Skip to main content
Log in

Parental care and EGG size in salamanders: An examination of the safe harbor hypothesis

  • Published:
Researches on Population Ecology

Summary

The safe harbor hypothesis includes the suggestion that parental care causes the embryonic stage to be the safest harbor, and, therefore, egg size will increase in populations with parental care to decrease the duration of subsequent, higher risk stages. Neither the safe habor hypothesis nor r and K theory seem adequate to explain the correlation between egg size and the presence/absence of parental care among salamanders, a group in which there is a further correlation between the larval (hatchling) habitat and egg size/parental care. Pond-breeding salamanders generally have small eggs and lack parental care, and stream-breeding salamanders generally have large eggs and parental care. I argue that the fundamental difference in the food available to hatchling salamanders between lentic (plankton-rich) and lotic (plankton-poor) environments selects for relatively lower parental investment in the lentic environment. From the standpoint of parental fitness, small (more numerous) hatchlings have a greater payoff where the available food is mall and dense (zooplankton in lentic environments), and large hatchlings are selectively advantageous where the food is of large size and less dense (benthic invertebrates in lotic environments). Selection for larger hatchlings in lotic environments results in longer embryonic periods and,ceteris paribus, greater total embryonic mortality. Embryo hiding and guarding have evolved among lotic-breeding salamanders as compensatory mechanisms to reduce the rate of embryonic mortality. In this view, parental care is a consequence of selection for larger egg size and not an umbrella that allows egg size to increase, contrary to the safe harbor hypothesis.

The relationship between variance in parental investment and food available to offspring, developed here for salamanders, may be of general significance. YosiakiItô, a critic of r and K theory, independently arrived at a similar conclusion from a broader data base.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alcher, M. (1981a) Reproduction en elevage deEuproctus platycephalus (Urodela, Salamandridae).Amphibia-Reptilia 2: 97–105.

    Google Scholar 

  • Alcher, M. (1981b) Sur l'existence de soins parentaux chezEuproctus montanus (Urodela, Salamandridae).Amphibia-Reptilia 2: 189–194.

    Google Scholar 

  • Allen, W. E. (1920) A quantitative and statistical study of the plankton of the San Joaquin River and its tributaries in and near Stockton, California, in 1913.Univ. Calif. Publ. Zool. 22: 1–292.

    Google Scholar 

  • Anderson, J. D. (1967) A comparison of the life histories of coastal and montane populations ofAmbystoma macrodactylum in California.Amer. Midl. Nat. 77: 323–355.

    Article  Google Scholar 

  • Anderson, J. D. (1968) A comparison of the food habits ofAmbystoma macrodactylum sigillatum, Ambystoma macrodactylum croceum, andAmbystoma tigrinum califoriense.Herpetologica 24: 273–284.

    Google Scholar 

  • Anderson, J. D. andG. K. Williamson (1976) Terrestrial mode of reproduction inAmbystoma cingulatum.Herpetologica 32: 214–221.

    Google Scholar 

  • Anderson, P. L. (1943) The normal development ofTriturus pyrrhogaster.Anat. Rec. 86: 59–63.

    Article  Google Scholar 

  • Antonelli, A. L., R. A. Nussbaum andS. D. Smith (1972) Comparative food habits of four species of stream-dwelling vertebrates (Dicamptodon ensatus, D. copei, Cottus tenuis, Salmo gairdneri).Northwest Sci. 46: 277–289.

    Google Scholar 

  • Avery, R. A. (1968) Food and feeding relations of three species ofTriturus (Amphibia Urodela) during the aquatic phases.Oikos 19: 408–412.

    Google Scholar 

  • Bell, G. (1974) The reduction of morphological variation in natural populations of smooth newt larvae.J. Anim. Ecol. 43: 115–128.

    Article  Google Scholar 

  • Bell, G. (1975) The diet and dentition of smooth newt larvae (Triturus vulgaris).J. Zool. (London)176: 411–424.

    Article  Google Scholar 

  • Bell, G. andJ. H. Lawton (1975) The ecology of the eggs and larvae of the smooth newt (Triturus vulgaris (Linn.)).J. Anim. Ecol. 44: 393–423.

    Article  Google Scholar 

  • Birge, E. A. andC. Juday. (1922) The inland lakes of Wisconsin. The plankton. I. Its quantity and chemical composition.Wis. Geol. Nat. Hist. Survey, Bull. Sci. ser 64 1–222.

