Artículo

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) Journal of Morphology. 278(5):652-664
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Chemical defenses in amphibians are a common antipredatory and antimicrobial strategy related to the presence of dermal glands that synthesize and store toxic or unpalatable substances. Glands are either distributed throughout the skin or aggregated in multiglandular structures, being the parotoids the most ubiquitous macrogland in toads of Bufonidae. Even though dermal glands begin to develop during late-larval stages, many species, including Rhinella arenarum, have immature glands by the end of metamorphosis, and their post-metamorphic growth is unknown. Herein, we compared the post-metamorphic development of parotoids and dorsal glands by histological and allometric studies in a size series of R. arenarum. Histological and histochemical studies to detect proteins, acidic glycoconjugates, and catecholamines, showed that both, parotoids and dorsal glands, acquire characteristics of adults in individuals larger than 50 mm; that is, a moment in which the cryptic coloration disappears. Parotoid height increased allometrically as a function of body size, whereas the size of small dorsal glands decreased with body size. The number of glands in the dorsum was not linearly related to body size, appearing to be an individual characteristic. Only adult specimens had intraepithelial granular glands in the duct of the largest glands of the parotoids. Since toxic secretions accumulate in the central glands of parotoids, allometric growth of parotoids may translate into greater protection from predators in the largest animals. Conversely, large glands in the dorsum, which produce a proteinaceous secretion of unknown function, grow isometrically to body size. Some characteristics, like intraepithelial glands in the ducts and basophilic glands in the dorsum, are limited to adults. © 2017 Wiley Periodicals, Inc.

Registro:

Documento: Artículo
Título:Post-metamorphic development of skin glands in a true toad: Parotoids versus dorsal skin
Autor:Regueira, E.; Dávila, C.; Sassone, A.G.; O'Donohoe, M.E.A.; Hermida, G.N.
Filiación:Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Laboratorio de Biología de Anfibios-Histología Animal, Universidad de Buenos Aires, Buenos Aires, C1428EGA, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, C1033AAJ, Argentina
Palabras clave:Bufonidae; chemical defense; granular glands; Rhinella arenarum; anatomy and histology; animal; Bufonidae; embryology; larva; metamorphosis; skin; Animals; Bufonidae; Larva; Metamorphosis, Biological; Skin
Año:2017
Volumen:278
Número:5
Página de inicio:652
Página de fin:664
DOI: http://dx.doi.org/10.1002/jmor.20661
Handle:http://hdl.handle.net/20.500.12110/paper_03622525_v278_n5_p652_Regueira
Título revista:Journal of Morphology
Título revista abreviado:J. Morphol.
ISSN:03622525
CODEN:JOMOA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03622525_v278_n5_p652_Regueira

Referencias:

