Plasticity of the duration of metamorphosis in the African clawed toad

In organisms with complex life cycles, such as amphibians, selection is thought to have minimized the duration of metamorphosis, because this is the stage at which predation risk is presumed to be highest. Consequently, metamorphic duration is often assumed to show little if any environmentally induced plasticity, because the elevation in the extrinsic mortality risk associated with prolonging metamorphosis is presumed to have selected for a duration as short as is compatible with normal development. We examined the extent to which metamorphic duration in the anuran amphibian Xenopus laevis was sensitive to environmental temperature. Metamorphic duration was influenced by body size, but independent of this effect, it was strongly influenced by environmental temperature: the duration at 181C was more than double that at 24 and 301C. We also compared the vulnerability of larval, metamorphosing and post metamorphic Xenopus to predators by measuring their burst swimming speeds. Burst swim speed increased through development and while we found no evidence that it was reduced during metamorphosis, it did increase sharply on completion of metamorphosis. We therefore found no evidence of a substantial increase in vulnerability to predators during metamorphosis compared with larval stages, and hence the slowing of metamorphosis in response to temperature may not be as costly as has been assumed.

[1]  T. Watkins The effect of metamorphosis on the repeatability of maximal locomotor performance in the Pacific tree frog Hyla regilla. , 1997, The Journal of experimental biology.

[2]  R. Huey Sprint Velocity of Tadpoles (Bufoboreas) Through Metamorphosis , 1980 .

[3]  D. Policansky Size, Age and Demography of Metamorphosis and Sexual Maturation in Fishes , 1983 .

[4]  E. Werner Amphibian Metamorphosis: Growth Rate, Predation Risk, and the Optimal Size at Transformation , 1986, The American Naturalist.

[5]  Res Altwegg,et al.  PATTERNS OF NATURAL SELECTION ON SIZE AT METAMORPHOSIS IN WATER FROGS , 2003, Evolution; international journal of organic evolution.

[6]  J. Faber,et al.  Normal Table of Xenopus Laevis (Daudin) , 1958 .

[7]  D. D. Brown,et al.  Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Kraft,et al.  Predator‐specific changes in the morphology and swimming performance of larval Rana lessonae , 2005 .

[9]  Daniel Sáenz,et al.  Body shape, burst speed and escape behavior of larval anurans , 2005 .

[10]  R. Tinsley,et al.  Biology of Xenopus , 1998 .

[11]  J. Arendt,et al.  Adaptive Intrinsic Growth Rates: An Integration Across Taxa , 1997, The Quarterly Review of Biology.

[12]  H. Shaffer,et al.  The Consequences of Metamorphosis on Salamander (Ambystoma) Locomotor Performance , 1991, Physiological Zoology.

[13]  M. Yamashita,et al.  Development of Contractile and Energetic Capacity in Anuran Hindlimb Muscle during Metamorphosis , 2003, Physiological and Biochemical Zoology.

[14]  S. J. Arnold,et al.  Differential Predation on Metamorphic Anurans by Garter Snakes (Thamnophis): Social Behavior as a Possible Defense , 1978 .

[15]  K. Sillar,et al.  Developmental segregation of spinal networks driving axial‐ and hindlimb‐based locomotion in metamorphosing Xenopus laevis , 2004, The Journal of physiology.

[16]  S. Twombly Timing of Metamorphosis in a Freshwater Crustacean: Comparison with Anuran Models , 1996 .

[17]  K. Miller Effect of Temperature on Sprint Performance in the Frog Xenopus laevis and the Salamander Necturus maculosus , 1982 .

[18]  H. Wilbur Complex Life Cycles , 1980 .

[19]  R. Bryce,et al.  Metamorphic duration: an under-studied variable in frog life histories , 2004 .

[20]  E. Azizi,et al.  Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata). , 2002, The Journal of experimental biology.

[21]  R. Wassersug Locomotion in Amphibian Larvae (or “Why Aren't Tadpoles Built Like Fishes?”) , 1989 .

[22]  K. Gosner,et al.  A simplified table for staging anuran embryos and larvae with notes on identification , 1960 .

[23]  C. Rose Integrating ecology and developmental biology to explain the timing of frog metamorphosis. , 2005, Trends in ecology & evolution.

[24]  T. Uller,et al.  Population divergence of developmental thermal optima in Swedish common frogs, Rana temporaria , 2001 .

[25]  D. Alvarez,et al.  Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion , 2002, Oecologia.

[26]  Nigel Blakley,et al.  Life History Significance of Size‐Triggered Metamorphosis in Milkweed Bugs (Oncopeltus) , 1981 .

[27]  DELAYED COSTS OF AN INDUCED DEFENSE IN TADPOLES? MORPHOLOGY, HOPPING, AND DEVELOPMENT RATE AT METAMORPHOSIS , 2001, Evolution; international journal of organic evolution.

[28]  Elizabeth Sherman Ontogenetic change in thermal tolerance of the toad Bufo woodhousii fowleri , 1980 .

[29]  R. Wassersug,et al.  The Relationships of Locomotion to Differential Predation on Pseudacris Triseriata (Anura: Hylidae) , 1977 .

[30]  D. Levitis,et al.  Heat hardening as a function of developmental stage in larval and juvenile Bufo americanus and Xenopus laevis , 2003 .

[31]  R. Wilson Consequences of Metamorphosis for the Locomotor Performance and Thermal Physiology of the Newt Triturus cristatus , 2005, Physiological and Biochemical Zoology.

[32]  The implications of shape and metamorphosis for drag forces on a generalized pond tadpole (Rana catesbeiana) , 1991 .

[33]  T. Watkins Predator-Mediated Selection on Burst Swimming Performance in Tadpoles of the Pacific Tree Frog, Pseudacris regilla , 1996, Physiological Zoology.