Skip to main content
SpringerLink
Log in

Heterochrony in Growth and Development in Anurans from the Chaco of South America

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Heterochrony refers to those permutations in timing of differentiation events, and those changes in rates of growth and development through which morphological changes and novelties originate during phyletic evolution. This research analyzes morphological variation during the ontogeny of 18 different anuran species that inhabit semi-arid environments of the Chaco in South America. I use field data, collection samples, and anatomical methods to compare larval growth, and sequences of ontogenetic events. Most species present a similar pattern of larval development, with a size at metamorphosis related to the duration of larval period, and disappearance and transformations of larval features that occur in a short period between forelimb emergence and tail loss. Among these 18 species, Pseudis paradoxa has giant tadpole and long larval development that are the results of deviations of rates of growth. In this species events of differentiation that usually occur at postmetamorphic stages have an offset when tail is still present. Tadpoles of Lepidobatrachus spp. reach large sizes at metamorphosis by accelerate developmental rates and exhibit an early onset of metamorphic features. The uniqueness of the ontogeny of Lepidobatrachus indicates that evolution of anuran larval development may occasionally involve mid-metamorphic morphologies conserving a free feeding tadpole and reduction of the morphological-ecological differences between tadpoles and adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Alberch, P., Gould, S. J., Oster, G. F., & Wake, D. B. (1979). Size and shape in ontogeny and phylogeny. Paleobiology, 5, 296–317.

    Google Scholar 

  • Altig, R. I., & Johnston, G. F. (1989). Guilds of anuran larvae: Relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3, 81–109.

    Article  Google Scholar 

  • Brown, D. D., Cai, L., Das, B., Marsh-Armstrong, N., Schreiber, A. M., & Juste, R. (2005). Thyroid hormone controls multiple independent programs required for limb development in Xenopus laevis metamorphosis. PNAS, 102, 12455–12458.

    Article  PubMed  CAS  Google Scholar 

  • Carroll, E. J., Jr, Seneviratne, A. M., & Ruibal, R. R. (1991). Gastric pepsin in an anuran larva. Development Growth and Differentiation, 33, 499–507.

    Article  CAS  Google Scholar 

  • Cei, J. M. (1981). Amphibians of Argentina. Monitore Zoologico Italiano, Monographia, 2, 1–609.

    Google Scholar 

  • de Sá, R. O. (1988). Chondrocranium and ossification sequence of Hyla lanciformis. Journal of Morphology, 195, 345–355.

    Article  Google Scholar 

  • Denver, R. J. (1997). Proximate mechanisms of phenotypic plasticity in amphibian metamorphosis. American Zoologist, 37, 172–184.

    CAS  Google Scholar 

  • Downie, J. R., Bryce, R., & Smith, J. (2004). Metamorphic duration: An under-studied variable in frog life histories. Biological Journal of the Linnean Society, 83, 261–272.

    Article  Google Scholar 

  • Downie, J. R., Sams, K., & Walsh, P. T. (2009). The paradoxical frog Pseudis paradoxa: Larval anatomical characteristics, including gonadal maturation. Herpetological Journal, 19, 1–10.

    Google Scholar 

  • Dunker, N., Wake, M. H., & Olson, W. (2000). Embryonic and larval development in the caecilian Ichthyophis kohtauensis (Amphibia, Gymnophiona): A staging table. Journal of Morphology, 243, 3–34.

    Article  PubMed  CAS  Google Scholar 

  • Emerson, S. B. (1988). The giant tadpole of Pseudis paradoxa. Biological Journal of the Linnean Society, 34, 93–104.

    Article  Google Scholar 

  • Fabrezi, M. (1992). El carpo de los anuros. Alytes, 10, 1–29.

    Google Scholar 

  • Fabrezi, M. (1993). The anuran tarsus. Alytes, 11, 47–63.

    Google Scholar 

  • Fabrezi, M. (2001). A survey of prepollex and prehallux variation in anuran limbs. Zoological Journal of the Linnean Society, 131, 227–248.

    Article  Google Scholar 

  • Fabrezi, M. (2006). Morphological evolution of Ceratophryinae (Anura, Neobatrachia). Journal of Zoological Systematics and Evolutionary Research, 44, 153–166.

    Article  Google Scholar 

  • Fabrezi, M., & Alberch, P. (1996). The carpal elements of anurans. Herpetologica, 52, 188–204.

    Google Scholar 

  • Fabrezi, M., & Barg, M. (2001). Patterns of carpal development among anuran amphibians. Journal of Morphology, 249, 210–220.

