Abstract
We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander, Ambystoma macrodactylum columbianum. Larvae in some populations of this species exhibit trophic polymorphism, with some individuals possessing exaggerated trophic features characteristic of a cannibalistic morphology in larval Ambystoma; e.g. a disproportionately broad head and hypertrophied vomerine teeth. We hypothesized that 1) head shape variation results from feeding upon different types of prey and that 2) cannibal morphs are induced by consumption of conspecifics. To induce variation, we fed three groups of larvae different diets: 1) brine shrimp nauplii only; 2) nauplii plus anuran tadpoles; 3) nauplii, tadpoles and conspecific larval salamanders. Comparisons of size (mass)-adjusted means revealed that this manipulation of diet induced significant variation in six measures of head shape, but not in the area of the vomerine tooth patch. For five of the six head traits, larvae that ate tadpoles and brine shrimp nauplii developed significantly broader, longer and deeper heads than did larvae that only ate brine shrimp nauplii. The ingestion of conspecifics, in addition to nauplii and tadpoles, significantly altered two head traits (interocular-width and head depth), compared to larvae only fed nauplii and tadpoles. Canonical discriminant function analysis detected two statistically reliable canonical variables: head depth was most highly associated with the first canonical variable, whereas three measures of head width (at the jaws, gills and eyes) and interocular width were most highly associated with the second canonical variable. Despite this diet-enhanced morphological variation, there was no indication that any of the three types of diet (including conspecific prey) induced the exaggerated trophic features of the “cannibal” morph in this species. These results illustrate that ingestion of different types of prey contributes to plasticity in head shape, but that some other proximate cue(s), either alone or in combination with diet variation, is essential to induce the extremes of trophic polymorphism in this species.
Similar content being viewed by others
References
Bentzen P, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Can J Zool 62: 2280–2286
Bernays EA (1986) Diet-induced head allometry among foliagechewing insects and its importance for graminivores. Science 231: 495–497
Collins JP (1981) Distribution, habitats and life history variation in the tiger salamander, Ambystoma tigrinum, in east-central and southeast Arizona. Copeia 1981: 666–675
Collins JP, Cheek JE (1983) Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum. Am Zool 23: 77–84
Collins JP, Mitton JB, Pierce BA (1980) Ambystoma tigrinum: a multispecies conglomerate? Copeia 1980: 938–941
Forsman A, Lindell LE (1993) The advantage of a big head: swallowing performance in adders, Vipera berus. Funct Ecol 7: 183–189
Gilbert JJ (1980) Developmental polymorphism in the rotifer Asplanchna sieboldi. Am Sci 68: 636–645
Greene E (1989) A diet-induced developmental polymorphism in a caterpillar. Science 243: 643–646
Harrison RG (1969) Harrison stages and description of the normal development of the spotted salamander, Amblystoma punctatum (Linn.). In: Harrison RG (ed) Organization and development of the embryo. Yale University Press, New Haven, Connecticut, pp 44–66
Holomuzki JR (1986) Intraspecific predation and habitat use by tiger salamanders (Ambystoma tigrinum nebulosum). J Herpetol 20: 439–441
Lannoo MJ, Bachmann MD (1984) Aspects of cannibalistic morphs in a population of Ambystoma t. tigrinum larvae. Am Midl Nat 112: 103–109
Lannoo MJ, Lowcock L, Bogart JP (1989) Sibling cannibalism in noncannibal morph Ambystoma tigrinum larvae and its correlation with high growth rates and early metamorphosis. Can J Zool 67: 1911–1914
Lavin PA, McPhail JD (1986) Adaptive divergence of trophic phenotype among freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Can J Fish Aquat Sci 43: 2455–2463
Meyer A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357–1369
Meyer A (1989) Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fish, Cichlasoma citrinellum. Oecologia 80: 431–436
