Gómez, R.O.; Regueira, E.; O'Donohoe, M.E.A.; Hermida, G.N."Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans" (2017) Zoologischer Anzeiger. 267:101-110
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Postembryonic skeletogenesis in anuran amphibians has been widely studied, yet less than one percent of the extant diversity has been covered and relatively few comparative studies exist. Here we document the sequence and timing of ossification of the Common Toad Rhinella arenarum, a large true toad (Bufonidae) from South America that is a model organism for varied ongoing research. We study histological sections and cleared-and-stained specimens of an ontogenetic series ranging from early larval stages to juveniles, documenting the ossification sequence of the entire skeleton. To diminish potential environmental biases we also study the skeletogenesis of the frog Leptodactylus latinasus (Leptodactylidae) from the same pond and season. We summarize comparative data from numerous anuran species to contextualize our results in a broad phylogenetic context. Histological data shows that skeletal calcification in R. arenarum is temporally dissociated from osteoid matrix formation and occurs later than in most other anurans, which is unexpected given its generalized pond-type larva and heavily ossified adult skeleton. At the onset of metamorphosis, exoccipitals, parasphenoid, and frontoparietals are the only ossified skull elements, whereas most of the postcranium has already started ossification. This pattern is rare among anurans but is shared by other bufonids, in which it has been previously linked to rapid development. Our comparative survey, however, suggests that the delayed bufonid pattern is not related to fast-developing larvae but instead might be a distinctive feature of true toads. © 2017


Documento: Artículo
Título:Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans
Autor:Gómez, R.O.; Regueira, E.; O'Donohoe, M.E.A.; Hermida, G.N.
Filiación:Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, IGEBA-CONICET, Ciudad Universitaria, Buenos Aires, C1428EGA, Argentina
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Ciudad Universitaria, Buenos Aires, C1428EGA, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Palabras clave:Anura; Bufonidae; Histology; Ossification sequence; Rhinella arenarum; Skeletogenesis; calcification; comparative study; histology; larva; osteology; phylogenetics; skeleton; survey; toad; Amphibia; Anura; Bufonidae; Leptodactylidae; Leptodactylus latinasus
Página de inicio:101
Página de fin:110
Título revista:Zoologischer Anzeiger
Título revista abreviado:Zool. Anz.


  • Altig, R., Johnston, G.F., Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats (1989) Herpetol. Monogr., 3, pp. 81-109
  • Attademo, A.M., Sanchez-Hernandez, J.C., Lajmanovich, R.C., Peltzer, P.M., Junges, C., Effect of diet on carboxylesterase activity of tadpoles (Rhinella arenarum) exposed to chlorpyrifos (2017) Ecotox. Environ. Saf., 135, pp. 10-16
  • Badawy, G., Sakr, S., Atallah, M., Comparative study of the skeletogenesis of limb autopods in the developing chick Gallus domesticus and toad Bufo regularis (2012) RJPBCS, 3, pp. 966-988
  • Banbury, B., Maglia, A.M., Skeletal development of the Mexican spadefoot, Spea multiplicata (Anura: Pelobatidae) (2006) J. Morphol., 139, pp. 439-476