    Article  PubMed  CAS  Google Scholar 

  • Fabrezi, M., & Emerson, S. B. (2003). Parallelism and convergence in anuran fangs. Journal of Zoology, 260, 41–51.

    Article  Google Scholar 

  • Fabrezi, M., & Goldberg, J. (2009). Heterochrony during skeletal development of Pseudis platensis (Anura, Hylidae) and the early offset of skeleton development and growth. Journal of Morphology, 270, 205–220.

    Article  PubMed  Google Scholar 

  • Fabrezi, M., & Lobo, F. J. (2009). Hyoid skeleton, related muscles, and morphological novelties in the frog Lepidobatrachus (Anura, Ceratophryidae). Anatomical Record, 292, 1700–1712.

    Article  Google Scholar 

  • Fabrezi, M., & Quinzio, S. I. (2008). Morphological evolution in Ceratophyinae frogs (Anura, Neobatrachia): the effects of heterochronic changes during larval development and metamorphosis. Zoological Journal of the Linnean Society, 154, 752–780.

    Article  Google Scholar 

  • Fabrezi, M., Quinzio, S. I., & Goldberg, J. (2009). The giant tadpole and delayed metamorphosis of Pseudis platensis Gallardo, 1961 (Anura. Hylidae). Journal of Herpetology, 43, 228–243.

    Article  Google Scholar 

  • Fabrezi, M., Quinzio, S. I., & Goldberg, J. (2010). The ontogeny of Pseudis platensis (Anura, Hylidae): Heterochrony and the effects of larval development in the postmetamorphic life. Journal of Morphology, 271, 496–510.

    PubMed  Google Scholar 

  • Faivovich, J., Haddad, C. F., Garcia, P. C. A., Frost, D. R., Campbell, J. A., & Wheeler, W. C. (2005). Systematic review of the frog family Hylidae, with special reference to Hylinae: Phylogenetic analysis and taxonomic revision. Bulletin American Museum of Natural History, 294, 1–240.

    Article  Google Scholar 

  • Farnum, C. E. (2007). Postnatal growth of fins and limbs through endochondral ossification. In B. K. Hall (Ed.), Fins into limbs. Evolution, development, and transformation (pp. 118–151). Chicago: Chicago University Press.

    Google Scholar 

  • Filipski, G. T. (1985). Staining nerves in whole cleared amphibians and reptiles using Sudan Black B. Copeia, 1985, 500–502.

    Article  Google Scholar 

  • Filipski, G. T., & Wilson, M. H. V. (1984). Sudan Black B as a nerve stain for whole cleared fishes. Copeia, 1984, 204–208.

    Article  Google Scholar 

  • Frost, D. R. (2011). Amphibian species of the World: An online reference. Version 5.5 (January 31, 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/American Museum of Natural History, New York, USA.

  • Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., et al. (2006). The amphibian tree of life. Bulletin of American Museum of Natural History, 297, 1–370.

    Article  Google Scholar 

  • Garda, A. A., Santana, D. J., & de Avelar São Pedro, V. (2010). Taxonomic characterization of Paradoxical frogs (Anura, Hylidae, Pseudae): Geographic distribution, external morphology, and morphometry. Zootaxa, 2666, 1–28.

    Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.

    Google Scholar 

  • Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge: The Belknap Press of Harvard University Press.

  • Grant, T., Frost, D. R., Cladwell, J. P., Gagliardo, R., Haddad, C. F. B., Kok, P. J. R., et al. (2006). Phylogenetic systematics of dartpoison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of American Museum of Natural History, 299, 1–262.

    Article  Google Scholar 

  • Haas, A. (1999). Larval and metamorphic development in the fast developing frog Pyxicephalus adspersus (Anura, Ranidae). Zoomorphology, 119, 23–35.

    Article  Google Scholar 

  • Haas, A. (2001). Mandibular arch musculature of anuran tadpoles, with comments on homologies of amphibian jaw muscles. Journal of Morphology, 247, 1–33.

    Article  PubMed  CAS  Google Scholar 

  • Haas, A. (2003). Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics, 19, 23–89.

    Google Scholar 

  • Hall, J. A., Larsen, J. H., Jr, & Fitzner, R. E. (2002). Morphology of the Premetamorphic larva of the spadefoot toad, Scaphiopus intermontanus (Anura: Pelobatidae), with an emphasis on the lateral line system and mouthparts. Journal of Morphology, 252, 114–130.

    Article  PubMed  Google Scholar 

  • Handrigan, G. R., & Wassersug, R. J. (2007). The anuran Bauplan: A review of the adaptive, developmental, and genetic underpinnings of frog and tadpole morphology. Biological Reviews, 82, 1–25.

