, Volume 136, Issue 1, pp 61–73 | Cite as

Cranial anatomy of the amazing bromeliad tadpoles of Phyllodytes gyrinaethes (Hylidae: Lophyohylini), with comments about other gastromyzophorous larvae

  • Florencia Vera CandiotiEmail author
  • Alexander Haas
  • Ronald Altig
  • Oswaldo Peixoto
Original Paper


The ecomorphological guild “gastromyzophorous” joins tadpoles that inhabit flowing water and have an abdominal sucker which is employed to adhere to substrates. Historically, gastromyzophorous larvae were known in the Bufonidae and Ranidae, but a new sucker-bearing hylid tadpole was recently described from phytotelmons in Brazilian forests. We describe the larval internal anatomy of Phyllodytes gyrinaethes and ask whether its exceptional external morphology is accompanied by derived anatomical internal features that can be related to the special habitat. We also compare it to the anatomy of sucker-bearing tadpoles from other families with a focus on characters exclusive of each lineage and the shared, convergent features. The skeleton of P. gyrinaethes is highly modified relative to that of pond-type hylines and shows a profound restructuring of the oral region, palatoquadrates, and the branchial baskets. Among the muscles, besides the overall reduction in the branchial musculature, the most unusual feature in this species are the enormous, anteriorly oriented mm. levatores mandibulae externus profundus that likely produce the abduction of the two halves of the snout. The presence of the abdominal sucker is coupled with changes in some muscle trajectories and hypertrophy of the subhyoid ligaments, and the sucker connectivity differs in some aspects compared with those of bufonids and ranids (e.g., the presence of massive mm. diaphragmatopraecordialis parallel to the sucker plane). P. gyrinaethes tadpoles, with their combination of both rare and unique morphological features plus their confined microhabitat with exceptional functional and ecological requirements, represent an extreme morphotype within Hylidae and anuran tadpoles in general.


Chondrocranium Levator mandibulae externus profundus Subhyoid ligament Three-dimensional reconstruction 










This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas, Agencia Nacional de Promoción Científica y Tecnológica, and Universidad Nacional de Tucumán Grants: PICTs 2012/2687, 2013/0404, 2014/1930, PIP 0875, and CIUNT-G430. We deeply thank E. Gretscher for serial sectioning and F. Pucci Alcaide for the photographs of histological sections. Also, we deeply thank F. Nascimento and B. Lisboa for the tadpole video recording and discussions about larvae behavior in the field.

Supplementary material

Supplementary material 1 (MP4 60918 kb)