    Google Scholar 

  • Bishop, S. C. (1920) Notes on the habits and development of the four-toed salamander,Hemidactylium scutatum (Schlegel).New York State Mus. Bull. 219: 251–282.

    Google Scholar 

  • Bishop, S. C. (1936) Notes on the habits and development of the mudpuppyNecturus maculosus (Rafinesque).New York State Mus. Bull. 268: 5–61.

    Google Scholar 

  • Bishop, S. C. (1941) The salamanders of New York.New York State Mus. Bull. 324: 1–365.

    Google Scholar 

  • Bishop, S. C. (1943)Handbook of salamanders. Comstock, Ithaca.

    Google Scholar 

  • Branch, L. C. andR. Altig (1981) Nocturnal stratification of three species ofAmbystoma larvae.Copeia 1981: 870–873.

    Article  Google Scholar 

  • Brandon, R. A. andR. G. Altig (1973) Eggs and small larvae of two species ofRhyacosiredon.Herpetologica 29: 349–351.

    Google Scholar 

  • Breder, C. M. (1935) The reproductive habits of the common catfish,Ameiurus nebulosus (LeSueur), with a discussion of their significance in ontogeny and phylogeny.Zoologica 19: 143–179.

    Google Scholar 

  • Briegleb, W. andJ. Schwartzkopff. (1961) Verhaltensweisen des Grottenolms (Proteus anguinus Laur.) und das Problem des Fortplanzungsraumes.Naturwissenschaften 22: 1–3.

    Google Scholar 

  • Brockelman, W. Y. (1975) Competition, the fitness of offspring, and optimal clutch size.Amer. Natur. 109: 677–699.

    Article  Google Scholar 

  • Brodie, E. D., Jr., J. L. Hensel, Jr. andJ. A. Johnson (1974) Toxicity of the urodele amphibiansTaricha, Notophthalmus, Cynops, andParamesotriton (Salamandridae).Copeia 1974: 506–511.

    Article  Google Scholar 

  • Brown, H. A. (1976) The time-temperature relation of embryonic development in the northwestern salamander,Ambystoma gracile.Can. J. Zool. 54: 552–558.

    Google Scholar 

  • Bruce, R. C. (1968) Life history studies of the salamanders of the genusPseudotriton (Caudata: Plethodontidae). Ph.D. Dissertation, Duke University.

  • Cadwallader, P. L. (1976) Breeding biology of a non-diadromous galaxiid,Galaxias vulgaris Stokell, in a New Zealand river.J. Fish. Biol. 8: 157–177.

    Article  Google Scholar 

  • Connon, F. E. (1947) A comparative study of the respiration of normal and hybridTriturus embryos and larvae.J. Exp. Zool. 105: 1–24.

    Article  CAS  Google Scholar 

  • Curtis, B. (1938)The life story of the fish. D. Appleton-Century Co., New York.

    Google Scholar 

  • Despax, R. (1923) Contribution a l'etude anatomique et biologique des batraciens urodeles, du groupe des euproctes et specialement de l'euprocte des PyreneesTriton (Euproctus) asper Duges Theses pour Docteur Sci. Nat. Toulouse, Ser. A, No.929.

  • Dodson, S. I. (1970) Complementary feeding niches sustained by size-selective predation.Limnol. and Oceanog. 15: 131–137.

    Google Scholar 

  • Duellman, W. E. andJ. T. Wood (1954) Size and growth of the two-lines salamander,Eurycea bislineata rivicola.Copeia 1954: 92–96.

    Article  Google Scholar 

  • Dunn, E. R. (1923) The breeding habits of salamanders and their bearing on phylogeny.Copeia 115: 25–28.

    Google Scholar 

  • Dunn, E. R. (1926)Salamanders of the family Plethodontidae. Smith College, Fiftieth Anniversary Publ. ser. Vol.7.

  • Ferrier, V. (1974) Chronologie du developpement de l'amphibien urodeleTylotriton verrucosus Anderson (Salamandridae).Ann. d'Embryol. et de Morphogenese 7: 407–416.

    Google Scholar 

  • Gallien, L. andO. Bidaud (1959) Table chronologique de developpement chezTriturus helveticus Raz.Bull. Soc. Zool. Fr. 84: 22–32.