    Article  PubMed  Google Scholar 

  • Hanken, J. (1992). Life history and morphological evolution. Journal of Evolutionary Biology, 5, 549–557.

    Article  Google Scholar 

  • Hanken, J. (1993). Model systems versus outgroups: Alternative approaches to the study of head development and evolution. American Zoologist, 33, 448–456.

    Google Scholar 

  • Hanken, J., & Hall, B. K. (1984). Variation and timing of the cranial ossification sequence of the oriental fire-bellied toad, Bombina orientalis (Amphibia, Discoglossidae). Journal of Morphology, 182, 245–255.

    Article  Google Scholar 

  • Hanken, J., & Summers, C. H. (1988). Skull development during anuran metamorphosis: III. Role of thyroid hormone in chondrogenesis. Journal of Experimental Zoology, 246, 156–170.

    Article  PubMed  Google Scholar 

  • Hanken, J., Summers, C. H., & Hall, B. K. (1989). Morphological integration in the cranium during anuran metamorphosis. Experientia, 45, 872–875.

    Article  PubMed  CAS  Google Scholar 

  • Hayes, T. B. (1997). Steroids as potential modulators of thyroid hormone activity in anuran metamorphosis. American Zoologist, 37, 185–194.

    CAS  Google Scholar 

  • Kupferberg, S. J. (1997). The role of larval diet in anuran metamorphosis. American Zoologist, 37, 146–159.

    CAS  Google Scholar 

  • Ledón-Rettig, C. C., Pfennig, D. W., & Crespi, E. J. (2010). Diet and hormonal manipulation reveal cryptic genetic variation: Implications for the evolution of novel feeding strategies. Proceedings of the Royal Society B, 277, 3569–3578.

    Article  PubMed  Google Scholar 

  • Ledón-Rettig, C. C., Pfenning, D. W., & Crespi, E. J. (2009). Stress hormones and the fitness consequences associated with the transition to a novel diet in larval amphibians. Journal of Experimental Biology, 212, 3743–3750.

    Article  PubMed  Google Scholar 

  • Maglia, A. M., & Pugener, L. A. (1998). Skeletal development and adult osteology of Bombina orientalis (Anura: Bombinatoridae). Herpetologica, 54, 344–363.

    Google Scholar 

  • Maglia, A. M., Pugener, L. A., & Mueller, J. M. (2007). Skeletal morphology and postmetamorphic ontogeny of Acris crepitans (Anura: Hylidae): A case of miniaturization in frogs. Journal of Morphology, 268, 194–223.

    Article  PubMed  Google Scholar 

  • Nieuwkoop, P. D., & Faber, J. (1956). Normal table of Xenopus laevis (Daudin). Amsterdam: North Holland Publ. Co.

    Google Scholar 

  • Nishikawa, K. C. (1987). Staining peripheral nerves with Sudan Black B: Progressive vs. regressive methods. Copeia, 1987, 489–491.

    Article  Google Scholar 

  • O’Reilly, J. C., Deban, S. M., & Nishikawa, K. C. (2002). Derived life history characteristics constrain the evolution of aquatic feeding behaviour in adult amphibians. In P. Aerts, K. D’aout, A. Herrel, & R. Van Damme (Eds.), Topics in functional and ecological vertebrate morphology (pp. 153–190). Maastricht: Shaker Publishing.

    Google Scholar 

  • Ogielska, M., & Kotusz, A. (2004). Pattern of ovary differentiation with reference to somatic development in anuran amphibians. Journal of Morphology, 259, 41–54.

    Article  PubMed  Google Scholar 

  • Orton, G. I. (1953). The systematics of vertebrate larvae. Systematic Zoology, 2, 63–75.

    Article  Google Scholar 

  • Orton, G. I. (1957). The bearing of larval evolution on some problems in frog classification. Systematic Zoology, 6, 79–86.

    Article  Google Scholar 

  • Perotti, M. G. (2001). Skeletal development of Leptodactylus chaquensis (Anura: Leptodactylidae). Herpetologica, 57, 318–335.

    Google Scholar 

  • Pfennig, D. W., Hudson, K. R., & Sherman, P. W. (1993). Kin recognition and cannibalism in spadefoot toad tadpoles. Animal Behavior, 46, 87–94.

    Article  Google Scholar 

  • Ponssa, M. L. (2008). Cladistic analysis and osteological descriptions of the frog species in the Leptodactylus fuscus species group (Anura, Leptodactylidae). Journal of Zoological Systematics and Evolutionary Research, 46, 249–266.