  • Almeida, D.P., Felsemburgh, F.A., Azevedo, R.A., Brito-Gitirana, D.L., Morphological re-evaluation of the parotoid glands of Bufo ictericus (Amphibia, Anura, Bufonidae) (2007) Contributions to Zoology, 76, pp. 145-152
  • Antoniazzi, M.M., Neves, P.R., Mailho-Fontana, P.L., Rodrigues, M.T., Jared, C., Morphology of the parotoid macroglands in Phyllomedusa leaf frogs (2013) Journal of Zoology, 291, pp. 42-50
  • Azevedo, R.A., Pelli, A.A., Ferreira-Pereira, A., de Jesus Santana, A.S., Felsemburgh, F., de Brito-Gitirana, L., Structural aspects of the Eberth-Katschenko layer of Bufo ictericus integument: Histochemical characterization and biochemical analysis of the cutaneous calcium (Amphibian, Bufonidae) (2005) Micron, 36, pp. 61-65
  • Brunetti, A.E., Hermida, G.N., Faivovich, J., New insights into sexually dimorphic skin glands of anurans: The structure and ultrastructure of the mental and lateral glands in Hypsiboas punctatus (Amphibia: Anura: Hylidae) (2012) Journal of Morphology, 273, pp. 1257-1271
  • Brunetti, A.E., Hermida, G.N., Luna, M.C., Barsotti, A.M., Jared, C., Antoniazzi, M.M., Rivera-Correa, M., Faivovich, J., Diversity and evolution of sexually dimorphic mental and lateral glands in Cophomantini treefrogs (Anura: Hylidae: Hylinae) (2015) Biological Journal of the Linnean Society, 114, pp. 12-34
  • Chammas, S.M., Carneiro, S.M., Ferro, R.S., Antoniazzi, M.M., Jared, C., Development of integument and cutaneous glands in larval, juvenile and adult toads (Rhinella granulosa): A morphological and morphometric study (2015) Acta Zoologica, 96, pp. 460-477
  • Clarke, B.T., The natural history of amphibian skin secretions, their normal functioning and potential medical applications (1997) Biological Reviews of the Cambridge Philosophical Society, 72, pp. 365-379
  • Cunha Filho, G.A., Schwartz, C.A., Resck, I.S., Murta, M.M., Lemos, S.S., Castro, M.S., Kyaw, C., Schwartz, E.F., Antimicrobial activity of the bufadienolides marinobufagin and telocinobufagin isolated as major components from skin secretion of the toad Bufo rubescens (2005) Toxicon, 45, pp. 777-782
  • Daly, J.W., The chemistry of poisons in amphibian skin (1995) Proceedings of the National Academy of Sciences of the United States of America, 92, pp. 9-13
  • Daly, J.W., Spande, T.F., Garraffo, H.M., Alkaloids from amphibian skin: A tabulation of over eight-hundred compounds (2005) Journal of Natural Products, 68, pp. 1556-1575
  • Delfino, G., Brizzi, R., Alvarez, B.B., Kracke-Berndorff, R., Serous cutaneous glands in Phyllomedusa hypochondrialis (Anura, Hylidae): Secretory patterns during ontogenesis (1998) Tissue Cell, 30, pp. 30-40
  • Delfino, G., Brizzi, R., Alvarez, B.B., Taddei, L., Secretory polymorphism and serous cutaneous gland heterogeneity in Bufo granulosus (Amphibia, Anura) (1999) Toxicon, 37, pp. 1281-1296
  • Delfino, G., Brizzi, R., Kracke-Berndorff, R., Alvarez, B., Serous gland dimorphism in the skin of Melanophryniscus stelzneri (Anura: Bufonidae) (1998) Journal of Morphology, 237, pp. 19-32
  • Duellman, W.E., Trueb, L., (1994) Biology of amphibians, , #x0026;, 2nd ed, Baltimore, MD, Johns Hopkins University Press
  • Echeverría, D.D., Filipello, A.M., Edad y crecimiento en Bufo arenarum (Anura: Bufonidae) (1990) Cuadernos de Herpetología, 5
  • Ferraro, D.P., Topa, P.E., Hermida, G.N., Lumbar glands in the frog genera Pleurodema and Somuncuria (Anura: Leiuperidae): Histological and histochemical perspectives (2013) Acta Zoologica, 94, pp. 44-57
  • Freeland, W.J., Kerin, S.H., Ontogenetic alteration of activity and habitat selection by Bufo marinus (1991) Wildlife Research, 18, pp. 431-443
  • Gallardo, J.M., (1987) Anfibios Argentinos: Guía para su identificación, , Buenos Aires, Librería Agropecuaria
  • Hammer, Ø., Harper, D.A.T., Ryan, P.D., PAST: Paleontological statistics software package for education and data analysis (2001) Palaeontol Electron, 4, p. 9
  • Hayes, R.A., Crossland, M.R., Hagman, M., Capon, R.J., Shine, R., Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): Toxin profiles and effects on predators (2009) Journal of Chemical Ecology, 35, pp. 391-399
  • (2016) The IUCN Red List of Threatened Species. Version 2016-2, , http://www.iucnredlist.org, Retrieved from, (accessed on 04 September, 2016)
  • Jared, C., Antoniazzi, M.M., Jordão, A.E.C., Silva, J.R.M.C., Greven, H., Rodrigues, M.T., Parotoid macroglands in toad (Rhinella jimi): Their structure and functioning in passive defence (2009) Toxicon, 54, pp. 197-207
  • Jared, C., Antoniazzi, M.M., Navas, C.A., Katchburian, E., Freymüller, E., Tambourgi, D.V., Rodrigues, M.T., Head co-ossification, phragmosis and defence in the casque-headed tree frog Corythomantis greeningi (2005) Journal of Zoology, 265, pp. 1-8
  • Jared, S.G., Jared, C., Egami, M.I., Mailho-Fontana, P.L., Rodrigues, M.T., Antoniazzi, M.M., Functional assessment of toad parotoid macroglands: A study based on poison replacement after mechanical compression (2014) Toxicon, 87, pp. 92-103
  • Jeckel, A.M., Saporito, R.A., Grant, T., The relationship between poison frog chemical defenses and age, body size, and sex (2015) Frontiers in Zoology, 12, p. 1
  • Kiernan, J., (1999) Histological and histochemical methods: Theory and practice, , 3rd ed, Oxford, UK, Butterworth Heinemann
