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Hatching asynchrony, survival, and the fitness of alternative adult morphs in Ambystoma talpoideum

Oecologia volume 140, pages 46–51 (2004)Cite this article

Abstract

The mole salamander, Ambystoma talpoideum, exhibits both aquatic (gilled) and terrestrial (metamorphosed) adult morphologies. Previous studies have shown the existence of body-size advantages associated with the terrestrial morph in A. talpoideum and other polymorphic salamanders (e.g., A. tigrinum). However, aquatic adult A. talpoideum mature at a younger age and often breed earlier than terrestrial adults. We tested the hypothesis that early maturation and reproduction in aquatic adults increase fitness (irrespective of body size). We reared larval A. talpoideum in mesocosms and varied the timing of hatching, with early-hatching larvae representing the offspring from early-breeding aquatic adults, and late-hatching larvae representing the offspring of later-breeding terrestrial adults. Our results demonstrate significantly higher survival rates among early-hatchlings relative to late-hatching conspecifics, supporting the hypothesis that early reproduction may be an important mechanism mediating the polymorphism in A. talpoideum. We discuss our results within the context of size-based models of the fitness of alternative life-cycles.

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References

  • Alford RA, Wilbur HM (1985) Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology 66:1097–1105

    Google Scholar 

  • Blaustein L, Margalit J (1994) Mosquito larvae (Culiseta longiareolata) prey upon and compete with toad tadpoles (Bufo viridis). J Anim Ecol 63:841–850

    Google Scholar 

  • Blaustein L, Margalit J (1996) Priority effects in temporary pools: nature and outcome of mosquito larva-toad tadpole interactions depend on order of entrance. J Anim Ecol 65:77–84

    Google Scholar 

  • Boone MD, Scott DE, Niewiarowski PN (2002) Effects of hatching time for larval ambystomatid salamanders. Copeia 2002:511–517

    Google Scholar 

  • Boorse GC, Denver RJ (2002) Acceleration of Ambystoma tigrinum metamorphosis by corticotrophin-releasing hormone. J Exp Zool 293:94–98

    Article  CAS  PubMed  Google Scholar 

  • Collins JP, Holomuzki JR (1984) Intraspecific variation in diet within and between trophic morphs in larval tiger salamanders (Ambystoma tigrinum nebulosum). Can J Zool 62:168–174

    Google Scholar 

  • Currens CR, Niewiarowski PH, Whiteman HH (2002) Effects of temperature and time of day on the resting metabolic rates of paedomorphic and metamorphic mole salamanders, Ambystoma talpoideum. Copeia 2002:489–495

    Google Scholar 

  • Day T, Rowe L (2002) Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350

    Article  Google Scholar 

  • Denoël M, Poncin P, Ruwet JC (2001) Sexual compatibility between two heterochronic morphs in Triturus alpestris (Caudata, Salamandridae). Anim Behav 62:559–566

    Google Scholar 

  • Fauth JE (1990) Interactive effects of predators and early larval dynamics of the treefrog Hyla chrysoscelis. Ecology 71:1609–1616

    Google Scholar 

  • Fauth JE, Resetarits WJ Jr (1991) Interactions between the salamander Siren intermedia and the keystone predator Notophthalmus viridescens. Ecology 72:827–838

    Google Scholar 

  • Harris RN (1980) The consequences of within-year timing of breeding in Ambystoma maculatum. Copeia 1980:719–722

    Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont

  • Ishii R, Higashi M (2001) Coexistence induced by pollen limitation in flowering-plant species. Proc R Soc Biol Sci Ser B 268:579–585

    Article  CAS  Google Scholar 

  • Jackson ME, Semlitsch RD (1993) Paedomorphosis in the salamander Ambystoma talpoideum: effects of a fish predator. Ecology 74:342–350

    Google Scholar 

  • Krebs EA (1999) Last but not least: nestling growth and survival in asynchronously hatching crimson rosellas. J Anim Ecol 68:266–281

    Article  Google Scholar 

  • Krenz JD, Sever DM (1995) Mating and oviposition in paedomorphic Ambystoma talpoideum precedes the arrival of terrestrial males. Herpetologica 51:387–393

    Google Scholar 

  • Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford

  • Lawler SP, Morin PJ (1993) Temporal overlap, competition, and priority effects in larval anurans. Ecology 74:174–182

    Google Scholar 

  • Leips J, Travis J (1994) Metamorphic responses to changing food levels in two species of hylid frogs. Ecology 75:1345–1356

    Google Scholar 

  • Moran NA (1994) Adaptation and constraint in the complex life cycles of animals. Ann Rev Ecol Syst 25:573–600

    Article  Google Scholar 

  • Morin PJ (1987) Predation, breeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology 68:675–683

    Google Scholar 

  • Morin PJ, Lawler SP, Johnson EA (1990) Ecology and breeding phenology of larval Hyla andersonii: the disadvantages of breeding late. Ecology 71:1590–1598

    Google Scholar 

  • Olsson M, Shine R (1997) The seasonal timing of oviposition in sand lizards (Lacerta agilis): why earlier clutches are better. J Evol Biol 10:369–381