    Article  Google Scholar 

  • Přikryl, T., Aerts, P., Havelková, P., Herrel, A., & Roček, Z. (2009). Pelvic and thigh musculature in frogs (Anura) and origin of anuran jumping locomotion. Journal of Anatomy, 214, 100–139.

    Article  PubMed  Google Scholar 

  • Pugener, L. A., & Maglia, A. M. (1997). Osteology and skeletal development of Discoglossus sardus (Anura: Discoglossidae). Journal of Morphology, 233, 267–286.

    Article  Google Scholar 

  • Pugener, L. A., & Maglia, A. M. (2007). Skeletal morphology and development of the olfactory region of Spea (Anura: Scaphiopodidae). Journal of Anatomy, 211, 754–768.

    Article  PubMed  CAS  Google Scholar 

  • Pugener, L. A., & Maglia, A. M. (2009). Developmental evolution of the anuran sacro-urostylic complex. South American Journal of Herpetology, 4, 193–209.

    Article  Google Scholar 

  • Quinzio, S. I., Fabrezi, M., & Faivovich, J. (2006). Redescription of the tadpole of Chacophrys pierottii (Vellard, 1948) (Anura: Ceratophryidae). South American Journal of Herpetology, 1, 202–209.

    Article  Google Scholar 

  • Roček, Z., Böttcher, R., & Wassersug, R. J. (2006). Gigantism in the tadpoles of the Neogene frog Paleobatrachus. Paleobiology, 32(4), 666–675.

    Article  Google Scholar 

  • Roelants, K., Haas, A., & Bossuyt, F. (2011). Anuran radiations and the evolution of tadpole morphospace. PNAS, 108, 8731–8736.

    Article  PubMed  CAS  Google Scholar 

  • Rot-Nikcevic, I., & Wassersug, R. J. (2004). Arrested development in Xenopus laevis tadpoles: How size constrains metamorphosis. Journal of Experimental Biology, 207, 1133–1145.

    Article  Google Scholar 

  • Ruibal, R. R., & Thomas, E. (1988). The obligate carnivorous larvae of the frog Lepidobatrachus laevis (Leptodactylidae). Copeia, 1988, 591–604.

    Article  Google Scholar 

  • Schoch, R. R., & Fröbisch, (2006). Metamorphosis and neoteny: Alternative pathways in an extinct amphibian clade. Evolution, 60, 1467–1475.

    PubMed  Google Scholar 

  • Schreiber, A. M., Das, B., Huang, H., Marsh-Armstrong, N., & Brown, D. D. (2001). Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. PNAS, 98, 10739–10744.

    Article  PubMed  CAS  Google Scholar 

  • Sheil, C. A., & Alamillo, H. (2005). Osteology and skeletal development of Phyllomedusa vaillanti (Anura: Hylidae: Phyllomedusinae) and a comparison of this arboreal species with a terrestrial member of the genus. Journal of Morphology, 265, 343–368.

    Article  PubMed  Google Scholar 

  • Smith, K. (2001). Heterochrony revisited: The evolution of developmental sequences. Biological Journal fo the Linnean Society, 73, 169–186.

    Article  Google Scholar 

  • Smith, K. (2002). Sequence heterochrony and the evolution of development. Journal of Morphology, 252, 82–97.

    Article  PubMed  Google Scholar 

  • Sokol, O. (1975). The phylogeny of anuran larvae: A new look. Copeia, 1975, 1–23.

    Article  Google Scholar 

  • Solano, H. (1987). Algunos aspectos de la biologia reproductiva del sapito silabador Leptodactylus fuscus (Schneider) (Amphibia: Leptodactylidae). Amphibia-Reptilia, 8, 111–128.

    Article  Google Scholar 

  • Stolow, M. A., Ishizuya-Oka, A., Su, Y., & Shi, Y.-B. (1997). Gene regulation by thyroid hormone during amphibian metamorphosis: Implications on the role of cell–cell and cell-extracellular matrix interactions. American Zoologist, 37, 195–207.

    CAS  Google Scholar 

  • Tamakoshi, T., Oofusa, K., & Yoshizato, K. (1998). Visualization of the initiation and sequential expansion of the metamorphic conversion of anuran larval skin into the precursor of adult type. Development Growth and Differentiation, 40, 105–112.

    Article  CAS  Google Scholar 

  • Taylor, A. C., & Kollros, (1946). Stages in the normal development of Rana pipiens larvae. Anatomical Record, 94, 7–23.