  • Lenzi-Mattos, R., Antoniazzi, M.M., Haddad, C.F.B., Tambourgi, D.V., Rodrigues, M.T., Jared, C., The inguinal macroglands of the frog Physalaemus nattereri (Leptodactylidae): Structure, toxic secretion and relationship with deimatic behaviour (2005) Journal of Zoology, 266, pp. 385-394
  • Licht, L.E., Initial appearance of the parotoid gland in three species of toads (genus Bufo) (1967) Herpetologica, 23, pp. 115-118
  • Maciel, N.M., Collevatti, R.G., Colli, G.R., Schwartz, E.F., Late Miocene diversification and phylogenetic relationships of the huge toads in the Rhinella marina (Linnaeus, 1758) species group (Anura: Bufonidae) (2010) Molecular Phylogenetics and Evolution, 57, pp. 787-797
  • Maciel, N.M., Schwartz, C.A., Pires, O.R., Sebben, A., Castro, M.S., Sousa, M.V., Fontes, W., Schwartz, E.N.F., Composition of indolealkylamines of Bufo rubescens cutaneous secretions compared to six other Brazilian bufonids with phylogenetic implications (2003) Comparative Biochemistry and Physiology—Part B, 134, pp. 641-649
  • Mailho-Fontana, P.L., Antoniazzi, M.M., Toledo, L.F., Verdade, V.K., Sciani, J.M., Barbaro, K.C., Pimenta, D.C., Jared, C., Passive and active defense in toads: The Parotoid Macroglands in Rhinella marina and Rhaebo guttatus (2014) Journal of Experimental Zoology Part A, 321, pp. 65-77
  • Navas, C.A., Jared, C., Antoniazzi, M.M., Water economy in the casque-headed tree-frog Corythomantis greeningi (Hylidae): Role of behaviour, skin, and skull skin co-ossification (2002) Journal of Zoology, 257, pp. 525-532
  • Phillips, B.L., Shine, R., Allometry and selection in a novel predator prey system: Australian snakes and the invading cane toad (2006) Oikos, 112, pp. 122-130
  • Portik, D.M., Papenfuss, T.J., Historical biogeography resolves the origins of endemic Arabian toad lineages (Anura: Bufonidae): Evidence for ancient vicariance and dispersal events with the Horn of Africa and South Asia (2015) BMC Evolutionary Biology, 15, p. 1
  • Quinzio, S., Fabrezi, M., Ontogenetic and structural variation of mineralizations and ossifications in the integument within ceratophryid frogs (Anura, Ceratophryidae) (2012) The Anatomical Record, 295, pp. 2089-2103
  • Rash, L.D., Morales, R.A., Vink, S., Alewood, P.F., De novo sequencing of peptides from the Parotoid secretion of the cane toad, Bufo marinus (Rhinella marina) (2011) Toxicon, 57, pp. 208-216
  • Regueira, E., Dávila, C., Hermida, G.N., Morphological changes in skin glands during development in Rhinella arenarum (Anura: Bufonidae) (2016) The Anatomical Record, 299, pp. 141-156
  • Saporito, R.A., Isola, M., Maccachero, V.C., Condon, K., Donnelly, M.A., Ontogenetic scaling of poison glands in a dendrobatid poison frog (2010) Journal of Zoology, 282, pp. 238-245
  • Schmidt-Nielsen, K., (1984) Scaling: Why is animal size so important, , Cambridge, UK, Cambridge University Press
  • Sciani, J.M., Angeli, C.B., Antoniazzi, M.M., Jared, C., Pimenta, D.C., Differences and similarities among parotoid macrogland secretions in South American toads: A preliminary biochemical delineation (2013) The Scientific World Journal, 2013, pp. 1-9
  • Terreni, A., Nosi, D., Greven, H., Delfino, G., Development of serous cutaneous glands in Scinax nasica (Anura, Hylidae): Patterns of poison biosynthesis and maturation in comparison with larval glands in specimens of other families (2003) Tissue Cell, 35, pp. 274-287
  • Toledo, R.C., Jared, C., Cutaneous adaptations to water balance in amphibians (1993) Comparative Biochemistry and Physiology—Part A, 105, pp. 593-608
  • Toledo, R.C., Jared, C., Cutaneous granular glands and amphibian venoms (1995) Comparative Biochemistry and Physiology—Part A, 111, pp. 1-29
  • Toledo, R.C., Jared, C., Brunner, A.B., Jr., Morphology of the large granular alveoli of the parotoid glands in toad (Bufo ictericus) before and after compression (1992) Toxicon, 30, pp. 745-753
  • Vaira, M., Akmentins, M.S., Attademo, M., Baldo, D., Barrasso, D., Barrionuevo, S., Basso, N., Zaracho, V., Categorización del estado de conservación de los anfibios de la República Argentina (2012) Cuadernos de Herpetología, 26, pp. 131-159
  • Vences, M., Wahl-Boos, G., Hoegg, S., Glaw, F., Spinelli Oliveira, E., Meyer, A., Perry, S., Molecular systematics of mantelline frogs from Madagascar and the evolution of their femoral glands (2007) Biological Journal of the Linnean Society, 92, pp. 529-539
  • Warton, D.I., Wright, I.J., Falster, D.S., Westoby, M., Bivariate line-fitting methods for allometry (2006) Biological Reviews, 81, pp. 259-291

Citas:

---------- APA ----------
Regueira, E., Dávila, C., Sassone, A.G., O'Donohoe, M.E.A. & Hermida, G.N. (2017) . Post-metamorphic development of skin glands in a true toad: Parotoids versus dorsal skin. Journal of Morphology, 278(5), 652-664.
http://dx.doi.org/10.1002/jmor.20661
---------- CHICAGO ----------
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" . Journal of Morphology 278, no. 5 (2017) : 652-664.
http://dx.doi.org/10.1002/jmor.20661
---------- MLA ----------
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" . Journal of Morphology, vol. 278, no. 5, 2017, pp. 652-664.
http://dx.doi.org/10.1002/jmor.20661
---------- VANCOUVER ----------
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. J. Morphol. 2017;278(5):652-664.
http://dx.doi.org/10.1002/jmor.20661