    Google Scholar 

  • Gallien, L. andM. Durocher (1957) Table chronologique de developpement chezPleurodeles waltlii Michah.Bull. Biol. Fr. Belg. 91: 97–114.

    Google Scholar 

  • Gasser, F. (1964) Observations sur les stades initiaux du developpment de l'urodele PyreneenEuproctus asper.Bull. Soc. Zool. Fr. 89: 423–428.

    Google Scholar 

  • Gould, S. J. (1977)Ontogeny and phylogeny. Belknap Press, Harvard UniversityCambridge.

    Google Scholar 

  • Green, N. B., P. Brant, Jr., andB. Dowler (1967)Eurycea lucifuga in West Virginia: its distribution, ecology, and life history.Proc. W. Virginia Acad. Sci. 39: 297–304.

    Google Scholar 

  • Hamilton, W. J., Jr. (1940) The feeding habits of larval newts with reference to availability and selection of food items.Ecology 21: 351–356.

    Article  Google Scholar 

  • Hardin, G. (1956) Meaninglessness of the word protoplasm.Sci. Monthly 82: 112–120.

    Google Scholar 

  • Hardy, J. D., Jr. (1969) A summary of recent studies on the salamander,Ambystoma mabeei.Chesapeake Biol. Lab. Ref. No.69-20: 1–3.

    Google Scholar 

  • Hirschfield, M. F. andD. W. Tinkle (1975) Natural selection and the evolution of reproductive effort.Proc. Nat. Acad. Sci. 72: 2227–2231.

    Article  Google Scholar 

  • Hutchinson, V. H. (1956) Notes on the plethodontid salamanders,Eurycea lucifuga (Rafinesque), andEurycea longicauda longicauda (Green).Occas. Paps. Natl. Speleol. Soc. 3: 1–24.

    Google Scholar 

  • Itô, Y. (1959)Comparative ecology. Iwanami, Tokyo (in Japanese).

    Google Scholar 

  • Itô, Y. (1970) Groups and family bonds in animals in relation to their habitat. 389–415. InL. R. Aronson, E. Tobach, D. S. Lehrman andJ. S. Rosenblatt (eds)Development and evolution of behavior. W. H. Freeman and Co., San Francisco.

    Google Scholar 

  • Itô, Y. (1980)Comparative ecology. Second ed., trans. byJ. Kikkawa. Cambridge University Press, Cambridge.

    Google Scholar 

  • Itô, Y. andY. Iwasa (1981) Evolution of litter size I. Conceptual reexamination.Res. Popul. Ecol. 23: 344–359.

    Google Scholar 

  • Iwasawa, H. andY. Kera (1980) Normal stages of development of the Japanese lungless salamander,Onychodactylus japonicus (Houttuyn).Jap. J. Herpetol. 8: 73–89 (in Japanese).

    Google Scholar 

  • Kaplan, R. H. (1980) The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders (Ambystoma).Evolution 34: 51–64.

    Article  Google Scholar 

  • Kerbert, C. (1904) Zur Fortpflanzung vonMegalobatrachus maximus Schlegel (Cryptobranchus japonicus v.d. Hoeven).Zool. Anz. 27: 305–320.

    Google Scholar 

  • Knight, F. C. E. (1938) Die Entwicklung vonTriton alpestris bei verschiedenen Temperaturen mit Normentafel.Wilhelm Roux's Archives 137: 461–473.

    Article  Google Scholar 

  • Kuramoto, M. (1978) Correlations of quantitative parameters of fecundity in amphibians.Evolution 32: 287–296.

    Article  Google Scholar 

  • Lack, D. (1954) The evolution of reproductive rates. 143–156. InJ. Huxley, A. C. Hardy andE. B. Ford (eds)Evolution, as a process. Allen and Unwin, London.

    Google Scholar 

  • Licht, L. E. (1975a) Comparative life history features of the western spotted frog,Rana pretiosa, from low-and high-elevation populations.Can. J. Zool. 53: 1254–1257.

    Article  Google Scholar 

  • Licht, L. E. (1975b) Growth and food of larvalAmbystoma gracile from a lowland population in southwestern British Columbia.Can. J. Zool. 53: 1716–1722.

    Google Scholar 

  • MacArthur, R. H. (1962) Some generalized theorems of natural, selection.Proc. Natl. Acad. Sci. 48: 1893–1897.