  • Boulenger, G.A., A list of the reptiles and batrachians of Amoorland (1890) Ann. Mag. Nat. Hist., 5, pp. 137-144
  • Brady, L.D., Griffiths, R.A., Developmental responses to pond desiccation in tadpoles of the British anuran amphibians (Bufo bufo, B. calamita and Rana temporaria) (2000) J. Zool. Lond., 252, pp. 61-69
  • Cei, J.M., Amphibians of Argentina (1980) Monit. Zool. Italiano N.S. Monogr., 2, pp. 1-609
  • Cope, E.D., On Trachycephalus, Scaphiopus and other Batrachia (1863) Proc. Acad. Nat. Sci. Philadelphia, 15, pp. 43-54
  • Cope, E.D., On the zoological position of Texas (1880) Bull. U. S. Natl. Mus., 17, pp. 1-51
  • Davies, M., Ontogeny of bone and the role of heterochrony in the myobatrachine genera Uperoleia, Crinia, and Pseudophryne (Anura: Leptodactylidae: Myobatrachinae) (1989) J. Morphol., 200, pp. 269-300
  • de Sá, R.O., Swart, C.C., Development of the suprarostral plate of pipoid frogs (1999) J. Morphol., 240, pp. 143-154
  • Dunlap, K.D., Sanchiz, B., Temporal dissociation between the development of the cranial and appendicular skeletons in Bufo bufo (Amphibia: Bufonidae) (1996) J. Herpetol., 30, pp. 506-513
  • Echeverría, D.D., Fiorito De López, L.E., Estadios de la metamorfosis en Bufo arenarum (Anura) (1981) Physis B, 40 (98), pp. 15-23
  • Etkin, W., Growth and resorption phenomena in anuran metamorphosis. I (1932) Physiol. Zool., 5, pp. 275-300
  • Fabrezi, M., Goldberg, J., Heterochrony during skeletal development of Pseudis platensis (Anura, Hylidae) and the early offset of skeleton development and growth (2009) J. Morphol., 270, pp. 205-220
  • Fabrezi, M., Heterochrony in growth and development in anurans from the Chaco of South America (2011) Evol. Biol., 38, pp. 390-411
  • Fouquet, A., Blotto, B.L., Maronna, M.M., Verdade, V.K., Junca, F.A., de Sa, R., Rodrigues, M.T., Unexpected phylogenetic positions of the genera Rupirana and Crossodactylodes reveal insights into the biogeography and reproductive evolution of leptodactylid frogs (2013) Mol. Phylogenet. Evol., 67, pp. 445-457
  • Frost, D.R., Amphibian Species of the World: an Online Reference (2016),, Version 6.0. American Museum of Natural History, New York, USA (Accessed 18 December 2016). Electronic Database accessible at; Gallardo, J.M., Nuevo género de Brachycephalidae (Amphibia Anura) (1961) Neotropica, 7, pp. 71-72
  • Les Figures des plantes et animaux d'usage en médecine, décrits dans la Matière Médicale de Mr. Geoffroy Médecin, , Desprez, Paris
  • Gaudin, A.J., The sequence of cranial ossification in the California toad, Bufo boreas (Amphibia, Anura, Bufonidae) (1978) J. Herpetol., 12, pp. 309-318
  • Gosner, K.L., A simplified table for staging anuran embryos and ae with notes on identification (1960) Herpetologica, 16, pp. 183-190
  • Haas, A., Larval and metamorphic skeletal development in the fast-developing frog Pyxicephalus adspersus (Anura, Ranidae) (1999) Zoomorphology, 119, pp. 23-35
  • Hall, J.A., Larsen, J.H., Postembryonic ontogeny of the spadefoot toad, Scaphiopus intermontanus (Anura: Pelobatidae): skeletal morphology (1998) J. Morphol., 238, pp. 179-244
  • Hammer, Ø., Harper, D.A.T., Ryan, P.D., PAST: paleontological statistics software package for education and data analysis (2001) Palaeontol. Electron., 4 (1), pp. 1-9