  1. Aguayo R, Lavilla EO, Vera Candioti MF, Camacho T (2009) Living in fast-water: morphology of the gastromyzophorous tadpole of the bufonid Rhinella quechua (R. veraguensis group). J Morphol 270:1431–1442CrossRefPubMedGoogle Scholar
  2. Altig R (2006) Discussions of the origin and evolution of the oral apparatus of anuran tadpoles. Acta Herpetol 2:95–105Google Scholar
  3. Altig R, McDiarmid RW (1999) Body plan: development and morphology. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, pp 24–51Google Scholar
  4. Böck P (1989) Romeis Mikroskopische Technik. Urban & Schwarzenberg, MünchenGoogle Scholar
  5. Böck JW, Shear CR (1972) A staining method for gross dissection of vertebrate muscles. Anat Anz 130:222–227PubMedGoogle Scholar
  6. Carr KM, Altig R (1991) Oral disc muscles of anuran tadpoles. J Morphol 208:271–277CrossRefGoogle Scholar
  7. Dietrich HF, Fontaine AR (1975) A decalcification method for ultrastructure of echinoderm tissues. Stain Technol 50:351–354CrossRefPubMedGoogle Scholar
  8. Faivovich J, Haddad CFB, Garcia PCA, Frost DR, Campbell JA, Wheeler WC (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294:1–240CrossRefGoogle Scholar
  9. Gan LL, Hertwig ST, Das I, Haas A (2015) The anatomy and structural connectivity of the abdominal sucker in the tadpoles of Huia cavitympanum, with comparisons to Meristogenys jerboa (Lissamphibia: Anura: Ranidae). J Zool Syst Evol Res 54:46–59CrossRefGoogle Scholar
  10. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  11. Haad MB, Vera Candioti F, Baldo D (2014) The stream tadpoles of Rhinella rumbolli (Anura: Bufonidae). Herpetologica 70:184–197CrossRefGoogle Scholar
  12. Haas A (2001) Mandibular arches musculature of anuran tadpoles, with comments on homologies of amphibian jaw muscles. J Morphol 247:1–33CrossRefPubMedGoogle Scholar
  13. Haas A (2003) Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19:23–89Google Scholar
  14. Haas A, Fischer MS (1997) Three dimensional reconstruction of histological sections using modern product-design software. The Anat Rec 249:510–516CrossRefPubMedGoogle Scholar
  15. Haas A, Hertwig S, Das I (2006) Extreme tadpoles: the morphology of the fossorial megophryid larva, Leptobrachella mjobergi. Zoology 109:26–42CrossRefPubMedGoogle Scholar
  16. Haas A, Pohlmeyer J, McLeod DS, Kleinteich T, Hertwig ST, Das I, Buchholz D (2014) Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole. Zoomorphology 133:321–342CrossRefGoogle Scholar
  17. Handrigan GR, Haas A, Wassersug RJ (2007) Bony-tailed tadpoles: the development of supernumerary caudal vertebrae in larval megophryids (Anura). Evol Dev 9:190–202CrossRefPubMedGoogle Scholar
  18. Inger RF (1966) The systematics and zoogeography of the Amphibia of Borneo. Fieldiana Zool 52:1–402Google Scholar
  19. Inger RF (1985) Tadpoles of the forested regions of Borneo. Fieldiana Zool 26:1–89Google Scholar
  20. Kaplan M (1997) Internal and external anatomy of the abdominal disc of Atelopus (Bufonidae) larvae. Caldasia 19:61–69Google Scholar
  21. Lannoo MJ, Townsend DS, Wassersug RJ (1987) Larval life in the leaves: arboreal tadpole types, with special attention to the morphology, ecology and behavior of the oophagous Osteopilus brunneus (Hylidae) larva. Fieldiana Zool 38:1–31Google Scholar
  22. Lavilla EO, de Sá RO (2001) Chondrocranium and visceral skeleton of Atelopus tricolor and Atelophryniscus chrysophorus tadpoles (Anura. Bufonidae). Amphibia-Reptilia 22:167–177CrossRefGoogle Scholar
  23. Lehtinen RM, Lannoo MJ, Wassersug RJ (2004) Phytotelm-breeding anurans: past, present and future research. Misc Publ Mus Zool Univ Mich 193:1–9Google Scholar
  24. Magalhães FM, Juncá FA, Garda AA (2015) Tadpole and vocalizations of Phyllodytes wuchereri (Anura: Hylidae) from Bahia, Brazil. Salamandra 51:83–90Google Scholar
  25. Noble GK (1929) The adaptive modifications of the arboreal tadpoles of Hoplophryne and the torrent tadpoles of Staurois. Bull Am Mus Nat Hist 58:291–337Google Scholar
  26. Orton GI (1953) The systematics of vertebrate larvae. Syst Zool 2:63–75CrossRefGoogle Scholar
  27. Peixoto OL, Caramaschi U, Freire EMX (2003) Two new species of Phyllodytes (Anura: Hylidae) from the state of Alagoas, northeastern Brazil. Herpetologica 59:235–246CrossRefGoogle Scholar
  28. Pusey HK (1943) On the head of the liopelmid frog, Ascaphus truei. I. The chondrocranium, jaws, arches, and muscles of a partly-grown larva. Q J Microsc Sci 84:105–185Google Scholar
  29. Raj P, Vasudevan K, Singh S, Aggarwal RK (2012) Larval morphology and ontogeny of Nasikabatrachus sahyadrensis Biju & Bossuyt, 2003 (Anura, Nasikabatrachidae) from Western Ghats, India. Zootaxa 3510:65–76Google Scholar
  30. Ramaswami LS (1943) An account of the chondrocranium of Rana afghana and Megophrys, with a description of the masticatory musculature of some tadpoles. Proc Natl Inst Sci India 9:43–58Google Scholar
  31. Roelants K, Haas A, Bossuyt F (2011) Anuran radiations and the evolution of tadpole morphospace. PNAS 108:8731–8736CrossRefPubMedPubMedCentralGoogle Scholar
  32. Rowley JJL, Tran DAT, Le DTT, Hoang HD, Altig R (2012) The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam. J Nat Hist 46:2969–2978CrossRefGoogle Scholar
  33. Sokol OM (1962) The tadpole of Hymenochirus boettgeri. Copeia 1962:272–284CrossRefGoogle Scholar
  34. Taylor W, van Dyke GC (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium 9:107–119Google Scholar
  35. Vera Candioti MF (2004) Morphology of premetamorphic larvae of Lysapsus limellus (Anura: Pseudinae) from Santa Fe, Argentina. Amphibia-Reptilia 25:41–54CrossRefGoogle Scholar
  36. Vera Candioti MF (2007) Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits. Zootaxa 1600:1–175CrossRefGoogle Scholar
  37. Vera Candioti MF, Haas A (2004) Three dimensional reconstruction of the hyobranchial apparatus of Hyla nana tadpoles (Anura: Hylidae). Cuad Herpetol 18:3–15Google Scholar
  38. Wassersug RJ, Hoff K (1979) A comparative study of the buccal pumping mechanism of tadpoles. Biol J Linn Soc 12:225–259CrossRefGoogle Scholar
  39. Zachariah A, Abraham RK, Das S, Altig R (2012) A detailed account of the reproductive strategy and developmental stages of Nasikabatrachus sahyadrensis (Anura: Nasikabatrachidae), the only extant member of an archaic frog lineage. Zootaxa 3510:53–64Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Florencia Vera Candioti
    • 1
    Email author
  • Alexander Haas
    • 2
  • Ronald Altig
    • 3
  • Oswaldo Peixoto
    • 4
  1. 1.Unidad Ejecutora Lillo (CONICET-FML)TucumánArgentina
  2. 2.Biozentrum Grindel und Zoologisches Museum HamburgHamburgGermany
  3. 3.Department of Biological SciencesMississippi State UniversityMississippi StateUSA
  4. 4.Departamento de Biologia Animal, Instituto de BiologiaUniversidade Federal Rural do Rio de JaneiroSeropédicaBrazil

Personalised recommendations