Articles
Re-description of external morphology and factors affecting body and tail shape of the stone frog tadpoles
Published 2022-05-14
Keywords
- Anuran larvae,
- Alsodidae,
- geometric morphometrics,
- allometry,
- streamlet depth
How to Cite
da Silva Gonçalves, B., Hendges, C. D., Madalozzo, B., & Santos, T. G. (2022). Re-description of external morphology and factors affecting body and tail shape of the stone frog tadpoles. Acta Herpetologica, 17(1), 59–70. https://doi.org/10.36253/a_h-11315
Abstract
Ecological studies testing the preponderance of environmental filters on ontogeny to explain the variation in tadpole morphology are scarce for Neotropical anurans. We used tadpoles of the stone frog Limnomedusa macroglossa (Alsodidae): (1) to assess the variation in body and tail shape; (2) to examine the effect of streamlet depth and allometry on tadpole shape, and (3) to re-describe and compare the tadpole external morphology with closely related species. We obtained the body shape and size from 150 tadpoles. The re-description was based on 57 qualitative and 24 quantitative characters, from 19 tadpoles between stages 30 and 37 and 31 to 37, respectively. Allometry was the major factor influencing the lateral view of body shape: smaller tadpoles had round bodies and eyes and nostrils positioned more laterally in comparison with larger ones. Thus, the power of ontogenetic variations reported here makes the tadpole developmental “climax” period a questionable concept that deserves additional attention. The depth gradient of streamlets also affected the shape: in shallower environments, the tadpoles presented a decrease in height of the body, fins and tail muscles, and an increase in body width. These results may indicate adaptations allowing better swimming performance in lotic environments with intense water flow. The external morphological characterization of L. macroglossa presented here differed from that previously reported, mainly due to coloration, body shape, nostril, anal tube, tail, shape and position of nostrils and snout. Additionally, we presented unknown traits for this species, making comparisons with closely related species within the Alsodidae family.
References
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Altig, R., McDiarmid, R.W. (2006): Descriptions and biological notes on three unusual mantellid tadpoles (Amphibia: Anura: Mantellidae) from southeastern Madagascar. Proc. Biol. Soc. Wash. 119: 418–425. https://doi.org/10.2988/0006-324X(2006)119[418:DABNOT]2.0.CO;2.
Altig, R., McDiarmid, R.W. (1999): Development and Morphology. In: Tadpoles The Biology of Anuran Larvae. pp. 24–51. University of Chicago Press, Chicago.
Arendt, J. (2010): Morphological correlates of sprint swimming speed in five species of spadefoot toad tadpoles: Comparison of morphometric methods. J. Morphol. 271: 1044–1052. https://doi.org/10.1002/jmor.10851.
Barrasso, D.A., Cotichelli, L., Alcalde, L., Basso, N.G. (2013): Re-description of the tadpole of Pleurodema somuncurensis (Cei, 1969) (Amphibia: Anura). Zootaxa 3681: 192–196. https://doi.org/10.11646/zootaxa.3681.2.10
Blotto, B.L., Nuñez, J.J., Basso, N.G., Úbeda, C., Wheeler, W.C., Faivovich, J. (2012): Phylogenetic relationships of a Patagonian frog radiation, the Alsodes+Eupsophus clade (Anura: Alsodidae), with comments on the supposed paraphyly of Eupsophus. Cladistics 1–19.
Bolzan, A.M.R., Saccol, S.A., Santos, T.G. (2016): Composition and diversity of anurans in the largest conservation unit in Pampa biome, Brazil. Biota Neotropica 16: e20150113. https://doi.org/10.1590/1676-0611-BN-2015-0113.
Bookstein, F.L. (1989): “Size and Shape”: A Comment on Semantics. Syst. Zool. 38: 173–180. https://doi.org/10.2307/2992387.