  • Hanken, J., Hall, B.K., Variation and timing of the cranial ossification sequence of the Oriental Fire-Bellied Toad, Bombina orientalis (Amphibia, Discoglossidae) (1984) J. Morphol., 182, pp. 245-255
  • Hanken, J., Hall, B.K., Skull development during anuran metamorphosis I. Early development of the first three bones to form—the exoccipital, the parasphenoid, and the frontoparietal (1988) J. Morphol., 195, pp. 247-256
  • Harrington, S.M., Harrison, L.B., Sheil, C.A., Ossification sequence heterochrony among amphibians (2013) Evol. Dev., 15, pp. 344-364
  • Hensel, R., Beiträge zur Kenntnis der Wirbelthiere Südbrasilens (1867) Arch. Naturgesch., 33, pp. 120-162
  • Hermida, G.N., Farías, A., Morphology and histology of the larynx of the common toad Rhinella arenarum (Hensel, 1867) (Anura, Bufonidae) (2009) Acta Zool., 90, pp. 326-338
  • The IUCN Red List of Threatened Species. Version 2016-2, ,, Downloaded on 04 September 2016
  • Jiménez de la Espada, M., Vertebrados del Viaje al Pacífico Verificado de 1862 a 1865 por una Comisión de Naturalistas Enviada por el Gobierno Español Batracios (1875), Miguel Ginesta Madrid; Kiernan, J.A., Histological and Histochemical Methods (1999), third ed. Hodder Arnold Publications New York; Laurenti, J.N., Specimen Medicum, Exhibens Synopsin Reptilium Emendatum cum Experimentis Circa Venena et Antidota Reptilium Austriacorum, Joan (1768), Thom. Nob. de Trattnern, Wien; Linnaeus, C., (1758) Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis, 1. , 10th edition L. Salvii Stockholm
  • Maglia, A.M., Pugener, A., Skeletal development and adult osteology of Bombina orientalis (Anura: Bombinatoridae) (1998) Herpetologica, 54, pp. 344-363
  • Maglia, A.M., Skeletal development of Pelobates cultripes and a comparison of the osteogenesis of pelobatid frogs (Anura: Pelobatidae) (2003) Sci. Pap. Mus. Nat. Hist. Univ. Kansas, 30, pp. 1-13
  • Pérez Ben, C.M., Gómez, R.O., Báez, A.M., Intraspecific morphological variation and its implication in the taxonomic status of ‘Bufo pisanoi’, a Pliocene anuran from eastern Argentina (2014) J. Vert. Paleontol., 34, pp. 767-777
  • Pollo, F.E., Bionda, C.L., Salinas, Z.A., Salas, N.E., Martino, A.L., Common toad Rhinella arenarum (Hensel, 1867) and its importance in assessing environmental health: test of micronuclei and nuclear abnormalities in erythrocytes (2015) Environ. Monit. Assess., 187, pp. 1-9
  • Pyron, R.A., Wiens, J.J., A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs salamanders, and caecilians (2011) Mol. Phylogenet. Evol., 61, pp. 543-583
  • Regueira, E., Sassone, A.G., Scaia, M.F., Volonteri, M.C., Ceballos, N.R., Seasonal changes and regulation of the glucocorticoid receptor in the testis of the toad Rhinella arenarum (2013) J. Exp. Zool. Part A, 319, pp. 39-52
  • Regueira, E., Scaia, M.F., Volonteri, M.C., Ceballos, N.R., Anteroposterior variation of the cell types in the interrenal gland of the male toad Rhinella arenarum (Amphibia, Anura) (2013) J. Morphol., 274, pp. 331-343
  • Regueira, E., Dávila, C., Hermida, G.N., Morphological changes in skin glands during development in Rhinella arenarum (Anura: Bufonidae) (2016) Anat. Rec. Part A, 299, pp. 141-156
  • Regueira, E., Dávila, C., Sassone, A.G., O'Donohoe, M.E.A., Hermida, G.N., Post-metamorphic development of skin glands in a true toad: parotoids versus dorsal skin (2017) J. Morphol.
