facing deteriorating habitats, such as pond drying, increasing density of predators and competitors, and decreasing food, to evade risks associated with the aquatic environment (Newman, 1989; Newman, 1992). However, the cost of metamorphosing early is sacrificing the potential opportunity to grow during the larval phase (Newman, 1992). Smaller size at metamorphosis decreases the ability to tolerate dehydration (Newman and Dunham, 1994) and the likelihood of post-metamorphic survival (Smith, 1987; Berven, 1990; Chelgren et al., 2006), delays * Corresponding author. Phone: +886-4-23550609; Fax : +886-4-23590296; E-mail:
[email protected] doi:10.2108/zsj.26.476
the time to maturity (Semlitsch, 1988; Berven, 1990), and reduces the size at maturity (Semlitsch, 1988), overall reducing recruitment to the breeding population (Smith, 1987). Salinity potentially influences the abundance and distribution of amphibians by imposing osmotic stress (Smith et al., 2007). The issue of salinity effects on amphibian biology and ecology has recently drawn more attention, for at least two reasons. First, several studies have revealed that amphibians breed in brackish water more commonly than originally thought, and that they exhibit interesting physiological and ecological adjustments to increased salinity stress (Ruibal, 1959; Gordon et al., 1961; Gordon and Tucker, 1965; Beebee, 1985; Uchiyama et al., 1990; Møbjerg et al., 2000; Gomez-Mestre and Tejedo, 2003; Gomez-Mestre et al., 2004; Haramura, 2004). Second, amphibians are important indicator species for freshwater ecosystems that face increased salinization due to natural causes (Nielsen et al., 2003; Rios-López, 2008), or to anthropogenic causes (Chinathamby et al., 2006; Smith et al., 2007) such as salt pollution resulting from road de-icing salt runoff (Sanzo and Hecnar, 2006; Karraker, 2007). Most amphibians do not adapt well to brackish water because their skin is highly permeable, posing problems for water and ion balance (Balinsky, 1981; Duellman and Trueb, 1994). Moderate salinity, i.e., 2–9 ppt (parts per thousand), can decrease survival, growth, and development (Gordon and Tucker, 1965; Beebee, 1985; Christy and Dickman, 2002; Gomez-Mestre et al., 2004; Chinathamby et al., 2006; Sanzo and Hecnar, 2006), and cause abnormalities in
Effects of Salinity on Tadpoles
tadpoles (Chinathamby et al., 2006; Karraker, 2007). Euryhaline tadpoles of Fejervarya cancrivora (formerly known as Rana cancrivora), which live in mangrove swamps experiencing wide salinity fluctuations (Alcala, 1962; Gordon and Tucker, 1965; Dunson, 1977; Uchiyama et al., 1990), can tolerate extremely high salinity (≥35 ppt) but suffer developmental retardation to the point of preventing metamorphosis (Gordon, 1961; Gordon and Tucker, 1965; Dunson, 1977; Uchiyama et al., 1990). Delayed time to metamorphosis incurs an increased risk of desiccation (Newman, 1992; Gomez-Mestre and Tejedo, 2002) and predation (Alford, 1999). Fejervarya limnocharis, a common species widely distributed throughout Asia, generally breeds in freshwater (Lue et al., 1999). Nonetheless, our field surveys have revealed that it also commonly breeds in the brackish water of coastal rock pools formed by uplifted coral on tropical Green and Orchid Islands, Taiwan (Fig. 1). These temporary pools used by F. limnocharis tadpoles vary in shape, size, and depth, and can be as close as 4 m to the shore waterline (Fig. 1). Tadpoles confined to these small pools face fluctuations in salinity resulting from rainfall, evaporation, and seawater spray. Salinity increases gradually due to high evaporation in temporary ponds, possibly reaching harmful levels. Being able to cope with such remarkable salinity fluctuation is critical for the successful development of F. limnocharis tadpoles. The purpose of this study was to assess the effects of salinity on the ecology and physiology of F. limnocharis tadpoles. Specifically, we studied the salinity tolerance of tadpoles and salinity effects on growth, development, and metamorphosis. We also tested whether tadpoles exhibit adaptive plasticity in development when exposed to osmotic stress. MATERIALS AND METHODS Study animals Fejervarya limnocharis (Rana limnocharis) is a medium-sized frog (30–60 mm) distributed throughout East, Southeast, and South Asia, including many small, isolated islands (Sumida et al., 2007). Allozyme data (Toda et al., 1997; Toda et al., 1998; Toda, 1999) suggest the occurrence of gene flow among East Asian F. limnocharis populations. In Taiwan, F. limnocharis is widely distrib-
Fig. 1. (A) Coastal rock pools formed by uplifted coral on tropical Green Island. The arrow indicates the site of some pools where tadpoles were found. (B) Close-up view of a pool inhabited by tadpoles. (C) Tadpoles in a rock pool.
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uted up to elevations of 1000 m on the main island and off-shore islands (Alexander et al., 1979; Yang, 1998; Lue et al., 1999). Although F. limnocharis has the potential for breeding the year around, it usually breeds only from February to September (Alexander et al., 1979). Breeding is correlated with rainfall and irrigation and is restricted by low temperatures (Alexander et al., 1979). This species usually breeds in temporary freshwater pools such as rice pools and roadside puddles, but some populations breed in the brackish water of rock pools in coastal areas. Amplexus occurs after midnight and spawning occurs at dawn (Alexander et al., 1979). Mean clutch size varies greatly, with a range of about 450–1800, and the larval period is less than two months (Alexander et al., 1963, 1979). Study areas and sites of tadpole collection Area and location Green Island (121.28°E, 22.35°N) and Orchid Island (121.33°E, 22.25°N) are two small tropical islands off the southeastern coast of Taiwan. The climate on both islands is characterized by high air temperature and abundant annual rainfall, with no distinct dry season (Ni, 2003). Typhoons are frequent between June and September on both islands, and usually bring abundant rains. Green Island covers an area of 15 km2. From 1998–2006, the average air temperature was 23.5°C and the annual rainfall was 2575 mm (data from the Central Weather Bureau). During the breeding season of F. limnocharis (February–September), the most abundant rains occurred mainly from July to September (average monthly rainfall about 290–320 mm). Orchid Island covers an area of 46 km2. From 1998–2006, the average air temperature was 22.8°C and annual rainfall was 3060 mm (data from the Central Weather Bureau). During the breeding season, the most abundant rains occurred mainly from May to September (average monthly rainfall about 260–370 mm). Characteristics of rock pools with tadpoles Fejervarya limnocharis usually breeds in rock pools above the high tide line. Some pools are quite near the sea (