Meyer A (1990) Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol J Linn Soc 39: 279–299
Mittelbach GG, Osenberg CW, Wainwright PC (1992) Variation in resource abundance affects diet and feeding morphology in the pumpkinseed sunfish (Lepomis gibbosus). Oecologia 90 8–13
Moore WJ (1965) Masticatory function and skull growth. J Zool 146: 123–131
Newman RA (1992) Adaptive plasticity in amphibian metamorphosis. BioScience 42: 671–678
Nyman S, Wilkinson RF, Hutcherson JE (1993) Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). J Herpetol 27: 78–84
Pedersen SC (1991) Dental morphology of the cannibal morph in the tiger salamander, Ambystoma tigrinum. Amphibia-Reptilia 12: 1–14
Pfennig DW (1989) Evolution, development, and behavior of alternative amphibian morphologies. PhD Diss, Univ of Texas, Austin
Pfennig DW (1990) The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia 85: 101–107
Pfennig DW (1992a) Proximate and functional causes of polyphenism in an anuran tadpole. Funct Ecol 6: 167–174
Pfennig DW (1992b) Polyphenism in spadefoot toad tadpoles as a locally adjusted evolutionarily stable strategy. Evolution 46: 1408–1420
Pfennig DW, Loeb MLG, Collins JP (1991a) Pathogens as a factor limiting the spread of cannibalism in tiger salamanders. Oecologia 88: 161–166
Pfennig DW, Mabry A, Orange D (1991b) Environmental causes and correlations between age and size at metamorphosis in Scaphiopus multiplicatus. Ecology 72: 2240–2248
Pierce BA, Mitton JB, Jacobson L, Rose FL (1983) Head shape and size in cannibal and noncannibal larvae of the tiger salamander from west Texas. Copeia 1983: 1006–1012
Pomeroy LV (1981) Developmental polymorphism in the tadpoles of the spadefoot toad Scaphiopus multiplicatus. PhD Diss, Univ of California, Riverside
Powers JH (1903) The causes of acceleration and retardation in the metamorphosis of Amblystoma tigrinum: a preliminary report. Am Nat 37: 385–410
Powers JH (1907) Morphological variation and its causes in Amblystoma tigrinum. Stud Univ Nebraska 7: 197–274
Reilly SM, Lauder GV, Collins JP (1992) Performance consequences of a trophic polymorphism: feeding behavior in typical and cannibal phenotypes of Ambystoma tigrinum. Copeia 1992: 672–679
Rose FL, Armentrout D (1976) Adaptive strategies of Ambystoma tigrinum Green inhabiting the Llano Estacado of west Texas. J Anim Ecol 45: 713–729
SAS Institute (1988) SAS/STAT user's guide, release 6.03 ed. SAS Institute Inc., Cary, North Carolina
Smith TB (1987) Bill size polymorphism and intraspecific niche utilization in an African finch. Nature 329: 717–719
Smith TB (1990) Resource use by bill morphs of an African finch: evidence for intraspecific competition. Ecology 71: 1246–1257
Tabachnick BG, Fidell LS (1989) Using multivariate statistics. 2nd ed. Harper Collins Publishers, New York
Thompson DB (1992) Consumption rates and the evolution of diet-induced plasticity in the head morphology of Melanoplus femurrubrum (Orthoptera: Acrididae). Oecologia 89: 204–213
Travis J (1993) Evaluating the adaptive role of morphological plasticity. In: Wainwright PC, Reilly S (eds) Ecomorphology: integrative organismal biology. Univ of Chicago Press, Chicago (in press)
Walls SC, Beatty JJ, Tissot BN, Hokit DG, Blaustein AR (1993) Morphological variation and cannibalism in a larval salamander (Ambystoma macrodactylum columbianum). Can J Zool (in press)
Wainwright PC (1988) Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69: 635–645
Wainwright PC, Osenberg CW, Mittelbach GG (1991) Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): effects of environment on ontogeny. Funct Ecol 5: 40–55
Wilbur HM (1980) Complex life cycles. Ann Rev Ecol Syst 11: 67–93
Wilbur HM (1990) Coping with chaos: toads in ephemeral ponds. Trends Ecol Evol 5: 37
Wimberger PH (1991) Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45: 1545–1561
Zaret TM (1980) Predation and freshwater communities. Yale Univ Press, New Haven
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Walls, S.C., Belanger, S.S. & Blaustein, A.R. Morphological variation in a larval salamander: dietary induction of plasticity in head shape. Oecologia 96, 162–168 (1993). https://doi.org/10.1007/BF00317728
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00317728