Borteiro, C., Kolenc, F. (2007): Redescription of the tadpoles of three species of frogs from Uruguay (Amphibia: Anura: Leiuperidae and Leptodactylidae), with notes on natural history. Zootaxa 1638: 1–20. https://doi.org/10.11646/zootaxa.1638.1.1.
Candioti, M.F.V., Nuñez, J.J., Úbeda, C. (2011). Development of the nidicolous tadpoles of Eupsophus emiliopugini (Anura: Cycloramphidae) until metamorphosis, with comments on systematic relationships of the species and its endotrophic developmental mode. Acta Zool. 92: 27–45. https://doi.org/10.1111/j.1463-6395.2010.00448.x.
Cerbo, A.R.D., Biancardi, C.M. (2010): Morphometric study on tadpoles of Bombina variegata (Linnaeus, 1758) (Anura; Bombinatoridae). Acta Herpetol. 5: 223–231.
Formas, J.R., Cuevas, C.C. (2017): The tadpole of Alsodes cf. norae (Anura: Alsodidae) with comments on the diagnosis of the genus Alsodes. Salamandra 53: 131–136.
Garriga, N., Llorente, G.A. (2012): Chondrocranial ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: geometric morphometric and allometric change analysis. Acta Zool. 93: 453–464. https://doi.org/10.1111/j.1463-6395.2011.00520.x.
Glime, J.M., Boelema, W.J. (2017): Anurans: Central and South American mossy habitats, in: Bryophyte Ecology. Michigan Technological University, p. 16.
Gosner, K.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.
Grant, T., Rada, M., Anganoy-Criollo, M., Batista, A., Dias, P.H., Jeckel, A.M., Machado, D.J., Rueda-Almonacid, J.V. (2017): Phylogenetic Systematics of Dart-Poison Frogs and Their Relatives Revisited (Anura: Dendrobatoidea). South Am. J. Herpetol. 12: S1–S90. https://doi.org/10.2994/SAJH-D-17-00017.1.
Grosjean, S. (2005): The choice of external morphological characters and developmental stages for tadpole-based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth, 1855) (Amphibia, Anura, Ranidae). Contrib. Zool. 74: 61–76. https://doi.org/10.1163/18759866-0740102005.
Haad, B., Vera Candioti, F., Baldo, D. (2011): Shape variation in lentic and lotic tadpoles of Melanophryniscus (Anura: Bufonidae). Stud. Neotropical Fauna Environ. 46: 91–99. https://doi.org/10.1080/01650521.2011.593124.
Iop, S., Mendes Lipinski, V., Madalozzo, B., Pereira Maragno, F., Zanini Cechin, S., Gomes Dos Santos, T. (2015): Re-description of the external morphology of Phyllomedusa iheringii Boulenger, 1885 larvae (Anura: Hylidae), with comments on the external morphology of tadpoles of the P. burmeisteri group. Acta Herpetol. 67-72. https://doi.org/10.13128/ACTA_HERPETOL-15547.
Johnson, J.B., Burt, D.B., DeWitt, T.J. (2008): Form, Function, and Fitness: Pathways to survival. Evolution 62: 1243–1251. https://doi.org/10.1111/j.1558-5646.2008.00343.x.
Kaefer, I.L., Both, C., Cechin, S.Z. (2009): Breeding biology of the rapids frog Limnomedusa macroglossa (Anura: Cycloramphidae) in southern Brazil. J. Nat. Hist. 43: 1195–1206. https://doi.org/10.1080/00222930902767474.
Klingenberg, C.P. (2011): MorphoJ: an integrated software package for geometric morphometrics: computer program note. Mol. Ecol. Resour. 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.
Larson, P.M. (2002): Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): Morphometric analysis of cranial allometry and ontogenetic shape change. J. Morphol. 252: 131–144. https://doi.org/10.1002/jmor.1095.
Larson, P.M. (2004): Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphology 123: 95–106. https://doi.org/10.1007/s00435-003-0092-1.