  • Reuss, A., Zoologischen miscellen (1833) Reptilian. Saurier. Batrachier. Mus. Senckenb., 1, pp. 27-62
  • Roelants, K., Gower, D.J., Wilkinson, M., Loader, S.P., Biju, S.D., Guillaume, K., Moriau, L., Bossuyt, F., Global patterns of diversification in the history of modern amphibians (2007) P. Natl. Acad. Sci. U. S. A., 104, pp. 887-892
  • Sedra, S.N., Michael, M.I., The metamorphosis and growth of the hyobranchial apparatus of the Egyptian toad, Bufo regularis Reuss (1958) J. Morphol., 103, pp. 1-30
  • Sedra, S.N., On the Homology of certain elements in the Skull of Bufo regularis Reuss (Salientia) (1949) Proc. Zool. Soc. Lond., 119, pp. 633-641
  • Sedra, S.N., The metamorphosis of the jaws and their muscles in the toad, Bufo regularis, correlated with the changes in the animal's feeding habits (1950) Proc. Zool. Soc. Lond., 120, pp. 405-449
  • Semlitsch, R.D., Evolutionary consequences of nonrandom mating—do large males increase offspring fitness in the anuran Bufo bufo? (1994) Behav. Ecol. Sociobiol., 34, pp. 19-24
  • Shearman, R.M., Maglia, A.M., Osteological development of cope's gray treefrog, Hyla chrysoscelis (2015) Acta Zool., 96, pp. 181-198
  • Sheil, C.A., Jorgensen, M., Tulenko, F., Harrington, S., Variation in timing of ossification affects inferred heterochrony of cranial bones in Lissamphibia (2014) Evol. Dev., 16, pp. 292-305
  • Sotelo, M.I., Bingman, V.P., Muzio, R.N., Goal orientation by geometric and feature cues: spatial learning in the terrestrial toad Rhinella arenarum (2015) Anim. Cogn., 18, pp. 315-323
  • Trueb, L., Hanken, J., Skeletal development in Xenopus laevis (Anura: Pipidae) (1992) J. Morphol., 214, pp. 1-41
  • Trueb, L., Bones, frogs, and evolution (1973) Evolutionary Biology of the Anurans, pp. 65-132. , J.L. Vial University Missouri Press Columbia
  • Trueb, L., A summary of osteocranial development in anurans with notes on the sequence of cranial ossification in Rhinophrynus dorsalis (Anura: Pipoidea: Rhinophrynidae) (1985) S. Afr. J. Sci., 81, pp. 181-185
  • Vaira, M., Akmentins, M., Attademo, M., Baldo, D., Barrasso, D.A., Barrionuevo, S., Categorización del estado de conservación de los anfibios de la República Argentina (2012) Cuad Herpetol., 26, pp. 131-159
  • Vera Candioti, M.F., Ecomorphological guilds in anuran larvae: an application of geometric morphometric methods (2006) Herpetol. J., 16, pp. 149-162
  • Vera, M.C., Ponssa, M.L., Skeletogenesis in anurans: cranial and postcranial development in metamorphic and postmetamorphic stages of Leptodactylus bufonius (Anura: Leptodactylidae) (2014) Acta Zool., 95, pp. 44-62
  • Voss, W.J., Rate of larval development and metamorphosis of the spadefoot toad, Scaphiopus bombifrons (1961) Southwest Nat., 6, pp. 168-174
  • Wassersug, R.A., Procedure for differential staining of cartilage and bone in whole formalin fixed vertebrates (1976) Stain Technol., 51, pp. 131-134
  • Weisbecker, V., Mitgutsch, C., A large-scale survey of heterochrony in anuran cranial ossification patterns (2010) J. Zool. Syst. Evol. Res., 48, pp. 332-347
  • Wild, E.R., Description of the adult skeleton and developmental osteology of the hyperossified horned frog, Ceratophrys cornuta (Anura: Leptodactylidae) (1997) J. Morphol., 232, pp. 169-206
  • Yıldırım, E., Kaya, U., Comparative skeletogenesis of the oriental tree frog Hyla orientalis (Anura: Hylidae) (2014) Zool. Anz., 253, pp. 361-371


---------- APA ----------
Gómez, R.O., Regueira, E., O'Donohoe, M.E.A. & Hermida, G.N. (2017) . Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans. Zoologischer Anzeiger, 267, 101-110.
---------- CHICAGO ----------
Gómez, R.O., Regueira, E., O'Donohoe, M.E.A., Hermida, G.N. "Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans" . Zoologischer Anzeiger 267 (2017) : 101-110.
---------- MLA ----------
Gómez, R.O., Regueira, E., O'Donohoe, M.E.A., Hermida, G.N. "Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans" . Zoologischer Anzeiger, vol. 267, 2017, pp. 101-110.
---------- VANCOUVER ----------
Gómez, R.O., Regueira, E., O'Donohoe, M.E.A., Hermida, G.N. Delayed osteogenesis and calcification in a large true toad with a comparative survey of the timing of skeletal ossification in anurans. Zool. Anz. 2017;267:101-110.