    Article  PubMed  CAS  Google Scholar 

  • MacArthur, R. H. andE. O. Wilson (1967) The theory of island biogeography. Princeton University Press, Monographs in Pop. Biol.1.

  • Martof, B. S. (1962) Some aspects of the life history and ecology of the salamanderLeurognathus.Amer. Midl. Natur.,67: 1–35.

    Article  Google Scholar 

  • Noble, G. K. (1927) The value of life history data in the study of the evolution, of the Amphibia.Ann. New York Acad. Sci. 30: 31–128.

    Google Scholar 

  • Noble, G. K. andM. K. Brady (1933) Observations of the life history of the marbled salamander,Ambystoma opacum Gravenhorst.Zoologica 11: 89–132.

    Google Scholar 

  • Nussbaum, R. A. (1969a) Nests and eggs, of the Pacific giant salamander,Dicamptodon ensatus (Eschscholtz).Herpetologica 25: 257–262.

    Google Scholar 

  • Nussbaum, R. A. (1969b) A nest site of the Olympic salamander,Rhyacotriton olympicus (Gaige).Herpetologica 25: 277–278.

    Google Scholar 

  • Nussbaum, R. A. (1985) The evolution of parental care in salamanders.Misc. Publ. Museum of Zoology, University of Michigan 169: 1–50.

    Google Scholar 

  • Nussbaum, R. A. andC. K. Tait (1977) Aspects of the life history and ecology of the Olympic salamander,Rhyacotriton olympicus (Gaige).Amer. Midl. Natur. 98: 176–199.

    Article  Google Scholar 

  • Nussbaum, R. A., E. D. Brodie, Jr. andR. M. Storm (1983) Amphibians and reptiles of the Pacific Northwest. University of Idaho Press, Moscow.

    Google Scholar 

  • Orr, L. P. andW. T. Maple (1978) Competition avoidance mechanisms in salamander larvae of the genusDesmognathus.Copeia 1978: 679–7685.

    Article  Google Scholar 

  • Parry, G. D. (1981) The meanings of r-and K-selection.Oecologia 48: 260–264.

    Article  Google Scholar 

  • Pearre, J. Jr. (1980) Feeding by Chaetognatha: the relation of prey size to predator size in several species.Mar. Ecol. Prog. Ser. 3: 125–134.

    Google Scholar 

  • Pennak, R. W. (1943) Limnological variables in a Colorado mountain stream.Amer. Midl. Natur. 29: 186–199.

    Article  CAS  Google Scholar 

  • Petranka, J. W. andJ. G. Petranka (1980) Selected aspects of the larval ecology of the marbled salamanderAmbystoma opacum in the southern portion of its range.Amer. Midl. Natur. 104: 352–363.

    Article  Google Scholar 

  • Petranka, J. W., J. J. Just andE. C. Crawford (1982) Hatching of amphibian embryos: the physiological trigger.Science 217: 257–259.

    Article  PubMed  CAS  Google Scholar 

  • Pianka, E. R. (1970) On r-and K-selection.Amer. Natur. 104: 592–597.

    Article  Google Scholar 

  • Pianka, E. R. (1978)Evolutionary ecology. Harper New York.

    Google Scholar 

  • Pope, C. H. (1924) Notes on North Carolina salamanders with especial reference to the egg-laying habits ofLeurognathus andDesmognathus.Amer. Mus. Novit. 153: 1–15.

    Google Scholar 

  • Regal, P. J. (1966) Feeding specializations and the classification of terrestrial salamanders.Evolution 20: 392–407.

    Article  Google Scholar 

  • Riemer, W. J. (1958) Variation and systematic relationships within the salamander genusTaricha..Univ. Calif. Publ. Zool. 56: 301–390.

    Google Scholar 

  • Salthe, S. N. (1969) Reproductive modes and the number and sizes of ova in the urodeles.Amer. Midl. Nat. 81: 467–490.

    Article  Google Scholar 

  • Salthe, S. N. andW. E. Duellman (1973) Quantitative constraints associated with reproductive mode in anurans. 229–249. InJ. L. Vial, (ed)Evolutionary biology of the anurans. Univ. Missouri Press, Columbia.

    Google Scholar 

  • Shine, R. (1978) Propagule size and parental care: the “safe harbor” hypothesis.J. Theor. Biol. 75: 417–424.