Larson, P.M. (2005): Ontogeny, phylogeny, and morphology in anuran larvae: Morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae). J. Morphol. 264: 34–52. https://doi.org/10.1002/jmor.10313.
Lavorel, S., Díaz, S., Cornelissen, J.H.C., Garnier, E., Harrison, S.P., McIntyre, S., Pausas, J.G., Pérez-Harguindeguy, N., Roumet, C., Urcelay, C. (2007): Plant Functional Types: Are We Getting Any Closer to the Holy Grail? In: Terrestrial Ecosystems in a Changing World. pp. 149–174. Springer Berlin Heidelberg, Nova York.
Marques, N.S., Nomura, F. (2015): Where to Live? How Morphology and Evolutionary History Predict Microhabitat Choice by Tropical Tadpoles. Biotropica 47: 227–235. https://doi.org/10.1111/btp.12199.
McDiarmid, R.W., Altig, R. (1999): Tadpoles The Biology of Anuran Larvae, 1a. ed. University of Chicago Press, Chicago.
McGill, B., Enquist, B.J., Weiher, E., Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21: 178–185. https://doi.org/DOI: 10.1016/j.tree.2006.02.002.
Pezzuti, T.L., Fernandes, I.R., Leite, F.S.F., De Sousa, C.E., Garcia, P.C.A., Rossa-Feres, D., (2016): The tadpoles of the neotropical Scinax catharinae group (Anura, Hylidae): Ecomorphology and descriptions of two new forms. Zool. Anz. - J. Comp. Zool. 261: 22–32. https://doi.org/10.1016/j.jcz.2016.02.002.
Pinto, G.S., Ávila-Pires, T.C.S. (2004): Crescimento alométrico, morfologia e uso do habitat em cinco espécies de Mabuya Fitzinger (Reptilia, Scincidae). Rev. Bras. Zool. 21: 161–168. https://doi.org/10.1590/S0101-81752004000200001.
Provete, D.B., Garey, M.V., Toledo, L.F., Nascimento, J., Lourenço, L.B., Rossa-Feres, D. de C., Haddad, C.F.B. (2012): Redescription of Physalaemus barrioi (Anura: Leiuperidae). Copeia 2012: 507–518. https://doi.org/10.1643/CH-10-142.
Pyron, A.R., Wiens, J.J. (2011): A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61: 543–583. https://doi.org/10.1016/j.ympev.2011.06.012.
Queiroz, C. de S., Silva, F.R., Rossa-Feres, D. de C. (2015). The relationship between pond habitat depth and functional tadpole diversity in an agricultural landscape. R. Soc. Open Sci. 2: 150165. http://dx.doi.org/10.1098/rsos.150165.
Rivera-Correa, M., Faivovich, J. (2020): The tadpole of the stream treefrog Hyloscirtus antioquia (Anura: Hylidae: Cophomantini). Stud. Neotropical Fauna Environ. 1–7. https://doi.org/10.1080/01650521.2020.1804814.
Rohlf, F.J., Slice, D. (1990): Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Syst. Zool. 39: 40–59. https://doi.org/10.2307/2992207.
Rohlf, F. (2015): The tps series of software. Hystrix Ital. J. Mammal. 26: 9–12. https://doi.org/10.4404/hystrix-26.1-11264.
Rojas, R.R., Fouquet, A., Ron, S.R., Hernández-Ruz, E.J., Melo-Sampaio, P.R., Chaparro, J.C., Vogt, R.C., De Carvalho, V.T., Pinheiro, L.C., Avila, R.W. (2018): A Pan-Amazonian species delimitation: high species diversity within the genus Amazophrynella (Anura: Bufonidae). PeerJ 6: e4941.
Sabbag, A.F., Lyra, M.L., Zamudio, K.R., Haddad, C.F.B., Feio, R.N., Leite, F.S.F., Gasparini, J.L., Brasileiro, C.A. (2018): Molecular phylogeny of Neotropical rock frogs reveals a long history of vicariant diversification in the Atlantic forest. Mol. Phylogenet. Evol. 122: 142–156. https://doi.org/10.1016/j.ympev.2018.01.017.