    Article  PubMed  CAS  Google Scholar 

  • Trueb, L. (1994). Patterns of cranial diversity among Lissamphibia. In J. Hanken & B. K. Hall (Eds.), The skull, Vol. 2: Patterns of structural and systematic diversity (pp. 255–343). Chicago: The University of Chicago Press.

    Google Scholar 

  • Trueb, L., & Alberch, P. (1985). Miniaturization and the anuran skull: A case study of heterochrony. In H.-R. Duncker & G. Fleisher (Eds.), Vertebrate morphology (pp. 113–121). New York: Gustav Fischer Verlag.

    Google Scholar 

  • Ulloa Kreisel, Z. E. (2002). Características morfológicas del tubo digestivo en larvas carnívoras de Lepidobatrachus laevis (Anura: Leptodactylidae). Acta Zoologica Lilloana, 46, 31–38.

    Google Scholar 

  • Wassersug, R. J. (1976). A procedure for differential staining of cartilage and bone in whole formalin fixed vertebrates. Stain Technology, 51, 131–134.

    PubMed  CAS  Google Scholar 

  • Wassersug, R. J., & Heyer, W. R. (1988). A survey of internal oral features of Leptodactyloid larvae (Amphibia: Anura). Smithsonian Contributions to Zoology, 457, 1–96.

    Article  Google Scholar 

  • Wassersug, R. J., & Hoff, K. (1982). Developmental changes in the orientation of the anuran jaw suspension: A preliminary exploration into the evolution of anuran metamorphosis. Evolutionary Biology, 15, 223–246.

    Google Scholar 

  • Wassersug, R. J., & Sperry, D. G. (1977). The relationships of locomotion to differential predation on Pseudacris triseriata (Anura, Hylidae). Ecology, 58, 830–839.

    Article  Google Scholar 

  • Wiens, J. J. (1989). Ontogeny of the skeleton of Spea bombifrons (Anura: Pelobatidae). Journal of Morphology, 202, 29–51.

    Article  Google Scholar 

  • Wilbur, H. M., & Collins, J. P. (1973). Ecological aspects of amphibian metamorphosis. Science, 182, 1305–1314.

    Article  PubMed  CAS  Google Scholar 

  • Wild, E. R. (1997). Description of the adult skeleton and developmental osteology of the hyperossified horned frog, Ceratophrys cornuta (Anura: Leptodactylidae). Journal of Morphology, 232, 169–206.

    Article  PubMed  CAS  Google Scholar 

  • Wild, E. R. (1999). Description of the chondrocranium and osteogenesis of the chacoan burrowing frog, Chacophrys pierottii (Anura: Leptodactylidae). Journal of Morphology, 242, 229–246.

    Article  PubMed  CAS  Google Scholar 

  • Yeh, J. (2002). The effect of miniaturized body size on skeletal morphology in frogs. Evolution, 56, 2628–2641.

    Google Scholar 

  • Yoshizato, K. (1992). Death and transformation of larval cells during the metamorphosis of Anura. Development Growth and Differentiation, 34, 607–612.

    Article  Google Scholar 

Download references

Acknowledgments

I am grateful to Natalia von Ellenrieder for many suggestions on the English written. Two anonymous reviewers contributed with many comments to improve the manuscript. Javier Goldberg, Silvia Quinzio, and Fernando Hongn provided many useful suggestions and comments. Fernando Hongn, Gladys Gonzo, Javier Goldberg, Silvia Quinzio, Roberto Bernal, and Soledad Valdecantos collaborated with field work. This research was supported Consejo Nacional de Investigaciones Científicas y Técnicas PIP 0239.

Author information

Authors and Affiliations

  1. Instituto de Bio y Geociencias—Consejo Nacional de Investigaciones Científicas y Técnicas, Mendoza 2, 4400, Salta, Republic of Argentine

    Marissa Fabrezi

Authors
  1. Marissa Fabrezi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marissa Fabrezi.