    Article  PubMed  CAS  Google Scholar 

  • Smith, B. G. (1907) The life history and habits ofCryptobranchus allegheniensis.Biol. Bull. 13: 5–39

    Google Scholar 

  • Smith, B. G. (1912) The embryology ofCryptobranchus allegheniensis, including comparisons with some other vertebrates.J. Morphol. 23: 61–157.

    Article  Google Scholar 

  • Smith, C. S. andS. D. Fretwell (1974) The optimal balance between size and number of offspring.Amer. Natur. 108: 499–506.

    Article  Google Scholar 

  • Stearns, S. C. (1977) The evolution of life history traits: a critique of the theory and a review of the data.Ann. Rev. Ecol. Syst. 8: 145–171.

    Article  Google Scholar 

  • Strathmann, R. R. (1977) Egg size, larval development, and juvenile size in benthic marine invertebrates.Amer. Natur. 111: 373–376.

    Article  Google Scholar 

  • Svärdson, G. (1949) Natural selection and egg number in fish.Institute of Freshwater Research, Fishery Board of Sweden. Rept. No.29: 115–122.

    Google Scholar 

  • Tago, K. (1929) Notes on the habits and life history ofMegalobatrachus japonicus.X e Congress Internatl. Zool. Budapest1: 828–838.

    Google Scholar 

  • Thorn, R. (1968) Les salamanders d'Europe, d'Asie, et d'Afrique du nord. Paul Lechevalier, Paris.

    Google Scholar 

  • Thorson, G. (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the sound (Oresund).Medd. Komm. Danm. Fisk.—og Havunders., Ser. Plankton 4: 1–523.

    Google Scholar 

  • Tilley, S. G. (1968) Size-fecudity relationships and their evolutionary implications in five desmognathine salamanders.Evolution 22: 806–816.

    Article  Google Scholar 

  • Tilley, S. G. (1970) Aspects of the reproductive ecology ofDesmognathus ochrophaeus in the southern Appalachian Mountains. Ph.D. Thesis, Univ. Mich, Ann Arbor.

    Google Scholar 

  • Twitty, V. C. (1936) Correlated genetic and embryological experiments onTriturus. I and II.J. Exp. Zool. 74: 239–302.

    Article  Google Scholar 

  • Twitty V. C. (1966)Of scientists and salamanders. W. H. Freeman, San Francisco.

    Google Scholar 

  • Utsunomiya, Y. andT. Utsunomiya (1977) On the development ofTylototriton andersoni.J. Fac. Fish. Anim. Husb., Hiroshima Univ. 16: 65–76 (in Japanese).

    Google Scholar 

  • Vance, R. R. (1973a) On reproductive strategies in marine benthic invertebrates.Amer. Natur. 107: 339–352.

    Article  Google Scholar 

  • Vance R. R. (1973b) More on reproductive strategies in marine benthic invertebrates.Amer. Natur. 107: 353–361.

    Article  Google Scholar 

  • Vandel, A. andM. Bouillon (1959) La reproduction du Protee (Proteus anguinus Laurenti).C. R. Acad. Sci. Paris 248: 1267–1272.

    Google Scholar 

  • Wake, D. B. (1966) Comparative osteology and evolution of the lungless salamanders, family Plethodontidae.Mem. So. Calif. Acad. Sci. 4: 1–111.

    Google Scholar 

  • Welch P. S. (1935)Limnology McGraw-Hill Book Co., Inc., New York.

    Google Scholar 

  • Werner, E. A. (1974) The fish size, prey size, handling time relation in several sunfishes and some implications.J. Fish. Res. Bd. Can. 31: 1531–1536.

    Google Scholar 

  • Wilbur, H. M., D. W. Tinkle andJ. P. Collins (1974) Environmental certainty, trophic level, and resource availability in life history evolution.Amer. Natur 108: 805–817.

    Article  Google Scholar 

  • Williams, G. C. (1966)Adaptation and natural selection: a critique of some current evolutionary thought Princeton University Press, Princeton, N.J.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nussbaum, R.A. Parental care and EGG size in salamanders: An examination of the safe harbor hypothesis. Res Popul Ecol 29, 27–44 (1987). https://doi.org/10.1007/BF02515423

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02515423

Keywords

Navigation