Warkentin, K.M. (1992): Microhabitat Use and Feeding Rate Variation in Green Frog Tadpoles (Rana clamitans). Copeia 1992, 731–740. https://doi.org/10.2307/1446149.
Xavier Jordani, M., Mouquet, N., Casatti, L., Menin, M., Cerqueira Rossa‐Feres, D., Albert, C.H. (2019): Intraspecific and interspecific trait variability in tadpole meta‐communities from the Brazilian Atlantic rainforest. Ecol. Evol. 9: 4025–4037. https://doi.org/10.1002/ece3.5031.
Altig, R., (2007): A primer for the morphology of anuran tadpoles. Herpetol. Conserv. Biol. 71–74.
Altig, R., Johnston, G.F. (1989). Guilds of Anuran Larvae: Relationships among Developmental Modes, Morphologies, and Habitats. Herpetol. Monogr. 3: 81–109. https://doi.org/10.2307/1466987.
Altig, R., McDiarmid, R.W. (2006): Descriptions and biological notes on three unusual mantellid tadpoles (Amphibia: Anura: Mantellidae) from southeastern Madagascar. Proc. Biol. Soc. Wash. 119: 418–425. https://doi.org/10.2988/0006-324X(2006)119[418:DABNOT]2.0.CO;2.
Altig, R., McDiarmid, R.W. (1999): Development and Morphology. In: Tadpoles The Biology of Anuran Larvae. pp. 24–51. University of Chicago Press, Chicago.
Arendt, J. (2010): Morphological correlates of sprint swimming speed in five species of spadefoot toad tadpoles: Comparison of morphometric methods. J. Morphol. 271: 1044–1052. https://doi.org/10.1002/jmor.10851.
Barrasso, D.A., Cotichelli, L., Alcalde, L., Basso, N.G. (2013): Re-description of the tadpole of Pleurodema somuncurensis (Cei, 1969) (Amphibia: Anura). Zootaxa 3681: 192–196. https://doi.org/10.11646/zootaxa.3681.2.10
Blotto, B.L., Nuñez, J.J., Basso, N.G., Úbeda, C., Wheeler, W.C., Faivovich, J. (2012): Phylogenetic relationships of a Patagonian frog radiation, the Alsodes+Eupsophus clade (Anura: Alsodidae), with comments on the supposed paraphyly of Eupsophus. Cladistics 1–19.
Bolzan, A.M.R., Saccol, S.A., Santos, T.G. (2016): Composition and diversity of anurans in the largest conservation unit in Pampa biome, Brazil. Biota Neotropica 16: e20150113. https://doi.org/10.1590/1676-0611-BN-2015-0113.
Bookstein, F.L. (1989): “Size and Shape”: A Comment on Semantics. Syst. Zool. 38: 173–180. https://doi.org/10.2307/2992387.
Borteiro, C., Kolenc, F. (2007): Redescription of the tadpoles of three species of frogs from Uruguay (Amphibia: Anura: Leiuperidae and Leptodactylidae), with notes on natural history. Zootaxa 1638: 1–20. https://doi.org/10.11646/zootaxa.1638.1.1.
Candioti, M.F.V., Nuñez, J.J., Úbeda, C. (2011). Development of the nidicolous tadpoles of Eupsophus emiliopugini (Anura: Cycloramphidae) until metamorphosis, with comments on systematic relationships of the species and its endotrophic developmental mode. Acta Zool. 92: 27–45. https://doi.org/10.1111/j.1463-6395.2010.00448.x.
Cerbo, A.R.D., Biancardi, C.M. (2010): Morphometric study on tadpoles of Bombina variegata (Linnaeus, 1758) (Anura; Bombinatoridae). Acta Herpetol. 5: 223–231.
