Post-metamorphic ontogenetic changes in head size and shape of the pool frog (Pelophylax lessonae, Ranidae)
Keywords:ontogeny, allometry, anurans, diet, maximum prey size
Post-metamorphic ontogenetic variations of head size and shape were investigated in the pool frog (Pelophylax lessonae, Ranidae). We showed that allometry is an important aspect of the post-metamorphic ontogeny of the pool frog as most of the differences between the head shape of subadults and adults were size-related adjustments. The largest changes affected by size variations included the posterior part of the head and the snout and eye region. In comparison to subadults, adults have wider heads, shorter snouts and relatively smaller eyes. Analyses of the relationships between head size and shape and the maximum size of the prey indicated the absence of correlations in adults. A positive correlation was found in subadults, but only between head width and the maximum size of the prey. Further studies will allow us to draw more generalized conclusions about the ecological relevance of the variations in head size and shape during post-metamorphic development of the pool frog.
Received: October 4, 2017; Revised: November 6, 2017; Accepted: November 10, 2017; Published online: November 22, 2017
How to cite this article: Vukov TD, Kuručki M, Anđelković M, Tomašević Kolarov N. Post-metamorphic ontogenetic changes in head size and shape of the pool frog (Pelophylax lessonae, Ranidae). Arch Biol Sci. 2018;70(2):307-12.
Hanken J, Hall BK. Mechanisms of skull diversity and evolution. In: Hanken J, Hall B, editors. The skull - Functional and evolutionary mechanisms. Chicago: University of Chicago Press; 1993. p. 1-36.
Cooper WE, Vitt LJ. Female mate choice of large male broad-headed skinks. Anim Behav. 1993;45:683-93.
Adams DC, Rohlf FJ. Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proc Nat Acad Sci USA 2000;97:4106-11.
Arif S, Adams DC, Wicknick JA. Bioclimatic modelling, morphology, and behaviour reveal alternative mechanisms regulating the distributions of two parapatric salamander species. Evol Ecol Res. 2007;9:843-54.
Barros FC, Herrel A, Kohlsdorf T. Head shape evolution in Gymnophthalmidae: does habitat use constrain the evolution of cranial design in fossorial lizards? J Evol Biol. 2011;24:2423-33.
Gans C. Amphisbaenians-reptiles specialized for a burrowing existence. Nature. 1969;99:146-51.
Walls SC, Belanger SS, Blaustein AR. Morphological variation in a larval salamander: dietary induction of plasticity in head shape. Oecologia. 1993;96:162-8.
Bonduriansky R, Rowe L. Interactions among mechanisms of sexual selection on male body size and head shape in a sexually dimorphic fly. Evolution. 2003;57:2046-53.
Vincent SE, Herrel A, Irschick DJ. Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). J Zool. 2004;264:53-9.
Herrel A, McBrayer LD, Larson PM. Functional basis for sexual differences in bite force in the lizard Anolis carolinensis. Biol J Linn Soc. 2007;91:111-9.
Kaliontzopoulou A, Carretero MA, Llorente GA. Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics. Biol J Linn Soc. 2008;93:111-24.
Vanhooydonck B, Herrel A, Van Damme R. Interactions between habitat use, behavior, and the trophic niche of lacertid lizards. In: Reilly SM, McBrayer LD, Miles DB, editors. Lizard ecology: the evolutionary consequences of foraging mode. Cambridge, United Kingdom: Cambridge University Press; 2007. p. 427-49.
Emerson SB, Bramble DM. Scaling, allometry, and skull design. In: Hanken J, Hall B, editors. The skull - Functional and evolutionary mechanisms. Chicago: University of Chicago Press; 1993. p. 384-421.
Richard BA, Wainwright PC. Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture. J Exp Biol. 1995;198:419-33.
Birch JM. Skull allometry in the marine toad, Bufo marinus. J Morphol. 1999;241:115-26.
Brown JH, West GB. Scaling in Biology. Oxford: Oxford University Press; 2000. 368 p.
Herrel A, O’Reilly JC. Ontogenetic scaling of bite force in lizards and turtles. Physiol Biochem Zool. 2006;79:31-42.
Monteiro LR, Abe AS. Allometry and morphological integration in the skull of Tupinambis merianae (Lacertilia: Teiidae). Amphibia-Reptilia. 1997;18:397-405.
Smith MT, Collyer ML. Regional variation and sexual dimorphism in head form of the prairie rattlesnake (Crotalus viridis viridis): comparisons using new analytical and collection methods. In: Hayes WK, Beaman KR, Cardwell MD, Bush SP, editors. The biology of rattlesnakes. Loma Linda Loma Linda, California: University Press; 2008. p. 79-90.
Piras P, Colangelo P, Adams DC, Buscalioni A, Cubo J, Kotsakis T, Meloro C, Raia P. The Gavialis-Tomistoma debate: the contribution of skull ontogenetic allometry and growth trajectories to the study of crocodylian relationships. Evol Dev. 2010;12:568-79.
Chiari Y, Claude J. Study of the carapace shape and growth in two Galápagos tortoise lineages. J Morphol. 2011;272:379-86.
Ivanović A, Cvijanović M, Kalezić ML. Ontogeny of body form and metamorphosis: insights from the crested newts. J Zool. 2011;283:153-61.
Shine R, Shine T, Shine B. Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effects of sex, body size, and colour pattern. Biol J Linn Soc. 2003;80:1-10.
Alford RA, Crump ML. Habitat partitioning among size classes of larval southern leopard frogs, Rana utricularia. Copeia. 1982;1982:367-73.