Appendix

Appendix

Localities Studied

Localities in which larval development was studied are placed in the Chaco region that comprises a plain of approximately 1.141.000 km2 in the south-central South America (from 16° 55′ S–33° 52′ and 67° 50′W– 57° 52′W). It is an arid and subtropical region of low forests and savannas traversed by only two permanent rivers: Pilcomayo and Bermejo that flow southeastward across the plain from their Andean headwaters to Paraguay River. The Chaco is subject to climates that vary from tropical in the north to warm-temperate in the south. The mean of annual temperature varies between 26º and 16º with an average of 22°C. The highest recorded temperatures for the continent occur in the Chaco with absolute maximums that may reach 54°C. There is marked seasonality, with warm summers with precipitations ranging with a West-East gradient from 300 to 1,000 mm. Evaporation losses (1,500–900 mm) sharply reduce the effective precipitation and give the Chaco an arid nature that is absent only in the permanent swamps and forests along Paraguay River. Specimens and field data presented in this research were obtained from three localities:

Locality 1:

Totoralejos, Córdoba, Argentina: 29°38′28.00′′S, 64°50′58.37′′W. Taxa found in this locality at the same time (late December 2004; January 2006): Ceratophryidae (Chacophrys pierottii, Lepidobatrachus llanensis), Leptodactylidae (Leptodactylus mystacinus)

Locality 2:

Provincial Route 5, between 24°44′8.00′′S, 64°12′8.23′′W–24°26′9.17′′S, 63°59′17.62′′W. Taxa found in this locality during the four rainy seasons (November–April 1994–1997, 2007): Bufonidae (Rhinella arenarum, R. schneideri), Ceratophryidae (Ceratophrys cranwelli, Lepidobatrachus llanensis), Cycloramphidae (Odontophrynus lavillai), Hylidae (Phyllomedusa sauvagii, Scinax fuscovarius, S. nasicus, Trachycephalus typhonius), Leiuperidae (Physalemus biligonigerus, P. cuqui; Pleurodema tucumanum), Leptodactylidae (Leptodactylus chaquensis, L. bufonius, L. fuscus, L. latinasus, L. mystacinus), Microhylidae (Dermatonotus muelleri, Elachistocleis bicolor)

Locality 3:

National Route 81, between 23°12′34.68′′S, 63°34′27.48′′W–23°14′49.96′′S, 63°21′11.64 W. Species found in this locality during several rainy seasons (November–April, 1996–2010): Bufonidae (Rhinella granulosa, R. schneideri), Ceratophryidae (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, L. llanensis), Hylidae (Dendropsophus nanus, Hypsiboas raniceps, Phyllomedusa azurea, P. sauvagii, Pseudis paradoxa, Scinax acuminatus, S. fuscovarius, S. nasicus, Trachycephalus typhonius), Leiuperidae (Physalemus biligonigerus, P. cuqui); Leptodactylidae (Leptodactylus chaquensis, L. bufonius, L. fuscus, L. latinasus, L. mystacinus), Microhylidae (Dermatonotus muelleri, Elachistocleis bicolor)

Geographical Ranges of Studied Species

Frost (2011) summarized the distribution of the studied species as follows:

Ceratophrys cranwelli: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Chacophrys pierottii: Chacoan region, Argentina, Paraguay, and Bolivia

Dermatonotus muelleri: Northern Argentina, eastern Bolivia; Paraguay; Brazil

Elachistocleis bicolor: Central Argentina and Uruguay, Paraguay, Bolivia and Amazonian Brazil.

Lepidobatrachus laevis:: Chacoan region, Argentina, Paraguay, and Bolivia

Lepidobatrachus llanensis: Chacoan region, Argentina, Paraguay, and Bolivia

Leptodactylus chaquensis: Chacoan region, Argentina, Bolivia, Paraguay and northern Uruguay, and southern Brazil.

Leptodactylus fuscus: Savannas from Panama throughout South America, east of the Andes, Brazil, Bolivia, Paraguay, and Argentina.

Leptodactylus latinasus: Chacoan region, Argentina, Bolivia, and Paraguay and Uruguay, and southern Brazil

Leptodactylus mystacinus: Bolivia, Brazil, Uruguay, Paraguay to central Argentina.

Phyllomedusa azurea: Chacoan region, Argentina, Paraguay, and Bolivia and pantanal and cerrado regions, Brazil with an isolated population in southern Brazil.

Phyllomedusa sauvagii: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Physalaemus biligonigerus: Northern and central Argentina; Bolivia; Paraguay; Uruguay; southern Brazil.

Pseudis paradoxa*: Lower Río Magdalena Valley as well as Arauca and Meta in Colombia; Guianas from northeastern Venezuela east through Guyana, Surinam, and French Guiana to the mouth of the Amazon, thence west in the Amazon Valley to northern Bolivia and southeastern Peru; Trinidad. * Populations in the northern of Argentina were recognized as Pseudis paradoxa by Garda et al. (2010).

Scinax acuminatus: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Scinax fuscovarius: Argentina, Bolivia, Brazil, and Paraguay, between 150 and 1,800 m elevation.