Formas, J.R., Cuevas, C.C. (2017): The tadpole of Alsodes cf. norae (Anura: Alsodidae) with comments on the diagnosis of the genus Alsodes. Salamandra 53: 131–136.
Garriga, N., Llorente, G.A. (2012): Chondrocranial ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: geometric morphometric and allometric change analysis. Acta Zool. 93: 453–464. https://doi.org/10.1111/j.1463-6395.2011.00520.x.
Glime, J.M., Boelema, W.J. (2017): Anurans: Central and South American mossy habitats, in: Bryophyte Ecology. Michigan Technological University, p. 16.
Gosner, K.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.
Grant, T., Rada, M., Anganoy-Criollo, M., Batista, A., Dias, P.H., Jeckel, A.M., Machado, D.J., Rueda-Almonacid, J.V. (2017): Phylogenetic Systematics of Dart-Poison Frogs and Their Relatives Revisited (Anura: Dendrobatoidea). South Am. J. Herpetol. 12: S1–S90. https://doi.org/10.2994/SAJH-D-17-00017.1.
Grosjean, S. (2005): The choice of external morphological characters and developmental stages for tadpole-based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth, 1855) (Amphibia, Anura, Ranidae). Contrib. Zool. 74: 61–76. https://doi.org/10.1163/18759866-0740102005.
Haad, B., Vera Candioti, F., Baldo, D. (2011): Shape variation in lentic and lotic tadpoles of Melanophryniscus (Anura: Bufonidae). Stud. Neotropical Fauna Environ. 46: 91–99. https://doi.org/10.1080/01650521.2011.593124.
Iop, S., Mendes Lipinski, V., Madalozzo, B., Pereira Maragno, F., Zanini Cechin, S., Gomes Dos Santos, T. (2015): Re-description of the external morphology of Phyllomedusa iheringii Boulenger, 1885 larvae (Anura: Hylidae), with comments on the external morphology of tadpoles of the P. burmeisteri group. Acta Herpetol. 67-72. https://doi.org/10.13128/ACTA_HERPETOL-15547.
Johnson, J.B., Burt, D.B., DeWitt, T.J. (2008): Form, Function, and Fitness: Pathways to survival. Evolution 62: 1243–1251. https://doi.org/10.1111/j.1558-5646.2008.00343.x.
Kaefer, I.L., Both, C., Cechin, S.Z. (2009): Breeding biology of the rapids frog Limnomedusa macroglossa (Anura: Cycloramphidae) in southern Brazil. J. Nat. Hist. 43: 1195–1206. https://doi.org/10.1080/00222930902767474.
Klingenberg, C.P. (2011): MorphoJ: an integrated software package for geometric morphometrics: computer program note. Mol. Ecol. Resour. 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x.
Larson, P.M. (2002): Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): Morphometric analysis of cranial allometry and ontogenetic shape change. J. Morphol. 252: 131–144. https://doi.org/10.1002/jmor.1095.
Larson, P.M. (2004): Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphology 123: 95–106. https://doi.org/10.1007/s00435-003-0092-1.
Larson, P.M. (2005): Ontogeny, phylogeny, and morphology in anuran larvae: Morphometric analysis of cranial development and evolution in Rana tadpoles (Anura: Ranidae). J. Morphol. 264: 34–52. https://doi.org/10.1002/jmor.10313.
Lavorel, S., Díaz, S., Cornelissen, J.H.C., Garnier, E., Harrison, S.P., McIntyre, S., Pausas, J.G., Pérez-Harguindeguy, N., Roumet, C., Urcelay, C. (2007): Plant Functional Types: Are We Getting Any Closer to the Holy Grail? In: Terrestrial Ecosystems in a Changing World. pp. 149–174. Springer Berlin Heidelberg, Nova York.
Marques, N.S., Nomura, F. (2015): Where to Live? How Morphology and Evolutionary History Predict Microhabitat Choice by Tropical Tadpoles. Biotropica 47: 227–235. https://doi.org/10.1111/btp.12199.