D'Amore A, Kirby E, McNicholas M. Invasive species shifts ontogenetic resource partitioning and microhabitat use of a threatened native amphibian. Aquat Conserv Mar Freshw Ecosys. 2009;19:534-41.
Toft CA. Resource partitioning in amphibians and reptiles. Copeia 1985;1985:1-21.
Werner EE, Anholt BR. Predator induced behavioral indirect effects: consequences to competitive interactions in anuran larvae. Ecology. 1996;77:157-69.
Emerson SB. Skull shape in frogs: correlations with diet. Herpetologica. 1985;41:177-88.
Larson PM. Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): morphometric analysis of cranial allometry and ontogenetic shape change. J Morphol. 2002;252:131-44.
Larson, PM. Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphology. 2004;123:95-106.
Larson PM. Ontogeny, phylogeny, and morphology in anuran larvae: morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae). J Morphol. 2005;264:34-52.
Ponssa ML, Candioti MFV. Patterns of skull development in anurans: size and shape relationship during postmetamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: Leptodactylidae). Zoomorphology. 2012;131: 349-62.
Shine R. Sexual selection and sexual dimorphism in the Amphibia. Copeia. 1979;1979:297-306.
Monnet JM, Cherry MI. Sexual size dimorphism in anurans. Proc R Soc Lond B Biol Sci 2002;269:2301-7.
Krizmanić II. Water frogs (Rana esculenta complex) in Serbia: morphological data. Arch Biol Sci. 2008;60:449-57.
Cardini A, Elton S. Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology. 2007;126:121-34.
Rohlf FJ. tpsDig2 Software. Stony Brook, New York: State Univ. of New York; 2015.
Rohlf FJ, Slice D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Biol. 1990;39:40-59.
Dryden IL, Mardia KV. Statistical shape analysis. New York: Wiley; 1998. 496 p.
Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 2002;56:1909-20.
Zelditch ML, Swiderski DL, Sheets HD. Geometric morphometrics for biologists: a primer. San Diego, California: Elsevier; 2012. 443 p.
Bookstein FL. Morphometric tools for landmark data: geometry and biology. New York, USA: Cambridge University Press; 1991. 435 p.
Good P. Permutation test: a practical guide to resampling methods for testing hypotheses. New York, USA: Springer-Verlag; 1994. 384 p.
Edgington ES. Randomization tests. New York, USA: Marcel Dekker; 1995. 147 p.
Klingenberg CP. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev Genes Evol. 2016;226:113-37.
Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11:353-7.
Garriga N, Llorente GA. Chondrocranial ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: geometric morphometric and allometric change analysis. Acta Zool. 2012;93:453-64.
Pierce BA, Mitton JB, Jacobson L, Rose FL. Head shape and size in cannibal and noncannibal larvae of the tiger salamander from west Texas. Copeia. 1983;1983:1006-12.
Bernays EA. Diet-induced head allometry among foliage-chewing insects and its importance for graminivores. Science. 1986;231:495-7.
Houston D, Shine R. Sexual dimorphism and niche divergence: feeding habits of the Arafura ﬁle snake. J Anim Ecol. 1993;62:737-48.
Queral-Regil A, King RB. Evidence for phenotypic plasticity in snake body size and relative head dimensions in response to amount and size of prey. Copeia. 1998;1998:423-9.
MacLeod CD, Reidenberg JS, Weller M, Santos MB, Herman J, Goold J, Pierce GJ. Breaking symmetry: the marine environment, prey size, and the evolution of asymmetry in cetacean skulls. Anat Rec. 2007;290:539-45.
Edwards S, Tolley KA, Vanhooydonck B, Measey GJ, Herrel A. Is dietary niche breadth linked to morphology and performance in Sandveld lizards Nucras (Sauria: Lacertidae)? Biol J Linn Soc. 2013;110:674-88.
Dollion AY, Measey GJ, Cornette R, Carne L, Tolley KA, Silva JM, Boistel R, Fabre A-C., Herrel A. Does diet drive the evolution of head shape and bite force in chameleons of the genus Bradypodion? Funct Ecol. 2017;31:671-84.
Wittorski A, Losos JB, Herrel A. Proximate determinants of bite force in Anolis lizards. J Anat. 2016;228:85-95.
Nicoară A, Nicoară M, Bianchini F. Diet composition during breeding period in populations of Bufo viridis, Pelobates fuscus and Rana esculenta complex from Ciric River’s basin (Iaşi. Romania). Analele Stiintifice ale Universitatii" Al. I. Cuza" din Iasi Sectiunea Biologie Animala. 2005;51:179-87.
Paunović A, Bjelić-Čabrilo O, Šimić S. The diet of water frogs (Pelophylax esculentus complex) from the Petrovaradinski Rit marsh (Serbia). Arch Biol Sci. 2010;62:797-806.
Cicort-Lucaciu AS, Pelle C, Borma IT. Note on the food composition of a Pelophylax ridibundus (Amphibia) population from the Dubova locality region, south-western Romania. Biharean Biol. 2013;7:33-6.
Balint N, Citrea L, Memetea A, Jurj N, Condure N. Feeding ecology of the Pelophylax ridibundus (Anura, Ranidae) in Dobromir, Romania. Biharean Biol. 2008;2:27-37.
Cogălniceanu D, Palmer MW, Ciubuc C. Feeding in anuran communities on islands in the Danube floodplain. Amphibia-Reptilia. 2001;22:1-19.