Scinax nasicus: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay and central Argentina, Uruguay, and southern Brazil

Trachycephalus typhonius: Lowlands of tropical Mexico, Central America, Trinidad and Tobago, Amazon Basin, Paraguay, northern Argentina.

Specimens Examined

Analyses of external morphology, measurements, and whole mounts of skeleton and peripheral nerves were obtained from the following list of specimens that are deposited in the Museo de Ciencias Naturales, Universidad Nacional de Salta, Argentina (MCN).

Ceratophryidae

Chacophrys pierottii
Locality 1:

MCN 1027 (60 specimens, larval stages 26–31, January, 16 2006); MCN 1028 (40 specimens, larval stages 31–36, January, 22, 2006), MCN 1029 (56 specimens, larval stages 35–46, January, 28, 2006), MCN 987 (nine males, three females, December, 29, 2004), MCN 1045 (one female, January, 16, 2006)

Lepidobatrachus llanensis
Locality 1:

MCN 986 (six males, 3 females, December 29, 2004), MCN 1122 (14 specimens, larval stages 39–46, January 28, 2006), MCN 1178 (36 specimens, larval stages 32–38, January 16, 2006)

Locality 2:

MCN s/n, (14 specimens, larval stages 31–37, November 15, 1996), MCN s/n (3 specimens, larval stages 39–41, November 21, 1996)

Locality 3:

MCN 567 (55 specimens, larval stages 33–39, December 1, 1998), MCN 932 (43 specimens, larval stages 31–37, November 25, 2000), MCN 665 (70 specimens, larval stages 36–41, January 5, 2000), MCN 1118 (45 specimens, larval stages 36–46, December 18, 2005), MCN 1319/1321 (36 specimens, larval stages 39–46, December 9, 2009)

Lepidobatrachus laevis
Locality 3:

MCN 936 (one juvenile, November 2, 1998), MCN 663 (15 specimens, larval stages 36–41, December 1, 1998), MCN 647 (25 specimens, larval stages 33–40, January 5, 2000), MCN 666 (seven specimens, larval stages 38–43 and one froglet, January 5, 2000); MCN 668 (one froglet, January 5, 2000), MCN 695/696 (three juvenile specimen, January 5, 2000), MCN 934 (one juvenile, November 25, 2000), MCN 931 (three adults, January 20, 2001); MCN 935 (one juvenile, January 2003); MCN 815 (one adult and three juveniles, December 15, 2003), MCN 814 (six specimens, larval stages 36–38, December 28, 2003), MCN 817 (three juveniles, December 28, 2003), MCN 989 (one female, April 15, 2005), MCN 1175 (35 specimens, larval stages 34–46, December 18, 2005), MCN 1174 (female, March 10, 2006), MCN 1341 (two specimens, larval stages 39, December 27, 2008), MCN 1324 (seven froglets, February 7, 2009), MCN 1320/1322 (56 specimens, stages 39–46, December 8, 2009)

Ceratophrys cranwelli
Locality 2:

MCN 414 (38 specimens, larval stages 28–33, December 1, 1995), MCN 413 (22 specimens, larval stages 37–46, December 16, 1995); MCN 415 (24 specimens, larval stages 26–31, January 18, 1996), MCN 420 (13 specimens, larval stages 36–40, January 26, 1996), MCN 425 (seven specimens, larval stages 42–46, February 2, 1996), MCN 1345 (58 specimens, larval stages 26–36, December 1, 2007), MCN s/n (25 specimens, larval stages 39–44, December 12, 2007)

Locality 3:

MCN 1190 (23 specimens, larval stages 33–38, December 18, 2005); MCN 1034 (27 specimens, larval stages 37–43, March 23, 2006), MCN 1318 (14 specimens, larval stages 34–37, December 8, 2009)

Hylidae

Phyllomedusa azurea
Locality 3:

MCN 1054 (44 specimens, larval stages 34–40, February 10, 2005); MCN 1177 (78 specimens larval stages 33–44, April 1, 2006); MCN 1309 (66 specimens, larval stages 36–44, March 13, 2007); MCN 1326 (80 specimens larval stages 33–41, February 27, 2010); MCN 1346 (54 specimens, larval stages 37–46, April 14, 2010)

Phyllomedusa sauvagii
Locality 3:

MCN 1159 (76 specimens, larval stages 31–39, December 29, 2004); MCN 1077 (69 specimens, larval stages 33–42, February 17, 2005); MCN 1309 (103 specimens, larval stages 37–43, March 13, 2007); MCN 1348 (46 specimens larval stages 32–41, February 27, 2010); MCN 1330 (45 specimens, larval stages 38–46, April 04, 2010)