McDiarmid, R.W., Altig, R. (1999): Tadpoles The Biology of Anuran Larvae, 1a. ed. University of Chicago Press, Chicago.
McGill, B., Enquist, B.J., Weiher, E., Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21: 178–185. https://doi.org/DOI: 10.1016/j.tree.2006.02.002.
Pezzuti, T.L., Fernandes, I.R., Leite, F.S.F., De Sousa, C.E., Garcia, P.C.A., Rossa-Feres, D., (2016): The tadpoles of the neotropical Scinax catharinae group (Anura, Hylidae): Ecomorphology and descriptions of two new forms. Zool. Anz. - J. Comp. Zool. 261: 22–32. https://doi.org/10.1016/j.jcz.2016.02.002.
Pinto, G.S., Ávila-Pires, T.C.S. (2004): Crescimento alométrico, morfologia e uso do habitat em cinco espécies de Mabuya Fitzinger (Reptilia, Scincidae). Rev. Bras. Zool. 21: 161–168. https://doi.org/10.1590/S0101-81752004000200001.
Provete, D.B., Garey, M.V., Toledo, L.F., Nascimento, J., Lourenço, L.B., Rossa-Feres, D. de C., Haddad, C.F.B. (2012): Redescription of Physalaemus barrioi (Anura: Leiuperidae). Copeia 2012: 507–518. https://doi.org/10.1643/CH-10-142.
Pyron, A.R., Wiens, J.J. (2011): A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61: 543–583. https://doi.org/10.1016/j.ympev.2011.06.012.
Queiroz, C. de S., Silva, F.R., Rossa-Feres, D. de C. (2015). The relationship between pond habitat depth and functional tadpole diversity in an agricultural landscape. R. Soc. Open Sci. 2: 150165. http://dx.doi.org/10.1098/rsos.150165.
Rivera-Correa, M., Faivovich, J. (2020): The tadpole of the stream treefrog Hyloscirtus antioquia (Anura: Hylidae: Cophomantini). Stud. Neotropical Fauna Environ. 1–7. https://doi.org/10.1080/01650521.2020.1804814.
Rohlf, F.J., Slice, D. (1990): Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Syst. Zool. 39: 40–59. https://doi.org/10.2307/2992207.
Rohlf, F. (2015): The tps series of software. Hystrix Ital. J. Mammal. 26: 9–12. https://doi.org/10.4404/hystrix-26.1-11264.
Rojas, R.R., Fouquet, A., Ron, S.R., Hernández-Ruz, E.J., Melo-Sampaio, P.R., Chaparro, J.C., Vogt, R.C., De Carvalho, V.T., Pinheiro, L.C., Avila, R.W. (2018): A Pan-Amazonian species delimitation: high species diversity within the genus Amazophrynella (Anura: Bufonidae). PeerJ 6: e4941.
Sabbag, A.F., Lyra, M.L., Zamudio, K.R., Haddad, C.F.B., Feio, R.N., Leite, F.S.F., Gasparini, J.L., Brasileiro, C.A. (2018): Molecular phylogeny of Neotropical rock frogs reveals a long history of vicariant diversification in the Atlantic forest. Mol. Phylogenet. Evol. 122: 142–156. https://doi.org/10.1016/j.ympev.2018.01.017.
Warkentin, K.M. (1992): Microhabitat Use and Feeding Rate Variation in Green Frog Tadpoles (Rana clamitans). Copeia 1992, 731–740. https://doi.org/10.2307/1446149.
Xavier Jordani, M., Mouquet, N., Casatti, L., Menin, M., Cerqueira Rossa‐Feres, D., Albert, C.H. (2019): Intraspecific and interspecific trait variability in tadpole meta‐communities from the Brazilian Atlantic rainforest. Ecol. Evol. 9: 4025–4037. https://doi.org/10.1002/ece3.5031.