    Article  Google Scholar 

  • Patterson KK (1978) Life history aspects of paedogenic populations of the mole salamander, Ambystoma talpoideum. Copeia 1978:649–655

    Google Scholar 

  • Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institute, Washington

  • Ryan TJ, Hopkins WA (2000) Sex and size interaction and standard metabolic rate of paedomorphic Ambystoma talpoideum: size does matter. Copeia 2000:808–812

    Google Scholar 

  • Ryan TJ, Semlitsch RD (1998) Intraspecific heterochrony and life history evolution: decoupling somatic and sexual development in a facultatively paedomorphic salamander. Proc Natl Acad Sci U S A 95:5643–5648

    Article  CAS  PubMed  Google Scholar 

  • Ryan TJ, Semlitsch RD (2003) Growth and the expression of alternative life cycles in the salamander Ambystoma talpoideum (Caudata: Ambystomatidae). Biol J Linn Soc 80:639–646

    Article  Google Scholar 

  • Scott DE (1990) Effects of larval density in Ambystoma opacum: an experiment in large-scale field enclosures. Ecology 71:296–306

    Google Scholar 

  • Scott DE (1993) Timing and reproduction of paedomorphic and metamorphic Ambystoma talpoideum. Am Midl Nat 129:397–402

    Google Scholar 

  • Semlitsch RD (1985) Reproductive strategy of a facultatively paedomorphic salamander Ambystoma talpoideum. Oecologia 65:305–313

    Google Scholar 

  • Semlitsch RD (1987a) Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying. Ecology 68:994–1002

    Google Scholar 

  • Semlitsch RD (1987b) Density-dependent growth and fecundity in the paedomorphic salamander Ambystoma talpoideum. Ecology 68:1003–1008

    Google Scholar 

  • Semlitsch RD, Gibbons JW (1985) Phenotypic variation in metamorphosis and paedomorphosis in the salamander Ambystoma talpoideum. Ecology 66:1123–1130

    Google Scholar 

  • Semlitsch RD, Reichling SB (1989) Density-dependent injury in larval salamanders. Oecologia 81:100–103

    Google Scholar 

  • Semlitsch RD, Ryan TJ (1998) Migration, amphibian. In: Knobil E, Neill JD (eds) The encyclopedia of reproduction, vol 3. Academic, New York, pp 221–227

  • Semlitsch RD, Wilbur HM (1989) Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution 43:105–112.

    Google Scholar 

  • Semlitsch RD, Fauth JE, Wilbur HM (1990) Paedomorphosis in Ambystoma talpoideum: maintenance of population variation and alternative life-history pathways. Evolution 44:1604–16013

    Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK, Gibbons JW (1996) Structure and dynamics of an amphibian community: evidence from a 16-year study of a natural pond. In: Cody ML, Smallwood J (eds) Long-term studies of vertebrate communities. Academic, San Diego, pp 217–250

  • Voss SR, Prudic K, Oliver J, Shaffer HB (2003) Candidate gene analysis of metamorphic timing in ambystomatid salamanders. Mol Ecol 12:1217–1223

    CAS  PubMed  Google Scholar 

  • Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341

    Article  Google Scholar 

  • Whiteman HH (1994) Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221

    Article  Google Scholar 

  • Whiteman HH (1997) Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51:2039–2044

    Google Scholar 

  • Wilbur HM, Alford RA (1985) Priority effects in experimental pond communities: responses of Hyla to Bufo and Rana. Ecology 66:1106–1114

    Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314

    Google Scholar 

  • Winne CT, Ryan TJ (2001) Aspects of sex-specific differences in the expression of an alternative life cycle in the salamander Ambystoma talpoideum. Copeia 2001:143–149

    Google Scholar 

Download references

Acknowledgements

This manuscript was improved by comments from Ray Semlitsch and two anonymous reviewers. We were supported by Long Term Graduate Research Fellowships awarded by the University of Georgia and the Savannah River Ecology Laboratory Education Program. This research was supported by a Doctoral Dissertation Improvement Grant (DEB 9801458) awarded to T.J.R. and R.D. Semlitsch and Financial Assistance Award Number DE-FC09-96SR18546 from the US Department of Energy to the University of Georgia Research Foundation.

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  1. Travis J. Ryan

    Present address: Department of Biological Sciences, Butler University, Indianapolis, IN 46208, USA

  2. Gordon R. Plague

    Present address: Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721-0088, USA

Authors and Affiliations

  1. University of Georgia’s Savannah River Ecology Laboratory, Drawer E, Aiken, SC 29802, USA

    Travis J. Ryan & Gordon R. Plague

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  1. Travis J. Ryan
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Correspondence to Travis J. Ryan.

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Ryan, T.J., Plague, G.R. Hatching asynchrony, survival, and the fitness of alternative adult morphs in Ambystoma talpoideum . Oecologia 140, 46–51 (2004). https://doi.org/10.1007/s00442-004-1563-x

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  • DOI: https://doi.org/10.1007/s00442-004-1563-x

Keywords

  • Life-cycle polymorphism
  • Intraspecific priority effects
  • Metamorphosis
  • Paedomorphosis