Pseudis paradoxa
Locality 3:

MCN 988 (35 specimens, larval stages 33–38, February 10, 2005); MCN 1171 (33 specimens, larval stages 33–42, March 10, 2006), MCN 1196 (54 specimens, larval stages 33–43, March 13, 2007); MCN 1197 (59 specimens, larval stages 33–46, April 4, 2007)

Scinax acuminatus
Locality 3:

MCN 1145 (48 specimens, larval stages 38–42, December 12, 2004); MCN 1339 (78 specimens, larval stages, 38–44, December 27, 2009); MCN 1347 (45 specimens, larval stages 37–46, April 14, 2010)

Scinax fuscovarius
Locality 3:

MCN 1134 (33 specimens, larval stages 34–38, November 2, 2001); MCN 1105 (43 specimens, larval stages 37–41, November 29, 2004); MCN 1144 (38 specimens, larval stages 38–44, December 29, 2004); MCN 1191 (60 specimens, larval stages 32–42, December 18, 2005); MCN 1315 (47 specimens, larval stages 38–46, January 05, 2008)

Scinax nasicus
Locality 3:

MCN 1350 (48 specimens, larval stages, 36–43, December 28, 2005); MCN 1349 (15 specimens, larval stages 37–44, December 30, 2006); MCN 1317 (53 specimens, larval stages 38–46, January 5, 2008)

Trachycephalus typhonius:
Locality 3:

MCN 1127 (49 specimens, larval stages 37–43, January 2, 2001); MCN 1337 (58 larval specimens, larval stages 37–42, December 27, 2007), MCN 1333 (33 specimens, larval stages 38–46, January 05, 2008)

Leiuperidae

Physalaemus biligonigerus
Locality 3:

MCN 1092 (45 specimens, larval stages 36–43, December 29, 2004); MCN 1097 (58 specimens, larval stages 37–46, February 17, 2005); MCN 1078 (35 specimens, larval stages 39–46, February 17, 2005), MCN 1079 (33 specimens, larval stages 38–42, March 12, 2005)

Leptodactylidae

Leptodactylus chaquensis
Locality 2:

MCN 1343 (56 specimens larval stages 35–37, December 1, 2007), MCN s/n (35 specimens, larval stages 40–42, December 12, 2007)

Locality 3:

MCN 1148 (78 specimens, larval stages 35–38, January 17, 2000); MCN 1335 (85 specimens, larval stages 39–44; 45, December 27, 2007)

Leptodactylus fuscus
Locality 2:

MCN 1344 (33 specimens, larval stages 39–43, December 1, 2007)

Locality 3:

MCN 816 (27 specimens, larval stages 38–42, December 28, 2003); MCN MCN 1089 (45 specimens, larval stages 39–43, December 29, 2004); 1336 (73 specimens, larval stages 39–44, December 27, 2007)

Leptodactylus mystacinus
Locality 3:

MCN 1351 (15 specimens, larval stages 39–46, December 30, 2006); MCN 1342 (25 specimens, larval stages 39–42, December 27, 2007)

Leptodactylus latinasus
Locality 3:

MCN 1126 (43 specimens, larval stages 37–42, February 10, 2005), MCN 1352 (140 specimens, larval stages 38–46, December 27, 2007)

Microhylidae

Dermatonotus muelleri
Locality 3:

MCN 1016 (60 specimens, larval stages 34–39, March 4; 2004); MCN 946 (55 specimens, larval stages 30–37, December 11, 2004); MCN 1094 (38 specimens, larval stages 38–43, December 29, 2004); MCN 997 (45 specimens, larval stages 31–37, February 9, 2005); MCN 1080 (23 specimens, larval stages 38–44, February 17, 2005), MCN s/n (100 specimens, larval stages 26–31, December 12, 2007), MCN 1340 (123 specimens, larval stages 35–39, December 27, 2007), MCN 1332 (75 specimens, larval stages 37–46, January 5, 2008)

Elachistocleis bicolor
Locality 3:

MCN 1164 (15 specimens, larval stages 37–42, January 17, 2000); MCN 1062 (22 specimens, larval stages 33–40, February 17, 2005); MCN 1081 (12 specimens, larval stages 32–37, March 12, 2005); MCN 1340 (5 specimens, larval stages 40–43, December 27, 2007)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fabrezi, M. Heterochrony in Growth and Development in Anurans from the Chaco of South America. Evol Biol 38, 390–411 (2011). https://doi.org/10.1007/s11692-011-9128-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-011-9128-5

Keywords

Search

Navigation